Functions: From Organisms to Artefacts (History, Philosophy and Theory of the Life Sciences, 32) 3031312708, 9783031312700

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History, Philosophy and Theory of the Life Sciences  32

Jean Gayon Armand de Ricqlès Antoine C. Dussault   Editors

Functions: From Organisms to Artefacts

History, Philosophy and Theory of the Life Sciences Volume 32

Series Editors Philippe Huneman, (CNRS/Université Paris I Panthéon-Sorbonne), Institut d’Histoire et de Philosophie des Sciences et des Techniques, IHPST, Paris, France Thomas A. C. Reydon, Institute of Philosophy & CELLS, Leibniz Universität Hannover, Hannover, Germany Charles T. Wolfe, Département de Philosophie & ERRAPHIS, Université de Toulouse Jean-Jaurès, Toulouse, France Editorial Board Members Marshall Abrams, University of Alabama, Birmingham, AL, USA André Ariew, University of Missouri, Columbia, MO, USA Domenico Bertoloni Meli, Indiana University, Bloomington, IN, USA Richard Burian, Virginia Tech, Blacksburg, VA, USA Minus van Baalen, Institut Biologie de l’Ecole Normale Supérieure, Paris, France Pietro Corsi, University of Oxford, Oxford, UK François Duchesneau, Université de Montréal, Montreal, QC, Canada John Dupre, University of Exeter, Exeter, UK Paul Farber, Oregon State University, Corvallis, OR, USA Lisa Gannett, Saint Mary’s University, Halifax, NS, Canada Andy Gardner, University of St Andrews, St Andrews, UK Jean Gayon, UFR de Philosophie, Université Paris 1 Panthéon-Sorbonne, Paris, France Guido Giglioni, University of Macerata, Civitanova Marche, Italy Paul Griffiths, University of Sydney, Sydney, NSW, Australia Thomas Heams, AgroParisTech, Paris Cedex 05, France James G. Lennox, University of Pittsburgh, Pittsburgh, PA, USA Annick Lesne, Sorbonne Université, Paris, France Tim Lewens, University of Cambridge, Cambridge, UK Edouard Machery, University of Pittsburgh, Pittsburgh, PA, USA Alexandre Métraux, Archives Poincaré, Nancy, France Hans Metz, Leiden University, Leiden, The Netherlands Roberta L. Millstein, University of California, Davis, Davis, CA, USA Staffan Müller-Wille, University of Cambridge, Cambridge, UK François Munoz, Université Montpellier 2, Montpellier, France Dominic Murphy, University of Sydney, Camperdown, NSW, Australia Stuart A. Newman, New York Medical College, Valhalla, NY, USA Frederik Nijhout, Duke University, Durham, NC, USA

Samir Okasha, University of Bristol, Bristol, UK Susan Oyama, The City University of New York, New York, USA Kevin Padian, University of California, Berkeley, CA, USA David Queller, Washington University in St. Louis, St. Louis, MO, USA Stephane Schmitt, Archives Poincaré, Nancy, France Phillip Sloan, University of Notre Dame, Notre Dame, IN, USA Jacqueline Sullivan, Western University, London, ON, Canada Giuseppe Testa, University of Milan, Milan, Italy J. Scott Turner, SUNY College of Environmental Science and Forestry, Syracuse, NY, USA Denis Walsh, University of Toronto, Toronto, ON, Canada Marcel Weber, University of Geneva, Geneva, Switzerland

History, Philosophy and Theory of the Life Sciences is a space for dialogue between life scientists, philosophers and historians – welcoming both essays about the principles and domains of cutting-edge research in the life sciences, novel ways of tackling philosophical issues raised by the life sciences, as well as original research about the history of methods, ideas and tools, which constitute the genealogy of our current ways of understanding living phenomena. The series is interested in receiving book proposals that • are aimed at academic audience of graduate level and up • combine historical and/or philosophical and/or theoretical studies with work from disciplines within the life sciences broadly conceived, including (but not limited to) the following areas: • Anatomy & Physiology • Behavioral Biology • Biochemistry • Bioscience and Society • Cell Biology • Conservation Biology • Developmental Biology • Ecology • Evolution & Diversity of Life • Genetics, Genomics & Disease • Genetics & Molecular Biology • Immunology & Medicine • Microbiology • Neuroscience • Plant Science • Psychiatry & Psychology • Structural Biology • Systems Biology • Systematic Biology, Phylogeny Reconstruction & Classification • Virology The series editors aim to make a first decision within 1 month of submission. In case of a positive first decision the work will be provisionally contracted: the final decision about publication will depend upon the result of the anonymous peer review of the complete manuscript. The series editors aim to have the work peer-reviewed within 3 months after submission of the complete manuscript. The series editors discourage the submission of manuscripts that contain reprints of previously published material and of manuscripts that are below 150 printed pages (75,000 words). For inquiries and submission of proposals prospective authors can contact one of the editors: Charles T. Wolfe: [email protected] Philippe Huneman: [email protected] Thomas A.C. Reydon: [email protected]

Jean Gayon  •  Armand de Ricqlès Antoine C. Dussault Editors

Functions: From Organisms to Artefacts

Editors Jean Gayon (deceased) herein represented by his wife Elisabeth Gayon Institut d’histoire et de philosophie des sciences et des techniques (IHPST)

Armand de Ricqlès Collège de France Paris, France

(CNRS/Université Paris I Panthéon Sorbonne)

Paris, France Antoine C. Dussault Centre interuniversitaire recherche sur la science et la technologie (CIRST) Collège Lionel Groulx Montréal, QC, Canada

ISSN 2211-1948     ISSN 2211-1956 (electronic) History, Philosophy and Theory of the Life Sciences ISBN 978-3-031-31270-0    ISBN 978-3-031-31271-7 (eBook) https://doi.org/10.1007/978-3-031-31271-7 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Introduction to the New English Edition1

On April 28, 2018, at the age of 68, our dear colleague and friend Jean Gayon passed away after a long illness. His “Festschrift” book, a retirement gift assembled by Merlin and Huneman (2018), was testimony to a community’s profound fellowship with, and gratitude for, an outstanding scholar, who significantly pushed the boundaries of studies in history and philosophy of biology in France. Well aware of his situation, Jean Gayon started in 2016 to give top priority to completing the remarkable historical, scientific, and philosophical dialogue he had begun with Victor Petit in 2010. These discussions culminated in the publication of La connaissance de la vie aujourd’hui (Gayon & Petit, 2018), translated as Knowledge of Life Today: Conversations on Biology (Gayon & Petit, 2019), an intellectual testament of remarkable quality. However, due to the circumstances, Jean Gayon had to leave a number of other projects to languish. Here, we must thank his wife, Elisabeth Valsecchi-Gayon, and certain close collaborators and friends (including Françoise Parot and Philippe Huneman), for promptly beginning the task of cataloguing the scholar’s papers: course outlines, lectures, correspondence, and reviews. Much of the work that was in progress has been stabilized and completed. It is a boon to all of us that their carefully structured Gayon archive is now housed in the library of the Institut Pasteur (Inventaire des archives de Jean Gayon (1949–2018), December 2018). One of the projects Jean Gayon especially cherished was an English translation of the essay collection Les fonctions, des organismes aux artefacts (Gayon & de Ricqlès, 2010). Published in French in 2010, it was spawned by the innovative interdisciplinary initiative he had piloted from 2002 to 2008. The introduction to the French edition, in the following pages, tells the reasoned, circumstanced story of the growth of this collective endeavor. We felt we had to fulfill Jean Gayon’s wishes by completing this translation project, which he had initiated with Springer for their series History, Philosophy and

 Translated from French by Anita Conrade.

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Theory of the Life Sciences directed by Charles Wolfe, Philippe Huneman, and Thomas Reydon. True, in the course of a decade the intellectual landscape has changed. The book was instrumental in spreading, if not introducing, into the French-speaking world, two naturalistic conceptions of function that had originated in English: the “etiological” theory (Wright, 1973) and the “systemic” theory (Cummins, 1975). Above all, Les fonctions, des organismes aux artefacts offered a rich sample of the new discussions and thoughts stirred by those conceptions in a broad range of fields, from the history and philosophy of science to technologies, not to mention the whole spectrum of biological and biomedical sciences. The present edition maintains all the texts published in the original edition, except for the article by Mossio, Saborido, and Moreno (“Fonctions: Normativité, téléologie et organisation”) omitted because most of its theoretical content is already available in other publications in English (Mossio et al., 2009; Saborido et al., 2011; Moreno & Mossio, 2015). We again thank Matteo Mossio for acting so efficiently as Jean Gayon’s general coordinator for the original edition. For this edition, in almost every case, the authors were given the opportunity to revise their essays, updating them and adding any supplemental bibliographical information they judged necessary. We felt it was interesting to enrich this edition with some original and previously unpublished contributions expanding the range of reflection on the concept of function. In Part I (Origins of Functional Discourse in the Life Sciences), there is a review by Pierre-Marie Pouget of the interesting “Symposium écrit” organized in Switzerland between 1976 and 1984 by the Institut de la Méthode (Association Ferdinand Gonseth) on the theme “Fonction et Finalité.” Looking back on this work, we see that it sheds light on some of the difficulties or aporias preceding the implementation of the two contemporary naturalistic theories of function. In Part II (Function, Selection, Adaptation), we have added a contribution by Gustavo Caponi which presents a critique of the etiological theory of function. Caponi argues that explanations involving natural selection, instead of being the basis for ascriptions of function, rely on these ascriptions. The author then suggests that these explanations be theorized as “design explanations” rather than functional explanations. In the same part, we have also added a chapter by Antoine C. Dussault. Dussault discusses the classical family of counterexample to the etiological, or selected effects, theory of function, epitomized by Mark Bedau’s case of clay crystals and other, more recently highlighted, cases. Items like clay crystals raise a challenge for the selected effects theory, because, although they meet the standard conditions for natural selection, they do not seem to bear functions. In Part V (Functions and Origins of Life), we have added a chapter by Aurore Dupin on the use of the concept of function in chemistry. In teaching, it is usual to consider the existence of “functions” in chemistry (the acid function, for example). But does this usage go beyond the mere verbal analogy with function in biology?

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In Part VIII (The Same Functional Reasoning in Engineering and Biology?), we have added Jean-Hugues Barthélémy’s presentation of the ideas on function of Gilbert Simondon (1924–1989). Although the concept is not central to Simondon’s thinking, function occupies a place that is both prominent and original. The original introduction to the book now deserves some brief comment, considering the feedback it elicited upon publication (Sartenaer, 2011). In the field of the history of ideas, some reviewers perceived the presentation of the history of the concept of function in this introduction as being somewhat cursory. Later, however, in his dialogue with Victor Petit (Gayon & Petit, 2018), Jean Gayon arrived at a much richer and more subtle presentation of this history (pp. 161–163), even outlining the early relationships it shares with the mathematical concept of function. Likewise, it may seem surprising that this introduction lacks any reference to the work of Jean Piaget (1896–1980) on function. This is because Jean Gayon had already published an important study about the question: “Functional Explanation in Piaget’s Psychology and Epistemology” (in Parot, 2008). Although the translation of this study could have been included in this volume, a decision was made to publish it as part of a corpus of translations of texts by Jean Gayon, edited by Philippe Huneman (in preparation). We sincerely thank all those who assisted us in bringing this book into being, especially Noak Blottière, Anita Conrade, Mark Gersovitz, Nathalie Gillès de Pelichy, Philippe Huneman, Françoise Parot, Carlotta Pavese, Catherine Porter, Françoise Thibault, and Elisabeth Valsecchi-Gayon. 

Armand de Ricqlès 

Antoine C. Dussault

References Cummins, R. C. (1975). Functional analysis. Journal of Philosophy, 72, 741–764. Gayon, J., & de Ricqlès, A. (Eds.). (2010). Les fonctions: des organismes aux artefacts. PUF. Gayon, J., & Petit, V. (2018). La connaissance de la vie aujourd’hui. ISTE Edition. Gayon, J., & Petit, V. (2019). Knowledge of life today: Conversations on biology. ISTE Edition. Huneman, P. (Ed.). (in preparation). Corpus of translations of texts by Jean Gayon. Merlin, F., & Huneman, P. (Eds.). (2018). Philosophie, histoire, biologie: Mélanges offerts à Jean Gayon. Matériologiques. Moreno, A., & Mossio, M. (2015). The autonomy of living systems: A philosophical enquiry into biological organization. Springer. Mossio, M., Saborido, C., & Moreno, A. (2009). An organizational account of biological functions. British Journal for the Philosophy of Science, 60, 813–841. Parot, F. (Ed.). (2008). Les fonctions en psychologie: Enjeux et débats. Mardaga.

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Saborido, C., Mossio, M., & Moreno, A. (2011). Biological organization and cross-generation functions. British Journal for the Philosophy of Science, 62, 583–606. Sartenaer, O. (2011). Les fonctions  : Des organismes aux artéfacts. Sous la direction de Jean Gayon et Armand de Ricqlès. Avec la collaboration de Matteo Mossio. Revue Philosophique de Louvain, 109, 835–839. Wright, L. (1973). Functions. Philosophical Review, 82, 139–168.

Introduction to the Original French Edition1

Since the Renaissance, the notion of function has structured thinking in three important fields: the life sciences and medicine, technology, and political and social sciences. In these three areas, the term “function” suggests that something plays a role in achieving a certain goal, and that the thing you are describing is supposed to carry out this role. For example, to say that the heart’s function is to pump blood amounts to saying that the heart plays a role in circulating blood, and that the heart is supposed to carry out this role. To say that the function of an engine valve is to regulate the flow of gases by opening and closing amounts to saying that the device plays a role in regulating the flow of gases, and that the valve was designed and installed for this purpose. In the field of social sciences, the term “function” is also long-standing common usage. Initially, it would seem that it was used as a synonym of duty, or office: such and such a job, public responsibility, or institution is a “function” in the sense that a social role, along with various effects specific to it, is assigned to a person or an organization. The French word “fonctionnaire” (commonly used to designate a civil servant or government employee) attests to the important social dimension of the discourse on function. Whether it is a matter of life sciences, mechanics, or social roles, the word “function” nearly always conveys the idea of teleology or normativity. These connotations are most obvious in the fields of social and political sciences. The give-and-take between the registers of biology and technology, however, has produced a different conceptual configuration, in which our attention is focused on the problem of causality. Any effort to define the function of an object or organic feature is bound to oscillate between two types of investigation: why this thing is there, and made the way it is (raising the problem of purpose); and how does it usually operate, i.e., how does it function (raising the problem of efficient causality, and highlighting the special inflection of the verb form “to function”). Here, we cannot help but think of René Descartes’s famous sentence at the very beginning of the Treatise on Man, when he suggests studying the human body as if it were a machine:

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Introduction to the Original French Edition I suppose the body to be nothing but a statue or machine made of earth, which God forms with the explicit intention of making it as much as possible like us. Thus God not only gives it externally the colours and shapes of all the parts of our bodies, but also places inside it all the parts required to make it walk, eat, breathe, and indeed to imitate all those of our functions which can be imagined to proceed from matter and to depend solely on the disposition of our organs. (Descartes, 1985, 99, A.T. XI, 120)

As Georges Canguilhem observed, these sentences characteristic of the mechanistic program actually attest to Descartes’s profound conceptual ambivalence. On the one hand, the philosopher invites us to explain the vital functions as the effects of the physical arrangement of the organs; while on the other hand, he introduces the idea of the body-machine, which requires that we accept a highly purpose-­ oriented fiction of a God who “deliberately shapes” (Canguilhem, 2008 [1965]). The exact historical conditions surrounding the appearance of the word and concept of function are not well known. It first appeared in print in medical texts in Latin in the sixteenth century. Usage quickly spread to the field of technology and that of administrative organization. We can say little else, because, surprising as it may seem, there is no historical study of the subject. We nevertheless believe that the interactions between the three fields to which the term applies are as lively as they were five hundred years ago, and that they shed significant light on the ambiguities and paradoxes associated with the usage of the term “function.” In this book, we have limited our investigation to the way the concept of function applies in the fields of biology and technology, where vigorous philosophical debates surround its usage. These controversies developed on the international scale in the late twentieth century. They concern the very meaning of the word “function,” the attribution of functions, and function-based explanations. It is therefore useful to recall the range of these philosophical endeavors, taken for granted in this book, before indicating this book’s specificity. In the 1950s, positivist philosophy of science instituted a climate in which the omnipresence and persistence of function-based statements in contemporary scientific writings seemed outrageous. Statements such as “the function of erythrocytes is to carry oxygen to cells” are almost always understood as tentative explanations. Yet from the viewpoint of scientific methodology, they are paradoxical, because they seem to suggest that a phenomenon can be explained on the basis of its effects. They therefore break all the usual rules for causal explanation. For example, if we say that in vertebrates, the function of the heart is to circulate blood, we not only mean that circulation is what the heart does, but also that the heart is present in vertebrates in order to cause circulation. It would be unthinkable for physicists or chemists to make similar statements. For example, as Ernest Nagel pointed out, it is hard to imagine a chemist explaining covalent bonding between atoms in the following terms: “atoms have outer shells of electrons in order to make chemical unions between themselves and other atoms possible” (Nagel, 1961, 401). A chemist is satisfied with deducing knowledge about atomic structure and quantum mechanics from the properties of covalent bonding. Similarly, a geographer would never write that the function of glaciers is to provide a regular flow of water to the inhabitants of valleys and plains – unless, as is currently the case in the Himalayas,

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technical means had been installed to limit glacier melting and reconfigure the glaciers for the specific purpose of preserving their ability to store water. Aside from exceptional cases like these, the function of glaciers is not to store water. Glaciers store water simply by virtue of their own physical properties. Biologists, by contrast, have absolutely no qualms about attributing functions to organ systems, organs, cells, and now molecules. Beginning in the 1950s, several philosophers set out to reconcile the preposterous statements and explanations about function, found in biology, psychology, and sociology, with scientific methodology. Carl Hempel played a crucial role in this effort. He tried to show that, for logical reasons, and within the framework of the nomological-deductive model of scientific explanation he advocated, the very notion of a functional explanation was indefensible (Hempel, 1959). This publication had a devastating effect. After Hempel, philosophers more or less abandoned the problem of functional explanation (conceived as the explanation of something by its function), and turned to the problem of the attribution of functions. Ernest Nagel pioneered this movement by attempting to show that the functional statements in the biological sciences could be translated into ordinary causal statements, and therefore did not pose any real problem (Nagel, 1961). According to Nagel, the crux of the problem was simply a difference in perspective: the biologist’s attention is focused on effects; he or she really has no intention of violating the principle of causality. However, Nagel’s solution soon proved to be limited.2 As a result, a certain number of philosophers suggested alternative accounts of functional attributions, although they frequently had to forfeit simplicity. In the mid-1970s, the situation changed drastically. Two philosophers, Larry Wright and Robert Cummins, suggested two different interpretations of functional statements. Wright was motivated chiefly by the construction of a theory of action, whereas Cummins specialized in the methodology of psychological and cognitive sciences. Although the original texts are challenging to read, the solutions they proposed have structured most of the discussion that has developed since. Wright called his theory of function the “etiological theory” (1973). Later renamed the “selected effects theory,” it gave rise to a prevailing tradition that interprets functional statements in reference to the theory of evolution by natural selection. Philosopher Karen Neander summarized it most succinctly: “The function of a trait is the effect for which that trait was selected” (Neander, 1991, 459; see also this book). In this conception, the attribution of a function to a trait (the heart, for example) refers to the past history of the systems that, through reproduction, led to  Nagel’s idea was especially simple. As long as the term “cause” is understood as “necessary condition,” the following two statements mean the same thing: “In vertebrates, the heart’s function is to pump blood,” and “In vertebrates, the heart is a necessary condition for pumping blood.” However, although elegant in appearance, a limit of this solution is its inability to differentiate between an accidental effect and a function. For example, it does not explain the difference in status between two typical effects of the heart in humans: pumping blood and the sound of the heartbeat. In either case, the heart is the necessary condition for both effects. But no biologist would say that the heart’s function is to make a sound. Therefore, Nagel’s suggestion that both statements are equivalent is untrue. It lacks something that is essential to assigning functions. 2

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the system or systems in which the trait is being considered at the moment t. In simpler terms, to attribute a function to the heart is to say that the heart was selected for in the ancestors of the heart-bearing organisms alive today. It matters little that Larry Wright, who was less interested in the philosophy of science (especially of biology) than in the theory of action,3 introduced as the “etiological theory” a far more complex conception, in which selection, although it did play a role, nevertheless did not belong to his definition of the term function. The fact is that after Wright, several philosophers in the fields of biology, psychology, and technology explored the link the etiological theory established between function and selection. This school of thought subordinates the understanding of the concept of function to a contemporary scientific theory – that of evolution by natural selection. It is characterized by its conspicuously realist interpretation of functions. The etiological conception of function is also commonly called the “selective etiological theory” or “evolutionist theory” of function, and sometimes the “teleological theory.” The other school of thought originated with Robert Cummins who, in 1975, proposed a quite different theory of function. According to Cummins (1975), when functions are attributed, whether the field is biology, engineering, or psychological or cognitive sciences, they must not be understood in reference to previous history. They concern systems considered in their current state, and the point is to understand how their capacities result from the behavior of their components. For Cummins, to say that X has function F means that X plays a “causal role” in the system that contains it, and contributes to the emergence of a capacity in that system. For example, by contracting, the diaphragm expands the lungs and causes the air pressure inside them to drop. Its function is thus nothing other than the causal role it plays in the terrestrial vertebrate respiratory system. This conception of function is commonly designated the “systemic theory” or the “theory of function as causal role.” Unlike the etiological theory, the systemic theory of function is generally not understood in a realist spirit. Functions are attributed in relation to the context of a given scientific explanation and to a specific methodology. Thirty-five years after the publication of the seminal texts by Wright and Cummins, the scope and productivity of the research and controversy they have spawned are surprising. In certain cases, especially those of the cognitive sciences and functional morphology, the debate has played an important role in the very development of scientific research. More generally, however, an unprecedented episode in philosophical investigation has begun. Astonishing as it may seem, the effort to clarify the concept of function, and to define it (rather than merely using it) is specific to the contemporary era. In writings from past centuries, spontaneous ideas about the notion of function could no doubt be identified, although they would still be fairly rare. But there has almost never been a direct examination of what function means or could precisely signify. Physiologist Claude Bernard’s comments on the  The much-regretted Marie-Claude Lorne analyzed this point superbly in her doctoral dissertation in philosophy (2005). Lorne showed that Larry Wright’s philosophical agenda differed from that of the philosophers of biology and psychology who followed in his wake in the name of the “etiological theory” of functions. 3

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subject, recalled in this book by François Duchesneau and by Jean-Claude Dupont, stand out as a remarkable exception. But even in this case, the writings are still more intuitive than analytic. Whereas physics and chemistry have prompted innumerable and prominent considerations about causality since the seventeenth century, the notion of function, an essential category in biology, the social sciences, and even technology, was not scrutinized with comparable thoroughness until the end of the twentieth century. These contemporary philosophical discussions form the background against which most of the essays in this book come into focus. Nevertheless, reviewing and developing the debates of analytical philosophers about the definition of the concept of functions is neither the exclusive nor the primary goal of this book. Certain articles contribute to gaining this insight: Neander, Huneman, Gayon, and Mossio/ Saborido/Moreno write about the usage of this idea in biology (Part II); and Krohs, Vermaas and Houkes, and Longy have studied its usage in the fields of technology and medicine (Parts VII and VIII). In this respect, we are especially happy to be able to offer the French public a set of original contributions on a subject that has been largely ignored by French philosophers, with the notable exception of Joëlle Proust (1995) and that of the previous publications of various authors who participated in this book. The original essay by Karen Neander, a major player in the debate, is a great honor. The reader should also take note of the importance we have attributed to the emerging field of theories of function extended to technical objects (Part VIII). However, the rest of the book obeys a different agenda, which sets it apart fairly clearly from the literature available in English on the subject.4 In the first place, we have granted a significant amount of attention to what might be called the “archeology” of theories of function. Historical studies of the subject are extremely rare, for the theories are indeed difficult to identify. As we noted above, before the second half of the twentieth century, the philosophical-­ methodological reflections on functions were essentially implicit and intuitive. They were immersed in a scientific practice which often had a dramatically pressing need for the term “function,” but which does not reflect critically upon itself. In this respect, Part I offers several studies describing the distant sources of discourse on functions  – particularly, in Greek and Hellenistic thought, even before the Latin word “function” appeared –, and its increasing influence in the seventeenth and nineteenth centuries, among the physiologists (like Haller and Claude Bernard), naturalists (Cuvier), and (already!) one philosopher (Auguste Comte). We must point out the extreme rarity of this type of approach, in the literature. James Lennox, François Duchesneau, and Laurent Clauzade are acting as pioneers. This part also contains a highly informative study of the history of the word and concept design, the fate of which has been closely tied to discourse on functions since the Renaissance. Actually, this term is revelatory: in the absence of explicit and critical commentaries on function, it brings the connections between the contexts

 Several remarkable collections attest to the liveliness of this debate: Block (1980); Allen et al. (1998); Buller (1999); Ariew et al. (2002); Krohs & Kroes (2009). 4

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(scientific, technological, aesthetic, and theological) of the discourse on function into sharp relief. In this respect, Daniel Becquemont’s study is extremely useful in showing us the reasons for the inflationist return of this concept in contemporary biological discourse and technological culture. In other parts (Parts V and VI) about specific aspects of the history of science, certain authors have also favored a historical approach to the variety of epistemological implications of the discourse on function. This is the case of the essays by Jean-Claude Dupont (physiology), Charles Galperin (genetics), Stéphane Tirard (origins of life), and Françoise Parot (behaviorist psychology). These studies reveal that the philosophical theories of function of the past few decades have yet to complete the endeavor of analyzing the effective usage of the concept of function. The second distinctive feature of this book is the way it systematically confronts philosophical reflections on the notion of function with contemporary research in biology: the fields of morphology and paleontology (Ricqlès and Cubo, Laurin, Part III); physiology, molecular biology, genetics, and immunology (Dupont, Morange, Galperin, Pradeu); origins of life (Tirard, Malaterre, Part V); and psychology and neuroscience (Parot, Forest, Part VI). The overall impression left by these essays, grouped in the second part of the book, is that the usage of the concept of function in the majority of the disciplines considered is at odds with the evolutionist vision of functions dominating among philosophers. The last specificity of this book is its accent on medicine and technology. It is not surprising to see reflection focus on non-functional and dysfunctional in the field of medicine. The contributions in Part VII (Krohs, Plagnol) are a timely reminder of the normative aspect inherent to the concept of function, which could easily be omitted in other fields of research. The relationships between the discourse on function and the concepts of normal, pathological, and healthy are complex and often counterintuitive. Lastly, the essays in Part VIII are devoted to the usage of the concept of function in the field of technology. These three chapters (Abourachid and Hugel, Vermaas and Houkes, Longy) raise the difficult question of whether any comparison is possible between the concepts of function used in the life sciences and those used in technology, and whether they mobilize more than intuitive analogies. This challenging question, which was already crucial in the seventeenth century, apparently has yet to be answered. We cannot omit mention of the circumstances that led to this publication. It is the fruit of a multi-disciplinary research program that involved 20 researchers between 2002 and 2008. They came from four Paris research units: one specializing in evolution and comparative anatomy,5 a second specializing in cognitive psychology,6 and two units researching philosophy and history of science,7 coordinated by Armand de  “Adaptations et évolution des systèmes ostéomusculaires” team, UMR 8570, Muséum national d’histoire naturelle/Université Paris 7/Collège de France/CNRS. 6  “Développement & fonctionnement cognitifs” research team from the Groupe d’Imagerie Neurofonctionnelle (GIN), CNRS UMR 6095, CEA LRC 36V, Universités de Caen et Paris-5. 7  “Recherche en épistémologie et histoire des sciences et des institutions scientifiques” unit, (REHSEIS), UMR 7596, CNRS/Université Paris 7 and “Institut d’histoire et de philosophie des sciences et des techniques,” UMR 8590 Paris 1/CNRS/ENS. 5

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Ricqlès, Olivier Houdé, Françoise Parot, and Jean Gayon, respectively. This ­experience has been extremely productive. Please allow us to thank all who were associated with it,8 whether they appear in this book or not, as well as the French Ministry of Research, which funded this effort with an “Action Concertée Incitative” (ACI) grant program.9 Likewise, we are grateful to the Collège de France for hosting the seminar that concluded the research program and for lending its support to the publication of this book. Françoise Longy, who launched the very idea of an in-depth investigation of functions, must also be singled out here for special thanks, as well as the colleagues who took on the task of translating into French contributions submitted in other languages (Françoise Longy, Christophe Malaterre, Johannes Martens, Matteo Mossio). We conclude our acknowledgments with warm thanks to Matteo Mossio for his discreet, disciplined, and efficient assistance in finalizing the texts. Lastly, this book is dedicated to the memory of Marie-Claude Lorne, a young philosopher enrolled in this research program who tragically died in September 2008. The overview she wrote on the current state of the philosophical debate about functional attributions and explanations is unique in the scientific literature, in France and internationally. Marie-Claude Lorne was simultaneously this program’s mind and soul. Jean Gayon 

Armand de Ricqlès

References Allen, C., Bekoff, M., & Lauder, G. (1998). Nature’s purposes: Analyses of function and design in biology. The MIT Press. Ariew, A., Cummins, R., & Perlman, M. (2002). Functions: New essays in the philosophy of psychology and biology. Oxford University Press. Block, N. (1980). Readings in philosophy of psychology (Vol. 1). Harvard University Press. Buller, D. J. (1999). Function, selection, and design. SUNY Press. Canguilhem, G. (2008). Machine and organism. In Knowledge of life (P.  Marrati-Guénoun & T. Meyers, Eds., S. Geroulanos & D. Ginsburg, Trans.) (pp. 75–97). Fordham University Press. Cummins, R. C. (1975). Functional analysis. Journal of Philosophy, 72, 741–64.

  Étienne Aucouturier, Daniel Becquemont, Alain Berthoz, Jean-François Braunstein, Éric Charmetant, Laurent Clauzade, Jean-Claude Dupont, Denis Forest, Charles Galperin, Jean Gayon, Élodie Giroux, Olivier Houdé, Philippe Huneman, Françoise Longy, Marie-Claude Lorne, Christophe Malaterre, Michel Morange, Matteo Mossio, Noemi Pizarroso, Arnaud Plagnol, Thomas Pradeu, Sabine Renous, Armand de Ricqlès, Maryse Siksou, Stéphane Schmitt, Stéphane Tirard. 9  This program was entitled “La notion de fonction dans les sciences humaines, biologiques et médicales.” 8

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Descartes, R. (1985). The philosophical writings of descartes vol. 1 (J. Cottingham, R. Stoothoff, & D. Murdoch, Trans.). Cambridge University Press. Hempel, C. G. (1959). The logic of functional analysis. In L. Gross (Ed.), Symposium on sociological theory (pp. 271–307). Row, Peterson and Company. Krohs, U., & Kroes, P. (2009). Functions in biological and artificial worlds: Comparative philosophical perspectives. MIT Press. Lorne, M.- C. (2005). Explications fonctionnelles et normativité: analyse de la théorie du rôle causal et des théories étiologiques de la fonction. Doctoral dissertation, EHESS. Nagel, E. (1961). The structure of science: Problems in the logic of scientific explanation. Routledge & Kegan Paul. Neander, K. (1991). The teleological notion of “function.” Australasian Journal of Philosophy, 69, 454–468. Proust, J. (1995). Fonction et causalité. Intellectica, 21, 81–113. Wright, L. (1973). Functions. Philosophical Review, 82, 139–168.

Contents

Part I Origins of Functional Discourse in the Life Sciences 1

 Biological Function: A Phylogeny of the Concept��������������������������������    3 James G. Lennox

2

 The Structure-Function Relationship in the Advent of Biology����������   19 François Duchesneau

3

Tissues, Properties, and Functions: The Term Function in French Biology in the Early Nineteenth Century ����������������������������   33 Laurent Clauzade

4

“Design,” History of the Word and the Concept: Natural Sciences, History, Theology, and Aesthetics����������������������������   45 Daniel Becquemont

5

Function and Purpose: Review of the “Written Symposium” (1976–1984) Organized by the Institut de la Méthode of the Ferdinand Gonseth Association ��������������������������������������������������   57 Pierre-Marie Pouget

Part II Function, Selection, Adaptation 6

How Are Traits Typed for the Purpose of Ascribing Functions to Them?������������������������������������������������������������   71 Karen Neander

7

 Attribution of Functions and Levels of Organization in Biology��������   85 Jean Gayon

8

Function and Adaptation: A Conceptual Demarcation, Instigated by Borderline Cases for Etiological Theory������������������������   95 Philippe Huneman

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9

 Function, Adaptation, and Design in Biology����������������������������������������  115 Gustavo Caponi

10 Do  Clay Crystals and Rocks Have Functions? Selected Effects Functions, the Service Criterion, and the Twofold Character of Function������������������������������������������������  135 Antoine C. Dussault Part III Structures and Functions in Morphology and Paleontology 11 The  Problem of Complex Causality at the Origin of the Structure-Function Relationship 1/Generality, 2/The Case of Bone Tissue����������������������������������������������������������������������  161 Armand de Ricqlès and Jorge Cubo 12 Structure,  Function and Evolution of the Middle Ear of Extant and Extinct Vertebrates: Paleobiological and Phylogenetic Interpretations��������������������������������  169 Michel Laurin Part IV Attributions of Function in Experimental Biology 13 The  History of Integration: From Spencer to Sherrington and Later������������������������������������������������������������������������  185 Jean-Claude Dupont 14 Assigning  Functions to Individual Macromolecules: A Complex History That Reflects the Transformations of Biology��������������������������������������������������������������������������������������������������  197 Michel Morange 15 F  unction, Functioning, Multifunctionality: Genetics of Development and Evolution������������������������������������������������  205 Charles Galperin 16 Does  the Immune System Have a Function? ����������������������������������������  221 Thomas Pradeu Part V Functions and the Origins of Life 17 Functions in Chemistry ��������������������������������������������������������������������������  233 Aurore Dupin 18 Heterotrophy  vs. Autotrophy: Carbon Metabolism in the Debate on the Origins of Life in the Middle of the Twentieth Century������������������������������������������������������������������������  257 Stéphane Tirard 19 What  Are Ribozymes for? Arguing for Function Pluralism����������������  265 Christophe Malaterre

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Part VI Functions in Psychology and Neuroscience 20 Functionalist  Psychologists from the School of Chicago and the Beginnings of Behaviorism��������������������������������������������������������  283 Françoise Parot 21 Face  Recognition and Functional Analysis��������������������������������������������  291 Denis Forest Part VII Function and Malfunction 22 Dys-,  Mal-, and Non-: The Other Side of Functionality ����������������������  303 Ulrich Krohs 23 Functional  Reasoning in Psychiatry������������������������������������������������������  313 Arnaud Plagnol Part VIII The Same Functional Reasoning in Engineering and Biology? 24 The  Idea of Function in Biology and Robotics as Reflected in the “RoboCoq” Project��������������������������������������������������  327 Anick Abourachid and Vincent Hugel 25 T  heories of Technical Functions: Sophisticated Combinations of Three Archetypes��������������������������������  335 Wybo Houkes and Pieter E. Vermaas 26 What  a Functional Explanation Explains: The Case of Bio-Artefacts ����������������������������������������������������������������������  351 Françoise Longy 27 Technical  Function, Use and Functioning in Simondon’s Ontogenetic Thought������������������������������������������������������  363 Jean-Hugues Barthélémy

Part I

Origins of Functional Discourse in the Life Sciences

Chapter 1

Biological Function: A Phylogeny of the Concept James G. Lennox

Abstract Concepts have histories, and tracing the historical origins and development of scientific and philosophical concepts can often be of value in understanding debates about their current meanings. In this chapter, I trace the history of the scientific concept of “function” back to its Classical Greek and Latin precursors and use that historical awareness as an aid to understanding the debate over Ruth Garrett Millikan’s concept of “proper function.” More positively, my goal is to answer the following questions: • • • •

What does happen to methodological concepts when background theories change? In what respects, and to what extent, does our understanding of them change? Do all changes in theory impact such concepts, or only certain changes? When the same term is involved across theoretical changes, how does one determine whether the term represents “different notions,” how does one determine how “closely related” they are and how should we capture that relationship? • When distinct terms are involved, how does one argue that different terms denote the same concept?

1.1 The Importance of a Concept’s History What is the value, for our current understanding of a theoretical concept—such as a concept that picks out a fundamental mode of explanation distinctive to a science— of a study of the phylogeny of that concept? How you answer that question depends, in part, on what you think concepts are. I am among those who think concepts must be understood as historical entities: they have origins, they persist through time, J. G. Lennox (*) Department of History and Philosophy of Science, University of Pittsburgh, Pittsburgh, PA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_1

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they develop, and they may go extinct or give rise to one or more other concepts. Their origin, persistence, and development may be discussed ontogenetically or phylogenetically; and while the question of the origin of many concepts used in everyday life may often be impossible to answer, the origin of a philosophical or scientific concept will often be clear, since they are often coined as part of the process of a new cognitive identification. As cognitive vehicles for uniting an unlimited number of similar things (and similar kinds of things), they facilitate, and are facilitated by, language and by our definitional and explanatory practices. Concepts and their definitions allow our limited cognitive capacities to organize and deal with the infinite variety and complexity we find in the world around us—they promote cognitive economy, reducing that variety and complexity to a manageable range. Take, for example, the concept “computer”: it ranges over a vast number of different objects with myriad similarities and differences, and allows us to treat them all as one cognitive unit. A good definition of “computer” will allow me to identify a wider group with which computers share broader similarities and from which they need to be differentiated. And ideally it does more—it makes reference to one, or a very small number, of differences that underwrite and ground many if not all of the others—it identifies, within the current limits of our knowledge, some essential difference or differences with an explanatory role to play.1 We learn constantly about the things our concepts unite together, and as we do we may well discover that a distinctive feature we took to be fundamental is in fact grounded in something more fundamental; or we may find that things that are similar at a superficial level of knowledge need to be clearly distinguished once we know more about them. It is not uncommon to discover, as biologists did with barnacles in the nineteenth century, that an entire class of things has been categorized, based on obvious similarities, with things that are fundamentally different. It is equally common for classes, once considered firmly differentiated, to turn out, on further investigation, to be fundamentally alike, as was the case with cephalopods, once considered a class coordinate with mollusks, now considered a sub-class of mollusks.2 What about concepts that play important methodological roles in the sciences, such as the concept “function,” which plays an important role in both the explanatory and classificatory practices of science? In her now classic “In Defense of Proper Functions,” Ruth Garrett Millikan claims to defend the idea that the concept of “proper function” “looks to the history of an item to determine its function rather than to the item’s present properties or dispositions” (Millikan, 1998[1989]: 296).3 She avoids certain challenges to this idea by arguing that she is not doing “conceptual analysis,” about which she has strong words, but rather offering a “theoretical  This understanding of concepts owes much to the theory developed in Rand 1990; in certain respects the notion of “essence” here is akin to that found in Paul Griffiths, 1996. 2  This theme and this example are discussed in greater detail in Lennox, 2012, 112–133. 3  For ease of reference, I give the page numbers to the reprints of Millikan, 1989 and Neander, 1991 in Allen et al., 1998. 1

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definition”: “according to my definition, whether a thing has a proper function depends on whether it has the right sort of history” (Millikan, 1998[1989]: 299). She is after “a unitary phenomenon that lies behind all the various sorts of cases in which we ascribe purposes or functions to things.” Proper functions explain what it is for something to have what are ordinarily called functions and to get behind the practice of grouping things conceptually by reference to function (Millikan, 1998 [1989]: 302–304). Despite a tendency in the literature to conflate them, she takes her position and that of Larry Wright to differ significantly. My position…is that although discovery of the sorts of mechanism and or dispositional structures that Wright and other theorists describe usually does license inference (inductive yet empirically certain inference) to a peculiar sort of explanation, this explanation is a straightforward historical explanation. Things just don’t turn up with inner mechanisms or with dispositions like that unless they have corresponding proper functions, that is, unless they have been preceded by a certain kind of history. (Millikan, 1998 [1989]: 307)

The slide here, from having a proper function to being preceded by a certain kind of history, strikes me as a bit quick. To make the case for decoupling “proper function” from “a certain kind of history,” I plan to outline a partial phylogeny of functional concepts in explanatory roles. Before turning to that task, however, I want to emphasize, and endorse, one aspect of Millikan’s position that often is missed in the give and take. She means by “proper function” the fully explicit recognition of the explanatory basis of our ordinary tendency to assign “functions” to things. What I aim to do is unravel two threads in that idea. I will argue that some very sophisticated natural philosophers from Aristotle through Cuvier had the notion of a “proper function” in the sense of a concept that identifies the function or goal of a structure or activity as explanatory of the existence of that structure or activity. Moreover, that historically connected group of natural philosophers distinguished this notion from the ordinary Greek, Latin, or French terms in everyday use to talk about what things are useful for. Where they differ from evolutionary thinkers is in denying that the phylogenetic history of the functional object “sets the norms” for making this distinction. However, in the Aristotelian tradition ontogenetic history, as it turns out, plays a parallel role!

1.2 The “Historical” Objection to Millikan “Proper Functions” As a transition to conceptual phylogeny, it is worth recalling that a standard objection to “Millikan proper functions” was, ironically, that her account ignored history! These historical objections nearly always invoke the name of William Harvey, and as far as I can tell, most of them were penned with very little attention to Harvey’s philosophical thought or its Aristotelian pedigree. The idea was that Harvey had correctly discovered the proper function of the heart—which we are told he thought

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was to pump or circulate blood—without having any ideas about selection histories. Ergo, having the appropriate selection history, cannot be part of what it means to be a proper function. This objection was summarily dismissed by Millikan and her supporters, but the grounds for dismissal are somewhat puzzling. Such criticisms are valid only if the project is an analysis of the concept of function. (Millikan, 1998 [1989]: 287) The [historical] objection depends on the idea that the etiological theory is a conceptual analysis of function—that it is a theory about what people mean by the word function. (Sterelny & Griffiths, 1999, 221)

Both these arguments are enthymemes so we will need to try and fill in the missing premises to see what they are objecting to. But since the idea is that this historical objection depends on a false assumption about philosophical method, it is safe to suppose there is an alternative method being implicitly advocated, in particular an alternative to conceptual analysis. What, then, is the full argument behind this summary dismissal? I suppose the objection is understood in the following ways: 1. If M. is doing conceptual analysis, then she is claiming that “being a historically selected effect” is part of the content or the meaning of the concept of “proper function.” 2. Before 1859 that could not have been part of the meaning of “function.” 3. Yet William Harvey was a competent user of the concept of function in the first half of the seventeenth century. 4. Therefore being a historically selected effect could not be part of the content or meaning of the concept. To which she, and her supporters, can apparently answer, “but I am not doing conceptual analysis.” Then what might she be doing? I suppose the thought is this: “I am trying to understand the concept of ‘function’ as it is embedded in the explanatory practices of post-Darwinian biologists.” If this is the nature of the response, it apparently sees the ‘historical’ objection as an aspect of the practice of conceptual analysis. It is thus surprising that the defender of conceptual analysis in this debate, Karen Neander, is equally dismissive about the historical objection: …how biologists understand the notion of a “proper function” might shift significantly with dramatic changes in these background theories. In other words, it is unproblematic if Harvey’s notion of a “proper function”, before the Darwinian Revolution, was different from the closely related notion used by biologists today, after the Darwinian Revolution. (Neander, 1998 [1991]: 322)

So understood, the argument for dismissal seems to be this: There was a concept of “proper function” in Harvey’s time, but given the commitments of a seventeenth-­ century English Aristotelian trained in Padua, it will have a meaning different from, though related to, that of post-Darwinian biology. Neander insists that she is doing conceptual analysis—but the concept being analyzed is that deployed by

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post-­ Darwinian biologists. For these purposes, she insists, such theoretically grounded shifts in meaning are “unproblematic.” She is talking about our concept and what is implied about meaning in our usage (“our” apparently does not include those millions of Americans who still reside blissfully in the pre-Darwinian era). The form of Neander’s dismissal raises, but does not answer, the questions I want to address here. • • • •

What does happen to methodological concepts when background theories change? In what respects, and to what extent, does our understanding of them change? Do all changes in theory impact such concepts, or only certain changes? When the same term is involved across theoretical changes, how does one determine whether the term represents “different notions,” how does one determine how “closely related” they are, and how should we capture that relationship? • When distinct terms are involved, how does one argue that different terms denote the same concept? • In such circumstances, is it possible to identify a single concept that remains stable across advances in theory? I will make a historical case for the claim that the terms most commonly translated from Greek or Latin into English as “function” (ἔργον, functio) are the conceptual ancestors to Larry Wright’s “function” or Ruth Millikan’s “proper function.” I will make the case that since Aristotle initiated the theoretical investigation of animals as part of natural science, there has been such a concept and one that has remained remarkable stable across major advances in that science. I will do this with a technique I refer to as phylogenetic tracing.4 Once one takes seriously the possibility that one can track a concept’s phylogenetic history, the above questions become central. And, just as Millikan thinks we can better understand various features of the deployment of the concept “proper function” by knowing the selection history of the functional entity, I want to claim that we can better understand the contemporary concept “function” by knowing more about its history in the evolving context of the theoretical investigation of living things. One more meta-historical point is worth stressing, before turning to history. There is a reason why philosophers of biology have published a small library of books and articles attempting to understand this concept. It is no ordinary scientific concept. It is, as Larry Wright pointed out, a word that smuggles in an explanation when it is deployed. When I learn the function of a flash drive, I don’t just learn what it does—I learn why there are flash drives. Moreover, the why question it answers is a rather special kind of why question: it is a teleological question, and its answer is a teleological explanation. That may not seem problematic when we are discussing flash drives, but when we are talking about organic structures and behaviors people see the specter of natural theology or vitalism and leap to the defense of

 See Lennox, 2001, 655–668.

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a “naturalistic” account of functions. I see the dissatisfaction of Millikan (and many others) with Larry Wright’s refusal to build past selection into the very meaning of etiological functions as such a leap. It is, in the end, the fact that the concept of function seems to play an almost identical role in the realm of artifacts and organisms that is one of its most enduring and problematic features. Moreover, when items are identified in functional terms, this also licenses special forms of classification and definition. Things that are radically different in structural architecture and mode of operation may well be classified and defined similarly if they exist in order to perform the same function. It is likely that considerations such as these, rather than assumptions about conceptual analysis, are what motivated the so-called “historical” objection to the “past selected effect” account of proper functions. That is, Charles Darwin represents, in some people’s eyes, a sea change in biological explanation. Prior to Darwin, there was no problem in seeing functional explanations as a form of teleological or “final cause” explanation. Organisms were the product of an allknowing, benevolent designer, and thus their adaptations were to be explained in precisely the same way as features of artifacts, by reference to the end for which that feature was designed. But after Darwin, or so it is commonly thought, such explanations are otiose. There is a natural mechanism, natural selection, which has as one of its consequences, the preferential perpetuation of adaptations, traits with proper functions, i.e., consequences that explain why populations have those traits. No pre-ordained ends, no conscious designer, purpose and design only in a weakly metaphorical sense. Functions are the result of a history of selection. The historical objection may, then, be both more problematic and also more telling than it at first appears. Its point may be that the pattern of explanation implied in function ascriptions looks to be the same, pre- and post-Darwin. Perhaps the nature of the underlying “because” is not what it is taken to be by the advocates of the “past selected effect” analysis—or perhaps the fact that the underlying “because” has changed is of less significance that we suppose.5 A little historical perspective on this debate will not hurt, and I think it may even help to give us a better understanding of the function of the concept “function” in the context of the theoretical investigation of anatomy and behavior.

 John Beatty (1990) and I (Lennox, 1992, 1993) have both written on the puzzlingly varied reactions among his contemporaries to Darwin’s continued use of the language of “ends” and “final causes” in his later writing, and of phrases in the Origin such as “natural selection considers only the good of each organism.” Darwin’s extremely positive reaction to Asa Gray’s praise of him for bringing teleology back into biology is interesting. (See Asa Gray, 1874, 79–81; and Darwin’s response, in Burkhardt et al., 2015, 278; cf. Lennox, 2010, 456–479.) Darwin’s response encourages me to think that the position I am inclined to would have met with his approval. 5

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1.3 A Branch of a Complex, Branching Phylogeny Since the name that was constantly invoked in using history to criticize the “past selected effect” analysis of function was that of William Harvey, I am going to look at two closely related classical traditions that shaped Harvey’s use of the concept of “proper function,” and due to space constraints, I will simply focus on the sources of those traditions, Aristotle and Galen. First a preliminary comment about concepts and vocabulary. Harvey wrote in Latin, at around the time the English word “function” first began to be used in the “proper function” sense (the third meaning given in the OED entry [“the special kind of activity proper to anything; the mode of action by which it fulfils its purpose”]). Below I will point out two things about this ubiquitously used historical counter-example: first, Harvey did not think that “pumping” or “circulating” blood was the proper function of the heart, though he certainly did think that the heart’s movements had the effect of sending blood out to the body through the arteries and that this was one of its activities (una actio); and second, the terms he would typically use for what we might call the proper function of an organ would be “final cause” (causa finalis), “use” (usu), or “utility” (utilitas). Harvey took it to be his most important, but also his most difficult, task as an Aristotelian natural philosopher to determine the use or final end of an anatomical structure. Early in his notes for his anatomy lectures at the Royal College of Physicians he states: Since the purpose of anatomy is to know or to recognize the parts and to know them through their causes for the sake of which and therefore for this reason [we must investigate] 1, action, 2, use…. (Harvey, 1619 6r)

Starting from Larry Wright’s insight that the crucial formal feature of all non-­ intentional teleological ascriptions, including function-ascriptions, “is the fact that when we say “A in order that B’ the relationship between A and B plays a role in bringing about A” (Wright, 1976, 21), I shall argue that the way to determine whether a theorist in the history of functional anatomy has a concept of ‘proper function’, is to investigate whether that theorist has grasped the idea of a special relationship between a structure and one of its consequences that accounts for that structure’s developing and persisting. We need to determine whether the theorist had the idea that there are one or more value-consequences for an organism of a given kind having a structure of a certain sort that explains why such organisms have that structure (trait, behavior).6 This is, I take it, what Millikan expresses by saying that such structures “don’t just turn up” with these functions; that is, they continuously and regularly turn up because they are the structures that perform these functions.

 The idea of a value-consequence is based on the idea of value-significance defended in Binswanger, 1991, 55–68. It is meant to build in a normative component to Wright’s view that is never made explicit. 6

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1.4 Aristotelian Proper Functions William Harvey was educated as a doctor at a time of a significant theoretical upheaval in the study of anatomy and the practice of dissection. As a scholarship student at Gonville and Caius (Cambridge) in the 1590s, he was in the first generation of “pre-meds” and would have been exposed to Aristotle’s logic and natural philosophy. But the crucial part of his education came when he was sent to Padua to earn his medical degree. In those years, 1598–1601, Galileo was teaching mathematics to the medical students, and Fabricius ab Aquapendente, as one of the most powerful and popular professors in Padua, was pushing forward with his agenda to elevate “philosophical anatomy” to a position of centrality in the natural philosophy curriculum. As part of this agenda, his students were encouraged to study Aristotle’s animal studies as much as Galen and Renaissance Galenic medical texts. The systematic challenge to Galen’s authority in medicine had begun decades before with Vesalius, of course—but Fabricius was challenging Galen on fundamental philosophical grounds and recommending a return to the Aristotelian idea that the study of animal parts and activities must be viewed as a universal and central part of the theoretical investigation of nature. It was natural philosophy; it was thus a science, not an art; and it was to range over all the animals that possessed the part or activity in focus. It therefore involved the comparative method as a crucial aspect of its inductive techniques. If you were studying respiration, your field of investigation was all breathers; if the heart, all animals with hearts. Anatomy was not ancillary to medicine; it was the part of natural philosophy to which medicine was subordinate.7 Educated in the midst of this revolution, Harvey became intimately familiar with all the available texts of Galen and Aristotle. He was much more likely, if his published work and lecture notes are any indication, to go back to the texts of the ancients than to those of their erstwhile scholastic followers. So what was he likely to find in Aristotle on this subject? At the level of theory, of course, a theory of explanation that identifies, in the case of most biology, four causal factors in a full explanation. Three of these—that for the sake of which, the form, and the source of development—are, Aristotle insists, in a way, reducible (Physics II. 7, 198a24–27). The fourth, matter, refers in the case of fully developed organisms to their anatomical structures; while in the case of development it refers to a uniform fluid that has the capacity to develop into those anatomical structures. The structures are, for the most part, there for the sake of their functions—and Aristotle’s most characteristic word for these is praxis, which he identifies as the telos of the structure, what it is for, and its form. Perhaps the most distinctive feature of his biological world-view, in fact, is that when it comes to organisms it is the full

 Looked at from a socio-cultural perspective, this also entailed first the elevation of the dissectors to chairs of anatomy; and eventually anatomists to chairs of natural philosophy. Thus this Aristotelian vision of dissection and anatomy entailed a more prestigious place in the University for its defenders. 7

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set of their functional capacities that he identifies with soul, while the bodily structure of an animal is identified with its matter—indeed, those structures tend to be defined and identified by reference to their functional capacities. (All translations of Aristotle are my own.) Since…each of the parts of the body is for the sake of…a certain activity (praxis), it is apparent that the entire body too has been constituted for the sake of a certain complete activity. For sawing is not for the sake of the saw, but the saw for sawing; for sawing is a certain use (chrêsis). So the body too is in a way for the sake of the soul, and the parts for the sake of the functions (erga) in relation to which each of them has naturally developed. (De partibus animalium [PA] I. 5, 645b15–20)

Moreover, in the case of sexual reproduction what causes the unstructured fluid in the female to develop epigenetically into an organism with those functional capacities is the nutritive capacity of the male parent. During intercourse that capacity is transferred to the appropriately prepared fluid in the female. As Aristotle puts it in De Anima II. 4, “the nutritional and generative capacity are one and the same”(416a19–20). That is the explanatory theory; how about his practice? The obvious place to turn in the case of Aristotle is PA III. 4, which concludes, “regarding the heart, then, what sort of thing it is, what it for the sake of, and the cause owing to which it is present in those animals that have it, enough said.” Book I of PA is a philosophical introduction to the study of animals, discussing causality, explanation, necessity, definition, division—generally speaking, the proper concepts and methods to be used in zoological inquiry. Books II–IV provide systematic explanations of animal structures. Book II begins with a discussion of how uniform parts (tissues and fluids) are related to non-uniform parts (organs), followed by a systematic part by part study of the uniform parts, beginning with blood, which on Aristotle’s view is the primary nutrient for all the others. Ignoring some subtle but important sub-divisions, from Chap. 10 of Book II through the end of Book IV, we find a systematic study of the non-­ uniform parts (organs) in blooded and then bloodless animals. PA III. 3 begins a discussion of the internal organs of blooded animals, with Chap. 4 devoted to the heart. Early on in Book II, in discussing blood, Aristotle announces that the perceptive, motive, and nutritive capacities or potentials are found, in all blooded animals, in the heart (647a24–31). In III. 4 he tells us that the heart is “the origin and spring of blood,” “the origin of perception and the awareness of pleasure and pain,” and the “primary receptacle for blood.” More than once in De Partibus, he reminds us that perception is the defining feature of animals, that which fundamentally differentiates them from plants, and here he adds that the heart is “the primary perceptive part.” Perhaps I can sum up Aristotle’s views with a quotation from On Youth and Aging in which he reviews his account of the heart and blooded in blooded animals: Now it is apparent that the mouth has the capacity to perform one nutritive activity and the stomach another; but the heart is most authoritative and contributes the end (to telos). So it is also necessary that the origin of the perceptive and nutritive soul in blooded animals be in the heart; for the functions (ta erga) of other nutritive parts are for the sake of its function. For the authoritative [organ] should accomplish ‘that for the sake of which’ (as a doctor

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J. G. Lennox does relative to health) rather than those things that exist for its sake. And likewise the authoritative [organ] among the senses in each of the blooded animals is the heart; for in this must be the sense receptor common to all the sense receptors. [469a2–13]

The crucial distinction is that between the organ that directly contributes “that for the sake of which” and those others that subserve the same function but only by being for the sake of the heart’s functions. What the heart is for, the reason why it comes to be and exists—its proper functions, as we might say—are perception, nutrition and (though I won’t have time to expound on this) locomotion. It is also the seat of the passions in Aristotle’s view. Hearts don’t just show up able to do these things—that hearts have the capacity to do these things is the reason why hearts come to be and exist—and in fact, for Aristotle, those activities define what it is to be a heart. That for the sake of which, as Aristotle argues in this great work’s first chapter, is the primary cause, and accounts for the regular, natural occurrence of an otherwise highly unlikely coordination of materials and movements needed to make a heart in animal development. For once the doctor has defined health, and the builder has defined house, either by thought or perception, they provide the accounts and the causes of each of the things they produce, and the reason why it must be produced in this way. Yet that for the sake of which and the good are present more in the works of nature than in those of art. (PA I. 1, 639b16–21)

In sum, then, for Aristotle, the distinctive anatomical structures that make up the body of a particular kind of organism come to be and are for the sake of performing the functions that constitute the life of that organism. Those life-sustaining functions account for the developmental process that produces a body with the appropriate functional capacities.

1.5 Galenic Proper Functions Galen lived roughly five centuries after Aristotle, during which significant advances had been made, especially by anatomists in Alexandria, in the use of the techniques of experimental vivisection to test physiological hypotheses, though all within a narrowly medical context. Galen was born in Pergamum, also a center of medical research, in what is now Turkey, and he studied there as well as in Athens and Alexandria. Though we have lost much of it, his written output was vast, ranging from highly abstract discussions of logic and method, through theoretical treatises on anatomy and physiology, through to detailed discussions of therapeutics, diagnosis, and treatment. He differs systematically from Aristotle on what it is the heart does that accounts for its presence in blooded animals, and while he shares with Aristotle a fundamentally teleological perspective on biological structures and behaviors, it is a very different sort of teleology, one that owes as much to Plato and the Stoics as it does to Aristotle. He is much more inclined to see intelligence lying behind biological design than Aristotle, who was inclined to see the teleology of

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artifacts as a poor imitation of what one finds in nature. While Aristotle treats the statement “Nature does nothing in vain but always does what is best among the possibilities for the kind of animals in question” as essentially a biological axiom, Galen regularly substitutes God or the Demiurge for “Nature” and thus likely sees the natural world as permeated by intelligent design, a view congenial to the medicine of the medieval and early renaissance period. What about the heart? Galen differentiates three fundamentally different categories of functional capacities associated with living things—there are “natural” capacities, “vital” capacities, and “psychic” capacities. So, while Aristotle has a concept of “soul” that encompasses nutrition and reproduction of any kind—and thus is comfortable saying that plants have the simplest kind of soul—Galen will say that plants have certain of the natural capacities but lack the “vital” and “psychic.” In animals he associates the three faculties with three “authoritative” organs— the liver with the natural capacities of generation, growth and nutrition; the heart with the “vital” capacity of maintaining and distributing warm, vital pneuma throughout the body, via the arterial system; and the brain with the psychic functions. Thus unlike Aristotle he did not see the heart as having a primary role either in perception or in nutrition. But they agree that the heart is a heat-generating organ and that the respiratory structures are there to subserve the heart and its functions by moderating its heat: It remains, then, that we breathe in order that there is a regulation of heat. This, then, is the principle use (megiste chreia) of breathing, and the second is to nourish the psychic pneuma. And the first [use] is brought about by both parts of breathing, both inhaling and exhaling; to the one belongs cooling and fanning, to the other evacuation of the smoky vapor… (Furley & Wilkie, 1984, pp. 132–33)

Likewise with the pulse: The following things have been stated and proven: [1] That the pulse is for the sake of the natural heat that is all over the entire animal, that it cools this during the expansions and purges it in the contractions, and that these motions are in every way like those of breathing; [2] that they are useful to the psychic pneuma; [3] that breathing and the pulse differ in only one way, in that the one is moved by the psychic power and the other by the vital power, though they are like in all other ways, both in the use for the sake of which and in their manner of motion. (Furley & Wilkie, pp. 226–227)

In Galen, then, the term that refers to an organ’s proper function is “use” (chreia), and in the sixteenth century anatomists, regardless of their classical allegiances, there are standardized distinctions between the concepts of “use,” “activity,” and “movement,” in descending order of teleological involvement. To discover what an organ’s use was, was to discover its final cause, what it is present for, what fundamental value it contributes to the organism’s life. There will often be an associated activity—say, breathing, in the case of lungs—which will often have the same use as the organ whose activity it is. And that activity will often involve a number of coordinated movements—say, the inhaling and exhaling involved in breathing. Note too, as this example was chosen to display, that two distinct activities of two distinct parts, such as breathing and pulse, may be for the same use. Galen had systematized these distinctions and Renaissance anatomists of all stripes found them very useful.

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1.6 Harverian Proper Functions Aristotle’s notion of an organ’s praxis (activity) or ergon (function, work) and Galen’s concept of chreia (use),8 which becomes “usus” in Latin translations of Galen, serve as the philosophical backdrop to Harvey’s careful distinction of action from use, and within the latter between mediate and final ends. Harvey admired the essentially Galenic treatises of André du Laurens (Historia anatomica humani corporis [1600]) and of Caspar Bauhin (Theatrum anatomicum [1605]) for their philosophical clarity and clear anatomical distinctions, and he absorbed the technical language associated with the neo-Galenists even as he rejected their narrowly medical outlook and their views about the heart and its proper functions. It is these concepts of praxis and usus that share with Millikan’s account of proper function the idea that “things like that just don’t turn up unless they have corresponding proper functions.” These thinkers, no less than Darwin or Millikan, aim to provide an underlying causal theory in which a particular feature (part, behavior, trait) is the basis of a benefit to the agent and is present for that reason. It is a primary feature of the nature of the organs, tissues, and behaviors of organisms that they come to be and exist for the sake of contributing to the life of their possessors. The “because” in their cases is underwritten by the idea that coming to be is for the sake of being and being in this case is living. Blooded animals have hearts for the sake of maintaining the proper balance of heat in the organism or for the distribution of nourishment—that is what hearts are for, that is their function, and that is why hearts regularly come to be part of a blooded animal’s anatomy and why hearts move as they do. What is most interesting about William Harvey in this respect is that he says very little new about the proper function of the heart, despite what the philosophical literature on proper functions claims. In De Motu Cordis et Sanguinis in Animalibus, Harvey feels he has demonstrated that the heart, by way of its complex movements, transfers the venous blood, which has traveled to the heart via the venous system, to the arterial system, by way of anastomoses in the lungs. Moreover, he thinks he has also demonstrated, by way of a thought experiment in which he invites his readers to estimate the volume per unit time of that transfer, that the blood that goes out to the body by way of the arterial system must somehow be transferred to the venous system at the extremities (and who knows if exposure to Galileo helped him to use thought experiment to calculate the volumetric implications from his experiments in this manner). But he does not think the heart is present for the sake of this merely mechanical movement. He is careful to say nothing about the possible purposes of

 It should be noticed, however, that Galen is simply “normalizing” language already present in Aristotle—see, for example, the fluid use of praxis, ergon, and chrêsis in the quotation from PA I. 5 on p. 11, above. 8

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circulation or the movements of the heart that produce it until the highly speculative9 17th chapter of De Motu, where he reveals his Aristotelian (and Royalist) colors: …the heart is the first part to exist and…was the seat of blood, life, sensation and movement before either the brain or the liver had been created, or had appeared clearly, or at least had been able to perform any function. With its special organs designed for movement the heart, like some inner animal, was in place earlier. Then, with the heart created first, Nature wished the animal as a whole to be created, nourished, preserved and perfected by that organ, to be in effect its [i.e. Nature’s] work and its dwelling-place. Just as the king has the first and highest authority in the state, so the heart governs the whole body. It is, one might say, the source and root from which in the animals all power derives, and on which all power depends. (Harvey, 1963 [1628], 108)

Notice that it is the place of the heart in epigenesis that Harvey think’s provides evidence as to its proper function. It is thus no surprise that his considered views on the final end of the heart become clearer in the much later De Generatione Animalium. He strongly disagrees with Aristotle that the heart precedes the blood and fashions it. In Harvey’s view the blood is present from the outset of generation and the heart is formed to subserve it. Blood appears to be ensouled from the outset, and that pulsing spot that Aristotle thought was the heart in the three-day old chick embryo is, Harvey argues, a point of blood, which has its own activity from the beginning, due to its own innate heat. In one sense the heart is there for the sake of circulating the blood, but only because it is there to insure that the heat of the innate pneuma, which is the material of which soul is the form, is distributed to all parts of the body. The circulation of the blood subserves this final end. Properly speaking, that is what the heart and its movements are for (Harvey, 1981 [1651], 247–58).

1.7 Aristotelians, Darwinians, and Proper Functions There are so many differences between the scientific worldview that finds expression in the traditions leading up to Harvey and that expressed in On the Origin of Species that it may seem odd to compare what they have to say about the biological investigation of proper function. And yet perhaps that is our anachronistic reading of Darwin at work, rather than an anachronistic reading of his predecessors. For a number of people whom Darwin considered to be members of his own culture of philosophical naturalists—Cuvier and Owen, for example—read Aristotle’s biology not for historical purposes but for philosophical guidance. And even in the 1870s, in his account of sexual dimorphism in a species of plant, Darwin was capable of

 He refers forward to this discussion in chapter 8 of De motu, when he is introducing the new idea that blood makes a circuit around the body, returning to the heart via the venous system. In that forward reference, he says he will later “speculate about the final cause” of this circuit. The wording is telling, since he thinks he has demonstrated the movement of the heart and the circuit of the blood, but can offer only speculation about why there is a circuit and thus why the heart is engaged in moving the blood in a circuit. 9

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expressing himself in the Proceedings of the Linnaean Society in ways that sound remarkably like Harvey: The meaning and use of the existence in Primula of the two forms in about equal numbers, with their pollen adapted for reciprocal union, is tolerably plain; namely, to favour the intercrossing of distinct individuals. With plants there are innumerable contrivances for this end; and no one will understand the final cause of the structure of many flowers without attending to this point. (in Barrett, 1977/2: 59)

Since most people assume that the “selected effects” account of function is a philosopher’s take on what Darwin was up to, I will close with a brief comment on Darwin’s adaptation explanations. In a previous paper (Lennox, 1993), I explored Darwin’s actually teleological explanations in his post-Origin botanical works. Without going into details, the schema that I was able to abstract from typical explanations in those works was [V = variation, P = population, E = effect] V is present in P. V has effect E. E is advantageous to members of P. Therefore V would be selectively favored in P. Therefore E is the cause of V in P. Darwin occasionally identifies the advantage or “good” provided to the organism by a variation as its “final cause” (he uses that expression, as in the above quotation, a number of times in these works), and more often as its “end” or “purpose.” It is this that underwrites the hypothesis that the variation would be selected. Moreover, Darwin is sensitive to the dangers of making too tight a connection between past selection and present functional advantage. In his study of adaptations in Orchids, Darwin writes: Although an organ may not have been originally formed for some special purpose, if it now serves for this end, we are justified in saying that it is specially adapted for it. (Darwin, 1984, 283)

Advantageous effects turn out to be more fundamental to these explanations than selection, because selection depends for its operation on variations in the value consequences of traits—or, to use Robert Brandon’s language, variations in “adaptive significance.” For Brandon, to postulate some feature as an adaptation is the first step in research aimed “to discover its ‘adaptive significance’…what it is selected for.”10 I believe Darwin saw the continuity between his explanatory project and those of his predecessors as clearly as he saw the differences.

 See Brandon, 1981, note 22, where he says this term is equivalent to ‘function, which he eschews “to avoid polemics.” If he used it, he says, he would do so “in a manner roughly following Wright, 1976.” See too Binswanger, 1991, ch. 5. 10

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1.8 Conclusion Both Millikan and Brandon refer to their accounts as theoretically “loaded”: as Brandon puts it, his is “deeply committed to a certain view of evolutionary theory….” Like Millikan, he too differentiates himself from Wright because, as he puts it, he “can’t see the interest in an account indifferent between divine creation and Darwinian evolution.” Though a committed Darwinian, I can see the interest, and importance, of such an account. Nor is the interest merely historical. Wright’s account is sensitive to the historical origins of the concept of “function,” and the phylogenetic baggage carried by the concept, independent of its most recent “cognitive adaptations.” What I have aimed for is an intermediate level of abstraction that allows us to see the deep, shared commitments between the sort of account of proper function (or, as Aristotle, Harvey—and Darwin—would say, “use” or “final end”) that we find in Harvey’s Aristotelian tradition (that we still find in Cuvier, I believe) and that which we find in selection explanations of the sort we have inherited from Darwin. This in turn explains why, despite deep differences in philosophical foundations, there is the appearance of a shared project of inquiry governed by a shared explanatory structure.

References Barrett, P. (1977). The collected papers of Charles Darwin (2 volumes). University of Chicago Press. Beatty, J. (1990). Teleology and the relationship between biology and the physical sciences in the nineteenth and twentieth centuries. In A. Durham & R. Purrington (Eds.), Some truer method: Reflections on the heritage of Newton. Columbia University Press. Binswanger, H. (1991). The biological basis of teleological concepts. The Ayn Rand Institute Press. Brandon, R. (1981). Biological teleology: Questions and explanations. Studies in History and Philosophy of Science, 12, 91–105. Burkhardt, F., et al. (Eds.). (2015). The correspondence of Charles Darwin (Vol. 22). Cambridge University Press. Darwin, C. (1984 [1862; 2nd ed. 1877]). The various contrivances by which Orchids are fertilized by insects. Second edition, revised; with a new foreword by Michael Ghiselin. University of Chicago Press. Furley, D., & Wilkie, J. (1984). Galen on the pulse and respiration. Princeton University Press. Gray, A. (1874). Scientific Worthies III. Charles Robert Darwin. Nature, 10(June 4), 79–81. Griffiths, P. (1996). What emotions really are. University of Chicago Press. Harvey, W. (1963 [1628]). On the movement of the heart and blood in animals. William Dent and Sons. Harvey, W. (1981 [1651]). Investigations of the generation of animals. Wiley Science Publications. Lennox, J. (1992). Teleology. In E. Lloyd & E. F. Keller (Eds.), Keywords in evolutionary biology. Harvard University Press. Lennox, J. (1993). Aristotle was a teleologist. Biology and Philosophy, 8(4), 409–421. Lennox, James (2001, October–December). History and philosophy of science: A phylogenetic approach. História, Ciências, Saúde, VIII(3), 655–668. Lennox, J. (2010, Winter). The Darwin/Gray correspondence 1857–1869: An intelligent discussion about chance and design. Perspectives on Science, 18(4), 456–479.

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Lennox, J. (2012). Ayn Rand on concepts, context and scientific progress. In A.  Gotthelf & J.  G. Lennox (Eds.), Concepts and their role in knowledge: Reflections on objectivist epistemology. Pittsburgh University Press. Millikan, R.  G. (1989). A defense of proper functions. In C.  Allen, M.  Bekoff, & G.  Lauder (Eds.), Natures purposes: Analyses of function and design in biology (Vol. 1998, pp. 295–312). MIT Press. Neander, K. (1991). Functions as selected effects: The conceptual analyst’s defense. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Natures purposes: Analyses of function and design in biology (Vol. 1998, pp. 313–334). MIT Press. Rand, A. (1990). Introduction to objectivist epistemology. Meridian Press. Sterelny, K., & Griffiths, P. (1999). Sex and death: An introduction to the philosophy of biology. University of Chicago Press. Wright, L. (1976). Teleological explanation. University of California Press.

Chapter 2

The Structure-Function Relationship in the Advent of Biology François Duchesneau

Abstract  In the constitution of biology, organized and inorganic bodies could not differ only in composition and structural ordering. Organized bodies would depend on “a creative power subject to laws of organic planning, of harmony […], and this is what makes the organism distinctive” (Müller JP, Manuel de physiologie. J.-B. Baillière, 1851: I, 16). This distinctive nature would involve an “economy” of vegetal and animal functions, even if explanations tended to be limited to analyzing physicochemical processes underpinning functions. With the advent of cell theory, “the complex phenomena of life [were] considered by physiology as boiling down to the combined activity of innumerable cells, subordinated and associated so as to form higher-order vital units” (Hertwig O, Éléments d’anatomie et de physiologie générale. C. Naud, 1903 [1898]). This analytic reductionism occasioned an apparent marginalization of explanations bearing on the functional raison d’être of organic systems. However, even in highly reductionist contexts, such as investigations of protoplasmic formations (for instance, by Brücke and Verworn) or developmental mechanics (for instance, by His, Roux, or Chabry), there subsisted a latent appeal to analogies with global functions for interpreting the more elementary phenomena. Wilson (The cell in development and heredity (3rd ed.). Macmillan, 1925 [1896]) would thus state: “every animal represents a sum of vital units each bearing in itself the complete features of life.” Why, in that historical phase of biology, did the analysis of elementary physiological mechanisms require such a functional principle?

F. Duchesneau (*) Département de philosophie, Université de Montréal, Montreal, Canada e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_2

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2.1 Introduction In the advent of biology as a science, the distinction between organized and inorganic bodies played an essential role. It was directly based on a difference in relation between structure and function, depending on whether one dealt with organisms or not. My aim is to show how the structure-function relation was presented in some representative expositions of physiology in the nineteenth century and to examine the role assumed by the cell theory in the transformations that discipline then underwent. The philosophical issue raised is about the forms of causality admitted within the framework of general physiology and the appeal to functions for providing explanations for physiological phenomena. In the context of a scientific approach that was intended to be experimental and analytic, as it was purported to be the case in general physiology, this question related to the methodological and theoretical options that underlay practices and modalities of investigation.

2.2 Functions and Physiological Properties The first mode of functional explanation we shall look at relates to the invention of “physiological properties.” The prototype of this mode was provided by Albrecht von Haller in the mid-eighteenth century (Steinke, 2005; Duchesneau, 2012a). The model for organisms that Haller had inherited from his teacher Herman Boerhaave implied small juxtaposed or boxed-in machines combining to form the complex organic being. It followed therefrom that the latter’s operations could in principle be mechanically explained from the structural dispositions thus achieved, to which laws similar to those of inorganic nature would apply. Haller conceived of physiology as “animated anatomy” (anatome animata) (Haller, 1754: v): prima facie this characterization seemed to drive us back to the model of the organism as a “machine of nature.” But in fact Haller conceived of physiology as a science of vital motions in their proper reality. The equation between integrative organic structures and the functions that they would yield appeared to him so complex to unravel that he proposed to identify, strictly by observation and experimentation, the dynamic properties (forces) and the functional constants (processes) specific to the various structural elements that are combined to form organs and systems. Yet his method of observation and experimentation would authorize hypotheses inferred from the empirical data and subject to experimental control: these hypotheses would be based on analogies transferred from one domain within the field of experience to the next. Thus, one could develop indefinitely perfectible physiological theories. Among the key hypotheses of physiology, Haller included that of the fiber makeup of organic bodies: “The fibre is for the physiologist what the line is for the geometer, namely, that from which all figures arise” (Haller, 1757–1766: I, 2). This element of vital organization enters the composition of the various organic structures; it gets diversified according to the dynamic properties it yields, and these in turn determine functional processes at higher levels. Haller would not reduce the functional properties of elementary fibers to the sole physicochemical properties of their material

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parts. Based on the analysis of organic structures and the processes they elicit, he would rather suppose that those units of vital organization own specific properties that may account for more global functional operations, in the same way that the properties of a unit of geometrical figure by combining with those of other units of figure may thus account for complex integrative structures. In the organic body, it is to the fiber unit that one may link the reason for the relationship between complex organic functions and the tiniest inner structures. For Haller, the levels of integration in organic bodies did not strictly correspond anymore to the mechanical order ensuing from the combination of small juxtaposed and boxed-in machines: in light of the microfiber arrangements and their specific functional properties, the physiologist had to determine how membranes resulting from those arrangements are combined to yield the functional motions that can be attributed to organs and organic systems. Haller undertook a series of experiments at the University of Göttingen from 1746 on, which resulted in the memoirs De partibus corporis humani sensilibus et irritabilibus in 1752. He aimed at setting up a system of vital motions with relation to types of fibers as elementary organic structures, endowed with specific dynamic dispositions. Irritable fibers are those which contract by spontaneous motions that cannot be reduced to mere elastic contractility, when they are physically stimulated. Sensible fibers are those which, when stimulated, convey the impression of this stimulation to the central organs of sensibility where it produces effects that yield signs of pain and uneasiness. Haller experimented systematically on those functional properties of elementary structures in order to set a typology of parts respectively endowed with such distinct dispositions on diverse scales of intensity. While collecting data on the types of fibers and the functional processes they display, and notwithstanding his averred methodological skepticism, he undertook to determine the theoretical import of his analyses on irritability and sensibility as vital properties. The notion of fiber irritability was thus made to signify the differential nature of the structures of organic life, starting with the cardiac muscles, while the organs of so-called animal life were connected with a capacity of stimulation embedded in the network of nerve fibers. And so Haller was able to state a law of structure-­ function correlation: “Sensibility is similarly proportional to the number of nerves and their nakedness, while irritability is generally proportional to the number of fibres exposed to the cause of irritation” (Haller, 1756–1760: IV, 92). However, this twofold law depended not only on the data collected from experience but also on the functional distinction between the agent of sensibility, responsible for exciting the nervous fiber network, and the more decentralized agents of the other vital motions, intervening separately within fibers of the muscular type. As a result, Haller opened the way to distinguishing the various forces operating within the organic body and questioning the relation of those forces as properties to the typology of elementary structures forming the organic makeup. Haller broke de facto the hegemony of a unitary system based on similar mechanical processes working uniformly among the various parts, as with Boerhaave and Friedrich Hoffmann (Duchesneau, 2012a), or on the regulation of the organic machine by a single soul, as with Georg Ernst Stahl (Duchesneau & Smith, 2016). If Haller adopted a decentralized conception of organic functions based on the physiological properties of elementary parts, he was nevertheless embarrassed in

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fixing the theoretical status of these functional properties. Indeed, he would identify them by applying an analogy with Newton’s force of attraction and tracing out the observable effects that manifest their presence and specificity. But, while he presented them as inherent forces (vires insitae) within those elementary living units that fibers form, he would leave at bay their status as vital forces, under cover of an unverifiable potential reduction to inner dispositions of some kind of organic mechanism: “A motion cannot be in the human body, except if there are sufficient causes of it in the structure of the part, and the effect could not be deduced without the cause” (Haller, 1756–1760: I, 297). Wouldn’t it be possible that the phenomena that irritability and sensibility signify are the outcome of special, though unreachable, mechanical arrangements in the units of organic combination? On the one hand, Haller argued for irreducible functional properties of the living considered as so many vital powers inherent in their elementary structures; he would, on the other hand, presume that the derivation of these properties from their causes might yield a “special mechanical hypothesis.” Faced with this theoretical dilemma, Haller shrank from siding with either of the two options that one can retrospectively link with the antinomy between mechanism and vitalism in the explanation of vital phenomena.

2.3 Functions and Correlations Between Elementary Vital Properties With the advent of biology, at the beginning of the nineteenth century, various perspectives seem to have combined so as to cause a change of style in functional explanation. These perspectives yielded new guideline principles for physiology: the notion of a general mode of development for living forms subject to epigenesis, the setting up of evolutionary schemes, and a generalization of comparative approaches across taxonomic series but, foremost, a will to account for the more complex forms by considering the more elementary ones as prototypical and comprising at once all sorts of potential variations and complexifications. The scheme of functional explanation was accordingly affected, as witnessed in the Cours de physiologie générale et comparée of Henri-Marie Ducrotay de Blainville (Blainville, 1833; Duchesneau, 2016). Concerning the functions of organisms, Blainville proposed as the sole methodological principle to combine all notions pertaining to the elements organic bodies are composed of. The idea was to substitute for tautological notions of global function notions that relate to the “intimate composition of organs” and the chemical combinations that result from this composition. Focusing on nutrition, absorption, exhalation, and respiration, the physiologist should first study “the modifications that the matter composing organic bodies undergoes, either in its chemical combinations, or in its texture or organic disposition” (Blainville, 1833: I, 104–105). The study of the functions or “dynamic phenomena” that may be attributed to systems cannot be directly made clear by the description of organs; one must first of all undertake to analyze the properties and molecular composition of tissues. But this

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analysis must be comparative, implying observations made on the living as well as the dead, on normal as well as pathological states, and on the successive developmental phases of organisms, and hypotheses drawing on comparisons with relevant data across taxonomic series. On such a basic study of organic elements and their properties – in this case those identified with tissues according to Bichat’s Anatomie générale (1801)  – one could hope to build explanations of functions: the latter would short-circuit in a way the appealing to sufficient reasons that would boil down to the very functions that are to be explained, which might be viewed as constituting an equivocation of explanans and explanandum. Blainville provided the following explanation: By following the road I have traced out, by thus resting on numerous observations diversely made, by not forgetting to take into account influences that many circumstances may exert on the obtained results, one will be able to collect, on the modifications that matter undergoes in the intimate composition of living bodies, notions exact enough to hope to deduce from these the explanation of the dynamic phenomena of those very bodies. (Blainville, 1833: I, 115–116)

According to this strategy, a very important role is imparted to an account of primordial organic forms that would represent, such stages as preceded the emergence of specialized organs. The elementary properties that show up then appear to be more “essential” than structures resulting from ulterior advances of the animal kind. Animals considered at the inferior levels of taxonomic series, instead of displaying duly formed muscular and/or nervous tissues, reveal rather “the general element of all organization,” from which organs endowed with “special characters” arise in more complex organisms (Blainville, 1833: I, 114–115). These emerge when they are required because of the more numerous and diversified relations the organism entertains with the external milieu – this seems to evoke a Lamarckian principle that would justify the development of adaptive functional dispositions. Similarly, a principle is annexed that was probably inspired by Karl Ernst von Baer’s biogenetic law according to which one would assist to a growing differentiation of ontogenetic phases as one goes up levels in the animal series (Duchesneau, 1987, 121). To grasp the full meaning of the program sketched by Blainville and resumed, following Auguste Comte, by physiologists of the positivist school, it may be useful to turn to the reference made by Émile Littré to Charles Robin’s Tableaux d’anatomie of 1851. Special physiology is held to deal with organs, systems, and the whole body: Organs have a specific use, unique or multiple, which has to be determined, the fact being that a single organ or instrument may serve for accomplishing one or several functions. Systems (appareils) respond to the idea of functions, a notion that is naturally adjusted according to this correspondence […] Finally, the body presents, as a dynamic attribute, the idea of more or less varied special actions in connection with vegetative, animal and social life. (Littré in Müller, 1851: I, x–xi)

By contrast, general physiology is concerned with elements, tissues, humors, and systems: these are the ultimate organic parts resulting from anatomical decomposition and from the combinations that the elements form in more and more complex arrangements. This theory, in Robin’s version, ignored cell organization as the primordial disposition of all organic formations for the benefit of an extension of tissue histology toward structural components at the microscopic level. The specific object

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of general physiology consists in the properties of elements. To elements is linked “the idea of life, that is, of a twofold continuous motion of composition and decomposition, hence growth, reproduction, decrease and end [death]” (Littré in Müller, 1851: I, ix). According to this scheme, elements display vital properties: these boil down to nutrition as assimilation-excretion; to reproduction, which implies segmentation, division, and a capacity to form similar elements; and to contractility and sensibility as fundamental animal properties, underpinning the specifically vital acts. The vital properties of elements can be empirically described as capable of displaying various modes depending on the latter’s integration into more complex organic combinations. And this is the case with processes that take place in tissues and systems: these processes are modified by the tissue properties which mostly depend on complex arrangements of molecules, whence particular conditions of extendibility, contractibility, elasticity, and osmotic exchange. The combination of the vital properties of elements with the conditions bred by the structural dispositions account for processes of nutrition, absorption, and secretion that tended to be identified with functions implemented by systems, at a much higher level of complexity. One could from then on avoid evoking functions as explanatory causes of more elementary processes, as if the organic structuring of systems and the whole organism determined a priori the harmony of organic parts and operations, “the term function being parallel to the term system (appareil) in anatomy” (Littré in Müller, 1851: I, 20 note). Secretion, for instance, previously a function, is reduced to a mode of nutrition in connection with tissue properties, and the same for absorption. As for nutrition or reproduction, these are fundamental properties that may be reduced to the dynamic features of elements: the operations of the systems involved represent only derivative modes of accomplishment. Similar arguments could be developed for setting the relationship between the systems of animal life and the properties of contractility and sensibility that elements are endowed with.

2.4 Functions and Cell Theory From the very time it was invented by Matthias Schleiden and Theodor Schwann in 1838–1839, the cell theory would influence the framing up of functional analyses. The demonstration Schwann had undertaken was aimed at establishing that all organic structures in animals, following the botanical analogies Schleiden had suggested, were cells or arose from transformed cells and that the formation and metamorphosis of cells could account for all organic functions, including those at a higher level. Schwann’s mistaken conception that cells are formed and reproduced by a “cytoblastemic” crystallization (that is, in and from a specific organic fluid) was in line with a reductionist approach that went beyond the idea that cells would form the elementary parts of organisms and that all organic structures would derive therefrom by analyzable metamorphoses, for it implied that cells were the true archetypes of organisms and that organisms in their unfolded complexity could be

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analyzed into interactions between cells, from both a physiological viewpoint, that of formative and metabolic processes, and a morphological one. This new mode of explanation is thus characterized as follows: […] Growth does not ensue from a power resident in the entire organism, but […] each separate elementary part is possessed of an independent power, an independent life, so to speak; in other words, the molecules in each separate elementary part are so combined as to set free a power by which it is capable of attracting new molecules, and so increasing, and the whole organism subsists only by means of the reciprocal action of the single elementary parts. So that here the single elementary parts only exert an active influence in nutrition, and totality of the organism may indeed be a condition, but is not in this view a cause. (Schwann, 1847: 191)

The “theory of cells” (Theorie der Zellen), at once a speculative hypothesis and a heuristic model, sets cell histology on the way to resume and address the physiological query par excellence: what is the functional integration of organisms based on? The new approach purports to reinforce the prerogative of analyses focusing on the morphological and metabolic properties of cells. Correlatively, these analyses should from now on set themselves free of any idea of causal implication involving the functional integration of the entire organisms. Concerning plastic, that is, morphogenetic phenomena, Schwann reinterprets the formation sequence, nucleolus → nucleus → membrane, as stages of stratified sedimentation worked out by a power of attraction. Exerting itself first in the nucleolus, which one might imagine as resulting from a sort of crystallization out of a concentrated cytoblastemic fluid, this power would produce the aggregation of specific molecules into successive layers; the differential expansions of those layers would generate the separation between cell membranes and intracellular fluids. Metabolic phenomena would undergo the same type of recasting: cells would chemically modify the organic fluids they absorb and at the same time alter their own structures accordingly. In view of his own and others’ experiments on alcoholic fermentation, Schwann points to the causal role played by living cells in those changes, and he even indicates that this power must depend on membranes and nuclei. But, because ultimately the metabolic power seems to reside in unobservable processes, beyond the limits of microscopic investigation, the procedure to favor will consist in establishing the determining conditions of phenomena, for instance, the role of heat, oxygen, and carbon dioxide. The universality of the metabolic role of cells in respiratory processes should also be noted, whether it be O2 absorption and CO2 exhalation or the reverse. This metabolic process and others of the same kind would condition the structural arrangement in multicellular organisms. In addition, the analysis of metabolic processes could follow the guideline of mechanical or chemical interactions along a scale of increasing combinations. In sum, expanding research on the phenomena of cell life, both plastic and metabolic, along those lines would offer the epistemic advantage of keeping within bounds of what can be deduced from phenomena. In conclusion of the physiological synthesis he had sketched, Schwann spelled out his opposition to conjectures based on appealing to a top-down functional order, and he would go to the point of stating contrariwise:

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Indeed, this theoretical model is reductionist but in a heuristic sense: it proposes analyzing cell processes as determining factors for more global functions, but could these be considered as ontologically reducible to sets of cell properties? This part of the question remained implicit and outspanned Schwann’s favored theoretical model: The view that organisms are nothing but the form under which substances capable of imbibition crystallize, appears to be compatible with the most important phenomena of organic life, and may be so far admitted, that it is a possible hypothesis, or attempt towards an explanation of these phenomena. It involves very much that is uncertain and paradoxical, but I have developed it in detail, because it may serve as a guide for new investigations. For even if no relation between crystallization and the growth of organisms be admitted in principle, this view has the advantage of affording a distinct representation of the organic processes; an indispensable requisite for the institution of new inquiries in a systematic manner, or for testing by the discovery of new facts a mode of explanation which harmonizes with phenomena already known. (Schwann, 1847: 215)

After Schwann’s histogenetic demonstration, this theory underwent transformations, first by the annexing of the Schwann cell theory by physiologists who appealed to the Bildungstrieb as a vital formative principle and opposed such a reductionism as had been advocated in the Mikroskopische Untersuchungen (Duchesneau, 1987): this part was contributed by Johannes Peter Müller, Schwann’s mentor, in the later editions of his Handbuch der Physiologie des Menschen (second edition of volume II, 1840; third edition of volume I, 1844). Then the reform went on further with the rejection of the cytoblastemic formation of cells conceived of  as stratified and boxed-in membranes. From 1855 on, Robert Remak and Rudolph Virchow, also disciples of Müller, imposed the principle Omnis cellula e cellula but also provided remarkable demonstrations about embryogenesis as the mode of development of multicellular organisms and the dynamic alteration of cell reproduction under pathological conditions. Finally, in the later decades of the nineteenth century, there occurred new developments concerning constituent structures of protoplasm and discoveries concerning mitosis and meiosis qua processes of nuclear replication. About that follow-up, I shall be content with signaling some typical interpretation of functional explanation that emerged within canonical presentations of the cell theory.

2.5 Functions, Instrumental Forms, and Vital Processes In contrast with the primacy of global functional explanation over the explanation of elementary processes, cell physiology will tend more and more toward an “instrumentalist” position. Claude Bernard supported that position, at least in the theoretical phase that succeeded his annexing of Virchow’s and Kölliker’s cell theory (Duchesneau, 1997, 2013). Thus, in 1867 Rapport he wrote:

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There is really but one general physics, one general chemistry and one general mechanics, in which all the phenomenal manifestations of nature will be accommodated, those of living as well as of plain bodies. In living beings, there occurs not a single phenomenon that does not find its laws outside of itself. So that one could say that all manifestations of life are composed out of phenomena borrowed, insofar as concerns their nature, from the external cosmic world, except that they become manifest under the forms and arrangements proper to organized matter and with the assistance of special physiological instruments. (Bernard, 1867: 223)

Émile Gley, some 40 years later, will phrase an enlightening comment on this model of special instruments. While attributing to Claude Bernard the creation of cell physiology – which seems quite excessive – he resumes Robin’s and Littré’s distinction between special and general physiology. The former comes out of analyses de usu partium; it essentially bears on the role of systems and the organs they are composed of; starting from lesions, ablations, and other alterations of the structures specifically featured in those organs and systems, its method consists in unveiling by contrast their particular functions. The functions so determined must enable analyses that reveal their “functional mechanisms” (mécanismes fonctionnels) as if they were instruments appropriate for the dynamic ends to which functions correspond. The development of general physiology makes it possible to decompose those mechanisms into mechanisms involving histological cellular elements: so the function is translated into “elementary phenomena” of a physicochemical nature, that is to say, metabolic processes operating in and by the cell components. We can thus raise issues about the organs of respiration at the global level of the constituted systems: a certain dynamics of the functions assumed by these organs in given types of organisms may get revealed, but one may as well proceed by analysis down to the metabolism of the involved gas exchanges. Organic structures from the macroscopic to the microscopic level represent more or less complex and integrative instrumental frameworks by which what can be considered as elementary physicochemical acts are performed. These appear to be specific, for they occur within living organizations, but they possess a strictly analogical relation with phenomena that unfold in inorganic nature. Physiological properties manifest themselves dynamically only under conditions of combined elementary forces which we should be able to submit to analysis, but the instrumental dispositions underpinning those physiological properties and the actions that can be assigned to components in these arrangements, down to submicroscopic levels, represent such a complexity in causal factors to unravel that an idea of functional intentionality tends to serve as a substitute for the latter: Certainly, the physicochemical properties of systems and elements start to act only under given circumstances; but it is the same with properties of inorganic bodies; except that the conditions that trigger on the properties of organized bodies are most often so complex that, being unable to determine the causes of vital actions, some may have believed in their spontaneity. (Gley, 1910: 3)

This propensity at transposing functional acts into theoretical entities presumably causing observable vital phenomena pollutes, so to speak, the analytic approach that purports to account for the structural and functional economy of higher processes

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from inferior ones. The account of cell differentiation illustrates this point well. Gley notes the functional polyvalence of unicellular organisms. In relatively simple multicellular organisms, each cell possesses in a way the physiological properties of all the others, so that isolated portions of such an organism can survive and accomplish functional acts. Then, along a series of ascending complexity, a “division of labor” occurs, by which cells get specialized according to specific structures and properties: thus, a predominance of functional determination arises among the organism’s elementary components. But, like Max Verworn (Verworn, 1900: 563), Gley reduces cell activity “to the set of reactions of two chemical complexes: nuclear substances and cytoplasmic ones” (Gley, 1910: 116). But he needs further to imply a “coordination of functions” between specialized cell clusters. He postulates that this coordination flows from the relations that occur between differentiated cells: epithelial cells assume through their various dispositions the nutrition function; germinal tissue cells are responsible for reproduction; cells of the muscular and nervous tissues underpin locomotion and sensibility respectively. The harmony between phenomena is therefore conceived to be pending on an integrative unity of the organism’s operations, while the analytic approach rests on a piece-by-­ piece inventory of correlations between the specialized arrangements that arise from the differentiation of cells as elementary organic instruments: In spite of the division of labor and the resulting multiplicity of physiological instruments, the life of the whole organism is not disturbed; on the contrary, it has remained easy and is fully accomplished: relations must therefore have been set between the diverse, most specialized, parts of an organism. From those relations the coordination of functions arises. (Gley, 1910: 115)

In this regard, the coordination of functions shows up as the rule imposed on the analytic interpretation of processes that originate from elementary dispositions. Ultimately, the latter’s special activity may only be understood as the effect of a division of labor that is geared toward achieving the functional – and so useful, unified, and integrative – order of global operations in the whole organism. The functional understanding of cell processes embodies the primacy of a synthetic vital order over the means required for its accomplishment.

2.6 Functions and Complex Chains of Mechanisms A long series of researches and developments tie up with this viewpoint. I shall only cite as an instance of it the presentation that Oscar Hertwig gave in Die Zelle und die Gewebe (1893–1898) concerning the integration of specialized cells. Specialized cellular structures are presumed subordinate to the emergent functional order that determines our understanding of physiological phenomena proper, which fares as the order of an organismic vital unit. The chosen formulas do not leave any doubt about the methodical association of analytic and synthetic approaches for interpreting phenomena. The purpose is to analyze “the general relations that follow from the arrangement that cells subsumed,” but this analysis could not be achieved

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without taking into account what can be considered an essential instrumental finality of those relations, namely, to transform cells “into fractions of a higher-order whole” (Hertwig, 1903: 3–4). However, Hertwig conceives of observable functional integrations in complex organisms as the end result of evolutionary processes, responsible for gradual adaptation-­yielding transformations. His evolutionism and conception of the hereditary transmission of acquired variations gave way to a theory of “biogenesis”  – inspired more by Lamarck than by Darwin – that formed a counterpart to August Weismann’s theory of the “germinative plasma.” Without entering the details of this theory, I shall stress that it supposed an orthogenetic tendency ruling over complexifications and underpinning the functional integration of the clustered elementary dispositions. The evolutionary viewpoint expressed did not waive the notion of a superior coordination imposing its sway over the analysis of elementary physiological processes that combine along the progressive complexification of structures. According to a strict meaning of “cause,” as illustrated in the sciences of inorganic nature, the degree in the effect should be proportional to the degree in the cause, whence the possibility of inferring the value of the presumed cause from that of the effect. In the case of organic life, by contrast, the cause does not generate a reaction proportional to the corresponding action, and the value of it cannot be estimated a priori from that of the effect. It seems that variation scales are not congruent on both sides and that disparity is bred into such a relation. A fortiori, the rupture in equivalence would be manifest when dealing with superior forms of animal  life, where motives more than causes seem to trigger the production of effects. However, there is no reason to doubt that the causal relation necessarily applies and that the effects are subsumed under laws that express efficient connections. Mechanical order would universally and univocally prevail over the entirety of natural phenomena, organic as well as inorganic. Differently built machines react differently to the action of a given cause. Hertwig takes as instances heliotropism and phototactism in some species of plants: in those light determines distinct and sometimes opposite effects according to the organs affected and their inner dispositions. Hence, Hertwig draws the consequence that organs in physiology, according to their fine cellular or intracellular structures, display special reactions, which he qualifies as their specific energy: The various organs of plants and animals, or, in more general mode, of unstable substances in diverse structures, behave in regard to a similar cause of excitation, as differently framed machines. In physiology, we say that the proper reaction of an organ, which depends on its proper structure, constitutes its specific energy. (Hertwig, 1903: 65)

In the case of organisms, the mediation between cause and effect is implemented by manifold interrelated micro-parts, which further offer multiple alternative ways for sequences of causal connections (Duchesneau, 2012b). And one should not reduce physiological processes only to effects of external causes but should also take into account systems induced by variable internal causes. This correlation principle of internal and external causes is particularly important when accounting for developmental processes by contrast with mere functional processes without morphological implications, if only such are to be found in the organic world.

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Replying to the reductionist presuppositions of Wilhelm His’s and Wilhelm Roux’s developmental mechanics (Entwicklungsmechanik), Hertwig resumed a classical topos: the distinction of organism from any kind of machines. The text underlines a notable difference in the structure-function relationship on both sides: A machine can only exert one or at best a few functions, which it does in an invariable, immutable mode, determined by its own construction. Its various parts cannot change their own make-up, nor combine otherwise than they have done, so as to be able to fulfill other functions, corresponding to those changes of combination. A machine is thus unable to react in a variable and particular mode to any external influence. […] The organism, on the contrary, is able to do so, in virtue of its very structure. In the machine, an absolutely determined set of energies unfolds in a single direction; the set of energies that unfolds in an organism is extraordinarily free and diverse. (Hertwig, 1903: 72)

In a machine, the structure-function relation is, to sum up, fixed and determined. The structural elements are not apt to modify themselves and to recombine in original and, so to speak, functionally adaptive fashion, so as to accomplish operations to which their whole is destined. The functions of the machine necessarily flow from its structural disposition, and they would not account for its genesis and arrangement, if not through the intention of the engineer who conceived of it. The positive explanation of its functioning will only detail its wheelworks and their actions accomplished in linear series. The case is different with an organism. Its structural elements can modify and transform themselves in various ways within the framework of a single and same system of organismic operations. This effect would be owing to manifold chemical reactions and combinations that could be achieved in it due to the diversified interaction among its elementary dispositions. The versatility of those sequences leaves the impression of a free display of forces in accomplishing processes subservient to the general ends of organic and animal life. These processes are functions, but, in contrast with those that the machine yields, they immanently determine the variable order of the elementary dispositions, at once morphological and biochemical, by which the state of life is maintained and evolves. Everything goes as if the global functional order, that of the integrative operations of living beings, ruled over the particular dynamics of those machines of nature, which cells form, as basic physiological units. The functional polyvalence of the whole organism can be understood at once in terms of the chemical operations and morphological operations of cells – along the order of analysis – and in terms of the integrative unity that comprises the functions of cell life, in turn conceived of as analogous to functions of the whole organism, along the order of synthesis.

2.7 Conclusion I have tried to show over a long historical period the way in which general physiology, at the core of an emerging biological science, had viewed the structure-function relationship. There is no doubt that the modern viewpoint was dominated by models of technological mechanisms. In these, the operations, the projected functions,

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flowed from their structural dispositions and therefore from their makeup qua machines. If the living were assimilated to machines of nature, the aim was initially to explain their functions, operations, and processes by the organic dispositions that would generate them, but the very arrangement of those dispositions needed in turn to be accounted for by the functions they would yield. The revolution Haller achieved in relation to this initial mechanist model consisted in focusing analysis on the physiological properties of the organism’s elementary structures: these were irritability and sensibility attributed to distinct kinds of fibers, whose combinations would account for the functions of organs and systems. At the advent of biology, the study of functions, that is of the dynamic phenomena attributable to organs and systems, would be viewed as implying a nexus of reasons that could be accounted for by analyzing the properties and molecular composition of tissues. This was at least the experimental orientation to promote, as witnessed by Blainville. The aim was to discover “the general element of all organizations,” that is, a set of morphological and dynamic properties underlying the framework of specialized organs in more and more complex systems of organic dispositions. Might we then dispense with projecting functions as explanatory causes for elementary and general processes and modes of organization? This option was considered in Schwann’s initial formulation of the cell theory. The structural and functional integration of the organism would only rest on the morphological and metabolic properties of cells, and it would be appropriate to detach physiological analyses from any causal status granted to an emergent organizing principle. This averred reductionism was nevertheless rejected by Johannes Müller and his disciples who recast the cell theory under a formal principle that would warrant the organism’s integrative unity. The phenomena specific to organized bodies could not be explained without a function assuming principle being presupposed. This requirement prevailed notably in developmental biology wherein it would have been difficult not to evoke an organizing force embodying the functional plan to implement. If, consequently, this principle tended to impose itself in explanations of elementary processes, it would essentially do so in an instrumentalist mode. As stated by Claude Bernard, vital phenomena occur under specific organizing conditions and arrangements that determine the emergence of functional characteristics as if these were the outcome of special instrumental dispositions. That model will be further developed with many variants. Above all, the complexity of those presumed instrumental arrangements will incite short-circuiting analytic procedures by appealing to a sort of regulative idea, a kind of immanent functional intentionality that would be a source of vital spontaneity. Oscar Hertwig illustrated that trait in enlightening fashion. Apparently, the analysis of vital processes in terms of physicochemical structures and operations would marginalize explanations invoking a functional raison d’être ruling over organic systems as wholes. But, even in rather reductionist contexts, such as those relative to the protoplasmic researches of Brücke and Verworn, for instance, or those concerned with developmental mechanics, there remained a tendency to interpret elementary phenomena by latent appeals to analogies with global functions. At the very end of the nineteenth century, Edmund B. Wilson introduced the synthesis he intended to draw between cytology and theories of heredity and evolution with a

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citation of Virchow: “Every animal appears as a sum of vital units, each of which bears in itself the complete characteristics of life” (Virchow, 1858: 12). This is because, in that historical phase of biology, the analysis of physiological mechanisms seemed to require a functional principle that Wilson interprets as the admission of a “fundamental common plan of organization that underlies [the] endless external diversity [of living organisms]” (Wilson, 1925: 1).

References Bernard, C. (1867). Rapport sur les progrès et la marche de la physiologie générale en France. Imprimerie impériale. Blainville, H.-M. D. d. (1833). Cours de physiologie générale et comparée. Germer Baillière. Duchesneau, F. (1987). Genèse de la théorie cellulaire. Vrin/Bellarmin. Duchesneau, F. (1997). Claude Bernard et le programme de la physiologie générale. In C. Blanckaert et al. (Eds.), Le Muséum au premier siècle de son histoire (pp. 425–445). Éditions du Muséum National d’Histoire naturelle. Duchesneau, F. (2012a). La Physiologie des Lumières: empirisme, modèles et théories. Classiques Garnier. Duchesneau, F. (2012b). Determinism and probability in the development of the cell theory. Progress in Biophysics and Molecular Biology, 30, 1–7. Duchesneau, F. (2013). Claude Bernard: théorie cellulaire et synthèse morphologique. In F. Duchesneau, J.-J. Kupiec, & M. Morange (Eds.), Claude Bernard: la méthode de la physiologie (pp. 33–48). Éditions Rue d’Ulm. Duchesneau, F. (2016). Laws of vital organization: Blainville and Müller. History and Philosophy of the Life Sciences, 38, 1–18. Duchesneau, F., & Smith, J. E. H. (2016). The Leibniz-Stahl controversy. Yale University Press. Gley, É. (1910). Traité élémentaire de physiologie. J.-B. Baillière. Haller, A. v. (1754). Primae lineae physiologiae. Apud Laurentium Basilium. Haller, A. v. (1756–1760). Mémoires sur la nature sensible et irritable des parties du corps animal. M.M. Bousquet. Haller, A. v. (1757–1766). Elementa physiologiae corporis humani. M.M.  Bousquet/Sumptibus Societatis typographiae. Hertwig, O. (1903 [1898]). Éléments d’anatomie et de physiologie générale. C. Naud. Müller, J. P. (1851). Manuel de physiologie. J.-B. Baillière. Schwann, T. (1847). Microscopical Researches into the Structure and Growth of Animals and Plants. Sydenham Society. Steinke, H. (2005). Irritating experiments: Haller’s concept and the European controversy on irritability and sensibility, 1750–90. Rodopi. Verworn, M. (1900). Physiologie générale. Schleicher Frères. Virchow, R. (1858). Die Cellularpathologie. Hirschwald. Wilson, E. B. (1925 [1896]). The cell in development and heredity (3rd ed.). Macmillan.

Chapter 3

Tissues, Properties, and Functions: The Term Function in French Biology in the Early Nineteenth Century Laurent Clauzade

Abstract  Bichat’s legacy to the posterity consists of two main theses: a vitalistic conception of life and a theory of vital properties which is problematically related to the elementary level of anatomical hierarchy: that of tissue. Bichat is indeed the well-known founder of histology. Two main problems arise from this legacy. The first one is the multiplication of vital properties, and the second lies in the correspondence between physiological and anatomical hierarchies: Bichat’s system precludes a rigorous overlap of anatomy, which studies tissues, and physiology, which studies vital properties. I propose in this chapter to show the major role played by the concept of “function” in the criticism addressed to Bichat by Magendie and Comte on these two issues. Beyond their different directions, their criticisms have a common goal: to posit and precise the levels of analysis, i.e. to draw a distinction between the level of vital properties and the level of functions and between the problem of tissues and the problem of organs and apparatuses. Such corrections are not only a critique of vital properties but can be considered as a rationalization of the theoretical concepts which organize biology and primarily the notion of function.

3.1 Introduction Why should we define scientific concepts? Or, in other words, for what reason does a concept turn out of great importance, assuming and condensing most of the difficulties of a theory? A part of the answer can be given by the study of the issues raised by the theory of Bichat. The rather intuitive and highly finalist notion of function is thought by Bichat as a degree in the anatomical and physiological hierarchy he sets out in his Anatomie générale (Bichat, 1801, 1824). While, on the one hand, L. Clauzade (*) Normandie Univ, UNICAEN, Caen, France e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_3

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this concept still remains a general instrument for global biological inquiries, on the other hand, Bichat gives a special meaning to it: “function” is the opposite of “properties” and is defined by its place in a quite precise anatomical nomenclature (tissues, organs, and apparatuses). It is undoubtedly this tension between a general and intuitive use of the notion and the requirements of a hierarchical integration which determines the evolution and the clarification of the concept of function. In what follows, we propose to show the key role played by the concept of function in the criticism addressed to Bichat by Magendie and Comte. Beyond the different standpoints taken by these authors, their criticisms have a common goal: to posit and precise the levels of analysis and to distinguish between the level of vital properties and the level of functions and the problem of tissues from the problem of organs and systems. Such corrections are not only a critique of vital properties but can be considered as a rationalization of the theoretical concepts which organize biology and primarily the concept of function.

3.2 Bichat’s Legacy Bichat’s legacy to the posterity consists of two problematic theses: a vitalistic conception of life and a complex theory of vital properties, which hardly agrees with his most elementary degree of the anatomical analysis, that of tissue. Before dealing with the concept of function, one must first characterize these two issues.

3.2.1 A Vitalistic and Agonistic Definition of Life Through its definition of life as “the totality of those functions which resist death,” Bichat advocates a vitalistic and agonistic understanding of life. The commentary which follows this definition develops these two features: Such is in fact the mode of existence of living bodies, that everything which surrounds them tends to their destruction. Inorganic bodies act upon them incessantly; they themselves exercise a continual action, the one upon the other; and would necessarily soon be destroyed, did they not possess a permanent principle of reaction. This principle is life; not understood in its nature, it can be known only by its phenomena; the most general of which is that constant alternation of action on the part of external bodies, and of reaction on the part of living body, the proportion of which alternation vary according to age. (Bichat, 1809, 1; 1800, 1)

The agonistic view is the first characteristic underlined by this quotation. “Everything which surrounds” living bodies, in other words the “action on the part of external bodies” or what we could call physical surrounding (milieu physique), tends to destroy them. Life can’t therefore rely on what surrounds it and has to find its principle of reaction in its own resources.

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Hence the second feature, which readily comes from the postulate that the vital principle is wholly independent from the physical powers of nonliving world. In Bichat’s theory, vitalism is implied by the isolation of living bodies from what surrounds them. This vitalistic and agonistic definition directly conflicts with two trends in philosophy of life. The first one is of course the materialist tradition (e.g., Broussais or Lamarck); the second one posits that the phenomenal world is in a way homogeneous: Comtian positivism advocates for such a continuism. We will deal with this point below.

3.2.2 A System of Vital Properties The second problem raised by Bichat’s writings is about the theory of vital properties. The characteristic of these properties is that they cannot be reduced to inorganic properties, such as gravity, chemical affinities, or elasticity. Vital properties are constitutive of vital phenomena, just as gravity is constitutive of physical phenomena. This theory poses two issues we have to deal with: first, the permeability of the classification of vital properties to functional analysis and, second, the difficulty to articulate vital properties with the properties of tissue. 3.2.2.1 The System of Vital Properties and the Division of Life into Organic and Animal Functions Let us shortly remind the classification of the five vital properties Bichat wrought out (Table 3.1). One might consider that such a classification stems from the crossing of two successive analyses. According to the first one, sensibility and contractility are the two basic properties of the living world, as opposed to those of the inorganic world. This principle is laid out from the very beginning of Anatomie générale, in a lapidary statement which is characteristic of Bichat’s style:

Table 3.1  Vital properties in Bichat’s theory

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L. Clauzade There are in nature two classes of beings, two classes of properties, and two classes of sciences. Beings are organic or inorganic, properties vital or non-vital, sciences, physiological, or physical. Animals and vegetables are organic. What are called minerals are inorganic. The vital properties are sensibility and contractility. The non-vital are gravity, affinity, and elasticity. (Bichat, 1824, i; 1801, vol. 1, xxxv)

For the second analysis, in order to divide these two fundamental properties, one has to follow the physiological distinction between two kinds of lives or functions. This well-known distinction which has been developed in Recherches physiologiques sur la vie et la mort rests on the division into organic life and animal life, each of these lives including a set of distinctive functions, such as digestion, respiration, circulation, etc., for organic life and sensation, locomotion, and cerebral functions for animal life. Bichat stresses the importance of this distinction in the “General considerations” of his Anatomy: I could, by a thousand other instances, prove that all disputes and differences of opinions, concerning vital properties, proceed solely from the not distinguishing those which preside over the functions of one life, from those that govern over the function of the other. (Bichat, 1824, lxxxiii; 1801, vol.1, cvi)

This quote shows that both the determination and the classification of vital properties depend on the determination and the classification of functions. In some way, the functional point of view compels to duplicate the number of vital properties. As we will see below, for a physiologist like Magendie, who claims the limitation of the number of vital properties, the application of such a functional perspective to the question of vital properties will be highly controversial. 3.2.2.2 The Articulation Between Properties and Tissues The second problem we have to deal with concerns the articulation between vital properties and the properties of tissue. Bichat does not only focus on vital properties; he is also interested in the physical organization of animals. From an anatomical point of view, he assumes that tissues are the simple elements from which the organs are made of: these 21 tissues “are the real organized elements of our frame” (Bichat, 1824, liii; 1801, vol. 1, lxxx). The problem of the articulation between the two levels comes from the way Bichat conceived of the life attached to tissues. On the one hand, Bichat stresses that the decomposition of an organ into its tissues is the relevant level of analysis in order to determine its “peculiar life”: Much has been said since Bordeu’s time, of the peculiar life of each organ, or that particular character which distinguishes the whole of the vital properties of one organ, from the vital properties of another. (…) From the sketch, therefore, that I have just drawn, it is obvious, that as the greatest part of the organs are formed of very different simple tissues, the idea of peculiar life can only be applied to these single tissues and by no means to the organs themselves. (Bichat, 1824, lvi; 1801, vol. 1, lxxxiii–iv)

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But, on the other hand, vital properties are in some way transversal to the different tissues. On this very point, one has to distinguish between the properties of tissue and vital properties. The properties of tissue are inherent in tissues: they “depend on the texture and the arrangement of the particles” of each tissue (Bichat, 1824, xliii; 1801, vol. 1, lxxii). These properties are also independent of life for, in the words of Bichat, “death does not destroy them; they adhere to organs when life has forsaken them” (Bichat, 1824, xliii; 1801, vol. 1, lxxii). On the contrary, vital properties are not inherently related to tissues. Admittedly, each elementary tissue is endowed with some vital properties. However, as Bichat put it, these properties don’t belong to organization but to life. Such dissociation is confirmed if the problem is laid down from the point of view of vital properties: the same property can belong to several tissues which differ from one another by their texture. The idea of “the peculiar life” of a tissue is far from being clear. First, this theory raises a problem of complexity: two kinds of properties are crossing each other in a same anatomical structure, in which they are differently inhering. The second problem, in a positivist perspective, is a philosophical and methodological one: how can we understand that some (vital) properties could belong to tissues without arising from their very texture?

3.3 The Polemical Use of the Concept of Function in the Attacks Against Bichat’s Theory Bichat leaves to posterity three difficult questions, with respect to the definition of life, the relation between a functional approach and the determination of vital properties, and finally the articulation between vital properties and properties of tissue. In the attacks against Bichat’s theses, and thus in the efforts to solve the questions, an in-depth understanding of the notion of function plays a major role. That is what we will verify through a study of two criticisms to which this notion of function is quite differently applied. Coming from Magendie, the first criticism is in some way internal and belongs to the experimentalist trend of Bichat’s lineage. It consists in returning to Bichat’s definition of function and to use it against the theory of vital properties. By doing so, Magendie gives a more precise and narrow version of this theory. The second criticism is formulated by Auguste Comte and is constructed in a quite different way, on the basis of a double conceptual analysis of life and function. This criticism aims at regularizing of the biological nomenclature.

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3.3.1 Magendie: An Internal Critique of Bichat’s Vital Properties In order to fully understand Magendie’s criticism, one has to precise the meaning of the word “function” in Bichat: such an attempt is not an easy task. 3.3.1.1 Bichat’s Notion of Function Although the determination of the different functions plays an essential role in Bichat’s theory both in the distinction of lives and in the classification or in the enumeration of vital properties, it is difficult to find an explicit definition of the concept of “function,” or a fortiori a conceptual work on this very concept. Hence, we face a rather vague notion that Bichat locates sometimes at the level of organs and sometimes at the level of apparatuses. In an obviously finalist acceptation, the word can be also equivalent to the concept of use or, in a weaker sense, to that of act. Meanwhile, commentators, and especially Albury (1977, 89), agree to claim that the prominent and pertinent meaning is connected with the idea of apparatus, which, in turn, is defined as “an assemblage of several organs contributing to the fulfilment of one function” (Bichat, 1829, vol. 1, x). It is thus possible to identify the physiological level of function in establishing a correspondence with the anatomical level of apparatus. The last works of Bichat clearly indicate that he took this direction on this very issue, and it seems retroactively that the level of apparatuses is the pertinent one to understand the physiological distribution laid out in the Recherches physiologiques (see Bichat, 1829, vol. 1, xii–xvii). One may see how this concept of function works by studying a passage of the General anatomy where Bichat tries to defend the claim that animal heat is not a chemical property (or “caloricity”) but a true organic function (or “calorification”) (Bichat, 1801, vol. 2, 520–4; 1824, 605). According to “modern chemists,” the capillary system of the lungs is conceived as the exclusive focus from whence heat proceeds. Against such an explanation, Bichat hypothesizes a complex process involving several organs and several systems: admission of the caloric in the blood mainly through respiration, circulation in the arterial system of the combined state of the caloric, and separation of this combined fluid to form free caloric in the general capillary system, or in other words in the various parts of the organism (see Bichat, 1824, 608–9; 1801, vol. 2, 522–4). Calorification is thus a complex process which duly deserves the name of function, as well as nutrition, exhalation, or secretion. It is this very concept of function that Magendie borrows from Bichat and directs against the classification of vital properties.

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3.3.1.2 Magendie’s Criticism: Animal Sensibility and Animal Contractility as “True Functions” It is well known that Magendie endeavors to limit as much as possible the number of vital properties. He only accepts nutrition and vital action (action vitale), to which he adds, at least from 1809, sensibility and motility. What we are concerned with here is precisely the argumentation against animal sensibility and animal contractility. The core of the argument is that a vital property has to correspond to a general and essential character of life. In order to show that animal sensibility doesn’t fit with such a principle, Magendie proposes the same argument as Bichat developed against calorification. Animal sensibility is not a property but a “true function” that involves the cooperation of several organs: Thus there can be animal sensibility only insofar as there exists, in the same being, a sense-­ organ, a nerve and a brain. If one of these organs is lacking, or if it is slightly altered, there is no animal sensibility at all. What is a complex vital property? - I confess that I cannot conceive how authors of the greatest merit have failed to take this objection into account. If, for the preceding reasons, we do not classify animal sensibility among the vital properties, how ought we to consider it? as a true function. A function is the common end of the action of a certain number of organs. (Magendie, 1977, 113–114)

Functional analysis, as previously pointed out, allowed Bichat to classify vital properties and finally to double their amount. On the contrary, the determination of the “true functions,” which are located at the level corresponding to the anatomical degree of apparatuses, leads Magendie to get rid of useless properties. It is worth noticing that the argument we have just described is exceptionally not experimental since it aims at rationalizing the use of classificatory concepts, and it is rather theoretical. By assigning contractility and sensibility to their appropriate physiological level, Magendie lessens the part of “useless and dangerous suppositions” in biology and increases the field of phenomena that it is possible to investigate by experiment. Functions are precisely the main object of such a field of research which is fully studied by the Precis élémentaire de physiologie (see Magendie, 1829, 19–20; 1816, vol. 1: 22–24).

3.3.2 Auguste Comte’s Criticism The criticism of Auguste Comte is primarily conceptual. It is a properly philosophical attempt which aims at analyzing and clarifying the operational scientific concepts. The analysis of the idea of function proceeds in two steps: the first one gives a general and abstract definition of function grounded on the definition of life and the second a restricted definition of function in relation with the scientific purpose of biology.

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3.3.2.1 The Large and Abstract Definition of Function In order to define the idea of function, Comte relies on an anti-vitalistic definition of life. Life is the result of a correlation between the living organism and its environment (milieu), hence the definition of function understood as the act which constitutes the correlation: We have seen that the idea of life supposes the mutual relation of two indispensable elements, - an organism, and a suitable medium [“milieu”]. […] It immediately follows that the great problem of positive biology consists in establishing, in the most general and simple manner, a scientific harmony between these two inseparable powers of the vital conflict, and the act which constitutes that conflict: in a word, in connecting, in both a general and special manner, the double idea of organ and medium [“milieu”] with that of function. (Comte, 1858, 307; 1975, vol. 1, 683)

Within this framework, the idea of function is described in a very abstract way as some sort of hypostasis of the conflict between organism and milieu. Accordingly, this analysis produced three terms biology would have to account for: organ, milieu, and function. Function is properly what links these terms together by operating the correlation. In consequence, the concept of function endorses the whole anti-vitalistic significance of the Comtian definition of life. In reference to Bichat, Comte indeed understands vitalism as conveying the “idea of an absolute antagonism between dead nature and living nature”: living nature, isolated from its environment, can only rest on its own vital principle. From that perspective, a definition of life which stresses the relative character of life (the correlation between organism and milieu) must be considered as anti-vitalistic. The concept of function understood as the act that constitutes the relation thus summarizes Comte’s anti-vitalistic stance. However, the conceptual work on the notion of function has to go further: the definition is indeed far too much abstract to be directly applied to the analysis of biological methods. For such a purpose, it is therefore necessary to restrict this first version. 3.3.2.2 The Narrow Definition of Function and the Scientific Aim of Biology As the previous analysis indicates, biology has to deal with three terms: organ, milieu, and function understood as the act which constitutes the correlation. However, to define “the scientific purpose of biology,” or, in other words, to have an efficient concept of function, Comte made two reductions. The first step consists in focusing exclusively on the organic outcomes of the conflict. As for the consequences of the act on the milieu, when important enough – which only happened in the case of the human species – it was for natural history to study them. Therefore, in this first step, it is only the physiological and present meaning of the term “function” that is retained.

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The second reduction amounts to the decision of eliminating the milieu from the fundamental equation of biology. The milieu remains almost stable for it isn’t significantly altered by the action of living bodies. To fully understand such an elimination, one must have in mind that the mathematical model of the notion of function is extremely present in Comte’s study. A mathematical function relates two quantities which vary together, i.e., which “are functions of each other” (Comte, 1858, 53; 1975, vol.1, 68–69). In a similar way, a sort of parametric function has here to be conceived of: the milieu parameter being invariant, it can be described as a constant we can neglect in the final formulation. Once these two reductions have been made, Comte can introduce the scientific aim a biological theory has to achieve: Biology, then, may be regarded as having for its object the connecting, in each determinate case, the anatomical and the physiological point of view; or, in other words, the statical and the dynamical. (…) The surrounding system being always supposed to be known, according to the other fundamental sciences, the double biological problem may be laid down thus, in the most mathematical form, and in general terms: Given, the organ or organic modification, to find the function or the act; and reciprocally. (Comte, 1858, 307; 1975, vol. 1, 683–4)

3.3.2.3 Cuvier’s Shadow? We may be tempted to draw this double definition of the function closer to Cuvier’s theses. Of course the correlation mentioned above does not relate directly with the principle of “correlation of forms” established by the naturalist. Comte actually intends to connect the organism with its “milieu” and not, as Cuvier does, to stress the natural correspondence of all the parts of an organic being, considered as a “unique and closed system” (Cuvier, 1992, 97). Yet we may legitimately draw a parallel between the result of the second Comtian definition and the principle of “conditions of existence.” The meaning Comte attributes to the principle, from a radically anti-finalist point of view, corresponds indeed strictly to the methodological imperative of an exact correspondence between the ideas of organization and of life: Attacking, in its own way, the elementary dogma of final causes, it has gradually transformed it into the fundamental principle of the conditions of existence, which is the particular aptitude of biology to develop and systemize […]. Science compels us to conclude that there is no organ without a function, and no function without an organ. Under the old theological influences, students are apt to fall into a state of anti-scientific admiration when […], having observed a function, anatomical analysis discloses a statical position in the organism which allows the fulfilment of the function. […] The philosophical principle of the conditions of existence is in fact simply the direct conception of the necessary harmony of the statical and the dynamical analyses of the subject proposed. (Comte, 1858, 331–2; 1975, vol. 1, 738)

We could perhaps be tempted to attribute to Cuvier’s principle the full extension which it contains, that is, conceive of it as focused on the possible existence of the total being, envisaged not only in itself but also and mostly as related “with those

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who surround it” (Cuvier, 1817, 6). This principle would then appear – by a shift in the meaning of “milieu” – as an anticipation of the first Comtian definition. Yet we think that the analyses of Comte follow another direction. Two arguments are here of capital importance. First, the Comtian definitions are concerned more with the organism than with the organization. We are entering a reflection on the organism, where live beings are first intended as individualized beings, whose understanding and definition cannot be severed from their relationship with a “milieu.” As Bernard Balan notices, with Blainville  – but it applies as well to Comte – the natural conditions of existence are part of the constitution of the biological object (Balan, 1979, 21). Cuvier’s principle, on the opposite, rests primarily attached to an abstract understanding of the organization as a closed system. The second argument consists in focusing on the main orientation of Comte’s definitional work. Comte inherits from Blainville not only a theory of the organism which renews Cuvier’s approach but also a deep interest in Bichat’s tissular theory (Clauzade, 2007). It was indeed rather logical that Comte, who endeavored to found abstract biology as a science which could not be reduced to physical sciences, should be interested in Bichat who had more than any other asserted the separation of physical and physiological sciences. Actually the definition of life as a relation, on the one hand, and the aim of positive biology – as we are going to see – must primarily be understood on the mode of contestation, related to Bichat’s theory. If we must ascribe a role to Cuvier, decisive indeed but very general, it has been recognized by every commentator: directing natural history and zoology toward physiology and giving the precedence to the function rather than to the anatomical structure (Daudin, 1926, vol. 1, 58–64). Under this assumption, all the analyses in this essay (for Magendie, see Albury, 1977, 87–94; Huneman, 1998, 93–95) follow his course, insofar as we accept the idea that he found the epistémé of his epoch. Such was actually his hyperbolic reading by Foucault (Foucault, 1966, 275–292). 3.3.2.4 The Harmonization of Physiological and Anatomical Hierarchies According to Comte, the necessity of establishing a rigorous correspondence between structures and acts at each level of the anatomical and physiological hierarchies is an immediate consequence of the definition of the scientific goal of biological science. Functions are thus identified as the physiological level which corresponds to the anatomic levels of organs and apparatuses. The following chart summarizes these coordinated hierarchies, which Comte borrows from Blainville – and from Bichat partly via Blainville (Table 3.2). But for the correspondence to be properly established, an in-depth criticism of Bichat’s system is needed, especially regarding the coordination between vital properties and the properties of tissues. From that perspective, the modification Comte brings to Bichat’s theory of vital properties is indeed a direct application both of the second definition of function and of the scientific aim of biology. What is questioned is not the idea of vital properties in itself, for Comte readily acknowledges that sensibility and irritability, to take the example of the exclusive

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Statics (anatomy) Tissues Organs Apparatuses Organisms

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Dynamics (physiology) Properties Functions Functions Results

properties of animal life, are truly original and unexplainable, just as gravity and heat for the physical world (see Comte, 1858, 369–70; 1975, vol. 1, 823). The disagreement bears on whether these vital properties and the properties of tissue have to be distinguished or not. In Bichat, as previously pointed out, vital properties were in some way transversal to tissues. On the contrary, Comte assimilates vital properties to the properties of tissue: Not only is there a secondary confusion between the properties of tissue and simple physical properties, but the principle of the conceptions is vitiated by the irrational distinction between the properties of tissue and vital properties for no property can be admitted in physiology without its being at once vital and belonging to tissue. In endeavouring to harmonize the different degrees of physiological and of anatomical analysis, we may lay down the philosophical principle that the idea of property which indicates the last term of the one must correspond with tissue, which is the extreme term of the other; while the idea of function, on the other hand, corresponds to that of organ: so that the successive ideas of function and of property present a gradation of thoughts similar to that which exists between the ideas of organ and of tissue, except that the one relates to the act and the other to the agent. (Comte, 1858, 363; 1975, vol. 1, 809)

Each vital property remains indeed unexplained and non-reducible, but it is unequivocally inherent in a particular tissue. An independent vital property of a given tissue is a metaphysical entity, which could not be included in a positive biological theory. Sensibility is thus exclusively related to the nervous tissue and irritability to the muscular tissue. Through his conceptual work on the concept of function, Comte therefore achieves to establish a complete program of analysis in abstract biology. From there, physiology as a whole can be ordered according to the various degrees of anatomical analysis. Such a program obeys both the epistemological standards of positive philosophy and the anti-vitalistic conception of life.

3.4 Conclusion We have tried to show that what is at stake in our corpus is the incorporation of the concept of function in a precise anatomical and physiological nomenclature. Such a problematic is typical of the paradigm of Bichat’s histology. For those who consult the medical dictionaries of the time, it is obvious that the decomposition of organs in tissues and of life in its properties is one of the main problems through which the science of living bodies is progressing.

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Magendie and Comte incontestably are referring to Bichat’s theory, either to get rid of vital properties and to build an efficient concept of function which can be used in an experimental physiology or to normalize the anatomical and physiological hierarchies for the scientific foundation of positive biology. These criticisms and these attempts correspond to a specific period in the history of the concept of function. Finally, we would like to point out the peculiar character of Magendie and Comte’s analyses. These are both genuine conceptual works on the theoretical categories Bichat’s anatomy and physiology promoted. The extremely complex and integrating work of Comte on definition is notably impressive: such a true philosophical reflection on a key concept of biology may be seen as the distant and incommensurate ancestor of the contemporary analyses on the notion of function.

References Albury, W.  R. (1977). Experiment and explanation in the physiology of Bichat and Magendie. Studies in the History of Biology, 1, 47–131. Balan, B. (1979). Organisation, organisme, économie et milieu chez Henri Ducrotay de Blainville (Vol. XXXII, pp. 5–24). Revue d’histoire des sciences. Bichat, X. (1800). Recherches physiologiques sur la vie et la mort Brosson, Gabon et Cie. English edition. Bichat, X. (1801). Anatomie générale appliquée à la physiologie et à la médecine. Brosson, Gabon et Cie. 4 vol. English edition. Bichat, X. (1809). Physiological researches upon life and death (T.  Watkins, Trans.). Smith & Maxwell. Bichat, X. (1824). General anatomy, Part the first, including the two first volumes (C.  Coffyn, Trans.). Shackell and Arrowsmith. Bichat, X. (1829). Anatomie descriptive (1st ed., pp. 1801–1803). Gabon. 5 vol. Clauzade, L. (2007). La notion de fonction dans la philosophie biologique comtienne. Revue Philosophique, 4, 505–525. Comte, A. (1975). Cours de philosophie positive (1st ed., 1830–1842), Hermann, 2 vol. English translation: 1858. The positive philosophy of Auguste Comte (H.  Martineau, Trans.) 1st ed. 1853. Calvin Blanchard. Cuvier, G. (1817). Le règne animal distribué d’après son organisation (Vol. 1). Deterville. Cuvier, G. (1992). Discours préliminaire: Recherches sur les ossements fossiles de quadrupèdes (1st ed., 1812). GF-Flammarion. Daudin, H. (1926). Cuvier et Lamarck. Les classes zoologiques et l’idée de série animale (2 vol). Alcan. Foucault, M. (1966). Les Mots et les choses. Gallimard. Huneman, P. (1998). Bichat, la vie et la mort. PUF. Magendie, F. (1816–1817). Précis élémentaire de physiologie. Méquignon Marvis. 2 vol. English translation: Magendie, François. 1829. An elementary compendium of physiology (E. Milligan, Trans.). John Carfrae and Son. Magendie, F. (1809). Quelques idées générales sur les phénomènes particuliers aux corps vivants. Bulletin des sciences médicales, publié au nom de la Société Médicale d’Émulation de Paris: 4. English translation: Magendie, F. (1977). Some general ideas on the phenomena peculiar to living bodies (W. R. Albury, Trans.). Studies in the History of Biology, 1, 107–115.

Chapter 4

“Design,” History of the Word and the Concept: Natural Sciences, History, Theology, and Aesthetics Daniel Becquemont

Abstract  The English word “Design” conveys so many possible connotations that its translation into French never came to a common agreement. In English, the plan, the action, and the result of the action were included in the same word which preserved until today a plurality of interpretations. In the eighteenth century, Design became almost synonymous for the whole economy of nature and a form of “physico-theology” which introduced the concept of “natural religion.” There could not exist a Design without a divine designer, and William Paley, in the beginning of the nineteenth century, popularized the “argument of Design.” The concept of Design was reintroduced in the end of the twentieth century, as “the organization of biological structure in relation with function.” A “strong” etiological theory was advanced by Larry Wright, where natural selection could play the part of Paleyan design, with gradual accumulation and continuous optimization, or could agree with a blind watchmaker in a kind of “Design without design.” On the contrary, the rejection of any form of teleology is implicit in the “dispositional” concept of function and in the views of some biologists who suspect the reintroduction of finality or do not trust the efficiency of analogy any more than David Hume did. And at last the idea that the analogical use of the word “function” was necessary but did not imply any positive knowledge – closer to Kant’s views – is part of the common sense of many biologists and philosophers of biology.

4.1 The Word The French language never managed to agree on a satisfactory translation of the English word “design.” The radiating polysemy of the English term  – reaching sometimes the limits of contradiction – did not agree with any French word offering a similar variety. The difficulty was increased by the problem of finding a similar D. Becquemont (*) Université Charles de Gaulle-Lille 3, Villeneuve d’Ascq, France © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_4

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root for Design and Designer, active and passive, deriving from the verb “to design.” Various translations of the series of terms picked in only two contemporary translations into French, The Blind Watchmaker by Richard Dawkins and Darwin’s Dangerous Idea by Daniel Dennett, can illustrate this multiplicity: conception, plan, intention, dessein, but, ordonnancement, architecture, dessin, and agencement, to which are added a few periphrases. To extend the search to more translations would probably not have added many other terms. To translate a similar word by different ones in different contexts is not in itself to be condemned. It raises nevertheless a problem when the term is a major concept which was applied to theology, biology, and aesthetics. The concept may even disappear in French when design work is translated by travail de conception, design space by espace du dessein, and argument from design remaining argument du dessein. If dessein and conception are the most usual French translations, the scattered possible interpretations may sometimes lose the polysemy of the English word. For instance, a designed thing is defined by Dennett as a living thing, a part of a living thing, or the artifact produced by a living thing, and Dawkins adds that Darwin and Wallace had the immense merit of understanding that “Good Design” implied that a complex conception could rise from mere simplicity. The English, French, and Italian words are all derived from the Italian designare (to show by some indications). In the Italian Renaissance, disegno denoted the initial graphic representation of a painting or a building. The aesthetic sense was the original meaning. In French, a dessin or dessein – the same word with two different spellings – was a projection, a plan, or even a sketch. The Dictionnaire Critique de la Langue Française by Féraud (1787–1788) adds that the new spelling dessin became frequent and useful to establish the distinction between dessein (plan) and dessin (art of drawing or work done by the person who draws). These two meanings of the same word had to wait until the end of the eighteenth century before they became two words in French and before the word dessein was considered as archaic in the sense of dessin. At the same period, the English theologian William Paley reinforced the English unity of the various acceptions of the term with his “argument from design.” The two meanings of the term, sketch and final result, remained united, as it was in the Italian disegno. This divergence between  dessein and dessin in French is certainly what makes it so difficult to translate – and understand – the English word “Design.” The chain “Constructeur-­ Construction-­Construit” (designer-design-designed) could perhaps have been adopted in French, but today its introduction could only add to the confusion. This confusion is not limited to France. In Great Britain, the word “Design” means in its final result the plan, the realization of the plan, and the constructed object. The plan, the action, and the result of the action were included in the same word, and it preserved until today a plurality of interpretations which allowed, for instance, Dawkins to speak of “Good Design” in The Blind Watchmaker – translated into French by “excellence de la conception” (a more popular translation closer to Dawkin’s vocabulary could have been du beau travail) – meaning the optimality of a structure unintentionally advancing toward the best, while asserting in the subtitle

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of his book that there is no design in nature, Design being thus intended as unintentional plan (though a distinction can be read between Design with a capital D and “design”).

4.2 The Concept The idea that natural phenomena can be considered as the proof or a sign of an order conceived by a Deity according to laws dates at least from the stoic philosophers. Cicero had already mentioned the example of a sundial in his De Natura Rerum, which surmised the existence of a connection between the order of nature and the products of human industry, and anticipated the example of the watch. The example was renewed with the scientific discoveries of the Renaissance, reinforced by the admiration of the perfection of the “secondary causes” which ruled the universe. They were the proof of the manifestation of a divine power. Physics, theology, and aesthetics advanced in unison, and the divine Design was reflected in the perfect design of organic beings. In the middle of the seventeenth century, Robert Boyle mentioned the perfect adaptation of the eye to sight in order to prove the existence of a good and intelligent Being which ruled the order of the world and its living creatures, and reintroduced the argument of the sundial. The invention of the watch at the same time, as a wonderful microcosm of the physical laws of the universe and man’s creativity, took quickly the place of the sundial with what was going to become the “argument of design.” In the beginning of the eighteenth century, John Ray  (1692) considered the equilibrium of nature and the adaptation of organic beings to their conditions of existence as a proof of divine wisdom, and his friend William Derham  (1713) popularized the use of the word in an argument where all the laws of the universe had been conceived (designed) by a conceiver or constructor (designer). From this conceiver were engendered the beauty, order, ingeniosity, variety, and adaptation of all the things and creatures to their various ends. The happiness of mankind and the beauty of the world implied its variety, as an example of the magnificence of the animal reign, as well as the design and wisdom of the Creator. According to Linné, the wonderful correlation of functions attributed to each particular species or element of any particular being implied that nature was a hierarchized network of functions and ends, and the contemplation of nature offered a wonderful view of its beauty, a marvelous knowledge of its laws, and the anticipation of heavenly pleasures. This “physico-theology” paved the way for a kind of “natural religion,” where the perfection and complexity of nature was considered as a proof of the power of a divine superior being; it was developed in Germany and more particularly in Great Britain, where during this period “design” had become almost a synonym for “economy of nature.” An “analogy of nature” tied together in a single concept the perfection of the laws dictated by the Deity and the perfection of the complex objects

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produced by an artisan: nature is the art of God (in the double meaning of aesthetics and engineering), had written Thomas Browne (1642), a sentence that Darwin copied later in his notebooks. The argument of design, a sentence used as soon as the beginning of the seventeenth century, had become the major demonstration of a natural religion where the perfection of the created universe was conceived by analogy with the ingeniosity of human labor. The Scottish philosopher Dugald Stewart stated that the harmony of “design” rested upon a network of analogies, and in the middle of the nineteenth century, John Stuart Mill asserted that “in many philosophical arguments, analogy and unity of design can be considered as practically synonymous expressions” (Mill, 1843: 289).

4.3 Paley: The Argument from Design In the last years of the eighteenth century, the religious power of the concept of natural religion was threatened from a theological standpoint by the reaffirmation of the impact of a revealed religion, and from a philosophical standpoint by a critique based on the uncertainty of the analogy upon which it was based. In 1809, when the theologian William Paley published his Natural Theology, he meant his work as a defense against such criticism and developed with more details the argument of the watch, which was definitely used as a substitute for the sundial of Cicero and Boyle. With the support of the Anglican establishment, he popularized the “argument from design,” which was more powerful than a whole dissertation: if you see a stone upon the land, it is natural to say that it has been there from the beginning of time. But if you see a watch, you must notice that its various and heterogeneous parts imply a purpose and are adjusted in order to produce a certain movement. The watch must have had a constructor or builder, who made it at a certain time and “designed its use.” Whatever its imperfections are, the existence of a design and a designer is obvious. It is not necessary that a machine is perfect for one to be able to see spontaneously, by common sense, what its design is. Possible dysfunctions do not imply the negation of design. If some parts are found whose function (or design) is unknown, experiments in suppressing their action will enable us to judge what the use and intention of this or that part are. No other reasoning was possible. It could not be interpreted either as a possible configuration of matter or an undefined order of matter, Paley adds, rejecting some materialist or “epicurean” theses which had been recently addressed against the physico-theological argument. Besides, the argument from design allowed us to see with closer details the physical adaptations of means to ends. We could then suppose – it could be conceived – that the watch had the power to produce another watch, exactly similar to itself; the first effect would then be the increase of our admiration for the contrivances of nature. It would be a superior reason to ascribe the existence of the watch to design and a supreme art. But this watch would not reproduce itself in the same way as a carpenter produces a chair. The argument of design would remain the same as it was in the argument of the

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watch; the following sentence is an indirect answer to Hume’s argument (see infra) of a generated world: We might possibly say, but with great latitude of expression, that a stream of water ground corn: but no latitude of expression would allow us to say, no stretch of conjecture could lead us to think, that the stream of water built the mill, though it were too ancient for us to know who the builder was by the application of an unintelligent impulse to a mechanism previously arranged, arranged independently of it, and arranged by intelligence, an effect is produced, viz. the corn is ground. The force of the stream cannot be said to be the cause or author of the effect, still less of the arrangement. Understanding and plan in the formation of the mill were not the less necessary, for any share which the water has in grinding the corn: yet is this share the same, as that which the watch would have contributed to the production of the new watch, upon the supposition assumed in the last section. Therefore, though it be now no longer probable, that the individual watch, which our observer had found, was made immediately by the hand of an artificer, yet doth not this alteration in anywise affect the inference, that an artificer had been originally employed and concerned in the production. The argument from design remains as it was. Marks of design and contrivance are no more accounted for now, than they were before … There cannot be design without a designer; contrivance without a contriver; order without choice; arrangement, without any thing capable of arranging; subserviency and relation to a purpose, without that which could intend a purpose; means suitable to an end, and executing their office, in accomplishing that end, without the end ever having been contemplated, or the means accommodated to it. (Paley, Natural Theology (1809, 10–11))

Such was, in its simplest expression, the argument of design. It applied to the contrivances of nature, which went further than those of art in their complexity. The argument went on with a closer analogy between organic beings and physical objects. Live beings, in many cases, were obviously as mechanical, adjusted to their ends, suited to their office, as the most perfect productions of human ingenuity. The eye and the telescope were both instruments, and even if the eye was an instrument which perceived while the telescope did not, such circumstances did not modify the analogy of nature.

4.4 Hume: The Analogy of Nature Criticized If Paley relied on the continuity between the human mind and the divine spirit, and between artifacts and organic beings, Hume, on the contrary, stressed the discontinuity between secondary causes and the final cause. Where Paley maintained that there existed a close analogy between the products of human intelligence and those of the divine creation, Hume considered this analogy as very loose and rather unconvincing. In his Dialogues Concerning Natural Religion – published only after his death – Hume wrote a dialogue between a believer in revealed religion, a follower of natural religion, and a skeptic, who obviously bore his own colors. The argument from design was first summarized as follows: the adaptations of means to ends in nature were very close (if not identical) to the contrivances of human design. It should be concluded that in nature as well as human design, there could not be any design without a Designer.

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The skeptic Philo answered that analogy depended on the degree of similitude of the various cases envisaged and its power on the number of differences between the compared cases: when seeing a house, we spontaneously supposed the existence of an architect, but the similitudes between the universe and a house did not constitute a perfect analogy. Even if we supposed that the world was a perfect production, it was not at all certain that the excellence of this world could be attributed to a craftsman. Many worlds could have been created, rudimentary or imperfect, with a progressive improvement in time of the art of building worlds. The idea that this world was similar to a machine and was ruled by Design was not more convincing than the idea that it was too unperfect to be attributed to a benevolent God, all powerful and intelligent. You could as well and convincingly imagine a world created by various designers, or by a small inferior and incompetent God, or by a suicidal God, or a corporeal God, or even a world engendered sexually by a male and a female. All these analogies were as plausible and hypothetical as the argument of design. Of course, the work of nature presented a strong analogy with that of the artificer, so that the causes presented a sort of analogy of proportion. But it looked more convincingly like an animal or a vegetable than like a watch or a weaving loom. It could as easily and perhaps  better have been generated. Important differences between art and nature implied a proportional difference between causes. The argument of design was not more probable than many other hypotheses.

4.5 Kant: A Necessary Analogy, but Without Foundations In his Critique of Pure Reason, Kant had asserted that our understanding imposed certain modes of thought to the sensation-perception, which formed the structural traits necessary for our experience of the world. The mind itself added the forms and organizing categories. But in his Critique of Judgment (Urteilskraft), he maintained that such categories necessary to the understanding of the world were not sufficient to explain the phenomena of life. It was necessary in this case to postulate a design, that is, an intellectual archetype which coordinated the principles of the organic beings. Whereas mechanical causality could imply that a cause produced an effect, in biology, the first steps could only have a meaning in relation to the final stages, so that it was impossible to reject the final causes. Our judgments on biological organization were thus analogous to our feeling of beauty. Teleology could not be eliminated from the field of biology, because doing so would mean to neglect one of its very objects. To call an object “purposive” (Zweckmässig) was to think as if a concept had guided his production. Kant did not attribute to the teleological functions the same logical status as that of the categories of the understanding in the construction of scientific experience. It was necessary to consider the morphology of live beings as if they had been created by an intelligent creator according to an archetype, but in the same time it was necessary to suppose that this idea has no foundations in experience. The ultimate

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noumenal reality remained hidden to the scientific understanding, which could only rely on an analogy of proportion. The analogy of design did not imply a real similarity between an organic being and any machine, but simply a link between living beings and a work of art. What mattered was not the real existence of structures “designed” in aesthetics or in nature, but the particular orientation of our knowledge when we considered something “purposive” (zweckmässig, which could be translated by designed). The ruling principles were prescriptions which we gave to ourselves and not to the things themselves as the best way to reach the objects of experience. They were by no means transcendental and could be revealed as false in a later time.

4.6 Decline and Revival of Design The controversies about the meaning of design – close or loose analogy, necessary or useless  – gradually involved, toward the beginning of the nineteenth century, debates between functionalists and morphologists on the opposition between “function” and “structure” (or form), and the word “design” sometimes came to disappear and be replaced by either “form” or “function.” In all his works, Darwin had mentioned “design” with a radical hostility; he considered the idea of Design as a dangerous reintroduction of finality in evolution. Even though he considered that some progress was at work in nature, this progress could not be explained by teleological reasonings, and certainly did not imply a regular law. If natural selection had a positive role and could be considered as active, its action could be compared to the action of the waves sculpting blindly a cliff. Natural selection did not imply in itself either progress or development and could theoretically be as well applied to cases of simplification or degeneracy. Some developments of the synthetic theory of evolution in the twentieth century led nevertheless some biologists or philosophers to consider that natural selection detained a power which Darwin did not envisage, so that paradoxically natural selection came to mean for them the equivalent of a Design, a term and a concept violently rejected by the inventor of theory. The argument of Design came again to the fore in the 1980s under the form of a blind watchmaker, good design tending toward perfection, but without a designer or Design (with a capital D).

4.7 Dawkins In The Blind Watchmaker, Dawkins considered an all-powerful natural selection endowed with a capacity bordering on perfection. The complexity of the Design of organic beings gave the key of the history of human beings, similar to the complexity of a computer producing more and more complex unintentional results (Good Design): Darwin had understood that complex design emerged from the original

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simplicity. Biology was the study of complex objects which seemed to have been conceived (designed) with a precise goal, and therefore the complex objects produced by man should belong to the same field of research. In the same way as Paley, Dawkins substituted the relationship living beings/ artifacts for the opposition complex/simple. Machines derived their complexity and their design from the living beings who had produced them: to find them on a heath as Paley had figured a watch was an obvious proof of the existence of life on Earth (Dawkins, 1984: 16). The question “what is the origin of life” was substituted for “why do complex objects exist.” The answer was that they were the fruit of a design, just as it was with the argument of Paley, with the difference that natural selection, source of this design, was a blind automatic process, which provided the illusion of a design advancing in a definite direction, “specified” (Dawkins, 1984: 21). Bats and radars had been designed by the same process of complexification inherent to the same idea of “Good Design.” Small changes accumulated in the same way as in a computer program. The organs were the products of a regular trajectory in the animal space, where each intermediary stage had contributed to their survival and their reproduction (91). Design was by definition “good” and “real,” and the function of any trait was expressed continuously in the animal space, even if a few imperfections survived in the final design. As a conclusion, the functional convergence imposed itself upon any structural or morphological force, inertia, or development. In other words, the dynamism of Design was on the side of function, and structure sided with conservative forces. Daniel Dennett, in Darwin’s Dangerous Idea, neglected the idea of design but added an extra turn of the screw to the paramount power of natural selection, whose impetus was irrefutable beyond the sphere of biology: it applied to the totality of the cosmos and of society. It was an algorithmic process blindly designed, extremely simple in its components, and infinitely complex in its details, progressing constantly toward an optimum. It was more than a mere order; it was the telos, the intentional exploitation of order. Environmental constraints could be reduced to mere necessary factors in space of design, so that Dennett went as far considering design and function as synonymous. “Some biologists are more careful and take care to avoid design or function in their works, while others built their career on the functional analysis of this or that… Some biologists think that one cannot speak of design without compromising with a dubious doctrine concerning progress” (Dennett, 1995; 126). George Lauder, at the same time, defined design as “the organization of the biological structure in relation with the function.”

4.8 Design and Function Today The discussions and controversies which rose in the last quarter of the century on the concept of function seemed to eliminate the very idea of design. The etiological theory initiated by Larry Wright (1973) turned toward the past and considered that

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the function of a trait was something gradually and continuously selected in the course of time. Another theory stressed on the contrary the “causal role” of functions, oriented toward the future. In the first case, where the selective history of a trait accounted for the whole function, the term design became almost useless. It became identified with function to such an extent that it disappeared in the etiological theories or remained in the vocabulary as a mere synonymous for “function.” If Dawkins had used “Design” as the pillar of his theory, the exponents of the etiological use of function did not appeal to it. The major exponent of the causal role theory, Robert Cummins (1975), uses frequently the word, but without any conceptual status, with the meaning of “form” or “structure.” The concept of “Design” came back to the fore in these controversies from the 1980 onward, when the etiological function met with practical difficulties, such as the necessity of accounting for each single detail of the constructive evolution of the trait, that is, the change in functions in the course of evolution. Design began to be used in what was called the weak etiological theories: considering the imperfections of the function of some traits and the difficulty of knowing the details of its complete history, it was possible in different ways of drawing a distinction between function and design. Allen and Bekoff  (1995), for example, gave various examples where function and design were not synonymous, advancing the idea of a “natural design” where it could be asserted that an object T was designed to do X not only if X was a biological function of T but also if T was the result of a historical process of change in structure caused by natural selection, which led to render T “more optimal” (sic) for X than the ancestral versions of T. Colin Allen added that the concept of design was more than the present utility – that is, the present function – so that “natural design” could not be reduced to a false synonymy between design and function. Philip Kitcher  (1993) admitted also the existence of many imperfections of functions and the beings produced by natural selection. It was necessary to reject the idea of optimality and admit that the function of any biological trait was “suboptimal,” remote from the adaptations of good design of Paley and Dawkins. Design was to be conceived as the virtual optimal order, and function as the suboptimal order existing through the disharmony and the perturbations, of history. Then it became possible to discern diverging conceptions of the relationship between design and function according to the power attributed to natural selection. Then theories could be expressed – or reenacted – which, rejecting the idea of “Good Design” of Paley and Dawkins, pleaded for the view of an irregular Design, which could not be defined in all its details or could even turn out to be mediocre. To identify a trait in the terms of its historical functions was not extremely important for the practice of biologists. Amundson and George Lauder (1994) maintained that it had been too hastily asserted that natural design was good without any serious mechanical evaluation of their performances. Perhaps, after all, the watch found by Paley on the land was a fake, of bad quality, incapable of showing the exact hour, and an awkward approximation of an illusory design – a supposition which David Hume would certainly have enjoyed.

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4.9 Conclusions The prodigious increase of biological knowledge has raised new questions on the various interpretations of the concept of function and more recently a possible reintroduction of a new concept of “design.” But, from a structural  – or perhaps morphological – point of view, it appears that the three types of theoretical position expressed at the turn of the eighteenth and nineteenth century, by Paley, Hume, and Kant, are not extremely remote from the contemporary assertions on the relationship between design and function. Paley’s conception would be very close to Dawkins’s and so would be the “strong” etiological position, in which natural selection can be considered as playing the part of design, gradual accumulation with continuous optimization, the very structure of Paley’s argument being unmodified by the substitution of the Divine watchmaker for by a blind natural selection. The rejection of any form of teleology in the concept of function could be found in the dispositional conception of function (Cummins, 1975), and also among many biologists and philosophers of biology closer to morphological studies or more cautious as regards what they consider as a form of finality. And at last the idea that the metaphorical or analogical use of the term function can be considered as necessary but does not really correspond to a positive form of knowledge belongs to the common sense of many biologists or philosophers of biology. A wide range of interpretations of the word Design can then be displayed in the field drawn by these three orientations, according to an assumed meaning of Design as a term presently used at large in the vocabulary or as a concept, according either to an assumed form of perfection or ideal of perfection or a chance or even very imperfect “bricolage,” sometimes far remote from perfection, either planned or haphazardly improvised. It depended finally on the various possible conceptions of continuity or discontinuity, resemblance or difference. An appeal to design as a concept is thus shown to reveal various implicit presuppositions and presents some danger. It may be added that in the case of analogies asserting the identity of the laws which rule organic beings and artifacts, we must admit that if every civilization has admitted an analogy more or less narrow between living beings and the tools which man produced – from the simplest bifaces to the sophisticated algorithms of our culture – only our industrial civilization was able to conceive an almost perfect harmony between macrocosm and microcosm, where the perfections of the adaptations of the living world to its conditions of existence can be read directly in the assumed perfect functionality of the machines created by man, just like some mystics saw the letters of the name of a Deity in the petals of a mysterious flower. To Dawkins, who asserted at times with certainty this identity, we can add the more complex judgment from the same author: The human mind is an inveterate analogizer. We are compulsively drawn to see meaning in slight similarities between very different processes… Darwin applied the idea of evolution in a discriminating way to living organisms changing in body form over countless generations. His successors have been tempted to see evolution in everything; in the changing

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form of the universe, in developmental ‘stages’ of human civilizations, in fashions in skirt lengths. Sometimes such analogies can be immensely fruitful, but it is easy to push analogies too far, and get overexcited by analogies that are so tenuous as to be unhelpful or even downright harmful.. The trick is to strike a balance between too much indiscriminate analogizing on the one hand, and a sterile blindness to fruitful analogies on the other. The successful scientist and the raving crank are separated by the quality of their inspirations. But I suspect that this amounts, in practice, to a difference, not so much in ability to notice analogies as in ability to reject foolish analogies and pursue helpful ones. (Dawkins, 1984:195)

References Allen, C., & Bekoff, M. (1995). Biological function, adaptation, and natural design. Philosophy of Science, 62(4), 609–622. Amundson, R., & Lauder, G. V. (1994). Function without purpose. Biology and Philosophy, 9(4), 443–469. Browne, T. (1642). Religio Medici, works, II, London, Simon Wilkins (1835). Cummins, R. (1975). Functional analysis. Journal of Philosophy, 72(November), 741–64. Dawkins, R. (1984). The blind watchmaker (2006). Penguin Books. Dennett, D. (1995). Darwin’s dangerous idea. Allan Lane. Derham, W. (1713). Physico-theology. Kessinger. Kitcher, P. (1993). Function and Design. Midwest Studies in Philosophy, 18(1), 379–397. Mill, J. S. (1843). A system of logic. Longmans, Green & Co. Paley, W. (1809). Natural theology. J. Faulder. Ray, J. (1692). The wisdom of god manifested in the works of creation. Smith. Wright, L. (1973). Functions. Philosophical Review, 82(2), 139–168.

Chapter 5

Function and Purpose: Review of the “Written Symposium” (1976–1984) Organized by the Institut de la Méthode of the Ferdinand Gonseth Association Pierre-Marie Pouget Abstract  During the 1970s, Jacques Monod’s best seller, Le hasard et la nécessité – essai sur la philosophie naturelle de la biologie moderne (Monod J, Le hasard et la nécessité: essais sur la philosophie naturelle de la biologie moderne. Éditions du Seuil, Paris, 1973), gave rise to lively debates among scientific, philosophical and theological communities on the issue of purpose. Should and could we, within biological sciences, get rid of the concept of purpose while still using that of Function? This was the question of the symposium Function and Purpose (1976–1984) held by the Institut de la Méthode of the “Ferdinand Gonseth Association”. Two views opposed each other: on the one hand, those who rejected the concept of purpose in sciences and restricted functions to their causal role and, on the other hand, those who supported the idea of a de facto purposiveness inherent to function. Our review of the symposium traces the evolution of the debate and ends by the fruitful dialog between one convinced of the purposiveness inherent to function and two Canadian scientists very reluctant to the idea of purpose in science.

Translated from French by A. de Ricqlès. P.-M. Pouget (*) Scientific and Philosophical Council of the Ferdinand Gonseth Association, Bienne, Switzerland © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_5

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5.1 Formula and Style of the “Written Symposium” The “Written Symposium” (1976–1984) organized by the Institut de la Méthode1 has marked an important stage in the life of the Ferdinand Gonseth Association (FGA).2 Before describing its context and the general views held by its participants, it seems useful to say a few things about its formula and style, which may reflect those that might be used in other similar academic exercises. Generally, the formula of the written symposium allows more in-depth discussion than an oral debate, which is necessarily improvised. It leaves time for thought and makes possible a better understanding of others’ positions and a well-supported argumentation. This is very useful when one deals with delicate problems, potentially loaded with misunderstandings. The aim is to be able to exchange ideas in complete freedom, even if they are not already ripe and well elaborated. The ideas will become more precise, thanks to the debate. Authors will have the opportunity to modify them more or less extensively at the next instalments. Contrary to a journal that offers a juxtaposition of mature texts, the written symposium promotes dialog. The reader is invited to jump in the discussion and to play a part through submitting his or her questions, critiques, remarks, objections and additional points. Authors and readers thus have the opportunity to confront their ideas and refine them and to build up their own judgement in the process. The style of the texts is amenable to every desirable change; it is that of a written discussion, close to an oral debate but retaining the advantage of offering the time to examine the proposed ideas and to build up the arguments. The symposium Fonction et Finalité is now available on the website of the Ferdinand Gonseth Association, at http://afg.logma.ch/ (direct link: http://afg. logma.ch/doc/FBFF.PDF).3 But what was its context?

 The Institut de la Méthode (IM) became in 2014 the Conseil scientifique et philosophique (CSPh).  The Ferdinand Gonseth Association was created in 1971 in Bienne (Switzerland). Its aim is to promote the work of the mathematician-philosopher Ferdinand Gonseth (1890–1975) and to continue its spirit of interdisciplinary dialog. Ferdinand Gonseth created in 1947 with Gaston Bachelard and Paul Bernays the journal Dialectica, an international review of philosophy of sciences. 3  Thanks to the care of Nicolas Peguiron, member of the CSPh, treasurer of the FGA. 1 2

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5.2 Context of the Symposium and Circumstances of Its Triggering Off I will start by emphasizing that the Institut de la Méthode had, significantly, thanks to its secretary and activity leader, the late François Bonsack,4 the ability to organize this symposium while another one was already in progress. A written symposium Quantic indeterminism and hidden variables had started in 1973 to end in 1981. During 5 years, from 1976 to 1981, the Institut de la Méthode was thus involved in two highly significant debates in the philosophy of sciences. To remind in a few words the interest stirred by the symposium Quantic indeterminism and hidden variables, I will note that internationally renowned physicists and philosophers took part in it and that it enjoyed a worldwide diffusion. For its part, the symposium Function and Purpose (515 p.) organized a dialog among 30 contributors: 15 from France, one from Belgium, one from Germany, two from Canada and 11 from Switzerland. It had addresses in Switzerland, France, Italy, Austria, Belgium, the Netherlands, Germany, England, Romania and Canada. In view of the magnitude and depth taken, right from the start, by the first symposium, one may wonder why and under what circumstances the secretary of the Institut de la Méthode did not wait until the end of the preceding symposium before launching a new one. J. Parrain-Vial, professor of philosophy at Dijon University, had organized a colloquium on comparative methodologies of sciences under the title Evolution and History. The debate collided with the issue of purpose in the evolution of living organisms. A controversy resulted between P.  Poirier (Académie des Sciences morales et politiques, Paris) and M. Delsol (professor of developmental biology at the Faculté catholique des sciences, Lyon). P. Poirier challenged the so-called synthetic theory of evolution emphasized by G.G. Simpson, while Delsol found it satisfactory for its activity of biologist. Participants of this discussion decided not to pursue it within the framework of the colloquium Evolution and History and wished that it would become the topic of a latter colloquium. It was agreed that this latter colloquium would be organized by the Institut de la Méthode of the Ferdinand Gonseth Association, somewhere in Switzerland. Taking into account that the disagreement between Poirier and Delsol was rooted in their own diverging conceptions of purpose and of function, François Bonsack proposed to prepare the colloquium through a written symposium he would organize. The proposal was accepted. Why did Bonsack take such a task when the successive deliveries of the other symposium were in full swing and already took a lot of his time? François Bonsack was seeking interdisciplinary dialog on themes dealing with fundamental issues able to have an effect upon our very concept of knowledge. In his mind, a  François Bonsack (1926–2006), PhD, physician, mathematician and physicist. His thesis in philosophy, Thermodynamique, Information, Vie et Pensée Paris: Gauthier-Villars, 1961, Paris, has been republished by Editions de l’Aire in 2000 (Bonsack, 2000). 4

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symposium on Function and Purpose was thus complementary to the one on indeterminism and hidden variables. The written symposium started in 1976. In a few months, six instalments took place, and two major positions emerged regarding the theme Function and Purpose. One was hostile to the concept of purpose, and the other thought it inseparable from the concept of function and focused the debate on the nature of the link between the two concepts. Accordingly, the colloquium that took place at Villa Rigot, the cultural University Centre of Geneva, 14 and 15 October 1977, has offered the opportunity of debates that expressed the disagreements between the two opposed parties. At the end of those 2 days, the general feeling was that the written symposium should be pursued further. It went on until 1984.

5.3 Influence of Monod on the Two Opposed Fronts in the Written Symposium and on Its Interspersing Colloquium This symposium written in the long term, interspersed by the October 1977 meeting, was pervaded by the intellectual climate of the 1970s. Regarding the issue of purpose, it was deeply influenced by Jacques Monod’s position in his book Le hasard et la nécessité: essai sur la philosophie naturelle de la biologie moderne (Monod, 1973). The controversies in all directions promoted by this book pervaded the intellectual atmosphere in the scientific, philosophical and theological communities. What granted it such a radiating power? Jacques Monod won the Nobel Prize of Physiology and Medicine in October 1965 together with his colleagues André Lwoff and François Jacob. His book was enshrined by the prestigious prize, as those of his two colleagues published in 1969 and 1970 (Lwoff, 1969; Jacob, 1970), and the three books were ones able to attract the interest of scientists, philosophers and a wide educated readership. Nevertheless, Monod’s book relegated the two other ones to a position of secondary importance. The main reason was, very likely, that it set itself apart by its somewhat adventurous attempt to extract from the most advanced and up-to-date data of molecular biology, the significance that it was meant to have for a view of human beings. The fundamental breakthroughs of this science were presented as definitively established and able to make us understand that we inexorably were the product of chance and necessity. It entailed that we were forced to exist in a world deaf to our quests and that our duty and destiny were not written anywhere. Jacques Monod’s book, through its existential dimension extracted from molecular biology, as it appeared to the reflection of the eminent scientist, resonated with some illustrious voices of the twentieth-century literature, especially the one of Albert Camus. Jacques Monod’s ideas on the methodological framework of science and the way it adapts to the study of living beings were in the air at the time of the symposium.

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Already with the first instalments, the teleonomy concept was supported by some and criticized, or openly rejected, by others. The concepts of chance and necessity were analysed, and their meanings became more subtle than in Jacques Monod’s book. As already mentioned, the symposium opposed those who excluded purpose from scientific research and those who accepted it as it related to function. For the former, intentional purpose was acknowledged at the human level but had nothing to do with the idea of function in the life sciences. For instance, the function of the heart, which is to make blood circulate in the organism, is nothing more than its causal role. Some of them restricted the legitimacy of purpose to metaphysics. Others only excluded it from the scientific realm without taking care of its legitimacy in metaphysics. For the latter, purpose was envisioned as stemming from function, understood as a selected effect because of its adaptive value. They interpreted it by reference to the theory of evolution by natural selection. They did not accept Jacques Monod’s thesis because, they said, one can observe a de facto purpose which is inherent to function. Now that the opposed views held in the written symposium as well as during the colloquium have been identified, the succeeding steps that have punctuated the symposium may be followed as a pathway from the first instalments of the symposium to the last ones. We will give a general picture of this pathway in two steps, one that preceded and prepared the colloquium and one that came after it. At the end of the first part, we will try to analyse the two preconceived philosophical views that confront each other about purpose, one for whom purpose should be excluded from science and the other one for whom it is inherent to the function concept as it is used in biological sciences.

5.4 General Overview of the Written Symposium from October 1976 to the Colloquium of October 1977 The first instalment, of 46 pages, is dated from October 1976. François Bonsack exposes and adheres to the ideas of Edmond Goblot about purpose (Goblot, 1899, 1900, 1903). He offers for discussion numerous extracts from Raymond Ruyer’s entry on purpose in Encyclopaedia Universalis (Ruyer, 1970). He also selects a series of relevant parts from Jacques Monod’s Le hasard et la nécessité in order to stir up the debate. J. Parrain-Vial, J. L. Parrot and P. Blandin also participate. It results that the four of them do not agree on the significance of the word “purpose”. To appreciate how difficult it was for them to find a common ground, one can consider, in instalment two (25 p. of December 1976), the three commentaries on J.  Parrain-Vial’s contribution: “Some thoughts on purpose”. The authors are H. Tintant (professor of palaeontology at Dijon University and strong supporter of the synthetic theory of evolution), F. Bonsack and M. Delsol. F. Bonsack expresses

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his criticism of Prof. Parrain-Vial’s position, while the two others roughly agree with her. Then, quite apart from the philosophical and scientific context of the former contributions, A. de Muralt sets in with a text entitled “Providence and Freedom”, where he supports a notion of purpose stemming from medieval theology. Finally, the instalment ends by an excerpt from Guy Cellerier’s paper “The Historical Genesis of Cybernetics: Is Teleonomy a Category of Understanding?” (Cellerier, 1976). The reader of the two first instalments will notice that the symposium, in spite of being rather unable to bring an agreement on the concept of purpose, nevertheless goes forward by trying to specify the extension of the concept. It appears that, for the symposium’s participants, this concept does not include the notion of a transcendental purpose,5 but only had to do, on the one hand, with the intentional activities of man and, on the other hand, with the non-intentional idea of function, in the lexical context where one speaks of the function of haemoglobin, the heart, the lungs, the liver, the kidneys, etc. The extension of the concept of purpose thus covers two irreducibly distinct plans, namely, the plan of the intentional order and that of the non-intentional order. Could this equivocal distinction be suppressed? In order to overcome it, François Bonsack invites participants to give a definition of purpose which is comprehensive and has a definite content, a definition that says “purpose is this or that”. He rejects the possibility of satisfying himself with a mere delimitation of the concept because, he states, one can know the concept’s extension limits only if one knows its content.6 Before it is explicitly defined, its extension will remain equivocal.7 In spite of all his efforts to reach beyond equivocity, he does not obtain the expected answer.8 That was the situation in December 1976; will it later evolve in the direction desired by Bonsack? From April to December 1977, four instalments were published: instalment 3 (42 p.) in April, instalment 4 (36 p.) in June, instalment 5 (83 p.) in August and instalment 6 (112 p.) in September. In the September instalment, Bonsack takes stock of what has been agreed upon and of the remaining divergences. He warns the reader in a few words that: summarizing in a few pages a written symposium of roughly 300 pages is a risky exercise, and even more so because about twenty authors were involved-either by original contributions or by quotations of texts already published […] I read everything again, checking the

 This is also true of the notion proposed by A. de Muralt.  Instalment 2, 4.2, Remarks about Professor Parrain-Vial’s 4.0 text. 7  Bonsack does not require that the definition be perfect from the outset but that participants would work on it, discuss it and try to apply it to the various domains where there is matter of purpose. 8  Instalment 1. 1.0, p. 4 to 33. E. Goblot and Purpose. 5 6

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subjects treated, then I tried to classify them, to put them in order. Thus I hope to have reached a balanced compromise between consistency and faithfulness.9

According to this synthesis report (instalment 6, 24.2, p.7–32), discussions circled around biology, palaeontology and evolution while also referring to intentional human purpose. They tried to delineate the scientific and philosophical domains. Regarding this latter issue, two positions collided. One insisted on distinguishing science as what answers to “how” questions and philosophy as what answers “why” questions.10 The other one emphasized continuity between science and philosophy and maintained that science was also concerned with the “why” of a purposive type, besides the “why” of a causal type that cannot be simply assimilated to the “how”.11 The second position progressively gained more and more support, in spite of the traditional reluctance of scientists regarding the purposive “why”. How could they do without it when dealing with the functions of, for instance, haemoglobin or the heart? It was specified that the relevant “why” consisted in a purely factual purposiveness (“finalité de fait”).12 This factual purposiveness did not involve consciousness or design, was independent of any intention and revealed itself as constituted by a series of causal chains. Thus, if all purposive processes could be explained causally, would it not make the quest for purpose irrelevant? At this stage, ideas bubbled up. For some, function was restricted to what an organ does, to what they called its “properties”. Biochemists supported this view, while physiologists considered it unsatisfactory. For the latter, it was essential that a function plays a role. The eye has the function of seeing: vision is included in its definition. In other words, vision is the function of the eye because its role is to see.13 To sum up, from instalment 1 of October 1976 to instalment 6 of September 1977, the debates were centred on the issue of the relationships between philosophy and the sciences. Indeed, one can grasp the nature of the disagreement about the legitimacy of the purposive “why” in scientific research, looking more closely at the preconceived views adopted by those who raise this issue and try to answer it. On the one hand, if one starts from the idea that the purposive “why” is legitimate, even indispensable, in order to discover what Prof. Parrain-Vial calls a “real” or “true” cause (4.0, instalment 1, p. 39–40), one affirms a priori that a metaphysics telling the “why” of everything is the main object of philosophy.  Instalment 6. 24.2, p. 16. Synthesis report on the six first instalments of the written symposium “Function and Purpose”. 10  In the context of the symposium, the “how” concerns the description of phenomena, whereas the “why” explains phenomena. 11  In the context of the symposium, the “why” of the causal type explains a “state B” from a “state A” by exposing in detail the process by which state A brings about state B. 12  P.  E. Pilet, physiologist, insists on factual purposiveness in “Some reflections on instalments 1–4” (Instalment 5, 19.0, pp. 49–52). 13  Under the word “role”, what physiologists had in mind is that it is not a complete synonym of function but introduces a supplementary idea: that the heart does not merely pump blood but also that it is there in order to do it (note proposed by the translator). 9

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As soon as the sciences renounce to it because of their methods, their languages and their models, it follows that philosophy’s domain becomes located beyond physics and that its vocabulary is devoid of any metrics or significance common with those of sciences, the latter being restricted to the “how” and to the description of phenomena. It belongs to philosophy to make explicit “the significance of phenomena the laws of which are determined by science” (ibid). The issue of purpose, namely, of the purposive “why”, thus brings back the issue of the significance, of the meaning of everything. It therefore has no room in scientific research. H. Tintant supports this view in a long contribution (18.0, instalment 5, pp. 25–45). M. Delsol concurs with Tintant in his remarks about Professor Parrain-Vial’s text 4.0 (4.3, instalment 2, pp. 8–9). On the other hand, if one starts with the notion that “research that takes objectivity as its aim has always been submitted to philosophical preconceptions” (E. Emery 23.0, instalment 6, p.65), the tight isolation of philosophy and sciences falls apart. One of the obvious tasks of philosophy then becomes that of making explicit the philosophical preconceptions underlying scientific research. When philosophical reflection undertakes such an effort, it will become clear that sciences do not merely describe; they also explain. For instance, if Newton’s law is certainly not the cause that explains gravity, nevertheless “localisation and amount of a mass explain intensity and direction of the gravitational field at a given place and accordingly the acceleration to which this mass will be submitted at this place” (Fr. Bonsack 4.2, instalment 2, p.5). As long as it examines scientific research, philosophy will notice that the purposive “why” is not reserved to the metaphysician. It will discover that, although sciences strive to restrict themselves to the causal “why” that explains a state “B” from a state “A”, by expressing the details of the process that drives from state “A” to state “B”, in the complex domain of life sciences, the causal “why” is not enough. Although the efforts to restrict explanations to a causal “why” have the merit of expunging from science explanations that appeal to a transcendental or cosmic purpose that no experiment could ever test, those efforts at the same time call attention to the necessity of a debate on the legitimacy of a purposive “why” in the life sciences. This written symposium, designed to prepare the oral colloquium of 14 and 15 October 1977 at Villa Rigot, had thus identified the source of the disagreement between those who excluded the purposive “why” from scientific research and those who accepted it as a purely factual purposiveness, independent of intentions and inherent to function (understood as function to circulate blood, to carry oxygen, etc.). The colloquium (22) took place without any plenary or formal talks: it had been decided that all the available time should be used for discussion.14 Sometimes blunt, the exchanges always remained within the bounds of mutual respect. The attendees expressed their desire for mutual understanding and sought to get rid of misinterpretations and to clearly formulate their arguments. Some of the arguments were ones

14

 The author (and the translator) took part to it.

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already presented in the symposium but were now exposed with the face-to-face of oral communication. At the end of those 2 days, the general agreement was that it was necessary to pursue the written symposium and this was decided.

5.5 General Overview of the Written Symposium from February 1978 to November 1984 Instalment 7 (80 p.) published in February 1978 started with the errata to instalments 1–6 (8p.). This same year, two instalments followed, one in June and another in November. An important precision on the concept of a factual purposiveness is given by Bonsack in instalment 7 (17.5–17.9) when he answers to O. Costa de Beauregard who defended the thesis of a symmetry between causality and purpose. Bonsack takes issue with this symmetry thesis and develops a scheme showing that, in spite of the appearance, a consequent in a causal chain never acts on an antecedent but instead on a later effect that it causes.15 Instalment 7 also features the radical anti-finalist position of E. Schoffenhiels: Some reflexions after the oral symposium (29.0, pp. 9–15). According to him, “it seems mandatory to stop using the words purpose and function even if one specifies ‘factual purposiveness’, etc.” (Ibid.). Responding to Schoffenhiels, J. L. Parrot asks whether the “anti-finalist” position is not untenable with respect to the biological realm (29.1, pp. 15–22). In instalment 8 (97 p.), François Morel puts forward the thesis that “function and purpose are relatively trivial properties of information” (38.0). Bonsack acknowledges “the very suggestive intervention of F. Morel” (38.1), namely, that “a function just is information that has proven successful”.16 Bonsack responds that he would rather say, to the contrary, that “without functional success, no information”,

 This fact, namely, that the consequent never acts on the antecedent, according to the thesis supported by Bonsack all along the symposium, “appears most clearly in the Darwinian view of reproduction. Selection never acts on the genome that has produced it […], Environment and selection act on the finished individual, built according to the program. They directly act on its phenotype, but reach through it the genome of its offspring, that it itself carries and that is linked to its own destiny. We touch here the fundamental role of reproduction in the Darwinian scheme, that is also the one of the ‘Synthetic’ Theory” (Instalment 6, 22.0, September 1977, p.  60). “For me, ‘reproduction depending of the result’ is the essential feature of purpose” (40.0, instalment 10, April 1979 p. 8). “The finalized action consists more essentially in the reproduction of the past than in the anticipation of the future” (40.2, instalment 11, August 1980, p. 16). Bonsack includes intentional purpose in this Darwinian scheme, focusing on the reproduction of the past that has been successful. 16  It is suggestive in that it introduces the idea of a possible link between function and information that the symposium had not considered so far. 15

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because the structures we are dealing with “have precisely the specificity that they work” (38.3 instalment 8, June 1978). In instalment 9 (45 p.) of November 1979 (4.6), Prof. J. Parrain-Vial (4.5) modifies her view. In the process of the debates, her distinction between science that describes and philosophy that explains becomes more ambivalent. Science also explains, but the purposive “why” still does not concern it and remains the domain of philosophy. Bonsack retorts that “man is in one piece, he can mobilize science in his aim to answer philosophical questions, and perhaps even metaphysical ones. On the other hand he can think philosophically about sciences - and every scientist does it, to a certain degree, even if he denies it”. Starting with instalment 10 (25 p.) of April 1979, Bonsack, convinced champion of the legitimacy of the purposive “why” in biological sciences,17 debates with the tandem Réjane Bernier-Paul Pirlot, co-authors of a book (Bernier & Pirlot, 1977) in which they reject the concept of purpose in the biological sciences (39.3, instalment 10, April 1979). Their written exchanges last up to 1981 and unfold in ten texts: 40.1 and 40.2, instalment 11 (17 p.), August 1980, and 40.3, 40.4, 40.5, 40.6, 40.7–9 and 40.10, instalment 12 (75p.), December 1981. A special attention is paid to the precision of the words used, and, in order to avoid misunderstandings, words or locutions to which attendees give different meanings are defined immediately when introduced. Thus, Paul Pirlot, speaking to François Bonsack, notes that “your usefulness having a raison d’être is what we [Bernier and Pirlot] call an adaptation that allows survival and descent” (40.9, instalment 12). Pirlot concludes: “thus I think that, on the whole, we are in large agreement, even if we do not use the same words or the same concepts for the same things” (Ibid). Indeed, for Bonsack, a mutation, when it appears, has no purpose, even if it is favourable, and it acquires a status of factual purposiveness only when it has been reproduced and has done so because it proved favourable. The symposium, regarding its main theme, ended on this confrontation between a position that accepts a factual purposiveness and a position that acknowledges functions, for instance, that of haemoglobin, without any appeal to purpose. For Réjane Bernier and Paul Pirlot, the concept of purpose carries an anthropomorphic load and cannot be accepted in science. But, ultimately, they may meet François Bonsack’s position, which reduces purpose to the reproduction of the favourable mutation.18 The remaining disagreements will fuel the discussion with the diversity necessary for a progressive evolution of research. The last instalment, the 13th (41p.), was published in November 1984. I. Schüssler, professor of philosophy at Lausanne University, contributes a 23-page text derived from a lecture she had delivered on “The problem of organic nature in Kant’s Critique of Judgment”. The discussion between Bonsack and Professor

 This purposive “why” being restricted to the reproduction of favourable mutations that are favourable to survival and reproduction. 18  It is assumed here that reproduction implies selection, according to the following scheme: mutation-selection-reproduction. 17

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Schüssler (41.1–42.3, pp. 24–41) has no direct bearing on the issue of purposiveness as it was discussed in the symposium and offers a final point to it.

5.6 Conclusion and General Overview The above summary indicates that theme of the written symposium was in fact Function and Purpose, not Purpose and Function. The use of the word function in biological sciences raises problems because of its semantic linkage with that of purpose. The debates made progress through making more precise the significance of those concepts in well-defined contexts. The analyses conducted have led participants, first, to clearly reduce the notion of purpose to a factual purposiveness, independent of intentions, and, next, to discuss the question of whether purpose so conceived was inherent or not to the notion of function. As we have seen, two attitudes emerged: one that excluded purpose from the sciences and one that conceived it as intrinsically linked to function. Some anti-finalist participants claimed to reduce function to mere ability, to what an organ does. But most accepted the scientific legitimacy of functions, in the sense of function of..., including those who excluded the notion of factual purposiveness from scientific methodology. Only a minority of anti-finalist participants were satisfied to deal only with abilities, i.e. what an organ does, arguing that the notion of function is useless and too contaminated by the idea of purpose, and what they saw as its unavoidably associated anthropomorphism. The most elaborate discussions of the concept of function took place in instalments 10, 11 and especially 12 between the Bernier-Pirlot tandem and François Bonsack. Taking into account the situation of the time about the concept of function, the debate occasionally refers to the then recent works of Robert Cummins (1975), John Canfield (1963), Hugh Lehman (1965) and Ernst Nagel (1977) but mostly to set itself apart from them. Réjane Bernier and Paul Pirlot emphasized the significance of the molecular level and even spoke of functions at the biochemical level, without which there would hardly be anything to select. Accordingly, function may be defined as what an element does, or what it can do. The views of Bernier and Pirlot nevertheless also referred to the past, to history. In this respect, they got closer to Larry Wright’s (1973) etiological theory now also known as the selected effect theory. Through this Darwinian prism, a fruitful dialog has grown between the duo Bernier-Pirlot and François Bonsack. With its ongoing disagreements, the written symposium Fonction et Finalité has retained an unfinished flavour, the mark of work in the making, which requires revision and improvement and which can be read again with interest, decades later, in the light of more advanced treatments of the topic. It is thus a milestone in the long history of discussions of the concept of function and its problematic relationship with that of purpose.

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References Bernier, R., & Pirlot, P. (1977). Organe et fonction: essai de biophilosophie. Maloine-Doin, Edisem. Bonsack, F. (2000). Information, thermodynamique, vie et pensée: esquisse d’une théorie générale des complexions. Gauthier-Villars. New edition, Editions de l’Aire. Canfield, J. (1963). Teleological explanation in biology. British Journal for the Philosophy of Science, 14, 285–295. Cellerier, G. (1976). La genèse historique de la cybernétique ou la téléonomie est-elle une catégorie de l’entendement ? Revue européenne de sciences sociales et Cahier Wilfredo Pareto, 14, 273–290. Cummins, R. C. (1975). Functional analysis. Journal of Philosophy, 72, 741–764. Goblot, E. (1899). Fonction et finalité. Revue Philosophique de la France Et de l’Etranger 47: 495–505; 632–645. Goblot, E. (1900). La finalité sans intelligence. Revue de Métaphysique et de Morale, 8, 393–406. Goblot, E. (1903). La finalité en biologie. Revue Philosophique de la France Et de l’Etranger, 58, 366–381. Jacob, F. (1970). La logique du vivant. Gallimard. Lehman, H. (1965). Functional explanation in biology. Philosophy of Science, 32, 1–20. Lwoff, A. (1969). L’ordre biologique: Une synthèse magistrale des mécanismes de la vie. Robert Laffont. Monod, J. (1973). Le hasard et la nécessité: essais sur la philosophie naturelle de la biologie moderne. Éditions du Seuil. Nagel, E. (1977). Teleology revisited. Journal of Philosophy, 74, 261–301. Ruyer, R. (1970). Finalité. Encyclopedia Universalis. Wright, L. (1973). Functions. Philosophical Review, 82, 139–168.

Part II

Function, Selection, Adaptation

Chapter 6

How Are Traits Typed for the Purpose of Ascribing Functions to Them? Karen Neander

Abstract  Most theories of function ascribe biological functions to token traits on the basis of their being traits of a certain type. This raises a circularity concern, given that, traditionally, biological traits are thought to be typed by their functions. This chapter discusses this circularity problem, primarily as a problem for etiological theories of function. Drawing on a proposal made in earlier works by herself and with Alex Rosenberg, Karen Neander suggests and defends an answer to the question of how traits should be typed for the purpose of ascribing them functions. She argues that, although many trait categories are functional-homologous categories that are partly sensitive to distinctions of function (and not strictly based on distinctions in lineage), this generates no vicious circularity. By locating a trait in a lineage that is parsed at those junctures where there are relevant changes in the direction of selection, one can at once determine its function and classify it with respect to a functional-­homologous classification. She shows how this proposal handles vestigial traits and exaptations, and how it helps with Robert Cummins’ worries about gradual selection and trait fixation.

Karen Neander died in May 2020 and had provided a finalized version of the text of the paper in 2019. The abstract was by the editors, and they and Mark Gersovitz supervised the final typesetting. Please address any queries to Mark Gersovitz, executor of the estate of Karen Neander. K. Neander (*) (deceased) Duke University, Durham, NC, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_6

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6.1 The General Circularity Problem At a first pass, etiological theories of biological function tell us that the function of a token trait is what traits of the type were selected for, but what types are relevant? Or, to ask the question in another way, how are traits typed for the purpose of ascribing functions to them? The details of etiological theories vary, but let’s refine the main idea a bit by proposing that the ‘innate’ biological function of a token trait is what traits of the type did in the past that, (i) was adaptive for the organisms that possessed a trait of the type and, (ii) as a result caused that type of trait to be selected by natural selection.1 One advantage of this account is how well it seems to allow for the function/ dysfunction distinction. Token traits can malfunction because they can lack the capacity to do what traits of the type were selected to do. Note that phylogenetic natural selection selects types, not tokens. Token traits (e.g., my heart or yours) come into and go out of existence, and contribute (or don’t) to the survival and reproduction of the individuals who have them, who also go in and out of existence. However, tokens do not increase or decrease proportionally in a population. Thus, there is selection of types, rather than of tokens, and it is only by virtue of being of a type that a token can have a function of this kind. Clearly, the question arises, how are traits typed for this purpose? Traditionally, biological traits were thought to be classified by their functions, but it is easy to see how a concern over circularity in that case arises. One suggestion is that, for these purposes, traits are classified by historical homology or, to use Millikan’s (1984) expression, by ‘reproductive families’. In other words, the suggestion is that token traits are linked to other traits of the same type by relations of replication or inheritance. This seems right, but is it the full answer? Consider the category of avian forelimbs. It is a homologous type, a reproductive family, and a lineage of traits linked together by relations of replication or inheritance. Yet the category seems too coarse-grained for the purpose, given that avian forelimbs have diverse functions. Some have the function of flight (and more specifically of soaring, hovering, and stroking), while others have the function of assisting in underwater swimming. Wings for flight can also have other functions, such as in food-begging, mating, and intimidation displays. In yet other cases, some parts of the reproductive family have long been selected for nothing, beyond benign reduction (to limit wasting resources and risk of disease). This seems to be the case with the vestigial wings of emus. In short, avian forelimbs cannot be treated as an undifferentiated lump for the purpose of ascribing functions to them. Those who support etiological theories of function sometimes maintain that traits can be classified, not only by relations of homology, but also on the basis of

 The requirement that the trait have been selected because it was adaptive for the individual is a feature of Godfrey-Smith’s (1994) modern history version of the etiological theory, which is discussed later. By an ‘innate’ biological function, I mean one derived primarily from phylogenetic natural selection, rather than other processes of selection (e.g., neural or intentional selection). 1

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their function. Indeed, Neander (2002) and Rosenberg and Neander (2009) argue that many trait categories are based on both function and homology. These functional-­homologous categories are not purely analogous categories, to which traits belong purely on the basis of their shared function (e.g., the category of wings for flight, which includes the wings of bats, many birds, and insects). Nor are these categories purely homologous, at least in a broad historical sense of ‘homology’, which does not require any shared function (e.g., the category of vertebrate forelimbs, which includes the front legs of horses, our own arms, an eagle’s wings, and a penguin’s flippers). Functional-homologous categories are sensitive to distinctions in both function and lineage. The suggestion made by Neander and Rosenberg was not offered in answer to the question asked in the title of this paper, but could it serve as an answer to it? On the face of it, not well. The suggestion that we use functional-homologous categories for the purpose of ascribing functions to token traits still seems circular (cf., Davies, 2001; Griffiths, 2007). If we need to first classify traits for the purpose of ascribing functions to them, we will need to do so without first sneaking a peek at these functions.2 This paper discusses this circularity problem, primarily as a problem for etiological theories of function. However, other theories of function also face this problem. Almost all theories of function ascribe biological functions to token traits by virtue of their being traits of a certain type. This is largely motivated by the need to allow for the possibility of malfunction. For example, Boorse’s (2002) biostatistical theory tells us that the normal function of a trait is what ‘it’ typically contributes to the survival and reproduction of organisms in the relevant reference class. The ‘it’ refers to types and not tokens. Boorse’s view is that malfunctioning traits cannot contribute what normal traits of the type typically contribute. There are two classificatory issues here. One is how to delineate the relevant reference class of organisms. Boorse at one point (in his 1977) suggests that it comprises an age group of a sex of a species. The other is how to type the traits, so that we can determine what traits of the relevant type typically contribute to these organisms. Cummins’ (1975) causal-role account might at first glance seem to avoid this problem, since it does not overtly appeal to types of traits (in its original form). However, it is at best underdeveloped with regard to how malfunction is to be handled. We are told that the function of a component, C, of a containing system, S, is to Z, in virtue of C’s capacity to contribute Z-ing to a complexly achieved capacity Z* of S, when Z* is under (what would now be called a ‘mechanistic’) analysis. We are not told whether ‘C’ stands for types or tokens. But, if this account is to allow for the function/dysfunction distinction, ‘C’ needs to stand for types of traits—Cs. If C were a token, the account would preclude the possibility of its malfunctioning, because it would then require, of some token, C, that it have the capacity to Z  I use the term ‘trait’ generically, to refer to heritable characters, processes, or phenotypic features. Our hearts are traits, as is their pumping. The wings of birds are traits, as are their elongated humeri and the flight stroke that birds employ. I also use ‘type’ and ‘kind’ interchangeably, without any commitment to the claim that the latter figure in special laws of nature, sensu stricto. 2

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(in order for it to have the function to Z) and yet lack the capacity to Z (if it were to malfunction with regard to Z-ing). Were ‘C’ to be read as standing for ‘Cs’, there would be room for malfunction. For, in that case, the normal function of a trait could be (say) a typical or characteristic capacity of C-type traits, and a given token could lack this capacity. Of course, this brings us back to the same prima facie circularity problem. We need to know how to categorize something as a C-type component in order to know the typical or characteristic capacity of Cs.3 The question posed in the title of this paper inverts what was once a more familiar question, which asked whether (and in what ways, or in what cases) the functions of traits are used to classify them. That led to the discussion of whether functional categories in biology are always analogous, and whether there are any scientifically significant analogous categories (Amundson & Lauder, 1994; Griffiths, 1994). Neander (2002) and Rosenberg and Neander (2009) argue that some scientifically significant categories are not merely analogous, but are demarcated by malfunction-­ permitting functions as well as other criteria (e.g., morphological or homological criteria). In any event, this paper focuses on the flip side of this question. Its focus is on what role trait classification plays in determining functions, rather than what role functions play in classifying traits. Of course, the responses we favor to the one may limit our options for the other. My plan in the sections that follow is to explain how the proposal made in Neander (2002) and Rosenberg and Neander (2009)—regarding functionalhomologous categories—fits with an adequate treatment of the circularity problem. My key claim is that traits do not need to be typed prior to ascribing functions to them, and that traits need to be located in a lineage that is parsed at those places where there are relevant changes in the direction of selection. I argue that function ascriptions can go hand in hand with trait classification, and there is no vicious circularity. In developing this, I further develop the problem with vestigial traits and exaptations in mind (in Sect. 6.2), and then describe several strategies for handling these kinds of cases, including the strategy I propose (in Sect. 6.3), and finally I explain how I believe this helps with Cummins’ (2002) worries about gradual selection and trait fixation (in Sect. 6.4).

6.2 Vestigial Traits, Exaptations, and the Etiological Theory Vestigial traits and some exaptations present the same kind of problem for the etiological theory of functions. A purely vestigial trait is one that has lost all function.4 An emu’s wings, for example, are thought to be purely vestigial. The term  When pressed in person (in 2002, when we were colleagues at UC Davis) Cummins opted for a statistical account to accommodate malfunction, but this was an ‘off the cuff’ reply, and not one to which he was committed. 4  This is a different kind of ‘loss of function’ than that to which physiologists refer when they speak of a token trait losing its function due to malfunction. In that case, we can distinguish among the 3

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‘vestigial’ can, however, be used in a relative sense. A penguin’s flippers are vestigial with regard to flight, but not with regard to underwater swimming. So, what counts as vestigial, and as an exaptation, could overlap. As Gould and Vrba (1982) use ‘exaptation’, there are different kinds. Sometimes they use the term for items for which there has been no selection at all, but which result from selection for other things (so-called piggyback traits, which hitch a free ride). But sometimes they use it for items that have been to some extent modified, or at least maintained by selection for their new use. Spandrels serve as a metaphor. In cathedrals, spandrels are the triangular spaces above where two arches meet. Initially, the intentional inclusion of arches for the purpose of support resulted in spandrels that also—merely fortuitously (we may suppose)—happened to be useful for other purposes (e.g., decorative and educative). They can be filled with paintings, mosaics, or (once material and architectural constraints permit) colored glass. Later, a cathedral might have been designed in part with these uses in mind. For example, the desire for beautiful spandrels could affect the placement and proportions of the arches. In principle, once concrete and steel made the supporting role of arches optional, an architect could include arches in order to produce spandrels. Extrapolating from this metaphor, biological exaptations could be pure side effects of selection for other things, or they could be modified and/or maintained by selection for the use for which they were co-opted. Gould and Vrba mention feathers as an example of an important exaptation, because feathers first evolved for thermoregulation, and were only later used for flight. Of course, flight feathers have been heavily modified and maintained for flight. An eagle won’t get far using downy feathers alone. Such exaptations are more the rule than the exception. Natural selection perpetually retools old tools for new uses, and any theory of functions that cannot handle such changes in function in a lineage of traits over time is in dire trouble. My interest here is in such losses of function and changes in function over time. Thus it is in vestigial traits, in the absolute and relative senses, as well as in traits exapted for new uses and then selected, and so maintained with or without modification, for these uses. I leave aside adaptive effects for which there has been no selection. According to an etiological theory, these are not functions, and so we need not worry about them, at any rate when we are worrying about how traits are typed for the purpose of ascribing functions. The penguin’s flippers and emu’s vestigial wings have both lost the function of flight, and present much the same problem in virtue of this. It is not clear how the etiological theory can best deliver the right result. How can a lineage of traits lose a function if the function depends on past selection, given that the past does not disappear as the future unfolds? As outlined in the introduction, the theory says (roughly) various incapacities of the particular trait in question. Some are and some are not relevant to its malfunctioning: Muriel’s collapsed lung does not count as malfunctioning by virtue of its inability to digest cellulose, but by virtue of its inability to absorb oxygen and expel carbon dioxide, since these are, despite its malfunctioning, its normal functions. There is a sense in which Muriel’s collapsed lung still has the function to do these latter things, although it has lost the ability to do them.

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that a trait’s function depends on what ancestral traits of the type did that was adaptive and that, as a result, caused traits of the type to be selected. But what type is relevant? Suppose we say that the relevant type is vertebrate forelimbs. This delivers a mixed verdict, since some ancestral vertebrate forelimbs assisted in flight, to adaptive effect, which caused them to be selected, but others did not. Of course, there can be indeterminate cases, but these are not such cases. Quite unequivocally, penguin and emu forelimbs do not have the function of flight, and do not malfunction by virtue of being unable to assist in flight.

6.3 Strategies for Dealing with Loss of Functions and Changes in Functions in a Lineage There are several strategies to consider. We might reply that the category of vertebrate forelimbs, or avian forelimbs, is just too broad. A penguin’s flippers, an emu’s vestigial little stumps, and an eagle’s soaring wings, can be considered different traits. This is true. But they can also be considered as belonging to the same type of trait, depending on how we type them. So the question is, what justifies choosing the less inclusive over the more inclusive type? To reiterate the problem, if we must look at the function of an item to decide which trait type to use, in determining the function of that item, we have a circularity problem. Another strategy is to require ongoing usefulness, or at least ongoing performance of the function. Ayala (1970) and Wright (1976) do this. Wright (1976) suggests that X has the function to Z if and only if (i) X does Z, and (ii) X is there (where it is and of the form that it is) because it does Z. He tells us that his formula is ‘tenseless’. Although it is expressed in the present tense, it is not necessarily to be interpreted in the present tense. Requirement (ii) is to be read, in effect, as saying that X is there because it does, did, or will do Z, depending on the details of the case. (The past tense is appropriate when natural selection is responsible for the ‘consequence etiology’, adverted to in requirement (ii), but other processes, such as intentional selection, can also be responsible for it, on Wright’s account.) Wright hopes that requirement (i) handles the problem of vestigiality, and it is hard to see how it can do that unless we take its use of the present tense somewhat seriously. Naturally, the present will need to be an expansive one. In the case of innate functions that depend on phylogenetic natural selection, it cannot be contained within the bounds of a single second, or a single summer, or even a single generation. Even so, this solution to the problem of vestigial loss of function comes at a cost, because one of the advantages of a pure etiological theory (Neander, 1983), which requires neither present performance, nor present usefulness, is that it does not preclude widespread dysfunction, or widespread maladaptive normal functioning.5

 Peter Schwartz’s (2002) ‘continuing usefulness’ proposal is a relative of Wright’s. Although its handling of these issues is more sophisticated, it seems to me to have related problems. 5

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Another influential and closely related strategy is proposed by Godfrey-Smith (1994), who suggests that (etiological-style) functions are “dispositions or effects a trait has which explain the recent maintenance of the trait under natural selection” (344). He took this to be the implicit view of those supporting etiological theories at the time. I will treat this as a variation on Wright’s requirement (ii), rather than a resurrection of Wright’s requirement (i). Notice that Godfrey Smith’s proposal doubly restricts the relevant selection. It says that it must be recent and maintenance selection. Let’s consider the idea that the relevant selection needs to be maintenance selection. I take it that the contrast here is with directional or originating selection, which takes a trait toward fixation, or to a distribution-sensitive equilibrium. In contrast, maintenance selection keeps a trait at fixation, or at a distribution-sensitive equilibrium, by eliminating alterations that arise. Some maintenance selection is ancient, and some recent selection is directional or originating, and so these are separate requirements. For example, wings able to assist in flight have been maintained in many lineages for at least 150  million years, but strong directional selection for lactase persistence in much of the human population is quite recent. Godfrey-Smith notes that what counts as recent is relative to the specific token trait in question. So, if a token trait, x, belongs to a creature alive at a given time t (say, a million years ago), the selection relevant to x’s function is recent relative to t (a million years ago). I see no reason to think that recent directional or originating selection cannot ground functions. I’ll give an example to illustrate the point in a moment, but by way of background note that it is a common mistake (not, of course, one that Godfrey-Smith makes) to think that human evolution has more or less ground to a halt, owing to our ability to control our environment. Against this, Hawks et al. (2007) argue that the rate of generation of positively selected genes in the human population has accelerated about a hundredfold during the past 40,000 years, initially due to agriculture, and then to industrialization. These dramatically altered the environment to which our genes were exposed, and also ushered in a tremendous expansion in the human population, which in turn increased the number of mutations available for selection or rejection. One of the best known and best studied of the traits under current directional selection is the lactase persistence allele most commonly responsible for the ability to digest lactose in human adults in Central and Northern Europe. It is thought to have spread rapidly since Roman times, and appears to be under strong selection. It is now at over 90% in Central and Northern Europe, although its prevalence is lower in Southern and Eastern Europe, and it is much lower still in other parts of the world (Burger et al., 2007). There appears to be recent strong directional selection for the digestion of lactose in adults, and for the year-round access to protein and calcium and other nutrients that this provides them. Selection has rapidly and recently driven the trait toward fixation in some populations. Maintenance selection, assuming it is to be understood as the elimination of deleterious fresh mutations by natural selection, might occur alongside directional or originating selection. So my claim is not that there is no maintenance selection of lactase persistence, while it is under strong directional selection. What I’m claiming

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is that there is no reason to privilege recent maintenance selection over recent directional selection, with regard to function ascriptions. Either can justify the claim that lactase persistence has the function of enabling adult digestion of lactose in those with the right ancestry. We have no good motivation for denying this. The requirement that the selection be recent is vague, and Godfrey-Smith anticipates the complaint and responds by saying that, “[t]he answer is not in terms of a fixed time—a week, or a thousand years. Relevance fades. Episodes of selection become increasingly irrelevant to an assignment of functions at some time, the further away we get” (356). Certainly, there is no fixed time that applies across the board, but I don’t think that relevance just fades with time. My concern is not that recency is a vague notion. Rather, I think that, in effect, we parse a history of selection, using changes in the direction of selection to do so. To illustrate what I have in mind, imagine, if you will, two species: the Seamites, who live in the sea, and the Streamites, who diverged from the Seamites after spreading upstream. Suppose, as well, that one mechanism that makes it possible for the Streamites to flourish in fresh water is a mechanism, x2, which derives with modification from an ancestral Seamite mechanism, x1. The latter excretes salt, while the former (the Streamites’ mechanism, x2) retains salt. If we focus only on the Seamites, it seems good enough to say that the relevance of past selection fades with time. However, if we focus on the Streamites, a different possibility suggests itself. Remember that the Streamites have budded off from the Seamites, and so the two species have the same ancestral population up to the time tf, when their lineages fork. Of course, the history of selection that pertains to the homolog—x1/x2— is also shared until then. So, if today’s Seamite mechanism (x1) has the function to expel salt, while the Streamite’s mechanism (x2) has the function to retain it, this must be despite their having equally recent maintenance selection for expelling it until tf. Of course, x1 has even more recent selection for expelling it, and x2 has even more recent selection for retaining it. But this type of example suggests to me that the relevance of past selection doesn’t merely fade with time. The change in the direction of selection in the x2 lineage seems to affect the relevance of selection prior to tf. If the relevance of selection in a lineage of homologs were to just fade with time, we’d be obliged to ascribe to x2s the function of retaining salt and expelling it. Maybe we could maintain that its second function is better grounded than its first, but this isn’t clearly entailed by Godfrey-Smith’s proposal. It is unclear how we are to weigh the very long history of selection for expelling salt, against the briefer but more recent history of selection for retaining it, if both are relevant to some degree. I think it is straightforward that x2 has the function of retaining salt and not expelling it, and that the long history of selection for expelling salt is rendered irrelevant by the change in the direction of selection in that lineage. Here is the intuitive idea behind my proposal. I’ll start by using intentional phenomena as an analogy. If you cease to have a goal you once formed, it being your goal doesn’t simply fade with time. If it is no longer your goal, that is because you’ve changed your mind, no matter how long ago, or how recently.

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Analogously, the relevance of past natural selection does not depend (certainly, does not just depend) on how much time has passed. It depends on whether, when, and in what ways the selection pressures operating on the lineage changed. Consider again the lineage leading to an individual Streamite’s x2. The relevance of past selection for the excretion of salt is affected by the change to selection for retaining it. In other words, the selection history can be parsed by changes in the direction of selection. More generally, whether a token trait, x, which exists at time t, has the function to Z in virtue of ancestral homologs having been selected for Z-ing at an earlier time, t−1, depends on whether and when there was a change in the direction of selection in that lineage between t−1 and t, vis-à-vis Z-ing. Of course, since such selection occurs over evolutionary timescales, there is still vagueness. Many changes in function occur gradually over vast stretches of time, which conflates the two factors I’m trying to de-conflate. But the main point is that the mere passing of time is one thing, and changes in the direction of selection during that time are another, and the second is highly significant.6 To return to the functions of penguin and emu forelimbs, neither has, to any degree at all—however negligible—the function of flight. This is not merely because selection for flight in their lineage is ancient. In both cases, past selection for flight is irrelevant because selection for flight ceased in the lineages in question. In the penguin’s case, it was replaced by selection for swimming underwater, and in the emu’s case, the relevant gene loci and developmental processes seem to have been mostly adrift, under no selection, or anyway no selection for flight (Maxwell & Larsson, 2007). How then do we type traits for the purpose of ascribing functions to them? We locate the token trait in a lineage, to which it is linked by relations of replication or inheritance, and then we consider the changes in the direction of selection in the lineage regarding the candidate function, Z-ing. We do not only ask, was there selection for Z-ing in that lineage before the token existed? In effect, we conceptually segment the lineage in line with changes in the direction of selection with regard to Z-ing. We ask if the token belongs to a segment of the lineage in which selection for Z-ing (the candidate function) had, prior to the token, taken place. In so doing, we determine its function. In so doing, we also classify it with respect to a functional-homologous classification. There is a superficial appearance of circularity, but it is not vicious. There is no Catch 22 here. One does them both together.

 I haven’t eliminated all vagueness. A cardinal displays his glorious colors to a female and wins a mate, but then flies off and is spotted by a predator. A warm coat helps a brown bear survive the winter but is burdensome in the summer heat. A capacity to store water is crucial in years of drought, but drought might only occur, on average, one year in ten. Are these hourly or yearly or longer alterations in selection pressures a problem on the present proposal? If these count as relevant changes in the direction of selection, we will derive some very odd results. However, stressing the significance of recency, or of maintenance selection, or of current performance and usefulness, is not helpful. So, to this type of worry, I think we must all respond that, when we ascribe functions, these are on too small a scale from an evolutionary perspective. 6

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6.4 Cumulative Selection and Trait Fixation Cummins’ (1975) early critique of Wright’s (1973) theory of functions is well known. His later (2002) objections to the etiological theory are different, and rely on two facts that I do not want to dispute. One is that complex adaptations, such as the mammalian heart or the wings of birds, result from cumulative selection. The other is that the genes associated with these complex adaptations long ago went to fixation. It is what follows from these facts that I dispute. Cummins claims that what follows is that, in the first place, there never was selection of hearts for circulating blood, nor selection of wings for powered flight, and, in the second place, that, even if there had been, it would have been remote and not recent, and thus a problem for Godfrey-Smith’s modern history version of the etiological theory (discussed in the previous section). Cummins claims that the etiological theory therefore cannot deliver paradigmatic functions. Obviously, Cummins is right to insist that there must be variation in order for selection to occur. But, as he sees it, in order for hearts to have been selected for circulating blood, there must once have been, contemporaneous within the same population, these alternatives—a heart that circulates blood, and an alternative (something) that does not. Along the same lines, as he sees it, in order for wings to have been selected for flight, there must have been, contemporaneous in the same population, these competing alternatives—wings that powered flight, and an alternative (other forelimbs) that did not. To be sure, this is not how hearts and wings first evolved. Cummins is right that such complex organs and limbs evolved by cumulative selection. One need not be a Darwinian Gradualist to think that most, if not all, complex adaptations evolved by selection first for one feature, and then selection for another, and then another, and so on. Modern hearts and wings evolved by means of an accumulation of incremental improvements. Cummins adds that, even if there were once a competition between winged and wingless creatures, and hearted and heartless creatures, in the same contemporaneous population, such originating selection must have taken place an immensely long time ago. So, he says, etiological theories that appeal to recent, rather than remote, selection history, would be in trouble, even if the requisite competition had occurred. Consider the case of the wing. Modern bird wings descend from other wings reaching back for at least 150 million years. One early bird is Archaeopteryx, from the Jurassic period. Some features of its skeleton suggest that it cannot have been a strong flyer, but it seems to have had some capacity for powered flight. If winged flight went to fixation at least 150 million years ago, then there has been no selection of wings for flight since then, or so Cummins seems to think. (Of course, hearts are more ancient still.) Wing design has not stood still since the Jurassic. As Cummins notes, there have been variants, and the competition among them has resulted in the selection of incremental improvements. Archaeopteryx had a flat sternum, whereas modern birds, excepting some that are flightless, have a keeled sternum to which the strong

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wing muscles attach. Archaeopteryx also lacked a modification to the wrist bone that makes the flight stroke of modern birds more rigid and powerful. In addition, modern birds that are strong flyers have hollow but strong bones, a thicker and shorter humerus, a long radius and ulna, and a fused clavicle, to mention some of the many improvements in the wing, and in other aspects of the bird’s skeletal and muscular structure, since the earliest days of avian flight. As well as selection for generic improvements to flight, there has also been much specialization. Hummingbirds can hover for long periods in one place and fly backward. Eagles can soar to great heights and swoop, catch, and heft heavy prey. The albatross, almost incredibly, can fly for hundreds (theoretically thousands) of miles without flapping its wings, using a technique known as ‘dynamic soaring’. Cummins allows that there has been relatively recent selection for some improvements and specializations in flight, but this is not (he insists) selection of wings and not for flight. Instead, it is relatively recent selection of this or that modification to the wing, for flying better, or flying more efficiently, or flying longer, or flying in a certain way. It is an interesting challenge, but the worry is overstated. Let’s take Cummins’ second point first—the lack of recent selection of wings for flight, even if it once occurred in ancient times. One missing ingredient in this attack on the etiological theory is any mention of maintenance selection. In the previous section, I argued that other selection, besides maintenance selection, is relevant. However, it cannot be stressed enough that maintenance selection is also relevant. As noted above, many alterations have occurred in the relevant lineages that are improvements or specializations, and beneficial mutations are less frequent than non-beneficial ones. The reason for this is that mutation is random, relative to whether it is beneficial to the organism, and a random change to a complexly organized and intricately co-adapted system is much more likely to do harm than good. It follows that, when there has been time for improvement and specialization, there will also have been time for degeneration, were it not for ongoing maintenance of the trait to keep it in working order. Degeneration would have resulted had there not been a persistent weeding out of variations that would have interfered with flight. Thus, contrary to Cummins’ claim, there would have been maintenance selection of wings for flight during more recent times. To vary the example, the loss of eye structure that occurs in troglobites, who spend their lives in completely dark caves, is a familiar and vivid demonstration of what can happen when selection for a capacity, such as sight, ceases. Numerous species of fish, as well as of insects, spiders, salamanders, and crustaceans, are known to have lost their eyes or eyesight after residing in caves for thousands of years. One mechanism by which regressive evolution can occur is the accumulation of neutral mutations (Nei, 2005). While sight still contributes to fitness, variants that diminish sight can be eliminated by selection for sight. But, once sight makes no positive contribution to fitness, as happens when a population takes to residing in a completely dark cave, the less well-sighted and sightless variants are not always eliminated.

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Another mechanism by which regressive evolution can occur is through positive selection for alternatives. One possibility is positive selection for less energy expensive tissue, which could account for loss of the retina, which is energetically very expensive (Protas et al., 2007). A second possibility is pleiotropy or gene linkage, in which the same genes or closely situated genes control both eye development and some other feature. In this case, once selection for sight ceases, selection operating on the other feature is no longer restrained by the need to maintain sight, with the result that the latter can easily become degraded in the process. For example, in the fish Astyanax, there is a trade-off between chemoreception and vision, so that enhancement of the former, which is adaptive for fish living in the dark, results in a reduction of the latter (Yamamoto et al., 2003). Of course, to return to the earlier examples, there are also examples of loss of flight, such as in the emu’s vestigial wings and the penguin’s flippers. As mentioned before, it is thought that an emu’s wings might be purely vestigial. Besides being tiny, in proportion to the size of this bulky bird, there appears to be much neutral variation accumulated in their structure (Maxwell & Larsson, 2007). Their wings contain far fewer muscles, even in comparison to other ratites, and these muscles are diverse in their structure, their placement, and even in whether they are present or absent in an individual. The penguin’s flipper suffered no such accumulation of neutral variation because, although selection for flight ceased in that lineage, intense selection for swimming occurred instead. Their elbow, as well as their wrist bone, is fused for an even stiffer stroke, and their wing bones are flat and broad to provide more power to their stroke through the denser medium of water. However, the result for flight is the same: absent selection for flight, the birds have become flightless. There has long ceased to be selection of wings for flight in their lineage, with a resulting loss of flight. That flight (or sight) is lost in lineages that do not maintain it is evidence of selection for flight (or sight) in those lineages that retain it. Perhaps the modern history version of the etiological theory can handle Cummins’ second line of criticism well enough, but some worry that it is at least possible that no episode of maintenance selection might occur for a long time, in a lineage in which a trait has gone to fixation. Perhaps deleterious mutations do not happen to arise, and so do not need to get weeded out. I doubt that in practice there is much to worry about here. However, the proposal I am making in this paper anyway secures the etiological theory against this (highly unlikely) contingency. It recognizes the importance of maintenance selection, but it also recognizes the importance of directional selection, and it does not require either to be recent. Nor does it require us to try to refine how recent is recent enough. Rather, it requires that, in lineages leading to wings that have the function of flight today, there has been selection of wings for flight, and since that time there has been no change in the direction of selection in that respect. If there were an absence of variation for a time, selection would have stalled for lack of variation, but this would not amount to a change in the direction of selection. What of Cummins’ claim that there never was selection of wings for flight (or of hearts for circulating blood)? Cummins seems to think that this would require wings (or hearts) to arise more or less fully formed, and not through the combination of

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this and then that modification. It is hard to see why he thinks this. In any event, even if the etiological theory required, say, flighted and flightless (and hearted and heartless) conspecifics to be contemporaneous, it is a moral certainty that they have been. Wingless chicks, or chicks with deformed wings that do not enable flight, will have been born. We do not see significant numbers of such abnormal birds, because there is such strong selection against them. (Similarly, there will have been heartless embryos, that have failed to develop and survive, for obvious reasons.) Again, this is maintenance selection against extremely deleterious variants. In short, there will have been flighted and flightless (as well as hearted and heartless) individuals in contemporaneous populations, even though wings for flight (and hearts for circulating blood) evolved through the cumulative selection of numerous incremental improvements. Is it anyway true that selection of wings for flight requires a competition between a phenotype that enables flight and one that does not? If it is granted that there has been selection for improved flight or for special ways of flying, does that not entail selection for flight of some kind? Perhaps the answer is not obvious. But if enabling flight is the candidate function (Z-ing) in question, it is a change in the direction of selection with regard to flight (in regard to Z-ing) that is relevant, on my proposal. A change in selection for doing Z one way, to doing Z another way, does not comprise a change in the direction of selection in regard to Z-ing as such. It only comprises a change in the direction of selection for doing Z one way to doing Z another way. If selection started to favor a new variant for its enabling flight with a longer stroke, over an older variant that only enabled flight with a shorter stroke, that does not constitute a change in the direction of selection with respect to flight, as such. It only constitutes a change in the direction of selection from flying with a shorter stroke to flying with a longer stroke, which in either case involves flying. Acknowledgments  My thanks to Alex Rosenberg for comments, and to those who organized and participated in the conference, “The Notion of Function: From the Life Sciences to Technology,” which was held in Paris, College de France, May 2008, at which an early version of this paper was presented. A slightly revised version was published in French as “COMMENT LES TRAITS SONT-ILS TYPÉS DANS LE BUT DE LEUR ATTRIBUER DES FONCTIONS?”, in the (2010) volume from that conference. For this English version, I have made minor changes for the sake of clarity and brevity. With apologies to those who have since contributed to this discussion, I have not altered it or updated it in the light of more recent publications.

References Amundson, R., & Lauder, G. V. (1994). Functions without purpose: The uses of causal role function in evolutionary biology. Biology and Philosophy, 9, 433–469. Ayala, F. J. (1970). Teleological explanations in evolutionary biology. Philosophy of Science, 37(1), 1–15. Boorse, C. (1977). Health as a theoretical concept. Philosophy of Science, 44(4), 542–573. Boorse, C. (2002). A rebuttal on functions. In A.  Ariew, R.  Cummins, & M.  Perlman (Eds.), Functions: New readings in the philosophy of psychology and biology (pp. 63–112). Oxford University Press.

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Burger, J., Kirchner, M., Bramanti, B., Haak, W., & Thomas, M.  G. (2007). Absence of the lactase-­persistence-associated allele in early Neolithic Europeans. Proceedings of the National Academy of Sciences, 104, 3736–3741. Cummins, R. (1975). Functional analysis. Journal of Philosophy, 72(20), 741–765. Cummins, R. (2002). Neo-teleology. In A.  Ariew, R.  Cummins, & M.  Perlman (Eds.), Functions: New readings in the philosophy of psychology and biology (pp. 157–172). Oxford University Press. Davies, P. S. (2001). Norms of nature: Naturalism and the nature of functions. MIT Press. Godfrey-Smith, P. (1994). A modern history theory of functions. Nous, 28(3), 344–362. Gould, S. J., & Vrba, E. S. (1982). Exaptation – A missing term in the science of form. Paleobiology, 8(1), 4–15. Griffiths, P. E. (1994). Cladistic classification and functional explanation. Philosophy of Science, 61(2), 206–227. Griffiths, P. E. (2007). The phenomena of homology. Biology and Philosophy, 22(5), 643–658. Hawks, J., Wang, E.  T., Cochran, G. M., Harpending, H. C., & Moyzis, R. K. (2007). Recent acceleration of human adaptive evolution. Proceedings of the National Academy of Science, 104(52), 20753–20758. Maxwell, E. E., & Larsson, H.  C. E. (2007). Osteology and myology of the wing of the Emu (Dromaius novaehollandiae), and its bearing on the evolution of vestigial structures. Journal of Morphology, 268(5), 423–441. Millikan, R. (1984). Language, thought and other biological categories. MIT. Neander, K. (1983). Abnormal psychobiology. La Trobe PhD dissertation. Neander, K. (2002). Types of traits: The importance of functional homologues. In A.  Ariew, R. Cummins, & M. Perlman (Eds.), Functions: New readings in the philosophy of psychology and biology (pp. 390–415). Oxford University Press. Nei, M. (2005). Selectionism and neutralism in molecular evolution. Molecular Biology and Evolution, 22(12), 2318–2342. Protas, M., Conrad, M., Gross, J. B., Tabin, C., & Borowsky, R. (2007). Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Current Biology, 17(5), 452–454. Rosenberg, A., & Neander, K. (2009). Are homologies (selected effect or causal role) function free? Philosophy of Science, 76(3), 307–334. Schwartz, P. (2002). The continuing usefulness account of proper functions. In A.  Ariew, R. Cummins, & M. Perlman (Eds.), Functions: New readings in the philosophy of psychology and biology (pp. 243–260). Oxford University Press. Wright, L. (1973). Functions. The Philosophical Review, 82(2), 139–168. Wright, L. (1976). Teleological explanation. University of California Press. Yamamoto, Y., Espinasa, L., Stock, D. W., & Jeffery, W. R. (2003). Development and evolution of craniofacial patterning is mediated by eye-dependent and -independent processes in the cavefish, Astyanax. Evolution & Development, 5(5), 435–446.

Chapter 7

Attribution of Functions and Levels of Organization in Biology Jean Gayon

Abstract  Biologists make liberal use of the term “function.” This is attested, in part, by the fact that they assign functions to almost all the sorts of structures and processes they study, and also by the fact that they use the word “function” in a variety of ways (e.g., when asking about “the function OF something,” or in the context of the structure/function pairing). In this chapter, we shall confront the liberality of biologists’ discourse on functions with two broad families of philosophical theory of function, namely, selective etiological theories and systemic theories. After giving a picture of the liberality of the biological discourse on function, we raise two questions. First, we examine three levels of organization for which it is problematical to attribute functions, namely, atoms and elementary molecules, organisms, and species. Although, at least in certain biological specialties, functions are attributed to these three sorts of structures, these attributions should not be taken for granted from the viewpoint of established philosophical theories. Second, we consider whether, in general, functions should be attributed to structures, or whether it is preferable to attribute them exclusively to processes; we argue in favor of the latter.

7.1 “Function”: Liberality of Biological Discourse, Parsimony of Philosophical Analysis Biologists make liberal use of the term “function,” as attested by two features of their discourse. In the first place, they assign functions to almost all the sorts of structures and processes they study. Where structures are concerned, the Translated from French by Anita Conrade. Jean Gayon 1949–2018. J. Gayon (*) (deceased) Institut d’histoire et de philosophie des sciences et des techniques (IHPST) (CNRS/Université Paris I Panthéon Sorbonne), Paris, France © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_7

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paradigmatic level of attribution is that of the “system” or “apparatus.” Nearly all the systems in all organisms (the respiratory, circulatory, reproductive, immune, digestive, etc.) are designated by terms that refer openly to function instead of to structure or form. A few exceptions to the rule exist, for example, the “nervous system,” “integumentary system,” “root system,” and “leaf system,” but they are rare. Moreover, in the majority of these exceptions (especially in animals), biologists characterize the systems according to function instead of structure. Biologists also assign functions to structures with levels of organization that are both below and above systems, as the schematic chart in Fig. 7.1 shows. Similarly, biologists assign functions to processes. For example, one can ask, “What is the function of paradoxical sleep in vertebrates who possess this ability?”; “What is the function of methylation in gene expression?”; and “What is the function of the Krebs cycle in aerobic organisms?” Sometimes, the “function” of things that are themselves called “functions” will be explored: “What is the function of the respiratory function?” (meaning “respiratory tract”) and “What is the function of the immune function?” (meaning “immune system”). The second sign of the liberality of the biologists’ discourse on functions is precisely concerned with the strange type of question we have just pointed out. The life sciences use the word “function” to mean two different things. Sometimes, in the first sense, “the function of something” is mentioned (for example, the function of the prostate); at other times, in the second sense, functions are spoken of in the plural: “respiratory functions,” “kidney functions,” “perceptive functions,” etc. In this latter case, the word is actually applied to a structure (generally complex, and highly integrated) considered with the function or functions (in the first sense) that it carries out. The average philosopher is shocked, or at least surprised, by this laxness, but it does not seem to bother the average biologist. If biologists were not allowed to take liberties with language, how could they talk about “the evolution of functions” (e.g., “evolution of space perception” or “evolution of the circulatory function”)? The

Fig. 7.1  Some levels of organization to which biologists currently attribute functions (list may be incomplete)

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existence of two definitions for the word “function” in biology makes it possible to understand why they see no problem in asking what the function of something they also designate as a function is. For example, “What is the function of respiration?” was an immense question that drove centuries of experimental research. Or “What is the function of immunity?” In Chap. 16, of this volume, Thomas Pradeu shows that the question is not at all easy to answer. Even though biologists commonly refer to the “immune function,” it is difficult to define what this expression actually means or designates. Biologists’ liberal terminological usage contrasts with the parsimonious usage of philosophers. The entire contemporary philosophical debate on functions, ongoing for about 50 years, concerned only the first meaning we indicated: the attributive sense, which always contains the question “What is the function of?” In their analyses of how functions are attributed, philosophers always presume the idea of “trait,”1 an extremely general idea that covers all sorts of structures, systems, and parts, as well as their behavior. This philosophical usage is parsimonious in terms of conceptual content, but its range is immense. It covers virtually the whole field of biological phenomena, at nearly every level of description and explanation. Also, contemporary philosophers have been almost totally indifferent to the “structure/function” (or “form/function”) relationship traditionally used by biologists, paleontologists, and even psychologists to explain their own usage of the term “function.”2 This does not mean that philosophers do not think structure is important. But apparently, they are not oriented according to the ordinary paradigm of innumerable biological studies. In a way, this paradigm wants structure and function to be thought of in parallel, for the purpose of asking one of two ritual questions: “Knowing the structure, what is the function?” and “Knowing the function, what is the structure?” Given this long-standing biological practice, the fact that philosophers deliberately avoid the structure/function pairing is troubling. There are two reasons for the philosophers’ approach. The first is that contemporary philosophers wanted to establish a definition of the term “function” that was as parsimonious and general as possible (therefore a definition that applies not only to structures, but also to behaviors and processes). The second reason lies in the overtly evolutionary, Darwinian ambience in which their discussions take place, even if their theory of function is not always based on evolution.3 As Jorge Cubo and Armand de Ricqlès (Cubo et al., 2008) point out, the structure/function pairing as an analytical tool is inherited from a pre-Darwinian, typically Cuvierian period, when the idea of pure morphology uncontaminated by functional considerations reigned. At that time, the relationship  On this subject, see Neander’s article, Chap. 6, this volume.  See articles by Ricqlès & Cubo (Chap. 11), Laurin (Chap. 12), Morange (Chap. 14), Dupont (Chap. 13), Galperin (Chap. 15), Tirard (Chap. 18), and Abourachid & Hugel, Chap. 24, this volume. Historical studies by Lennox (Chap. 1), Duchesneau (Chap. 2), and Clauzade (Chap. 3), concerning periods earlier than the contemporary period, tend to agree. 3  Several excellent collectively written books give an idea of the scope of these debates: (Allen et al., 1998; Buller, 1999; Ariew et al., 2002). 1 2

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between structure and function was thought of as a static relationship of reciprocal adjustment. Conversely, in a Darwinian perspective, there is no longer a place for a purely structuralist perspective on morphology. The link between morphology and function is direct, and its operation and origin can be analyzed causally. No doubt this Darwinian atmosphere is what led contemporary philosophers to avoid pairing structure and function as an approach to the problem of functions, and to favor the more open notion of “trait” in both “etiological-selective” and “systemic” theories of function. Philosophers assuredly brought an uncustomary rigor to the question of the very nature of functions and their attributions, by clarifying the possible meanings of the term “function.” In fact, it is only in philosophy that the “theory of function” is discussed. The expression is totally unknown in biologists’ circles. In the study that follows, we shall confront the liberality of biologists’ discourse on functions with common philosophical theories of functions. We raise two questions. First, we shall examine a few levels of organization for which it is problematical to attribute functions, from the standpoint of the commonly discussed philosophical theories. Then we will wonder whether it is valid to attribute functions to these structures.

7.2 Structures That Challenge the Attribution of Functions We shall consider three levels of organization to which it is difficult to ascribe functions: atoms and elementary molecules, organisms, and species. In ordinary biological discourse, functions are attributed to these three sorts of structures, at least in certain biological specialties. However, these attributions should not be taken for granted, from the viewpoint of established philosophical theories of function. For the needs of this demonstration, we shall limit ourselves to a brief characterization of the two great families of philosophical theory of functions. These two schools of thought have been the center of most of the discussion since the mid-­1970s, when two founding essays were published: one by Larry Wright (1973) and one by Robert Cummins (1975). “Selective etiological theories” establish a fundamental causal bond between function and selection. The most widespread version of the etiological conception4 consists in saying “the function of a trait is the effect for which it was selected” (Neander, 1991). Another version consists of linking a function to its current contribution to “fitness,” the selective value of an organism, instead of to the past history of a trait. As for systemic theories, they define the function as the causal role that an item plays in the system containing it. For example, the function of the diaphragm is to

 Successive versions of the etiological theory, and particularly their subtle divergence from Larry Wright’s original conception, are analyzed and discussed very well in Lorne, 2005. 4

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expand the chest cavity, thereby contributing to the emergence of a capacity to inhale in terrestrial vertebrates. The etiological theory, on the other hand, would say something like this: The function of the diaphragm is to expand the chest cavity, because that is what it was selected to do (and/or is currently subject to selective pressure to fulfill this function).5 The two sorts of theory of function are not contradictory. In most cases, they can also be applied to biological traits. But they do not say the same thing, and in certain cases, they are applied unevenly, in practice. Let us look at how they fare in three test cases, in which we shall examine specific levels of organization.6

7.2.1 Atoms and Elementary Molecules Is it possible to attribute a function to an atom, an ion, or an elementary molecule like oxygen (O2)? Let us consider the case of the ferrous ion Fe++. It is one of the components of the molecule hemoglobin. Each of the four globins that make up this huge protein complex incorporates a porphyrin structure, itself containing a ferrous ion. Depending on the levels of oxygen and carbon dioxide in immediate proximity to the hemoglobin, the porphyrin is able to bind to the oxygen or, on the contrary, to release the O2 molecule. The ferrous ion plays a necessary role in these phenomena. Can we say that it has a function in this context? Within the framework of the selective etiological theory, we cannot. The ferrous ion as such was not selected and, in the present time, does not contribute, to the fitness of the organism. The elements with evolutionary meaning are the globin (the protein) incorporating the ferrous ion, the metabolic processes determining the formation of the porphyrin associated with the globin, and the association itself. It is obviously essential for the porphyrin to contain an iron atom to function. But we cannot assert that the iron atom was selected to play the physiological role it plays. Selection operated in the case of the complex trait in which the ferrous ion plays a role. From the standpoint of the  etiological theory, a distinction must be made between the fact of having a function and the fact of having a biological role. Undeniably, iron plays a role in respiration, but it does not have a “function,” strictly speaking. The systemic theory is more accommodating. The ferrous ion is indeed a genuine part of mature hemoglobin, and it plays a specific causal role in oxygen binding. It contributes to the emergence of an ability in the nested systems containing it: heme, globins, hemoglobin, red blood cells, and respiratory system. Therefore, it has a function, because it plays a causal role in the emergence of the capacity in the system or systems containing it.

 See the analysis given by Neander (in this volume) of this problem of time scale suitable for evaluating the relationship between function and natural selection. 6  Here, we reprint the conclusions of the analysis we suggested in Gayon, 2007. 5

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Let us consider a second example, that of the oxygen molecule O2. In modern general theories of respiration (i.e., theories applicable to all aerobic organisms), its role is to be the final acceptor of four electrons and four protons in the respiratory chain, inside the mitochondria (or in the cell protoplasm itself, in the case of prokaryotes). If we allow ourselves a teleological turn of language, we could say that the oxygen molecule pulls the whole biochemical mechanism. Throughout the Krebs cycle and the respiratory chain, this molecule makes it possible to break down pyruvate, therefore all of the carbohydrates that happen to have broken down into pyruvate at one point or another. Therefore, oxygen clearly plays a biological role. Nevertheless, from the standpoint of the etiological theory, it seems risky to say that the molecule has a function: It is not selected and has not been selected in the past. Evolutionary significance is possessed by the proteins in the respiratory chain, the morphology and development of the mitochondria, and the whole respiratory apparatus, all of which, ultimately, use oxygen. They are inheritable traits of different degrees of complexity, and therefore, they are the properties of the lineages subject to selection, not of the oxygen itself. From the standpoint of the systemic theory, it is also a little hazardous to say that oxygen has a function. Actually, oxygen is not really a component part of the respiratory system. It is an external element needed for the system to function. Oxygen is to respiration as photons are to vision. In other words, photons are needed for the implementation of the ability to see, but they are not part of the vision system. Likewise, oxygen is necessary to respiration and plays a crucial causal role in the process. But it is problematical to attribute a function to oxygen, because it is only temporarily part of respiration, from a dynamic viewpoint. If we accept these last qualifications, oxygen can be said to have a function in the respiratory chain.

7.2.2 Organisms In a certain number of cases, organisms or, more precisely, types of organisms have been assigned a function in ordinary biological usage. For example, castes within colonies of social insects, or other forms of colonial life, are said to perform “functions” for the colonies to which they belong. Likewise, males and females are said to have a “function” in the sexual reproduction of innumerable organisms. However, such a situation is somewhat rare in biology. Generally, functions are attributed to the traits of organisms, not the organisms themselves. Let us test the philosophical theories of function with the idea that types of organisms, as such, have a “function.” For the systemic theory, no serious problem arises, as long as the system containing the type of organisms to which a function is attributed is precisely identified. Colonies of social insects are such systems. The case of sexual reproduction is more ambiguous. Is the containing system the couple, the local population, or the species? Doubtless, species is the best candidate, insofar as it is the most inclusive

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reproductive community. The species is doubtless what authorizes the assignment of specific functions to males and females, from the standpoint of the systemic theory. But the difficult problems to which this type of concept might lead are obvious. The “species” system is not really that easy to represent according to the diagrams of causal relationships so dear to Cummins, compared to such systems as the blood-sugar regulation. With the selective etiological theory of functions, the matter is considerably more serious. Indeed, in the standard natural selection model, individual fitness is what is maximized. A trait is selected when it maximizes the fitness of the class of organisms carrying it. Within this framework, it is impossible to see how organisms as such could be said to have a “function.” Of course, nothing forbids us from choosing a different theoretical framework, for example, by accepting a group selection theory. In fact, the very existence of sexual reproduction, and its maintenance, in particular, is commonly explained on the basis of group selection (Maynard Smith, 1978). In such a context, it is easier to attribute functions to organisms. But if so, it means that the applicability of the etiological theory depends on the specific biological theories being considered.

7.2.3 Species Is it possible for species to have “functions”? Again, biologists – ecologists or biogeographers, at least  – do not mind saying they do. For example, the ecological theory of biodiversity allows that different species can have the same function in a certain type of ecosystem (see Blandin, 2007). For the systemic theory of function, again, species function does not raise any major problems. A system has been identified (the ecosystem), and a given species (or class of species) may play an essential causal role in maintaining this ecosystem or enabling it to evolve. For example, in the “prairie” ecosystem, grazing animals play a crucial role in scattering seeds. As a result, a given species or group of species can therefore be said to have a function, and it can be imagined that such or such a species might be replaced by another vicarious species. Conversely, for the etiological theory, attributing functions to species as such appears problematical to us. It is a fact that ecosystems do not reproduce. They either survive or disappear. Some authors allow that they are sometimes replaced by other ecosystems playing the same role, but this phenomenon does not fit the strict definition of reproduction. In these conditions, it is hard to say how species might have a function in an ecosystem similar to the function of inheritable traits in organisms that reproduce differentially depending on the traits they possess. True, certain ecologists have developed significant theories of selection that can be applied to ecosystems. But once again, we see that the applicability of the etiological theory of function depends on the use of specific scientific models. Having briefly considered these extreme cases (atoms and elementary molecules, organisms, and species), we can draw the following conclusion. We have observed

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that the systemic theory was probably more liberal than the etiological theory. The systemic theory applies better to marginal cases, at both extremes of the organizational scale of material objects considered by biologists. Although the etiological theory hardly ever makes it possible to attribute functions at certain levels (atoms, for example), or operates only as long as a particular model of natural selection is specified (the cases of organisms, species, and incidentally ecosystems), the systemic theory can accommodate nearly all the extreme cases fairly easily. This agrees with the fact that it was not specifically constructed for biological objects (it was explicitly inspired by engineering). The sloppy side of the systemic theory has often been noted: It is meaningful only in relation to a certain arrangement of the object by the experimenter, due to their theoretical objectives (see Huneman, Chap. 8, this volume, and Lorne, 2005).

7.3 Structures and Processes We shall end by stating a much more radical reservation about the usual philosophical approaches to the notion of function. At the beginning of our chapter, we said that biologists attribute functions sometimes to structures and sometimes to processes. But it cannot be taken for granted that these attributions are appropriate to structures. Philosopher William Wimsatt (1972, 2002), in this case atypical on this problem, argued that functions should never be attributed to “physical objects” (i.e., material structures or systems). In his opinion, only behavior and operations, or even “processes,” could be said to have functions. For example, we should not attribute a function to the heart, only to “what the heart does.” The heart contracts and relaxes, and the function of this beating motion is to pump blood. Similarly, the heart beats faster at some times and slower at others, and this varying rate also has functional significance for the organism (i.e., in this case, to respond to varying metabolic demands). If Wimsatt is correct, then functions should not be attributed to a given part of the organism; they should only be attributed to the behaviors of these parts, in specific inner and environmental conditions. This is a stimulating proposal. To our mind, it has several important implications. In the first place, this conception of functions avoids making them intrinsic properties of physical objects. It forces us to adopt a relational viewpoint: attributing a function makes sense only within a defined organizational context, in a defined environment, and in relation to a defined biological theory. In the second place, and contrary to a school of thought that has been the dominant one in philosophical debates for almost 40 years, this conception makes it possible to bring the notion of function close to the notion of operation. As a result, functions are attributed within a dynamic framework. This solves the most striking paradox noted above, the case of oxygen. Strictly speaking, oxygen does not appear to have a function in respiration for either the etiological or the systemic theory. In fact, oxygen does not have a function inherent to it, any more than any other structure does. But the capture of protons and electrons by oxygen undoubtedly has a

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major biological function in molecular systems (highly complex, and based on properties that are extremely robust from the standpoint of their evolutionary seniority and inheritability) made up by aerobic organisms. Let us also note that if functions are attributed to behaviors instead of to structures, the problems related to the transitivity of functions are solved. Functions are not transitive unless they are attributed to structures nested one inside another. They are not transitive if they belong to behaviors that are causally related to other behaviors that are causally related in the systems encompassing them. Lastly, anchoring functions in behaviors or processes makes it possible to pinpoint the flaw in the traditional “structure/function” pairing, which simultaneously organizes and traps a good part of ordinary biological discourse in endless equivocations. It is not the structures that have a function, but what they do, their effect in a particular context. Functions are not monadic properties of structures. Perhaps this proposal will be judged too radical. For us, it has the advantage of restoring considerations like organization, movement, and environment, without which the attributions of function are meaningless.

References Allen, C., Bekoff, M., & Lauder, G. (Eds.). (1998). Nature’s purposes. Analyses of function and design in biology. MIT Press. Ariew, A., Cummins, R., & Perlman, M. (Eds.). (2002). Functions. New essays in the philosophy of psychology and biology. Oxford University Press. Blandin, P. (2007). L’écosystème existe-t-il ? Le tout et la partie en écologie. In T. Martin (Ed.), Le tout et les parties dans les systèmes naturels (pp. 21–46). Vuibert. Buller, D. J. (Ed.). (1999). Function, selection and design. State University of New York Press. Cubo, J., de Ricqlès, A., Montes, L., de Margerie, E., Castanet, J., & Desdevises, Y. (2008). Phylogenetic, functional and structural components of variation in bone growth rate of amniotes. Evolution & Development, 10(2), 217–227. Cummins, R. (1975). Functional analysis. The Journal of Philosophy, 72, 741–765. Gayon, J. (2007). Où s’arrête la régression fonctionnelle en biologie ? In T. Martin (Ed.), Le tout et les parties dans les systèmes naturels (pp. 67–74). Vuibert. Lorne, M.-C. (2005). Explications fonctionnelles et normativité: analyse de la théorie du rôle causal et des théories étiologiques de la fonction, thèse de doctorat de philosophie, EHESS. Maynard Smith, J. (1978). The evolution of sex. Cambridge University Press. Neander, K. (1991). The teleological notion of function. Australasian Journal of Philosophy, 69, 454–468. Wimsatt, W. (1972). Teleology and the logical structure of function statements. Studies in History and Philosophy of Science, 3, 1–80. Wimsatt, W. (2002). Functional organization, analogy, and inference. In A. Ariew, R. Cummins, & M.  Perlman (Eds.), Functions new essays in the philosophy of psychology and biology (pp. 173–221). Oxford University Press. Wright, L. (1973). Functions. Philosophical Review, 9, 139–168.

Chapter 8

Function and Adaptation: A Conceptual Demarcation, Instigated by Borderline Cases for Etiological Theory Philippe Huneman

Abstract  Insofar as in etiological theory, “the function of X is Z” means that X has been selected for Z, while evolutionary biology often defines adaptation as what results from natural selection, the concepts of adaptation and function overlap. Should we then finally eliminate the selection-related notion of function, replace it with that of adaptation and use “function” only when it is a question of functions sensu the causal-role theory? I examine two limit cases for the etiological theory, in which emerges a tension between the notions of function and adaptation. First, there are cases of superiority of heterozygotes, such as sickle cell anemia. Here, from an etiological point of view, the recessive allele seems to have a function (equal to its adaptive character), whereas it is at the same time dysfunctional. The other problem is the selfish genetic elements (e.g. “selfish DNA”,), which also raise the question of levels of functionality in reference to adaptations. The selfish genetic elements make visible a presupposition of the etiological theory of function, namely a homogeneity or alignment in the levels of selection. In this sense, the acknowledgment of levels of selection motivates a rethinking of the etiological notion of function.

8.1 Introduction The etiological theory of functions (ET), initially formulated by Larry Wright (1973), and then refined by Millikan (1984) and Neander (1991), has put forth a realist interpretation of the concept of function in biology. If function attributions are indeed grounded in evolutionary history, insofar as this causal history is real, they are themselves objective properties of organisms. This is one of the great divergences with the systemic or “causal role” theory of functions  – proposed by P. Huneman (*) Institut d’histoire et de philosophie des sciences et des techniques (CNRS/Université Paris I Panthéon Sorbonne), Paris, France e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_8

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Cummins (1975) – which, while supporting that the function of an item is its causal role in a system, makes the functional ascriptions dependent on the choice of the system one considers. ET has been largely adopted by many philosophers and biologists (e.g. Godfrey-Smith, 1994; Walsh, 1996; Kitcher, 1993) in various formats, because of its realist character as well as its ability to confer meaning to the normative aspect of functional ascriptions. In this perspective, normativity can indeed be accounted for by the difference established between the typical effect of X – the only one involved in evolutionary history, where it concerns the ancestral populations of X – and the corresponding effect of a token of X, which can have or not have the typical effect (as a result of damage to a mechanism, for example). Nevertheless, the concept of function in biology may ultimately thereby appear as a close relative, and even a redundant version, of the concept of adaptation. After Darwin, the concept of “adaptation” has indeed been clarified, and saying that “X is an adaptation” means that X is the result of natural selection (e.g. Sober, 1984; Brandon, 1990). Therefore, “X has the function Z” and “X is an adaptation for Z” seem like synonyms, which raises doubts about the interest of the notion of function. In a word, if the term “function” has meaning only within an evolutionary context, and if evolution can describe everything with the concept of adaptation, the concept of function becomes superfluous. In order to avoid this consequence of the ET theory, the present chapter aims to specify the demarcation between adaptation and function, while indicating, from cases where ET is challenged, how the concept of function must distinguish itself from that of adaptation.

8.2 Selected-Effects Functions and Adaptation Neander (1991) labels “selected-effect (SE) functions” those functions which fall under ET. When paleontologists say that the function of the crest of a lambeosaur (a hadrosaurid sub-family) is social communication (Currie & Padian, 1997), they identify an SE function: the horn in question was selected for the reason that it made noise, communicating information to congeners about the proximity of other nearby congeners, etc. (Turner, 2000). This etiological theory obviously concerns function attributions at all levels. Thus, when molecular biologists show that the function of protein HsP90 is protein folding, a function performed by assisting this folding and by preventing the aggregation of wrongly folded proteins (Queitsch et al., 2002), they are making a statement on the role of these effects of the protein that has led to its maintenance within a very large group of clades, in the evolutionary history. In accordance with Wright’s initial claim, one can thus translate the functional statement of Queitsch et al.: “The protein HsP 90 is there because it warrrants, in diverse ways, the folding of proteins.” But by so interpreting “the function of X is Z” as “X is there because it makes Z” and ultimately as “X has been selected because it makes Z,” this theory seems to bring the concept of function down to that of adaptation, insofar as “being an

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adaptation” means “having been selected” (Williams, 1966; Brandon, 1990; Sober, 1984; Grandcolas, 2015). For instance, when Darwin says (Origins of Species, ch. 6) that the webbed feet of the ducks are an adaptation for moving at the surface of water, he says in essence that this shape of feet has been selected for its yielding the ability to move on the surface of water, which can easily be translated into a functional statement sensu the etiological theory. In this sense, the etiological theory makes the concept of function a natural and objective property of organisms at the possible cost of redundancy with the concept of adaptation. It thus seems that what falls under the etiological concept of function falls under the concept of adaptation, and reciprocally. Nevertheless, that does not make the two concepts equivalent. All that falls under the concept “mountain” falls under the concept of “mountain less than 10,000m high,” but the two concepts are different, since there are more satisfaction conditions in the latter than the former. This latter predicate is clearly in accordance with all the items that fall under the former concept, but that is only a contingent fact. Hence, in this example, the two concepts are different, even if their known extensions overlap with each other. Is it not the same for the concepts of function and adaptation? At first glance, these concepts seem to differ if one takes into account  their respective semantics. The concept of adaptation has at least two meanings: one according to which it signifies certain traits that result from natural selection (the one used up to here), the other where one considers the value of the current fitness of the trait in the population (Reeve & Sherman, 1993); and lastly, independent of these two meanings that concern traits, there is a meaning which concerns the whole organism: adaptation in the sense of “overall adaptedness” of an organism to its environment. This last meaning has a complex connection with the first two, since, roughly speaking, the more an organism has adaptations, or more precisely, adaptive traits, the more it is adapted; but that is not always valid, because it can happen that the adaptive value of traits adds up poorly, in particular when the adaptive value of one trait relates to survival and that of the other to reproduction. This underlies the well-known issue of adaptationism (Gould & Lewontin, 1979). While Huxley (1942) labelled organisms “bundles of adaptations,” implying that explaining an organism boils down to explaining each of it strait as an adaptation, it appears that the inference from “explaining n traits as adaptations” to “explaining the whole organism and its adaptedness” is not straightforward, given those cases where we can’t add up adaptive values of traits considered in isolation.1 Nevertheless, it seems that this conceptual formulation of the triad adaptation-­ adaptive-­adaptedness, in which the use of the concept of adaptation is embedded, doesn’t involve the concept of function. In particular, when we use “function” within an etiological perspective, it is difficult to think of it in quantitative terms (namely, having more or less of a function?), while the notions of “adaptive” and “adaptedness” are quantifiable: a trait can be more adaptive in the sense that it

 See Huneman (2017) on “trade-off adaptationism “as a way to save this inference, and the notion of developmental constraint as a major critique. §8.4 below will return to adaptationism. 1

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increases fitness as compared to another one, an organism will be more adapted than another. Furthermore, the concept of function exclusively concerns traits; and it is difficult to imagine how one could extend it to organisms, which makes for a conceptual difference with adaptedness: organisms themselves can be “more or less adapted” than others, but they could not “have a function,” at least within the framework of ET.2 To specify the conceptual distinction just indicated here – between function and adaptation – I will now approach two cases where the etiological account of functions seems to be missing something.

8.3 Problems with Etiological Theory 8.3.1 The Case of Sickle-Cell Anemia Hemoglobin is coded by many loci. With one of them, some recessive alleles display an anomaly – which is that the heterozygote will code for red blood cells in the form of sickles, which are less suitable for oxygen. More precisely, the recessive homozygote of this allele is quasi-lethal; but the heterozygote has, in some regions of Africa, the effect of providing protection against malaria, which implies that its fitness is higher than that of the dominant homozygote with the coding allele for the normal form of hemoglobin. This example, which is an instance of what is called “heterozygote superiority,” is recurrently used in the philosophy of biology within various contexts. It is interesting here because it puts ET to the test. The function (SE) of dominant alleles is simple: they are there because they code for molecules that bind oxygen; therefore, their function is the binding of oxygen. As the locus is thus defined by hemoglobin, one can say that the recessive allele is dysfunctional since  when it is here, the genotype at this locus does not allow for the proper binding of oxygen, while the alleles in this locus should be there for this reason. But if we consider the African environment, we see that the recessive alleles are presumably there because they protect against malaria, so that one could well say that their function (SE) is to protect against malaria, and thus that they are not so dysfunctional. The functional status of the recessive allele is therefore not clear; but whatever it is, these alleles plausibly are an adaptation to the African environment: selection has kept them because of their effect against malaria, while they would be wiped out in other environments. How should we then treat such a case from the point of view of the etiological theory? The alternatives seem to me to be the following:

 Even if this would be possible within an ecological framework; but then it would be necessary to go back to the theory of functional systems to account for it: see Bouchard (2009). 2

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–– Either we consider that, in this case as in numerous others undoubtedly, ET is unsatisfactory, and we stand with the causal role theory of functions, à la Cummins, or another alternative to ET, for example organizational theory (Mossio et al., 2009), goal-contribution theory, dispositional theory (Bigelow & Pargetter, 1987). We would say that the causal role of the alleles of this locus in the organism is to contribute to the production of hemoglobin and, transitively, to bind oxygen, and that the recessive alleles fulfil this role less well. We will add that, furthermore, the recessive allele is an adaptation against malaria in African environments. But we could switch to another system, let’s say a human population residing in Africa, and then the sickle cell allele would be granted the function of protecting it against malaria. –– Or we keep the two notions of SE function and adaptation, but revise the meaning of the former. To explore this solution, I will now look at a second difficult case for ET, namely what we call “selfish genetic elements.”

8.3.2 The Function of Selfish Genetic Elements The idea of selfish genetic elements evokes the notion of “selfish DNA” based on the idea of Richard Dawkins’ famous “selfish gene” (Dawkins, 1982).  The first cases of selfish DNA were studied by Orgel and Crick (1980) and Doolittle and Sapienza (1980); they described genetic sequences which apparently did not code for phenotypic effects, but instead remained integrated within the genome. There also exist alleles which, in spite of their harmful effect on the organism, are present all the same in the genome and are transmitted from generation to generation, like the t allele in mice, which causes sterility while remaining homozygotic (Lewontin & Dunn, 1960). Burt and Trivers (2006) published a survey of the work on the selfish genetic elements, which have been discovered since the 1970s (a number that turned out to be extremely high). Some of them alter meiosis so that they are over-­ represented in the following generation (“segregation distorters”), others are on a chromosome and diminish the chances of representation of the paired chromosome’s alleles during meiosis; sometimes they are alleles on the chromosomes linked to sex, at other times they are alleles on autosomes. Scientists have distinguished many of the strategies of these elements: (a) Sequences whose replication speed exceeds those of their neighbors so that they are over-represented in the following generation, even if they do not have a function for the organism. (b) Sex-linked killers or autosomal killers which alter meiosis by sidestepping the representation of the other chromosome so that less than 50% of its genes are present after meiosis, which often comes at a high cost for the organism. (c) The DNA sequences which practice gonotaxis, that is, those that preferentially go with the germinal line while distancing themselves from the somatic line.

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An example of strategy (b) is provided by alleles on certain Y loci that disturb the formation of spermatozoids containing the X chromosome in the mosquito species Aedes egypti and Culex pipiens. As for strategy (a), an instance is given by the gene types HEG and BGC, which both profit from the possible advantages provided by the DNA repair machinery. An active form of this strategy, the Homing endonuclease genes (HEG) code for an enzyme which recognizes and cuts those chromosomes which do not contain a copy of them; during the repair, HEG itself is then copied. Furthermore, this genetic element is often circulated through lateral transfer, which, if one considers the questions of function attribution, would pose a problem for etiological theories, since they  associate function and selection, and, as Millikan suggests (1989), anchor functions within families of reproducers. As the Biased gene conversion (BGC) HEG are essentially sub-products of biases in the DNA repair mechanisms. What is the function of these elements? Are they adaptations? In his revision of the etiological concept of function, Godfrey-Smith (1994) discusses this; but at the time, the richness of the world of selfish genetic elements, involved mechanisms, and transmission types was unsuspected. A more detailed study of the implications of this research on the very concept of function itself could be undertaken; but for lack of space, I will simply sketch out the solution I am proposing. In a general fashion, these studies highlight cases of selection at many levels. As it is well known, basic group selection in the form of “selection favoring the good of the group” (herd, species) has been debunked by Williams (1966) among others. It has been explained away by Hamilton’s conception of kin selection (Hamilton, 1964), as well as by the notion of reciprocal altruism (Trivers, 1971) in case of the lack of genetic kinship. But other forms of group selection came back to the forefront to explain certain phenomena of altruism and cooperation. This was particularly salient in the work of David Sloan Wilson (Wilson, 1980; Sober & Wilson, 1998), who coined it “multi-level selection.” Briefly said, according to him, natural selection can be understood as multi-level selection in those cases where multiple individual are divided into groups3: thus, competition  occurs within  the groups (namely, the competition between individuals) and competition is at play between groups; selection itself will be the sum of these two effects. Altruism, most generally, is a behavior (understood in the largest sense as in behavioral ecology) which is such that it has beneficial fitness consequences for others and a cost for the actor (West et  al., 2007) We may appeal to multi-level selection to explain certain forms of altruism in which the reason of the altruists’ maintenance is precisely the contribution that they bring to the sustainability of their group within a context of strong competition between groups (Sober & Wilson, 1998). Major controversies affect the use of multi-level selection, its difference with kin selection, and many biologists claim that kin selection and multi-level selection are identical (Kerr & Godfrey-Smith, 2002), or that the most fundamental process is

 One of the essential contributions of David Sloan Wilson has been the theoretical redefinition of the notion of group within this context, as a “trait group.” See Okasha, 2006, chap. 3. 3

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kin selection (e.g., Gardner et al., 2011). While formal for mathematical identities hold between those two forms of selection, one may still debate about their relation as purportedly distinct causal processes (Birch, 2017 for an overview); yet this is not directly relevant for this chapter, as long as multi-level selection is not deemed vacuous. These precisions having been made, the case of selfish genetic elements brings to light a multi-level selection at infra-organismic scales. If selection at the level of organisms should counter-select some of these genetic elements insofar as they are often harmful for the organism, they are maintained because a selection between alleles is taking place, and their clear benefit at this level exceeds the cost that they pay for letting the fitness of the organisms carrying them become lower. In this sense, their existence is due to a selection at the level of alleles themselves; and it is necessary to take this fact into account in order to apply the etiological theory when we ask about their function. But it does not seem problematic to say that selection at many levels defines adaptations at each of these levels, which can be antagonistic towards each other. Strategies (a), (b), or (c) – which are defined above as the activities of certain alleles that disrupt the paired chromosome (or “kill” it) by either introducing themselves into the germ line or by becoming parasites within the DNA replication mechanism – are indeed the reason why these elements are reproduced every time, whether in the organism during mitosis or in the following generations after meiosis (in the cases of sexual reproduction). In this sense, they are the reason why these elements are better transmitted than others, why they fix themselves in populations and are maintained in the germ line and in organisms. Their presence is thus the result of an infraorganismic selection in favor of these properties, and such elements, given the most general understanding of “adaptation” (see above), are therefore adaptations. What about their functions? Here, we see a gap between the vernacular usage of the term and the one that should be used within the etiological theory, according to which the adaptations under focus should be seen as functions. To the question “What is the function of a killer genetic element in X?”, a molecular biologist would surely not respond: “To disrupt meiosis.” Likewise, certain selfish DNA elements are meant to not have a function: this is in opposition to what etiological theory would say, which would attribute to them as a function the reason why they are there, namely self-replicating faster than the other genetic sequences. Here, the etiological theory seems to not take account of the difference made by biologists between biologically functional and non-functional elements. Furthermore, causal role theory preserves this difference since these selfish genetic elements have no causal role in the organism’s system. Thus, how can we respond when confronted to this discrepancy between Etiological Theory’s usage of functions and that of biology? Here again, many solutions are possible: We can look at the etiological conception of functions as a “theoretical definition,” which creates a norm for the concept (in a sort of conventional way, as it is omnipresent in mathematics: “I call circle a figure such that”). In this sense, this philosophical conception can in certain cases deviate from the standard usage; but

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this is the price to pay for having a genuine theoretical definition, which is Millikan’s position vis-à-vis such account. Notice also the difference with the sickle cell anemia case: here, the selfish genetic element has been selected for its disrupting effect. There is no way it can be said at the same time functional and dysfunctional, as the sickle cell allele. Therefore, having a theoretical definition of ‘function’ that deprives it of any function is not problematic, while it would be more problematic to adopt a concept of function that deprives the sickle cell allele of any functionality. But the problem is that insofar as this notion contradicts the ordinary use of the term “function” in these cases of selfish genetic elements, these marginal cases would justify the pure and simple removal of “function” in its etiological sense. In effect, considering that it is coextensive with the notion of adaptation – which itself does not create semantic problems  – it seems reasonable to stand with the sole notion of adaptation, since it is apparently substitutable to ‘function’ in all biologically sensible contexts. Which brings us to the second and third options: • We can get rid of “function” in its etiological sense and only keep functions of the “causal role” type, which in the cases considered above corresponds to the biological use of the term. And what etiological theorists call “function” is in fact adaptation. This was one of the conclusions suggested in the former case (sickle-­ cell alleles). • A last option would be to revise the concept of etiological function. This option (the second one suggested earlier) becomes more concrete here as we have resources to reformulate the etiological notion in a satisfying manner with the case of selfish genetic elements. The rest of this chapter will build up this solution.

8.4 Redefining the Etiological Notion of Function in the Case of Multi-level Selection 8.4.1 Refining the Etiological Theory on the Basis of Levels of Selection Consideration: The Incorporation Clause (I) Considering the issue raised by selfish genetic elements for the etiological theory of functions, I advocate a revision of the theory that will integrate the contemporary theory of multi-level selection. The basic idea is as follows. The notion of function is still grounded in evolutionary history; in other words, we keep the essential intuition of the etiological theory, according to which the idea that “X has the function Z” explains that X is there through the fact that Z evolutionarily accounts for the presence of X. But we add the (I) clause, namely, that X is incorporated into a relevant system; thus, the selfish genetic element (unlike mitochondria, or a coding allele on the same chromosome) does not have a function because it is not

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incorporated within the system  named “organism”. The remaining question concerns what “incorporated” and “relevant system” mean. Granted, this solution falls into the list of theoretical conciliations that have been suggested between ET and causal role theory (Kitcher, 1993; Walsh & Ariew, 1996; Millikan, 2001), which all go on to emphasize the integration of functional traits within systems. But the case of selfish genetic elements allows us to refine the blurry reference to an “incorporating system” because here we can make use of the notion of multi-level selection. So let’s unpack what “incorporated” means. For an “ordinary” allele, namely an allele whose phenotypic contribution affects traits of the organism contributing to the fitness of this organism and, as a consequence, equally its own fitness, selection at the level of the organism and at the level of the gene are aligned; in other words, the gene and the organism have the same evolutionary interests. The part and the whole, so to speak, are in agreement from the point of view of selection; but this agreement is not a necessity governing selective processes at all levels, and in fact, it does not occur in regard to selfish genetic elements. To this extent, and by generalizing the case of alleles vis-à-vis the organism, one can define the notion of an “SE-functional part” in a system in the following way. X is an SE functional part of S iff: “X is a part of S and is strictly included in S; considering selective pressures on S and on X, the selective pressures at these two levels are aligned.4” From there, saying that “the function of X is Z” means that X is there because there was a selection of X for Z and that there exists an S system such that X is an SE-functional part of S. This concept allows us to keep the core etiological sense of “function” – that is to say, the link between function and selection –while resolving the contradiction between the usage of the terms “adaptation” and “function” in the case of selfish genetic elements: those are adaptations, as I said, but they don’t have functions, since they are not SE functional parts. The notion of SE-functional parts can appear problematic for two reasons, each concerning one of the clauses that define it. A first issue arises when one considers that not all parts of an organism are subject to selection, in particular because all parts do not emerge from a level where one can identify replicators. Simply said, it seems at first glance that often “parts” of organisms are not such that they pertain to a level of selection, or that there is a selection on them (while there is selection on organisms and on genes, according to the most standard views, or at least views that allow for multi-level selection.) But if a trait does not belong to a level that is susceptible to selection (e.g. a morphological trait like a limb, which is a phenotype conditioned by an vast number of genes),  A question about temporality is asked here: since when are they not in conflict? Here, we again look at Godfrey-Smith’s analysis (1994), according to which the relevant period for defining a function (and thus for the relationship between selection levels) is the recent period. 4

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we could easily say as a first approximation that its level of selection is that of the being in which it is immediately included for its reproduction, meaning the immediate upper level, which, in the example of the limb, would be that of the organism. Here, the SE functional part is simply a part, e.g. the limb, and we can recover the standard etiological theory (there is only one selective level). Now, if we accept multi-level selection (in a style like that described by Sloan Wilson & Sober, 1998), certain behaviors that involve many individuals within a group, for instance the defense of a bee colony, or the mounting of a termite mound, will be likely to be viewed as functions of individuals in this group, since there is a selection at the level of the whole colony, and the cluster of insects operating the behavior is not in conflict with the direction of the selection on the whole colony. This last clause means that the cluster of individuals to which the function is ascribed undergoes a selective pressure that does not contradict the selection on the group: it is not always the norm for a random group, but when a group is robust enough, as is a beehive, a termite mound or a slime mold, then there exist regulatory or policing mechanisms that prevent a selection favoring selfish individuals and, therefore, align individual selection with the selection due to intergroup competition (Clarke, 2010; Gardner, 2013).5 In the context of the research on “transitions towards individuality” (see below), I called these groups “component individuals” to distinguish them from “complete individuals,” such as metazoan organisms, in which the parts (e.g. my cells) don’t reproduce by themselves independently any more (Huneman, 2013b).6 This reasoning exemplifies how the notion of SE functional part enlarges the morphological or anatomical notion of a biological part. The other difficulty of the notion of SE-functional part concerns the cases where one finds it hard to identify what is actually a part, for instance when one considers behaviors: is the specific killing of bees by hornets a behavior or a part of a general behavior called territoriality? Nevertheless, it seems to me that these problems do not differ in nature from the general problem of defining the evolutionarily relevant trait when we consider the behaviors as possible objects for natural selection; but from the moment where the behavioral trait is defined, we can identify the level at which selection acts relative to the other levels of selection (which can, e.g., involve

 These policing mechanisms are crucial, since they ensure that the direction of selection upon parts (cells, genes, etc.) will be aligned with the selection upon the et of parts (the whole). They include bottlenecks in metazoan, killing of emerging queens in some bee species, immune systems (Pradeu, 2013), etc. Whatever the mechanisms, they are an evolutionary result; initially they do not exist, and therefore, the alignment I’m talking about is always an evolutionary outcome. Initially, in a group of reproducing elements, the ones reproducing by themselves always have a higher fitness; a group becomes somehow an individual, or transitions towards individuality when its structure makes the selfish behaviour of elements more costly in fitness terms. 6  Many philosophers and biologists agree on the idea that there is no sharp boundary between individual and non-individual in biology and that there exists a continuum or a hyperspace of individuality in which herds, beehives or mammals can be located. I present my own version of this view in Huneman (2020). 5

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cultural selection, or “coevolution gene-culture” in the sense of Boyd & Richardson, 2005) and so finally define SE functional parts. The present framework, intended to solve the issues ET faces with selfish genetics elements (§8.3.2), proves to be a general solution for cases where adaptation and function break apart, such as the first case we discussed (sickle-cell anemia). The point here is that in the case of the dominant allele and in that of the recessive which correlates to sickle-cell anemia, the levels of SE functional parts are not identical. For the normal allele, the allele itself is the SE functional part, because selection aligns itself with the course of selection for the organism. As for the recessive allele, the SE functional part is at the level of the genotype: it is the entire heterozygote locus which is the object of selection7 in a converging direction with the selection regarding organisms. This is why standard ET gave contradictory results if one applied it to the two alleles identically. Once we have considered the incorporation requirement (I), functional ascriptions according to ET allow us to say that the dominant allele has the function of coding for oxygen binding, while the function of the heterozygote genotype is to protect against malaria. Here is the way we can solve the case of sickle cell allele that was puzzling for the standard etiological theory, as seen in §8.3.1.

8.4.2 General Consequence: Functions, Etiology and Adaptation The present analysis joins the list of contributions that have attempted to preserve the fundamental core of ET – knowing that the explanatory meaning of functional attributes is given by natural selection – while doing justice to the fact that natural selection is not the entirety of evolution: certain traits are there because of genetic drift; others evolve because they are tied, morphologically or genetically, to traits that are selected because of one of their effects, etc. (Kitcher, 1993; Godfrey-Smith, 1994, etc.). More broadly, Buller (1998) (in what he calls “Weak Etiological Theory”) argued that etiology, when involved within the etiological notion of function, is wider than selection, and concerns evolution itself. This, however, seems to forget the strength of Wright and Millikan’s intuition, namely that functional explanations pinpoint things that traits do to the very extent that those traits are there for what they do.8 By contrast, the traits that are there due to drift are not there for whatever it is that they do. Thus, I don’t concur with Buller’s weak etiological  For understandable reasons, this case of sickle-cell anemia has been given as an example type of the irreducibility of a genotypic description of selection to an allelic description (Sober & Lewontin, 1982; Sterelny & Kitcher, 1988; Waters, 1991). 8  I defended elsewhere a weak version of realism in the etiological theory, which is quite different from Buller’s weak etiological theory (Huneman, 2013a, b). Here, I do not consider the relation between this weak theory and the present argument regarding SE functional parts. This is a topic for another paper. 7

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theory, since I propose an account that supplements the general idea that function means something related to selection, and add a component taken from reflections on multi-level selection. The generalized recognition of the importance of the phenomena of multi-level selection within evolution – whether it is an ontological fact, or rather a property of our best models – has generated important theoretical work for understanding its forms and structure (Damuth & Heisler, 1988; Kerr & Godfrey-Smith, 2002; Okasha, 2006; Sober & Wilson, 1998, etc.). I will here lay out, in general, the consequences this bears for a theory of function that is based on the idea of natural selection. The analysis put forward from the case of selfish genetic elements has indeed the four following consequences: –– The requirement (I) of incorporation into a system S explains why the concepts of function and adaptation are not equivalent and why, in certain cases, their extensions do not coincide, which agrees with the common use by biologists. And contrary to the normative position discussed above (the “theoretical definition” option in §8.3.2), this does not require any alteration to biologists’ standard way of speaking. –– The system S and the SE functional part X are defined through natural selection; in this sense, insofar as the appeal to a causal history in selectionist terms saved the realism of etiological theory (Huneman, 2013a) in regard to causal role theory, this realist grounding is maintained here in spite of the call for a reference system, whereas in the causal role theory of function an arbitrary reference system is needed and introduced an element of epistemic dependence, preventing the account to be a realist account of functions. –– Most of the time, for reasons due to the evolutionary history of the “organism” form (Michod, 1999; Michod & Roze, 2001; Frank, 2006; Huneman, 2013b), which suggests conflict policing mechanisms between intra-organismic genes or elements, selection at the level of the organism and selection at the level of alleles are aligned. This fact accounts for the fact that most often instances of adaptation and of function coincide, since in these cases the cellular or allelic elements are SE functional parts. As a consequence, considering an element as an adaptation implies ipso facto that the reason why it is an adaptation is the reason why it was selected in its organismal system, and therefore is its function. –– Last, this analysis helps to shed light on why functional ascriptions according to ET and according to causal role theory most often overlap, even though they assign different explananda to the functional explanations they consider. Indeed, functions in the etiological sense also presuppose a system that is defined in terms of convergence of selection levels; and when this system is one that a biologist considers (e.g. the organism, as is most often the case), the causal roles of parts in this system (for instance in the case of physiology) will coincide with the functions of SE functional parts.

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8.4.3 Summarizing: Etiological Theory and Multiple Selection Levels The condition of incorporation allows for a sort of generalized etiological theory of functions. Let’s imagine a “simple” world where there is only one level of selection. In this world, a system S can be considered as the sum of its traits Xi, because no trait has evolutionary interests that are not aligned with S’s interests. Now, if Xi is selected for Ai, we can say that Xi is an adaptation for Ai; but we can also say that Xi is there because it does Ai, and therefore that its function (etiologically speaking) is Ai. In this world, adaptations and SE functions in the standard etiological sense correspond to each other and coincide furthermore with CR functions in the sense of causal role theory when the considered system is S. In our real world, the adaptive status of X - namely, if and why it was selected and is, therefore, present - does not necessarily correspond to its role in a system S, especially an organism. X can indeed be selected for an effect which on average is damaging for the organism, as in the case of segregation distorters or autosomal killers seen above. The plurality of levels of selection thus implies that the triple correspondence (adaptations - SE functions - CR functions) which held in our imagined “simple” world is not taking place anymore. In particular, entities or traits which are parts of the system can thus have adaptations that are not functions for organisms, as with selfish DNA. The expanded etiological theory sketched in §8.4.1, which added the clause (I) of incorporation and defined SE functional parts in terms of selection, is therefore an extension of etiological theory in the real world, where the levels of selection do not always overlap. And this is so even though, in many cases, and in particular with respect to the fair amount of biological cases involving ordinary organisms which are mentioned as typical examples in philosophical debates about functions (the heart, the kidneys, etc.), considering one single selection level is still a good approximation of what happens. However, accounting for the theory of selfish genetic elements and cases of heterozygote superiority like sickle cell alleles requires us to reconsider the standard theory and to integrate the plurality of selection levels.

8.5 Connecting the Debate About Functions to the Debate About Adaptationism 8.5.1 Gould and Lewontin’s Critique and the Debate Over the Standard Etiological Theory of Functions The notion of SE functional parts and the reference to multi-level selection, appealed to in the context of the demarcation between concepts of functions and concepts of adaptations, allows us to reconsider the relationship between two important controversies in the philosophy of biology – that of functions and that of adaptationism.

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The latter, first appearing in the famous paper by Gould and Lewontin (1979), concerns the legitimacy of a method that would analyze organisms through a sum of atomized traits, each resulting from a process of optimization by natural selection.9 In this context, Gould and Lewontin highlighted that the organism is an integrated totality, so this method of atomization/optimization cannot justify the organism’s systematic integration, which they call Bauplan according to the tradition of the transcendental morphologists of the nineteenth century (e.g. Rehbock, 1983). Insofar as adaptation and function in the sense of standard etiological theory overlap, one can say that Gould and Lewontin’s critique is directed against an all-­ sufficient comprehension of organisms from the sum of the (etiological) functional explanations of traits. And on the other hand, I indicated that numerous critics of etiological theories have examined the question of the systematic integration of functional traits: the concept of design came back to the forefront of the scene (Kitcher, 1993; Godfrey-­ Smith, 1994; Buller, 2002; Wouters, 2007; Huneman, 2013a) to mean the systematic whole within which all traits that have etiological functions concur and converge, but which is not the simple sum of these traits. This is why some of these authors have argued that the standard etiological theory could not account for the totality of functional explanations in biology and that it should be complemented by a causal role approach (Kitcher, 1993; Wimsatt, 2002; Wouters, 2006), which is mandatory in certain disciplinary fields such as morphology (Amundson & Lauder, 1994). In substance, the criticism aimed at etiological theory highlights that it could not on its own make sense of the functional architecture of organisms: some traits are not here because they do something, but because they are part of an organism, and therefore are here just because of their being connected to other traits. Morphology features such connections, for instance the laws of allometry make the size of some body parts dependent upon other parts. In other cases, the selection for an upright stance entailed consequences for the whole body, such as the existence of a chin or the disposition to suffer backache. More vividly, the female clitoris, like the male nipples, is there because of the general body plans of hominids; it does not owe its existence to its doing anything, as argued by Lloyd (2005). And at the genetic level, correlations exist to the extent that many alleles are pleiotropic, namely they have an effect on distinct traits. These can be morphological traits as well as behavioral traits, such as life history theory has shown, for instance in the case of the “antagonistic pleiotropy” theory of senescence first suggested by Williams (1957).10

 For an analysis of what “adaptationism” means, see Godfrey-Smith, 2001. For an analysis of the reasons why giving up adaptationism should require a reformatting of the structure of evolutionary biology, see Huneman (2017). 10  According to Williams, senescence occurs because alleles that have antagonistic effects at distinct periods – especially a positive net effet on reproduction at reproductive time and a negative effect on survival at a later time – will be selected and accumulate (Williams, 1957). It constitutes the basis of one of the two major evolutionary explanations for the phenomenon of aging and natural death. See Huneman 2023, section 2 for a systematic analysis of this account, and the structure of the evolutionary theories of aging and death. 9

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Those correlations imply that not all traits should be ascribed a function in the etiological sense, even when they seem to do something useful for the organism. Those considerations indeed call for a complementation of the standard etiological theory: Wouters (2006) emphasized design explanations, which refer to those things a trait does within a design and can be explanatory of the overall functioning of the organisms even though it is not an etiological function; Huneman (2013a) indicated that in some cases the etiological function is not enough fine-grained and should be supplemented by such a design analysis. We see here that the limits superimposed on the standard etiological theory by all these phenomena pertaining to the integrated architecture of organisms directly overlap the major reasons for Gould and Lewontin’s critique of adaptationism. Nothing surprising here since the concepts of function, according to etiological theories, and of adaptation are partly overlapping: limits to the claim that adaptation is overarching therefore convert into limits to the claim that everything has a function, and reasons for pointing out the first limits are reasons to conceive of the second limits. Moreover, regarding the standard etiological theory, the adaptation/ function overlap seems complete (§8.2 above), and therefore, radical adaptationism and generalized quest for functions fall together. Thus, my demarcation between adaptation and function (§8.4), based on the incorporation clause may shed a light on the explanatory role the architecture of an organism plays regarding both functional ascriptions and adaptation research. If having a function Z means, as I said, being something selected for doing Z, and part of a system undergoing converging selection pressures, then only adaptations can be functions, and not traits connected to these adaptations through an architecture. But some adaptations are not functions, as we saw, hence limits to adaptation are not limits to functional attributions.

8.5.2 Functions, Levels of Selection and the Limits of Adaptationism From our perspective, understanding the notion of an organism’s architecture in evolutionary terms implies placing the organism into an evolution that has in some way brought genetic or selfish cellular elements into integration within a single being which lives and reproduces for itself. Understanding this integration process constitutes a research program first introduced by Buss (1987), who examined the emergence of the sequestration of the germinal line in metazoan organisms, and then pursued under the name of “major evolutionary transitions in individuality” (Maynard-Smith & Szathmary, 1995). It is the search for the general and particular models and scenarios explaining the emergence of collective individuals on the basis of elements previously living by themselves, such as the way from bacteria to multicellular organisms (e.g Michod, 1999; Bouchard & Huneman, 2013). Most of the theoretical attempts elaborated within this research program rely on multi-level

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selection models (namely selection antagonistically taking place at the level of the individual and at the level of the group). Within the context of the present chapter, the amendments to the etiological theory proposed by the authors mentioned above can thus be understood as reflecting the necessity of situating the etiological account within the framework of a general presupposition about the coherence and the alignment of selection levels, an alignment which is itself a result of evolution. The requisite of an incorporation clause (I) constitutes the expression of such a  general presupposition, and therefore, it can be seen as the most general expression of a revised etiological theory that does not fall under the objection of using hyperbolically or excessively the assumption that selection is at play and shapes functions. Furthermore, most generally, the presupposition of the existence of an evolved architecture, which was brought up here to qualify the standard etiological theory, is not restricted to the relationship between organisms and sub-organismic levels. Actually, molecular biology, often in the form of systems biology (e.g. Green, 2015), more and more brings architectures to light at the genomic level (e.g. Hansen & Wagner, 2001; Fenster & Galloway, 2000) and examines their evolution11 as well as their robustness (Wagner, 2005). Along the lines of what I just said, the problems of architecture, in general, can be understood as problems of integration of selection levels, which are thereby also evolutionary questions. Then, whatever their level (organismic, infra- or supra-organismic), functional ascriptions must undoubtedly assume the existence and the robustness of such architectures as a fact. As I said, the critique of adaptationism, as well as the efforts to criticize or rectify the standard etiological theory, seem to share a common worry about placing selectionist considerations within the systematic contexts of architecture. The incorporation of clause (I), and thus my emphasis on the notion of “SE functional parts,”, was initially intended to solve some issues regarding the etiological theory, and more generally, attempted to put it within the more general context of multi-level selection theory (while multi-level selection wasn’t taken into account in its first formulations by Wright, Millikan or Neander). This should also have consequences regarding the limits of adaptationism, given the coextensiveness of the concepts of adaptation and etiological function, and the subsequent affinity between critiques of adaptationism and reforms of etiological theory. Briefly said, the argument here would be the following: (a) Not all traits are adaptations; many traits are purely architectural traits. (b) Functional explanations of traits should assume an architecture in which traits take place. (c) By so doing, one can rely on a sort of default hypothesis, namely, traits are architectural traits, and ask whether traits should be explained otherwise, with a more “onerous” (Williams, 1966) concept, namely by appealing to adaptations or functions.

 See, e.g., Lynch, 2007, for a plausible hypothesis about the evolution of the architecture of the genome. 11

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(d) Finally, this architecture is itself the robust result of an alignment of selected processes at the level of its whole and at the lower levels; parts of this architecture are the SE functional parts described above. To this extent, the present revision of the SE theory, which was intended to avoid the “redundancy objection” (namely the objection that “SE function” is redundant with “adaptation”), also supports an answer to the critique of adaptationism. To sum up, regarding the extensions of various concepts used in evolutionary biology: Organisms have traits and parts. (Against extreme adaptationism) Some, but not all, traits and parts are adaptations (namely they result from some selection). (Against the standard etiological theory) Among them, some, but not all, have a function. Regarding these, for the same reasons as the reason why they have a function  – namely they are SE functional parts – chances are high that their function will coincide with their causal role according to physiology.

8.6 Conclusion I wanted to examine the difference between the concepts of function and adaptation within the etiological theory. Borderline cases such as sickle-cell anemia and selfish genetic elements suggested that, notwithstanding a quasi-general overlap of these two notions, they sometimes enter into conflict. In this sense, adaptation and function are two distinct concepts, in spite of the fact that the same entities often instantiate the two. To clear up this conceptual difference, I have called on the theory of multi-level selection, which is massively mobilized in the research on selfish genetic elements (e.g. Burt & Trivers, 2006) and on evolutionary transitions in individuality Michod (1999). According to my analysis, the conceptual difference between adaptation and function in the etiological sense is the presence of conditions – within the notion of function  – that concern the relationships between selection levels on a system and on its parts. These conditions are most often unnecessary or implicit since there are not always conflicts between selection levels. Developing this view, we can envision an etiological theory of function which is to the recently developed notion of multi-level selection what the theories of Millikan and Neander were for natural selection in general. In this sense, this expanded theory could be integrated into a general reflection about the relationships between organism architecture and functionality, such as they were outlined from the philosophical criticism of adaptationism. Further reflections should be deployed to connect this revised etiological theory of functions to the weak realistic etiological theory (Huneman, 2013b) and to discuss the relations of the idea of an assumed architecture here  –  based on the notion of selection alignment –, with distinct notions of architecture at various levels (organism, cell, genome, holobiont (Rosenberg & Rosenberg, 2018), ecosystems).

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Huneman. (2017). Variation, extension and selection: A synthesis of the reasons for a new evolutionary synthesis. In P.  Huneman & D.  Walsh (Eds.), Challenging the modern synthesis. Development, inheritance and adaptation (pp. 68–110). Oxford University Press. Huneman, P. (2020). Biological individuality as weak individuality: A tentative study in the metaphysics of science. In A. S. Meincke & J. Dupré (Eds.), Biological identity (Vol. 2020, pp. 40–62). Routledge. Huneman, P. (2023). Death. Perspectives from the Philosophy of Biology. Palgrave McMillam. Huxley, J. (1942). Evolution: The Modern Synthesis. Harper and Brs. Kerr, B., & Godfrey-Smith, P. (2002). Individualist and multi-level perspectives on selection in structured populations. Biology and Philosophy, 17(4), 477–517. Kitcher, P. (1993). Function and design. In P.  A. French, T.  Uehling, & H.  Weltstein (Eds.), Midwest studies in philosophy (Vol. xviii, pp. 379–397). Lewontin, R., & Dunn, L. (1960). The evolutionary dynamics of a polymorphism in the house mouse. Genetics, 45, 65–72. Lloyd Elisabeth, A. (2005). The Case of the Female Orgasm: Bias in the Science of Evolution. Harvard University Press. Lynch, M. (2007). The Origins of Genome Architecture. Sinauer. Maynard-Smith, J., & Szathmary, E. (1995). The major evolutionary transitions. Freeman. Michod, R. E. (1999). Darwinian dynamics. Oxford University Press. Michod, R. E., & Roze, D. (2001). Cooperation and conflict in the evolution of multicellularity. Heredity, 81, 1–7. Michod Richard E., Nedelscu A. M. (2003). Cooperation and conflict during the unicellular- multicellular and prokaryotic-eukaryotic transitions, In Moya, Font (Ed.), Evolution: From molecules to ecosystems (pp. 195–208). Oxford University Press. Millikan, R. (1984). Language, thought and other biological categories. Cambridge, MIT Press. Millikan, R. (2001). Biofunctions: Two paradigms. In A.  Ariew, R.  Cummins, & R.  Perlman (Eds.), Functions: New essays in the philosophy of psychology and biology (pp.  113–144). Oxford University Press. Mossio, M., Saborido, C., & Moreno, A. (2009). An organizational account of biological functions. British Journal for the Philosophy of Science, 60(4), 813–841. Neander, K. (1991). Functions as selected effects: The conceptual analyst’s defence. Philosophy of Science, 58, 168–184. Okasha, S. (2006). Evolution and the levels of selection. Oxford University Press. Orgel, L. E., & Crick, F. H. (1980). Selfish DNA: the ultimate parasite. Nature, 284, 604–607. Pradeu. (2013). Immunity and the emergence of individuality. In F. Bouchard & P. Huneman (Eds.), From groups to individuals: Evolution and emerging individuality (pp. 77–96). MIT Press. Queitsch, C., Sangster, T. A., & Lindquist, S. (2002). Hsp 90 as a capacitor of phenotypic variation. Nature, 17, 618–624. Reeve, H. K., & Sherman, P. W. (1993). Adaptation and the Goals of Evolutionary Research. The Quarterly Review of Biology, 68(1), 1–32. Rehbock Philip F. (1983). The Philosophical Naturalists: Themes in Early Nineteenth-Century British Biology. University of Wisconsin Press. Rosenberg, E., & Zilber-Rosenberg. (2018). I. The hologenome concept of evolution after 10 years. Microbiome 6, 78. Sober, E. (1984). The nature of selection. MIT Press. Sober, E., & Lewontin, R. (1982). Artifact, cause and genic selection. Philosophy of Science, 44, 157–180. Sober, E., & Wilson, D. S. (1998). Unto others. Harvard University Press. Sterelny, K., & Kitcher, P. (1988). The return of the gene. Journal of Philosophy, 85, 339–360. Trivers, R. L. (1971). The evolution of reciprocal altruism. The Quarterly Review of Biology, 46, 35–57. Turner, D. (2000). The functions of fossils: Inference and explanation in functional morphology. Studies in History and Philosophy of Biology and Biomedical Sciences C, 31, 193–212.

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Chapter 9

Function, Adaptation, and Design in Biology Gustavo Caponi

Abstract  The main misunderstanding of the etiological conception of the concept of function is to confuse this notion with the concept of adaptation. The explanations by natural selection do not justify function attributions: They explain the configuration of an organic structure by considerations that, among other elements, also include references to the functional performance of this structure. That is why, the best manner of characterizing them is to say that they are design explanations. However, for a correct formulation of the idea of design, it will be necessary to adopt a conception of the function attributions that could avoid the difficulties of the etiological conception. For this, it will be necessary to think of functions as causal roles.

9.1 Introduction Despite its unjustifiably restrictive character, the etiological approach to the concept of function, initially outlined by Larry Wright (1972, 1973) and later taken up by Karen Neander (1998) and Ruth Millikan (1998, 2002), has succeeded to preserve its hegemony in the field of Philosophy of Biology (cf. Hardcastle, 1999, p.  27; Buller, 1999, p. 19; Lewens, 2007, p. 530). Protected by the well-deserved prestige This chapter resulted from the discussion held during my lecture “Explication fonctionelle et explication sélective,” which I gave on 20 June 2006 during a session of the Séminaire Structure et Fonction  – L’inférence fonctionnelle organized by Jean Gayon and Phillippe Huneman at the Institut d’histoire et philosophie des sciences et des techniques of Sorbonne. To both organizers, and to all those who participated in the discussion, my sincere thanks. In addition, I also must thank the valuable observations made by the reviewers of Signos Filosóficos: They allowed me to improve my work. This was originally published, in Spanish, in the issue 24 of that Mexican journal (cf. Caponi, 2010), which has been generous enough to allow its inclusion in this volume. G. Caponi (*) Federal University of Santa Catarina, Florianópolis, Brazil © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_9

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of the Theory of Natural Selection, this conception has been held in spite of the flagrant error implied in the questioning of any function attribution that is not based on a selective explanation. This questioning, in fact, can only be accepted if we disregard how these attributions are legitimated in those domains of Life Sciences where they are more common: Physiology and Autecology. I believe, however, that the fundamental error of this position is not that one. I think, and this is what I will sustain in this chapter, that making function attributions dependent on selective explanations is wrong because it implies not knowing that these last explanations already presuppose the acceptance of function attributions and functional analysis. Selectional explanations, I think it is necessary to clarify this point, are not functional analyses. They do not explain how something operates or how something works. They explain the configuration of an organic structure, or the attributes of a living being, resorting to considerations that, of course, include references to the functional performance of that structure or to the exigencies that the living being must respond to survive and reproduce. Therefore, perhaps the best way to characterize selectional explanations, is by saying that they are design explanations: They explain why living beings are designed in the way they are (cf. Dennett, 1990, p. 187, 1996, p. 186). However, for reaching an accurate formulation of the idea of biological design, it will be necessary to adopt a conception of function ascriptions that could avoid the difficulties of the etiological conception; for that, I will appeal to something very close to its official challenger: the causal role conception of the concept of function defended by Robert Cummins (1975). Although, in fact, my understanding of this concept derives, mainly, from some theses exposed by Margarita Ponce (1987) in The Teleological Explanation.

9.2 The Major Mistake of the Etiological Conception The etiological conception of function was originally proposed by Larry Wright (1972), who already presented it as being valid for both organisms and artifacts. Assuming that conception, if we consider a part or piece that integrates a device designed by a human being (or by any other intentional agent), we will say that the function of this item is the effect on the operation (or total performance) of the device that the designer was looking for when she decided to place that element where, in fact, it is (Lawler, 2008, p. 332). From this perspective, the function of the bicycle crossbar would be not to carry an extra passenger as we used to do in childhood but to make steadier the structure of the vehicle. That is to say: Despite the occasional use that may be given to that part of the bicycle, its function, in a strict sense, its proper function, is that use effectively foreseen and sought in the process of designing the vehicle. Thus, both in the case of the bike and in the case of any biological structure, the etiological perspective leads to thinking that a function attribution always obeys this scheme that Wright (1972, p. 211, 1973, p. 161) had highlighted:

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To say, “the function of x (in the system or process z) is y” supposes to accept that [1] X produces or causes y. [2] X is there (in z) because it produces or causes y. In the case that z is a system or process designed and built by an intentional agent, clause [2] means that the designer placed and/or configured x, in z, the way it did, because she expected the effect y to be effectively produced. Therefore, strictly speaking, carrying an extra passenger would not be a function of the bicycle crossbar. It would be, in any case, an accidental function that the manufacturer, at the time of meeting the warranty, should not know that the crossbar was performing when it broke. Meanwhile, in the case of unintentionally designed biological systems or processes, clause [2] will allude to the process of natural selection that configured z and x by rewarding the production of y. Thus, in the context of the Life Sciences, function attributions, as argued by the proponents of the etiological perspective, have to obey this particular variant or specification of Wright’s scheme: To say that “the function of x (in the z system or process) is y” supposes to accept that [1] X produces or causes y. [2] X is there (in z) because natural selection rewarded the realization of y in the ancestral forms of z. However, and as obvious as it may seem, at first sight, this way of understanding function entails serious difficulties that have already been mentioned by several authors. Those difficulties have to do with the extremely restrictive character of the etiological schema: If it is assumed, many function attributions that currently occur in the discourse of biological sciences go delegitimized. Yet, although those difficulties are very well known, I think that it is still convenient to remember them for understanding what I consider to be the main error, the fundamental mistake, of such etiological conception. The first of these difficulties has to do with the possibility of attributing a function to structures not selected to fulfill that function. The second one has to do with the very idea of considering function attributions as if they were dependent on the Theory of Natural Selection. This idea lies in tension with the fact that such attributions have been made, and continue to be made, in moments and contexts of biological sciences in which that theory did not exist or in which it does not play any epistemic role. The two difficulties, however, are indissolubly linked. Let consider, first, unselected structures that may be functional or even structures that could be selected for a certain function but also fulfill another function for which they were not selected. This is the idea implied in the concept of exaptation proposed by Stephen Gould and Elisabeth Vrba. Even if in that paper they follow George Williams (1966, p. 9), reserving the word “function” to denote the selected effect of a feature (Gould & Vrba, 1998, p. 520), the main point of their argumentation is better understood if we refuse that restriction. The very idea that there are inherited structures that are useful in the fulfillment of certain biological role for which they were not selected indicates that it is only by a terminological decision,

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and not by some deeper theoretical commitment, that Gould and Vrba do not speak of a “not selected function” (cf. Gould & Vrba, 1998, p. 522). Such would be the case, for example, of the hypertrophied clitoris of the spotted hyena. This structure apparently plays a rearing function, an important role, in the mating rituals of that species (Crocuta crocuta), but its evolution may be a side effect of other selective pressures that rewarded females with more androgen secretion by virtue of the larger size they could reach (Gould & Vrba, 1998, p. 529). It could be said, of course, that this accidental social function of the hyena’s clitoris is not its proper function: This mating accidental function was not selected for. However, even to introduce the difference between accidental and proper functions, it is already necessary to assume a concept of function more general than that of function as a selected effect.1 Without that more general concept of function, the very idea of exaptation would not have any sense. I allow myself to say this because it is obvious that that notion was not proposed for referring to not selected effects like the allergic reaction that is, in me, caused by the hair of cat, or like the noise that produces the heart when beating. The idea of exaptation was proposed to qualify those effects that, even if not selected, are functional in some sense that, evidently, is not captured by the etiological conception of functions (cf. Ginnobili, 2009, p. 9). However, there is another difficulty in the etiological conception of function, and it is even more obvious than the first I pointed. I allude to that other difficulty which arises from the fact that the etiological conception makes function attributions conceptually dependent on explanations by natural selection. This, as it has already been observed, implies to deny or ignore everything that happens in the field of Physiology (cf. Nagel, 1998, p. 221; Davies, 2001, p. 112), and to see that it is not necessary to remember the remote pre-Darwinian efforts made by William Harvey (1963 [1628]) for establishing the role, or function, of the heart. From Claude Bernard onward, functional biologists have not stopped working according to a methodological rule that was also Harvey’s rule. That is, for every process, or structure, normally present in a living being, the causal role that this component fulfills in the overall functioning of the organism must be identified (cf. Caponi, 2002, p. 70; Gayon, 2006, p. 486). And it is that causal role that functional biologists call “function” without waiting for a Darwinian justification, and even less a theological justification, of their conclusions (cf. Ghiselin, 1997, pp.  286–287; Weber, 2004, pp. 36–38). Therefore, if, as Ruth Millikan (1998, pp. 297–298) claims, the analysis of the concept of function has to be adapted to the current theoretical frameworks (cf. Lewens, 2007, p. 535), the function attributions made by physiologists must also be considered. If a modern physiologist discovers that the excretion of a malodorous substance allows an animal to eliminate toxic substances existing in its diet, she will not wait for an evolutionary justification for saying that this excretion has the

 Remarks that are similar to that I am making here may be found in Davies (2000, p. 36 n8, 2001, p. 55, 2009, p. 141) and also in Rosenberg and McShea (2008, p. 92). 1

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function of detoxifying the body of that animal. She, in any case, will try a countertest à la Bernard, trying to prevent that excretion, in order to see if the animal goes indeed intoxicated (cf. Schaffner, 1993, p. 145; Delsol & Perrin, 2000, p. 142). If detoxification was really the selected function of that excretion, or if it was selected as a defensive resource to scare away predators, it will be something the physiologist, in the end, will not care about. For her: If the organism is intoxicated and dies when that process of secretion is impeded, detoxification should be considered as a function of that process. For this reason, in physiology, Darwinian conjectures are rather sporadic. Interestingly, such conjectures may also be absent from the observations of naturalists working in the domain of autecology. If a field ecologist analyzes the living conditions of the animal in the previous example and she establishes that it sustains itself by eating toxic plants that would poison it if that excretion did not occur, she will say that she has discovered an important biological role, in the sense of Bock and Wahlert (1998, p. 131), of that operation. But, as these two authors remarked, there the word “function” could be used as a synonym of “biological role” (Bock & Wahlert, 1998, p.  125). That is, it could be used to denote that important role performed by the excretion of those toxic substances in the history of life, or in the vital cycle, of that animal. Likewise, this same ecologist could also discover that this excretion serves, at the same time, to scare away predators; then, she would say that she has discovered another function, without this compromising her to decide, through an evolutionary study, which of these two functions was initially selected. And I think that something analogous could be said of the functional inferences made in paleontology (cf. Rudwick, 1998; Turner, 2000). Although there, in paleontology, the attributions of biological roles are much more difficult to justify than in autecology (Bock & Wahlert, 1998, p. 132; Gans, 1998, p. 560), those attributions still point to the function that a structure could be thought to fulfill in the life cycle of the organism under study. They speak of a past moment because they talk about an extinct being, but they do not refer to the history of the structure which is under analysis.2 Conjugated in past tense, those function attributions and analysis also fulfill what Niko Tinbergen (1963, p.  424) always made very clear: One thing is to ask how a structure contributes, or contributed, to the survival of a living being; and another thing is to ask about its evolutionary history (cf. Lewens, 2004, p. 116). The first questions ask for observing how the considered living being interacts with its environment, which are the problems it has to solve for living and reproducing, and what are the means that it has for solving those problems. Or it is done, in some cases, by trying to reconstruct those interactions and those problems. The reconstruction of the evolutionary history, on the other hand, is always more complicated and requires another type of inquiry. Although the problems of survival that a structure solves at any given moment may give us an important clue about its

 Cuvierian Paleontology always made function attributions to fossil bones, denying, at the same time, any history of the biological structures. 2

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evolutionary history, it is possible that this current function ends up being a misleading indication with regard to the past functions of the structure. It may be that the feature in question is just an exaptation for the biological role detected, and it can hide the true nature of the selective pressures involved in its evolution. The hypertrophied clitoris of spotted hyenas would be a good example of this, and the bony plates of the stegosaurus could give us another (cf. Lewontin, 1978, p. 217). I would not say, however, that making function attributions dependent on explanations by natural selection is wrong just because it is a too restrictive a thesis. I think the error goes beyond that. Making function attributions dependent on selective explanations is wrong, above all, because these explanations already presuppose function attributions (Davies, 2001, pp.  55–57; Ginnobili, 2009, pp.  7–8). Assuming the framework of the Theory of Natural Selection, the frequency of a feature is explained by its performance in the fulfillment of a function, and its configuration is explained by the requirements of that performance. This entails that the functional performance may be identified before the construction of the selectional explanation. Once the function is established, analysis is made of whether the feature under study is an adaptation that evolved due to the demands derived from that exercise, or if it evolved for other causes; thus, it is decided if the feature constitutes a true adaptation, or a mere exaptation, for that function. It can be said, therefore, that the great misunderstanding that is at the very foundations of the etiological conception of functions is to have confused this concept with that of adaptation. This conception ignores that the concept of adaptation is logically subsequent to the concept of function: First, we have to establish the function of a structure, and later we have to determine whether it is an adaptation for that function. That is, whether it evolved by natural selection by virtue of the requirements derived from that functional performance or whether it did so by virtue of other functional requirements that we will also have to identify. Selective explanations, to say it briefly, do not justify function attributions. They assume, or demand, them; considering other facts (cf. Brandon, 1990, p. 165), they allow to attribute to a feature the quality of adaptation. It is this attribution, and not the function attribution, that has an etiological character. Therefore, it is mandatory to seek an elucidation of a general concept of function that is independent and prior to the Theory of Natural Selection (Ginnobili, 2009, pp. 7–8); this can be done by thinking in a consequential way (cf. Garson, 2008, p. 537), not in an etiological way. That is, instead of trying to delimit the concept of function by virtue of the genesis of the functional item, we should do so by virtue of the effect or consequence that the operation or occurrence of that item produces (cf. Garson, 2008, p. 538). It is in this way that we will be able to arrive at a biological concept of function that overcomes the difficulties and misunderstandings of the etiological conception that we have just examined. To do that, however, we will have to proceed in two steps: First, we will have to delimit a general concept of function; and then we will introduce the concept of biological function as being a particular specification of that more encompassing concept.

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9.3 Functions and Life Cycles The general concept of function to which I am alluding is, in fact, a broader formulation of the concept of function as a causal role proposed by Cummins (1975): It is not necessarily referred to “systems” but to any causal process. By assuming it, we will be accepting that saying that the “function of x (in the process or system z) is y” only requires assuming that: [1] X produces or causes y. [2] Y has a causal role in the occurrence or operation (or functioning) of z. Thus, given any causal process (z), it can be said that an item (x) has a function within that z, if and only if, the operation or presence of that element has a role or a causal role, some effective incidence, in the occurrence or fulfillment of z. It is very important to stress that it goes for any causal process: the operation of a machine, a physiological phenomenon, the explosion of an aircraft during its take-off, or the movement of the tides. If the movement of the pedals is transmitted from the big sprocket to the small sprocket, and the small sprocket moves the rear wheel, driving the bicycle ahead, we will say that the function of the pedals is to drive the bicycle. If heartbeats make the blood circulate, we will say that pumping blood is the heart’s function in the circulatory system. In the same way, if a plate (accidentally let on the runway of an airport) is sucked by the turbine of an airplane that is taking off, making it explode, we will say that the plate had a function in the plane crash. In the same manner, if we determine that, by virtue of the gravitational attraction exerted on the great masses of liquid, the moon affects the ebb and flow of the tides, we will say that the moon has a function, a causal role, in these movements. Of course, I am not suggesting that a low-budget terrorist group let the plate on the take-off runway for producing that accident. Nor I am suggesting that the moon’s raison d’être is to produce the tides, and that it was created, or placed there, for that purpose.3 I am simply saying that the moon intervenes in that process as the plate might have played a causal role in the explosion of the plane, and it is only by reference to those particular processes that we attribute a function to such objects. Given a larger process, a particular process, or event, takes on a functional relevance within the larger one, without implying that it was there for performing that function. From this perspective, a function attribution does not imply any hypothesis about the origin or construction of the functional system, nor does it imply the denying that, given another reference process, the event or item that was the object of that first attribution may be the object of another or no function attribution.

 The concept of function should not be confused with that of raison d’être. Contrary to what is assumed by the defenders of the etiological conception, the function of something is not always its raison d’être. Even designed devices can fulfill functions that do not explain their existence: A bottle, for example, can function as a projectile. 3

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It is obvious that this way of understanding function attributions supposes that these statements can be done in relation to any causal process: not only in relation to organic processes or to artifacts constructed by intentional agents. This has motivated the objection that this concept of function is too liberal (cf. Kitcher, 1998, p. 494; Amundson & Lauder, 1998, p. 346; Walsh, 2008, p. 353; Perlman, 2010, p. 61). Assuming it, in fact, we can speak, as we often do, of the function of clouds in the water cycle or of the function of the movement of geological plates in the tectonic system. However, for the defenders of the notion of function as a causal role, this alleged excessive liberality is not a difficulty. It just shows that this way of understanding functions envisages all the varied contexts in which we can formulate, and we do formulate, function attributions (cf. Davies, 2001, p. 85). Function attributions, the identification of causal roles, are ubiquitous because the world is a network of causal processes that can be analyzed from a functional perspective. In this regard, the apparently radical attitude of Margarita Ponce (1987, p. 106) seems to be the most correct and coherent. According to her point of view, in functional analysis, the functional entity “is just the phenomenon, or fact, that, in a particular explanation, we understand by virtue of its consequences.” Meanwhile, “the function is the effect of the functional thing that contributes to the achievement of the state of things or of the phenomenon by whose causes we inquire in that same explanatory process” (Ponce, 1987, p. 106). I, however, would prefer to express this idea by saying that in functional analysis the functional entity is just the phenomenon, or element, whose contribution or intervention in the occurrence of a particular process we wish to understand or highlight. The function, meanwhile, is the contribution or intervention of that entity in the aforementioned process. Where there are causal explanations, we could say, there will always be possible functional analyses and attributions. This is so, because these analyses and attributions, as Margarita Ponce (1987, p. 103) also says, are only the reverse of these causal explanations and attributions. It is worth remembering, however, that Ponce goes beyond a simple general legitimation of functional analyses and attributions. In fact, her objective was a full rehabilitation of the ideas of teleology and teleological explanation. For her, the goal of a process or system is nothing but “a state of things that the subject highlights by virtue of her cognitive interests”; it is that assumption that also allows Ponce (1987, pp. 106–107) to affirm that “not only living beings but any fact or any phenomenon can be teleologically explained.” Thus, if this way of understanding teleology proposed by Ponce is accepted, and I see no inconvenience in doing so, the claim that the notion of function as a causal role is devoid of any teleological character or commitment (cf. Cummins, 2002, p.  158; Cummins & Roth, 2010, p. 75) can also be dismissed. Although I remark it, this would not result in rejection but in a better understanding of such conception. Anyway, even if we refuse this weak characterization of teleology proposed by Margarita Ponce, I think that it is still possible to accept that the only restriction that limits function attributions is the interest of the researcher in analyzing a particular process rather than another one (cf. Ponce, 1987, p. 10). If the noise produced by heart when beating does not seem to be a function of heartbeat, it is because we are

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presupposing that the process under consideration is blood circulation. But if we think of the numbness of a baby when it is in his mother’s or father’s lap, we may think that this noise, if regular and slow, may have a role, a function, in that process. In fact, and unlike the causal relations that are binary (x is the cause of y), functional relations are always ternary (y is the function of x in the process z). If we consider that, we will assume that functional imputations are always restricted and ordered by this ternary character that is inherent to every functional relation. This is what prevents moving from ubiquity to excessive liberality: To have a function is always to have a function within a particular process or system of reference; and when the process of reference is the life cycle of an organism, we arrive at the concept of biological function. Thus, if we accept to say that the inherent, intrinsic, and defining goal of every organism is to establish and preserve its organizational autonomy (despite the contingencies and disturbances of the environment), and if we also accept to call this process (which includes reproduction) “autopoiesis” (Maturana & Varela, 1998, p. 69), we can say that the concept of biological function always alludes to the contribution, or causal role, of a structure, or phenomenon, in the performing of that “autopoiesis.” In this sense, to say that the “biological function of x is y” would simply mean accepting that: [1] X is part of a process or autopoietic system z. [2] X produces or causes y. [3] Y has a causal role in z, or it is a response to a disturbance suffered by z. But, if for some reason the word “autopoiesis” does not sound convenient or entirely appropriate, it is possible to replace it with the word “self-re-production,” which was proposed by Gerard Schlosser (1998). The organisms, in fact, can be characterized as complex self-reproducing systems (Schlosser, 1998, p. 329, 2007, p. 122). They are systems that self-produce and self-preserve, and doing both things, they sometimes reproduce. Thus, considering that it is possible to characterize as functional any effect of a structure or process that, being part of the phenotype (in the extended sense) of such systems (Dawkins, 1999) contributes to its self-­ sustainability and reproduction (Schlosser, 2007, p. 123). Adopting Schlosser’s terminology, it could also be affirmed that, when saying that the “biological function of x is y,” we are assuming that: [1] X is part of a self-reproducing system z. [2] X produces or causes y. [3] Y has a causal role in the self-reproduction of z, or it is a response to a disturbance suffered by this process. Anyway, it is possible to appeal to a more classical language. Instead of using the expressions “autopoiesis” and “self-re-productive system,” we can use the expression “life cycle” as it was used, for instance, by Edward Stuart Russell (1945, p. 5) in The directiveness of organic activities. In that case, the general scheme of biological functional imputations could be outlined in its broader way, making clearer that such imputations not only allude to phenomena related to physiology and

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development but also allude to those processes and structures, generally studied by autecology, which, like mimetic colorations, assure or facilitate the adjustment of an organism to its environment. In this case, to say that the “biological function of x is y” would mean accepting that: [1] X is part of the life cycle z. [2] X produces or facilitates y. [3] Y has a causal role in the accomplishment of z, or it is a response to a disturbance or threat suffered by z. But I insist: This last one and the two previous ones are only different versions of the same idea about the function attributions that occur in the biological sciences, an idea that, furthermore, can be characterized as a classic: It is already explicitly formulated in the writings of Claude Bernard (1878, p. 370). Although, as one might expect, in this case, it only seems to refer to functions in a strictly physiological sense, development and ecology are not considered there. Likewise, it also appears enunciated in all its generality in the old dictionary of Abercrombie et al. (1957). “The function of a part of an organism,” as they said, “is the way in which that part helps maintain the organism to which it belongs alive and able to reproduce” (Abercrombie et al., 1957, p. 93); much would have been gained if the current discussions on the concept of function had begun there and not by Wright’s etiological conception.

9.4 The Limitations of Consequential Conception The fact, however, is that this consequential way of understanding function attributions does not seem to satisfy some requirements that the defenders of the etiological conceptions have pointed out as inescapable for any elucidation of the concept of function. The accusation of excessive liberality has been answered here referring to the fact that all function attributions are relative to a particular process and pointing out that the biological functions are always relative to those processes that we call “life cycles.” That, however, is not enough to answer the accusation that the consequential conceptions allow function attributions that do not satisfy these other three requirements that some insist on considering as inherent to that type of statements (cf. Lewens, 2004, pp. 88–89, 2007, pp. 530–531): –– Function attributions must have explanatory value: They must serve to explain why the functional item is there, and, to some extent, why it is as it is. –– Function attributions must be different from the attribution of a supposed benefic accidental effect. –– Function attributions must have a normative character. The first requirement, of course, could never be satisfied by a general causal role conception of functions. Considered from this point of view, the functional relation is, of course, the reverse of a causal relation as long as it is considered as part of a

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process. In that sense, attributing to something a function implies to accept that, in a certain way, the operation of that item explains, at least partly, how the occurrence of the functional effect affects the process that gives sense to that function attribution (Buller, 1999, p. 14). But, differently from what supposedly occur with the etiological conception of functions (Buller, 1999, p.  13), the explanatory operation implicit in that causal role general concept says nothing about the origin and the process of configuration of the functional item (cf. Gayon, 2006, p. 485); this also occurs in the specific case of biological functions. From the mere individualization of the function that the heart fulfills in the organic economy, it is not inferred anything about how beings endowed with heart came to exist, neither is inferred the history of a machine from the simple analysis of its feedback mechanisms. Such analyses, it is true, may give us essential clues to reconstruct the history of machine and organism designs, but these explanations do not follow immediately from such functional analyses. Therefore, if we have to attribute a legitimately teleological character to the functional analyses of physiology or autecology, that will not depend on the fact that such functional analyses imply some information about the history of the functional item in question and about the history of the system analyzed. For that reason, if those analyses can be considered as being teleological, it will be so just because they show the causal contribution of the presumed functional item in the achievement, or preservation, of what we consider the goal or privileged state of the analyzed system (cf. Goldstein, 1951, p.  340; Merleau-Ponty, 1967, p. 165; Polanyi, 1962, p. 360). However, this is just the classic intraorganic teleology that Claude Bernard (1878, p. 340), following Kant (1995 [1790], ∫66),4 already recognized as a fundamental element of the physiological perspective (Caponi, 2002, p. 70). A kind of teleology that, at last, can also be considered a fundamental element of autecological analyses focused on what Bock and Wahlert (1998, p. 131) called biological roles (Caponi, 2002, p. 75), a teleology that, in both cases, is independent of any retrospective etiological consideration: It only refers to the causal contribution that an item, or functional process, makes in the preservation or achievement of the intrinsic goal of a system already configured.5 In this sense, the biological concept of function introduced here seems to weaken the explanatory power of functional imputations. This, of course, is not the case with the etiological conception. For this one, as we saw, to attribute a function to a structure already implies to be able to give an explanation about the history of that  Concerning this aspect of Kant’s thought, see Rosas (2008).  Prima facie, the idea of organic teleology, based on the assumption of goals intrinsic to living beings, seems more restrictive than the notion of teleology proposed by Margarita Ponce. This is so because the first position assumes that the goal in question does not depend on a mere theoretical choice but on something that is proper to or inherent in the object of study. Nevertheless, if we accept that the recognition that a particular physical system constitutes an organism presupposes a functional analysis of its parts in which these are considered by virtue of their causal contribution to the operation and constitution of the whole, that difference is diluted (cf. Kant, 1995 [1790], § 66; Merleau-Ponty, 1967, p. 165; Polanyi, 1962, p. 359). The organic teleology may be thought as just a special case of that generalized teleology pointed out by Ponce. 4 5

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structure (cf. Gayon, 2006, p. 485). It is for this same reason that the conception defended here does not allow to distinguish between the proper function and an accidental, but beneficial, effect, for any structure (cf. Ginnobili, 2009, p. 6). This is obvious in the case of the general concept of function that we assume when, to explain an aircraft accident, we attribute a causal role, or function, to the suction that the aircraft’s turbine makes of a metallic plate left carelessly on the runway. This notion, by itself, does not imply, nor does it suppose, any distinction between proper or selected functions, and accidental effects of a supposed functional item. The situation, however, is not entirely different in the case of the attribution of a biological function. When we regard a life cycle, it may be asserted, or it may be denied, that a particular phenomenon has a function within that process, but if that function is ascertained, that ascertainment will not enable us to say whether that function is or is not only accidentally beneficial. If the excretion of some substances existent in an animal’s diet keeps this animal detoxified, we cannot infer from this fact, whether the anatomical-physiological conformation which permitted such operation was, indeed, rewarded by natural selection for allowing such detoxification, or whether the rewarded effect was the rejection which that excretion produced on predators. Once again, the conception of function defended here seems to weaken the cognitive value of function attributions. And from the etiological point of view, that weakening would be ratified by the fact that the consequential point of view does not allow to discriminate between the bad or good performance of a functional item. From the etiological point of view, attributing a function to a structure implies being able to make judgments about the good and bad functioning of that structure; that discrimination, in the case of many function attributions considered valid under the causal role conception of function, is not possible (cf. Walsh, 2008, p.  354; Krohs & Kroes, 2009, p. 9; McLaughlin, 2009, p. 95). If a plate, accidentally left on the runway of an airport, is not sucked into the turbine of an aircraft on takeoff because it was too heavy, it does not seem to make sense to say that it works badly, or that it did not fulfill its “destructive function.” On the other hand, if the brake system of an airplane fails in a landing, and this produces an accident, it will be compulsory to conclude that the dispositive did not work or that it did not work correctly. This is so, as the defenders of the etiological conception consider because we are supposing that the brake system was designed and was there to fulfill that function that, in fact, it did not fulfill (cf. Lawler, 2008, p.  334). The etiological conception, unlike the causal role conception of function, allows speaking of functions legitimately ascribed, but circumstantially not fulfilled. However, this weakness in the causal role conception of function seems less evident in the case of a biological function. This last notion allows distinguishing between functional items that contribute to the realization of an organism’s life cycle and dysfunctional items that positively conspire against that realization. We can say that a tumor is dysfunctional without knowing anything about its etiology. Furthermore, once we know the contribution, perhaps accidental, that a structure makes to the realization of the life cycle of an individual organism, we can evaluate its performance. If this structure stops making this contribution (to the metabolism,

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the development, or the ecological interactions of the organism), we will say that this structure has lost the biological function that it performed. In the same way, if the structure begins to do so with lesser efficiency than before, we will say that it is no longer fulfilling this function with the same degree of efficiency (cf. Walsh, 2008, p.  356). Inevitably, our evaluations will have to be based on comparative analyses, but those comparisons will not be arbitrary: They will be relative to the contribution that those functional items make in the fulfillment of the life cycle of the organism under consideration (cf. Cummins & Roth, 2010, p. 79).

9.5 The Etiological Illusion Those judgments and evaluations of efficiency also happen in the case of structures that fulfill similar functions in different organisms with similar life cycles. In the case of structures that perform similar or identical biological functions, we can establish comparisons between the functional performances of both, which is essential in the construction of selective explanations. Those explanations suppose differences and comparisons of functional performance between the variants of a structure in organisms of the same population and with similar life history. Far from giving support to functional analyses, the selectional explanations suppose their preexistence (cf. Davies, 2001, p. 55). This is the same as repeating what we also said when we criticize the etiological conception of function: The notion of adaptation supposes the notion of function, and this latter notion is conceptually independent of the former (cf. Ginnobili, 2009, pp. 20–21). Thus, considering these latter remarks, the supposed advantages of the etiological perspective vanish like an illusion. It is undeniable that, when thinking about functional analyses in reference to life cycles, we accept to lose the supposed explanatory capacity that the etiological conception attributes to such analyses. Likewise, it is also undeniable that, when thinking in that way, we accept that function attributions do not allow discriminating between accidentally beneficial structures and adaptations, or between accidental functions and proper functions. Even so, we cannot overlook that this fact is also undeniable: Either for formulating a selectional explanation of the functional structure or for establishing the difference between adaptations and exaptations, we need previous functional analyses of the structures under consideration. Without such analysis, I repeat, there is no selective explanation; without this cognitive operation, we can neither explain the history of a functional structure nor discriminate between genuine adaptations and mere exaptations. The defenders of the etiological conception, nevertheless, superimpose and confuse these selective explanations (based on consequential functional analyses founded on the idea of biological function) with supposed etiological functional analyses. That is why they attribute to those analyses the capacity to explain the history of those functional structures, considering them as the key for discriminating between adaptations and exaptations. However, if we avoid this confusion, and we recognize that selective explanations and functional analyses are different cognitive operations that aim different cognitive

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targets, we will be able to accept these supposed limitations of the biological conception of function. We will recognize that functional analyses are not responsible for providing histories of the analyzed systems, and we will understand that they do not and must not permit discrimination between adaptations and exaptations. Those histories and discriminations, we will see, are the matter of those selective explanations that explain the design of organic structures, relying, although not exclusively, on knowledge of their functioning. But, it is also very important to understand that, between those different cognitive operations, there is a perfect complementarity. The selective explanations of organic design provide knowledge that is inaccessible from a purely functional perspective, but those selective explanations are not possible without previous functional analyses. The selectional explanations are built on functional analyses, and they allow the establishment of etiologies and discriminations which is not the job of functional analysis to establish. The supporters of the etiological perspective are right to assume that in biology there is more than mere functional analysis of the contribution that an organic structure can make to the realization of a life cycle, and they are also right to assume that the history of those structures can be explained by distinguishing between adaptations and exaptations. They are wrong, however, for not seeing that this is a matter for that other cognitive operation called “selective explanation.” However, some defenders of the consequential conceptions of function are also mistaken. Those that, à la Cummins (2002, p.  162), do not want to recognize the legitimacy and viability of investigations that, by their nature and objectives, are irreducible to the mere functional analysis do not see an important part of the question. Without incurring in the pluralism on the notions of function proposed by authors such as Godfrey-­ Smith (1998), Amundson and Lauder (1998), Beth Preston (1998), Millikan herself (1999), Robert Brandon (2006), and Mark Perlman (2009), we must recognize that adaptation and function are different notions and that they obey different cognitive operations. The first one is proper of Evolutionary Biology, and the other one is key in Functional Biology and in Autecology.

9.6 Explanations and Attributions of Design Selective explanations are not functional analyses. Their ultimate target is to explain the features and not the functioning of living beings. That is why it is possible to characterize them as design explanations. Their objective is not to explain how living beings function or how they interact with the environment, but to explain why living beings are the way they are, why they have the shape they have and not some other shape, and even why they interact with the environment the way they do. To achieve this objective, selective explanations appeal, although not exclusively, to functional analyses that allow us to infer the selective pressures capable of explaining organic profiles. Maybe, it would be suitable to say that selective explanations are morphological explanations. They, as I just said, explain the characters of the different lineages of

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living beings, and choosing this expression would avoid possible misunderstandings. Although the idea of biological design is commonplace in the discourse of modern Biology (cf. Wainwright et al., 1980; Weibel et al., 1998), those penultimate vicissitudes of natural theology that today appeal to the so-called “intelligent design,” for explaining the profiles of living things, seem to have made the use of that word uncomfortable again. I prefer, however, to continue to use the expression “explanation of design.” The questions about organic profiles that are answered by explanations by natural selection, as Dennett (1996, pp. 212–213) has shown, promote a hermeneutic of the living beings that keep a clear and significant isomorphism with reverse engineering. In both cases, it is assumed that each feature of an organism or artifact was selected in virtue of the fact that, at a given moment, that feature was the best alternative, effectively, available for the fulfillment of a certain function. Furthermore, the expression “design explanation” makes clearer the idea that natural selection is something different from a simple physical process that generates forms, such as the wind erosion that shapes a stone, or the play of physical forces that forms an oil bubble in a glass of water. Natural selection not only configures biological structures but also carves them by increasing their functional performances, and that is why it must be considered as a design-producing process – a process whose steps have a raison d’être that it is not a purely physical necessity, like the one that governs the formation of a cloud, the structure of a crystal, or even a hormonal reaction. Evolutionary Biology formulates and answers questions about the raison d’être of organic structures that have paragon neither in physics nor in functional Biology; it is the theory of natural selection which legitimizes these questions and allows to answer them (cf. Mayr, 1976, p. 360; Dennett, 1996, p. 129). It is also necessary to clarify what I understand by design explanation is different from what Arno Wouters (2007) denotes with that expression. For him, an explanation of design is a cognitive operation that does not refer to the history of the system or functional item under study, but to a functional correlation among its parts. According to Wouters (2007, p. 72), once it is established that, for being viable, a particular system must comply with certain functions, some of its profiles or elements, or of its total configuration, can be explained, either by showing that, without those profiles or elements, or without that general configuration, such system could not comply with those functions that we attribute to it or by showing that those functions would be complied less effectively if the system’s design were some other. And that is which he proposes to call “design explanation.” Thus, the occurrence of the functional item, or the general configuration of a system, is understood or explained, as Polanyi (1962, p.  360) pointed out in Personal Knowledge, by considering the organizational requirement of such a system, and without making an etiological hypothesis about its history. I do not pretend, however, that Wouters is not highlighting a cognitive operation, a type of analysis, which is very important in biological sciences, that produces biologically relevant knowledge, and that has not yet been duly considered in the discussions on the categories of design and function. I am just saying that we must pay attention to the fact that such alleged “design analyses” are not genuine causal,

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or etiological, explanations of why living things have to accomplish the functions that they accomplish. If we say that gazelles’ legs are suitable for developing high running speeds, we still have to explain why they need to be so fast, which is done by selectional explanations. That is why, the term “design explanation” should be reserved for them. The design analyses pointed by Wouters allow us to understand the functioning of organisms and machines, but they do not say why this way of functioning was required. Appropriately, Wouters (2007, p. 79) says that these analyses allow knowing the requirements that have to be satisfied by the living, to be able to live. They, using the language of George Cuvier (1817, p. 6), show the correlations between structure and function that living beings must satisfy for keeping their conditions of existence (cf. Caponi, 2008, p. 41). However, those analyses do not explain why those conditions’ existence have, or had, to be satisfied in the particular way in which they are, or were, in fact, satisfied by some particular group of living beings. So, even though it is obvious that organs such as the lungs are necessary for air-breathing, without knowing that such structures derive from the swimming bladder of fish, it could never be explained either why the lungs are the way they are or why there were lineages of fish that evolved toward that mode of breathing; these are precisely the issues which Darwinian selective explanations seek to clarify. Therefore, although it is true that those analyses, pertinently highlighted by Wouters, are a fundamental condition for these etiological or evolutionary explanations, it is also true that they do not replace them (cf. Lauder, 1998, p. 514): A functional requirement is never enough to explain the design. This is so for several reasons: because the very conditions that impose those needs can be circumvented; because there is not always a single way to meet those needs; and because the alternatives available to do so depend, basically, on the very history of the organic design being studied. Insects, for example, exercise aerial respiration without lungs. Further, besides explaining the origins of biological designs, selective explanations also help to justify design attributions. They allow saying, not that a structure fulfills a function, or even that it is a necessary condition for its fulfillment, but that the structure evolved to be able to fulfill it or to fulfill it in a more efficient way. They, in short, allow to decide whether a structure is or not a genuine adaptation; to say that, to define a structure as an adaptation, is to formulate a design attribution: It is to affirm that the structure considered is naturally designed. The structure is as it is because it evolved in attendance to selective pressures that rewarded the increase of its functional performance. As Collin Allen and Marc Bekoff (1998, p.  578) showed, it is possible to characterize a structure x as being (naturally) designed to do y, if the following conditions are met: [1] Y is a biological function of x. [2] X is the result of a process of change (anatomical or behavioral) due to natural selection that made x more efficient to perform y than its ancestral versions. But unlike Allen and Bekoff (1998, p. 574), I believe that for this characterization of the design concept to be satisfactory, we must avoid the error of accepting an

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etiological conception of function. If we do not avoid it, the definition of the naturally designed object would be burdened with the difficulties and misunderstandings that afflict the etiological conception of function. Contrary to Ulrich Krohs (2009, p. 73), and also contrary to Philip Kitcher (1998, p. 479), I consider that the notion of design must be defined using the notion of function. Function is a concept more primitive, more basic and simple, than design, so function can and must be used to define design (and that without incurring in pleonasm). For that, it is necessary to leave aside the etiological perspective and to assume a consequential conception of the concept of function as I proposed here. If it can be established that some profiles of any organic structure were selected by virtue of the best fulfillment of some functions relevant to the life cycle of its carriers, then it can be said that the structure is designed by virtue of the fulfillment of that function. Thus, even if an organic structure plays a relevant role in the life cycle performance of a given organism, if it was not selected for the fulfillment of that function, or if its profiles were not modified by virtue of that performance, it cannot be said that it is designed to fulfill that function. This is the same as saying that that structure, instead of being an adaptation, is merely an exaptation for that function. To be designed is not the same as to be convenient or adequate for the fulfillment of a function: To be designed implies to have been modified or built by virtue of that fulfillment, and for that reason, it can be said that the vestigial structures that today do not fulfill any function are also designed structures. The human appendix, in that sense, can be considered an adaptation even if it is concluded that, now, it does not fulfill any biological function (cf. Sterelny & Griffiths, 1999, pp. 217–218). This structure had a function in the past of our lineage, and its form evolved by virtue of that function. That is why, we can say that it is designed, like a Paleolithic ax which nobody uses to hit anymore but it fulfilled that function. On the other hand, even though an organic structure may fulfill a function in the life cycle of an organism, it will not be said that it is designed for that function as long as it is not established that it evolved, and was modified, by virtue of a more efficient fulfillment of its causal role within that process. Incidentally, the aroma produced by a plant when it metabolizes a toxic substance which contaminates the soil in which it grows may help it to drive away insects which have just invaded the region; in that case, it may be said that, in such circumstances, the aroma performed an important function in the life cycle of the plant. But even so, it cannot be said that the ability to produce that aroma is a designed feature: It cannot be said that it is an adaptation. This capacity did not arise in response to the selective pressure resulting from the presence of the pest; therefore, although it is useful as protection, this capacity cannot be considered as an adaptation to such a function. With regard to this function, it can be concluded that it will only be a mere, albeit opportune, exaptation. Anyway, if the pest becomes a constant presence and the capacity to generate that protective aroma presents a hereditary variability, such that some plants could be capable of producing a more intense and repellent aroma than other plants of the same population, then there will be the emergence of a selective pressure that will reward any

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hereditary metabolic modification that could increase that capacity.6 In that case, those modifications promoted by the selective pressure may be considered as adaptations or, which is the same, as naturally designed traits.

References Abercrombie, M., Hickman, C., & Johnson, M. (1957). A dictionary of biology. Penguin. Allen, C., & Bekoff, M. (1998). Biological function, adaptation, and natural design. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 571–588). MIT Press. Amundson, R., & Lauder, G. (1998). Function without purpose: The uses of causal role function in evolutionary biology. In C.  Allen, M.  Bekoff, & G.  Lauder (Eds.), Nature’s purpose (pp. 335–370). MIT Press. Bernard, C. (1878). Leçons sur les phénomènes de la vie communs aux animaux et aux végétaux. Baillière. Bock, W., & Wahlert, G. (1998). Adaptation and the form-function complex. In C.  Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 117–168). MIT Press. Brandon, R. (1990). Adaptation and environment. Princeton University Press. Brandon, R. (2006). Teleology in self-organizing systems. In B.  Feltz, M.  Crommelinck, & P. Goujon (Eds.), Self-organization and emergence in life sciences (pp. 267–281). Springer. Buller, D. (1999). Natural teleology. In D. Buller (Ed.), Function, selection, and design (pp. 1–28). SUNY Press. Caponi, G. (2002). Explicación seleccional y explicación funcional: la teleología en la Biología contemporánea. Episteme, 14, 57–88. Caponi, G. (2008). Georges Cuvier, un fisiólogo de museo. UNAM/Limusa. Caponi, G. (2010). Función, adaptación y diseño en Biología. Signos Filosóficos, 24, 71–101. Cummins, R. (1975). Functional analysis. The Journal of Philosophy, 20, 741–765. Cummins, R. (2002). Neo-teleology. In A. Ariew, R. Cummins, & M. Perlman (Eds.), Functions (pp. 57–172). Oxford University Press. Cummins, R., & Roth, M. (2010). Traits have not evolved to function the way they do because of past advantages. In F. Ayala & R. Arp (Eds.), Contemporary debates in philosophy of biology (pp. 72–88). Wiley/Blackwell. Cuvier, G. (1817). Le règne animal, Tome I. Deterville. Davies, P. (2000). Malfunctions. Biology and Philosophy, 15, 19–38. Davies, P. (2001). Norms of nature. MIT Press. Davies, P. (2009). Conceptual conservatism: The case of normative function. In U.  Krohs & P. Kroes (Eds.), Functions in biological and artificial worlds (pp. 127–146). MIT Press. Dawkins, R. (1999). The extended phenotype. Oxford University Press. Delsol, M., & Perrin, L. (2000). Médecine et Biologie: quelle logique? Masson. Dennett, D. (1990). The interpretation of texts, people and other artifacts. Philosophy and Phenomenological Research, 50(supplement), 177–194.

 For the configuration of a selective pressure, two factors are needed: The environmental factor is needed, which can be a threat or an opportunity for the living beings affected; it is also needed the existence of hereditary variants that favor a better or worse response to this threat or a better or worst harnessing of this opportunity. The ecological variables, by themselves, do not configure selective pressures. A poison that kills indiscriminately and a resource that everyone can use equally are important variables in the ecological environment of a population, but they do not define the selective environment that guides the evolution of the lineage to which that population belongs. 6

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Dennett, D. (1996). Darwin’s dangerous idea. Penguin. Gans, C. (1998). Adaptation and the form-function relation. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 541–570). MIT Press. Garson, J. (2008). Function and teleology. In S. Sarkar & A. Plutynski (Eds.), A companion to the philosophy of biology (pp. 525–549). Blackwell. Gayon, J. (2006). Les biologistes ont-ils besoin du concept de fonction? Palevol, 5, 479–487. Ghiselin, M. (1997). Metaphysics and the origins of species. SUNY Press. Ginnobili, S. (2009). Adaptación y función. Ludus Vitalis, 17(31), 3–24. Godfrey-Smith, P. (1998). Functions: Consensus without unity. In D. Hull & M. Ruse (Eds.), The philosophy of biology (pp. 280–291). Oxford University Press. Goldstein, K. (1951). La structure de l’organisme. Gallimard. Gould, S., & Vrba, E. (1998). Exaptation: A missing term in the science of form. In C.  Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 519–540). MIT Press. Hardcastle, V. (1999). Where biology meets psychology. MIT Press. Harvey, W. (1963 [1628]). Movement of the heart and blood in animals. In W. Harvey (Ed.), The circulation of the blood and other writings (pp. 1–112). Everyman’s Library. Kant, I. (1995 [1790]). Kritik der Urtheilskraft. Köneman. Kitcher, P. (1998). Function and design. In C.  Allen, M.  Bekoff, & G.  Lauder (Eds.), Nature’s purpose (pp. 479–504). MIT Press. Krohs, U. (2009). Functions as based on a concept of general design. Synthese, 166, 69–89. Krohs, U., & Kroes, P. (2009). Philosophical perspectives on organismic and artifactual functions. In U.  Krohs & P.  Kroes (Eds.), Functions in biological and artificial worlds (pp.  3–12). MIT Press. Lauder, G. (1998). Historical biology and the problem of design. In C.  Allen, M.  Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 507–518). MIT Press. Lawler, D. (2008). La complejidad del lenguaje normativo empleado para evaluar técnicamente a los artefactos técnicos. Scientiae Studia, 6(3), 329–344. Lewens, T. (2004). Organism and artifacts: Design in nature and elsewhere. MIT Press. Lewens, T. (2007). Functions. In M.  Matthen & C.  Stephens (Eds.), Philosophy of biology (pp. 525–548). Elsevier. Lewontin, R. (1978). Adaptation. Scientific American, 239(3), 212–231. Maturana, H., & Varela, F. (1998). De máquinas y seres vivos. Ed. Universitaria. Mayr, E. (1976). Cause and effect in biology. In E.  Mayr (Ed.), Evolution and diversity of life (pp. 357–407). MIT Press. McLaughlin, P. (2009). Functions and norms. In U.  Krohs & P.  Kroes (Eds.), Functions in biological and artificial worlds (pp. 93–102). MIT Press. Merleau-Ponty, M. (1967). La structure du comportement. Press Universitaires de France. Millikan, R. (1998). In defense of proper functions. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 295–312). MIT Press. Millikan, R. (1999). An ambiguity in the notion of function. In D. Buller (Ed.), Function, selection, and design (pp. 115–122). SUNY Press. Millikan, R. (2002). Biofunctions: Two paradigms. In A.  Ariew, R.  Cummins, & M.  Perlman (Eds.), Functions (pp. 113–143). Oxford University Press. Nagel, E. (1998). Teleology revisited. In C.  Allen, M.  Bekoff, & G.  Lauder (Eds.), Nature’s purpose (pp. 197–240). MIT Press. Neander, K. (1998). Functions as selected effects. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 313–334). MIT Press. Perlman, M. (2009). Changing the mission of theories of teleology: DOs and DON’Ts for thinking about function. In U. Krohs & P. Kroes (Eds.), Functions in biological and artificial worlds (pp. 17–36). MIT Press. Perlman, M. (2010). Traits have evolved to function the way they do because of past advantages. In F. Ayala & R. Arp (Eds.), Contemporary debates in philosophy of biology (pp. 53–71). Wiley/ Blackwell.

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Polanyi, M. (1962). Personal knowledge. Chicago University Press. Ponce, M. (1987). La explicación teleológica. UNAM. Preston, B. (1998). Why is a wing like a spoon? A pluralistic theory of function. The Journal of Philosophy, 95, 215–254. Rosas, A. (2008). Kant y la ciencia natural de los organismos. Ideas y Valores, 137, 5–23. Rosenberg, A., & McShea, D. (2008). Philosophy of biology. Routledge. Rudwick, M. (1998). The inference of function from structure in fossils. In C. Allen, M. Bekoff, & G. Lauder (Eds.), Nature’s purpose (pp. 101–116). MIT Press. Russell, E. (1945). The directiveness of organic activities. Cambridge at the University Press. Schaffner, K. (1993). Discovery and explanation in biology and medicine. Chicago University Press. Schlosser, G. (1998). Self-re-production and functionality: A systems-theoretical approach to teleological explanation. Synthese, 116, 303–354. Schlosser, G. (2007). Functional and developmental constraints on life-cycle evolution. In R.  Sansom & R.  Brandon (Eds.), Integrating evolution and development (pp.  113–172). MIT Press. Sterelny, K., & Griffiths, P. (1999). Sex and death. Chicago University Press. Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20, 410–433. Turner, D. (2000). The function of fossils: Inference and explanation in functional morphology. Studies in History and Philosophy of Biological and Biomedical Sciences, 31, 191–212. Wainwright, S., Biggs, W., Currey, J., & Gosline, J. (1980). Mechanical design of organism. Wiley. Walsh, D. (2008). Function. In S. Psillos & M. Curd (Eds.), The Routledge companion to philosophy of science (pp. 349–357). Routledge. Weber, M. (2004). Philosophy of experimental biology. Cambridge University Press. Weibel, E., Taylor, R., & Bolis, L. (Eds.). (1998). Principles of animal design. Cambridge University Press. Williams, G. (1966). Adaptation and natural selection. Princeton University Press. Wouters, A. (2007). Design explanation: Determining the constraints on what can be alive. Erkenntnis, 67, 65–80. Wright, L. (1972). Explanation and teleology. Philosophy of Science, 39, 204–218. Wright, L. (1973). Functions. The Philosophical Review, 82, 139–168.

Chapter 10

Do Clay Crystals and Rocks Have Functions? Selected Effects Functions, the Service Criterion, and the Twofold Character of Function Antoine C. Dussault Abstract  This chapter discusses the type of counterexample to the selected effects theory of function classically epitomized by Mark Bedau’s case of clay crystals, and more recently illustrated by Justin Garson’s case of rocks differentially eroding on a beach. These counterexamples purportedly show the excessive liberality of the selected effects theory by identifying items that are subject to selection processes, but do not seem to bear functions. I review three broad lines of responses to such counterexamples: the bite the bullet response, which contends that it is perfectly fine to ascribe functions to clay crystals, rocks, and the like; the population response, which argues that clay crystals, rocks, and the like are excluded from the selected effects theory because they do not form populations of an appropriate type; and the service response, which maintains that clay crystals, rocks, and the like are excluded from the selected effects theory because they are not selected for contributions to complexly organized systems. I argue that the service response is the most appropriate one. By attending to what I call the systemic dimension of function, this response yields better unity between the selected effects theory and the non-selected-effects uses of the concept of function that occur in many biological subdisciplines.

10.1 Introduction The selected effects theory of function and its antecedent, the etiological theory, are arguably the most influential theories of function developed in the philosophy of biology (e.g., Wright, 1973; Millikan, 1989; Neander, 1991; Godfrey-Smith, 1994). A. C. Dussault (*) Collège Lionel-Groulx, Sainte-Thérèse, QC, Canada Centre interuniversitaire de recherche sur la science et la technologie (CIRST), Montréal, QC, Canada e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_10

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According to the former, an item’s function is the effect on account of which it was favored under past natural selection. Recently, Justin Garson broadened the selected effects theory, advocating a generalized selected effects theory which ascribes functions to results of any selection process operating on a population (Garson, 2016, chap. 3; 2017, 2019). This includes, besides selection processes involving differential reproduction, those involving differential persistence between entities. Garson’s expansion of the selected effects theory reinforces the case for it by making it more straightforwardly applicable to items such as antibodies in the immune system, synapses in the brain, and behavior dispositions. These items are not subject to natural selection, as commonly understood, but are nevertheless subject to some selection processes. In this chapter, I will discuss a family of counterexamples to the selected effects theory of function (both classical and generalized) whose importance has resurfaced in recent discussions: that of items that are subject to selection processes but do not seem to bear functions. Such items raise a concern of excessive liberality for the (generalized) selected effects theory, because it seems wrongly committed to ascribing functions to these items (Bedau, 1991; Price, 2001, chap. 2; Wakefield, 2005; Garson, 2016, chap. 3; 2017, 2019; Schulte, 2021; Bourrat, 2021). A classical case is Mark Bedau’s (1991) clay crystals, which achieve something roughly equivalent to differential reproduction, and a more recently discussed one is rocks on beaches that differentially persist through their differential erosion (Garson, 2016, 60–61). This type of counterexample has prompted three broad lines of response from proponents of the selected effects theory: first, the bite the bullet response, which contends that it is perfectly fine to ascribe functions to clay crystals, rocks, and the like (Millikan, 1993, 39n7); second, the population response, which argues that clay crystals, rocks, and the like are excluded from the selected effects theory because they do not form populations of an appropriate type for selection processes operating on them to endow them with functions (Garson, 2016, 54–55, 58–61; 2017, sec. 5; 2019, sec. 6.3–6.4; 2022, sec. 3; Schulte, 2021); and third, the service response, which maintains that clay crystals, rocks, and the like are excluded from the selected effects theory because an item may acquire a selected effects function only in virtue of being selected for a service that it provides, or a contribution that it makes, to another system, while selection operating on clay crystals, rocks, and the like do not involve such services or contributions (Price, 2001, sec. 2.2; Wakefield, 2005, 884–885). I will argue here that the service response is the most adequate one. I will do so by maintaining that a theory of function should be able to account for what I call the systemic dimension of function, that is, the idea that functions are contributions to the capacities or activities of complexly organized systems. This dimension, I will argue, is embedded in the pretheoretical concept of function of which theories of function purport to give a principled account, along with another dimension, which I call the teleological dimension of function. The teleological dimension of function consists in the idea that functions are effects that explain the presence of the items that produce them. The items produce the effects because they are advantageous to themselves and/or to a system to which they are related. Together, the teleological

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and systemic dimensions constitute what I call the twofold character of the pretheoretical concept of function. They respond, respectively, to two distinct natural phenomena with which the concept of function has become associated: the self-­promotion phenomenon by which some natural items produce effects that promote their own occurrence, and the system-contribution phenomenon by which some natural items are involved in the realization of the capacities of complexly organized systems. The pretheoretical concept of function has this twofold character by virtue of the fact that the teleological and systemic dimensions are jointly present in paradigmatic cases of biological function bearers, that is, the traits and parts of individual organisms. By linking functions to selection processes, the selected effects theory suitably accounts for the teleological dimension of function. It makes it the case that the functional effects of items explain the presence of these items. However, the selected effects theory can account for the systemic dimension of function only through incorporating a service dimension, that is, through restricting functions to effects that are selected for their contributions to the fitness of a complexly organized system. Although I observe that the teleological and systemic dimensions are both embedded in the pretheoretical concept of function, my defense of the service response is not primarily based on this observation. Instead, I argue that the service response, and the incorporation of a service criterion into the selected effects theory that it entails, are called for by the fact that they yield better unity between the selected effects theory and the non-selected-effects uses of the concept of function that occur in many biological subdisciplines (e.g., ecology). Hence, the key reason why clay crystals, rocks on beaches, and the like do not bear selected effects functions, I argue, is that they achieve differential proliferation and/or persistence in a stand-alone manner, rather than through contributions to the fitness of complexly organized systems. This difference between items like clay crystals and rocks, on the one hand, and paradigmatic function bearers like the traits and parts of individual organisms, on the other hand, explains and justifies our reluctance to ascribing functions to the former. Considerations over whether items like clay crystals and rocks form populations of some appropriate type have no bearing on whether they bear functions (although, as I will suggest in the conclusion, such considerations may bear on whether such items should be seen as teleological or design-like). In Sect. 10.2, I will present the clay-crystal and rocks-on-a-beach counterexamples, and I will highlight the challenge they raise for the (generalized) selected effects theory of function. I will also discuss the population response to counterexamples of this type, and highlight some issues and subtleties that arise with it. In Sect. 10.3, I will present the service response to counterexamples of this type, and propose an improved version of it that draws on Peter Godfrey-Smith’s (1994, 349–350) treatment of a similar challenge raised to the selected effects theory by items like selfish DNA and segregation distorter genes. In Sect. 10.3, I will give support to the service response, by linking it with the above mentioned systemic dimension of function, and by arguing that this response yields better unity between the selected effects theory and the non-selected-effects uses of the concept of function that occur in many biological subdisciplines.

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10.2 Clay Crystals, Rocks on Beaches, and the Population Criterion A classical counterexample to the selected effects theory of function, purported to highlight its excessive liberality, is Mark Bedau’s (1991, 651–654) case of clay crystals.1 A striking feature of clay crystals is that they promote their own growth. Crystals present in a sufficiently saturated solution of silicic acid exert a seeding effect that leads to the formation of new layers of crystals. Clay crystals meet the standard conditions for natural selection (Lewontin, 1970; Godfrey-Smith, 2009). They exhibit variation: The crystals in a set of crystals differ from each other with regard to the patterns they realize. They exhibit inheritance: New layers of crystals tend to replicate the patterns of those from which they are seeded. The crystals thus grow and eventually cleave, and then the resulting pieces become seeds for new crystals with similar patterns. Clay crystals also exhibit variation in fitness: Pattern variations among crystals affect the speed of their growth and the frequency at which they cleave and become seeds for new crystals. This leads some crystal patterns to become prevalent in sets of crystals, in part because they promote the growth and proliferation of the crystals that realize them. Given these aspects, the selected effects theory seems committed to ascribing functions to clay crystals. Clay crystals with growth-enhancing and proliferation-enhancing patterns are differentially present because of the patterns they realize. Clay crystals, however, are not usually considered to bear functions. Since clay crystals involve something analogous to reproduction, the challenge they raise applies to both the classical and the generalized versions of selected effects theory. Another counterexample, brought out more directly in relation to the generalized selected effects theory, has become prominent in recent discussions: rocks on beaches (Garson, 2016, 60; 2017, 535; 2019, 102–103). Large rocks on a beach that vary in their hardness achieve differential persistence. Softer rocks erode more quickly than harder ones. Thus, all else equal, harder rocks come to prevail on a beach because their hardness promotes their persistence.2 The generalized selected effects theory thus seems committed to ascribing functions to rocks. Hard rocks are differently present because of their hardness. Rocks on beaches, however, are not usually considered to bear functions.3  Bedau’s discussion of crystals is partly based on A. G. Cairns-Smith (1982).  Garson adapts this example from Justine Kingsbury (2008, 496). Tim Lewens (2004, 92, 128) discusses the similar example of the “longshore drift,” which leads small pebbles to accumulate at one end of a beach and larger pebbles to accumulate at the other. Pierrick Bourrat (2021, 66) reports yet another similar example, initially presented by Leigh Van Valen (1989, 2), of selection among grains of minerals (mainly feldspars and quartz) composing granite, which differ in their hardness. 3  Similar examples have been brought out by other authors. Stars differentially persist: Larger stars have shorter life spans than smaller ones because they are more susceptible to gravitational collapse. Small mass, however, does not seem to be a function of stars (Wimsatt, 1972, 16). A (fictional) cloner machine differentially replicates ball bearings based on their smoothness. Ball 1 2

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Proponents of the (generalized) selected effects theory of function have adopted three broad lines of response to counterexamples like clay crystals and rocks on beaches. Some simply bite the bullet. Ruth Millikan (1993, 39n7), for instance, states: “so if crystals can have functions, … that is fine by me.” A second line of response appeals to the notion of population (Garson, 2016, 54–55, 58–61; 2017, sec. 5; 2019, sec. 6.3–6.4; 2022, sec. 3; Schulte, 2021). And a third one introduces a service criterion into the selected effects theory (Price, 2001, sec. 2.2; Wakefield, 2005, 884–885).4 In the remainder of this section, I will be concerned with the population response. I will discuss the service response in the next section. The population response is simple in its basic idea, but becomes more complicated when one gets into the details. The basic idea is this: Differential reproduction and persistence bestow functions only when achieved by entities that form populations in the appropriate sense, and neither clay crystals nor rocks on beaches form such populations. Garson (2016, 54–55, 58–61; 2017, sec. 5; 2019, sec. 6.3–6.4; 2022, sec. 3) develops this response by appealing to the view, influential among philosophers of biology, that a set of entities forms a population that can evolve by natural selection only to the extent that the entities interact in ways that affect one another’s fitness (i.e., ability to survive and reproduce) (Godfrey-Smith, 2009, sec. 3.3; Millstein, 2009; Matthewson, 2015). Garson applies this view to selection processes other than natural selection covered by his generalized selected effects theory. He thus restricts generalized selected effects functions to features of entities that interact in ways that affect one another’s fitness – which here may be understood as their ability to persist and/or to produce new entities similar to themselves. bearings in such a scenario, however, do not seem to bear functions (Schaffner, 1993, 383–384). Convective cells that form in a beaker of water heated from beneath differentially persist: Cells of a size that is optimal for the viscosity of the water persist, whereas ones of a size smaller than optimal fuse and ones of a size larger than optimal break up. The optimally sized cells, however, do not seem to bear functions (Walsh, 2000, 143). 4  A fourth line of response which I set aside here, the one favored by Bedau (1991), introduces a reference to values, and claims that only effects that are good for the entities involved can bear functions. Like other thinkers, I do not find this solution very promising (e.g., Price, 2001, 35; Boorse, 2002, sec. 1.4; Garson, 2016, 53–54). First, as critics have argued, given enduring metaethical uncertainties over the ontological status of values, Bedau’s reference to values makes it unclear whether, on this value response, functions would remain objective features of the natural world, or whether they would become either mere subjective projections, or metaphysically mysterious features. Second, in the case of many organisms, such as plants, fungi, and many invertebrate animals, which presumably have no subjective experiences, it is hard to see how the notion of being good for could be explained except in terms of function (or closely related concepts), thus making the account circular. Being good for a plant, fungi, or nonsentient animal seems to ultimately amount to helping these organisms achieve their functions (or something closely related). Or, at least, I am not aware of any developed alternative explanation of goodness for a nonsentient organism (for a discussion of this point, though one presented in relation to theories of health, see Dussault, 2021). I consider this fourth line of response as distinct from the service response, because, although the two responses may look similar in that “X serves Y” may seem to imply “X is good for Y,” the service response, as introduced by Price and as understood by other proponents of it, draws no relationship between functions and values. All that it implies is the contribution of a functional item to some other system.

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Since, Garson argues, items like clay crystals and rocks on beaches do not interact in ways that affect one another’s fitness, they do not form populations in the appropriate sense for selection processes operating on them to endow them with functions. The (generalized) selected effects theory, therefore, is not committed to ascribing functions to items like clay crystals and rocks on beaches. As Garson himself recognizes, this simple version of the population response seems easily countered by slightly modified versions of the clay crystal and rocks on beaches cases. Garson (2016, 55) considers a modified case of crystals that do affect one another’s ability to persist and produce new crystals similar to themselves. Suppose there are two types of crystals with different patterns, which both grow in a creek containing dissolved silicic acid. Suppose also that crystals realizing the first pattern grow and replicate very quickly, leading them to utilize a sufficiently large amount of the silicic acid available in the creek for their growth and replication to hinder that of crystals realizing the other pattern. Then the two types of crystals seem to form a population in the above specified sense. They interact in ways that affect one another’s fitness. Garson (2016, 60; 2017, 537; 2019, 106) also considers a modified case (suggested to him by Karen Neander) of rocks on beaches that do affect one another’s ability to persist. The rocks are now arranged in piles, and when the waves come, they start to move and slam against each other, such that their differential erosion is in part caused by their collisions. The rocks now do interact in ways that affect one another’s fitness. They therefore form a population in the above specified sense. Hence, with regard to these two modified cases, the population criterion as formulated in the previous paragraph still does not help. The (generalized) selected effects theory is still committed to ascribing functions to items like clay crystals and rocks. Garson thus further specifies the population criterion in order to exclude these modified cases (he focuses on the rocks case, but I will consider whether his response also works for crystals).5 Drawing on John Matthewson’s (2015) account of populations, he proposes that, in order to form a population, the members of a set of entities must achieve fitness-relevant interactions not just with a few other members of their putative population, but with a large number of them (Garson, 2016, 61; 2017, 537–538; 2019, sec. 6.4). Hence, one may conclude that clay crystals and rocks on beaches do not bear functions, because individual crystals and individual rocks do not interact with a sufficient proportion of the other crystals or rocks for them to form populations in the appropriate sense. In other words, sets of crystals and rocks do not achieve a sufficiently high degree of connectedness for selection among their members to endow them with functions. As Garson highlights, this verdict applies the connectedness specification in a categorical way, but one could also apply it in a graduated way and so consider that selected effects functions come in degrees (for a defense of this graduated take on selected effects function, see  Garson (2016, 55) is willing to accept the conclusion that crystals that affect one another’s “fitness” do bear functions. I think this conclusion should not be accepted, in part for the reasons I develop in Sect. 10.4 below, but it is worth considering whether the population criterion is able to exclude it. 5

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Matthewson, 2020). Selected effects could then be more or less functional, or functional from low to high degrees. The upshot would be that clay crystals and rocks do bear functions, but that they do so only to a very low degree, given that sets of crystals and rocks are population-like only to a very low degree (Garson, 2017, 538; Garson, 2019, 108). Garson (2019, 107–108) adopts the graduated alternative. As some critics have argued, this introduction of a connectedness requirement still does not make the population response to cases like clay crystals and rocks fully successful (Schulte, 2021; Bourrat, 2021). Once again, one can further modify the rocks on the beach case so that it provides an adequate degree of connectedness between rocks. Schulte (2021, 373) describes a setting of rocks rolling down the slope of a high mountain, haphazardly bouncing against each other.6 Bourrat (2021, 65) pictures a situation involving piles of rocks that are now sufficiently small to become suspended in the water when the waves come, and hence to be moved along the beach by wave action. The waves then mix the rocks, leading them to interact with a large subset of the other rocks present on the beach. In these two settings, there is a high level of connectedness among the rocks, such that they meet the connectedness criterion as specified above. It also seems possible to elaborate a modified version of the clay crystal case that provides for high connectedness among crystals. Perhaps the water in the creek is swirly and mixes quickly enough for the silicic acid concentration to remain even throughout the creek. The growth of one crystal then potentially hinders that of all other crystals in the creek. Hence, the connectedness specification does not help with respect to the further modified versions of the clay crystals and rocks on beaches cases: the (generalized) selected effects theory is still committed to ascribing (full-blown) functions to clay crystals and rocks in such modified cases. Garson (2022, sec. 3) recognizes this and therefore, again, further specifies the population criterion. He adds the requirement that the fitness-relevant interactions that make a set of items a population in the relevant sense be ones that concern access to resources (here, he partly draws on a suggestion from Schulte, 2021, sec. 4). Hence, a set of individuals belong to the same population to the extent that they affect one another’s access to resources, either negatively, through competition for these resources, or positively, through making the resources more easily accessible to one another.7 This further restriction of the population criterion aptly deals with the Schulte and Bourrat’s “rockfall” and “rock mixing” versions of the rocks-on-­ the-beach case. However, it seems ineffective with respect to the above modified version of the clay crystal case involving crystals that compete with each other for dissolved silicic acid. Moreover, it again seems possible to imagine a version of the rocks case that meets the further specified criterion. Consider again Bourrat’s rocks that are sufficiently small to become suspended in the water when the waves come,  This example is inspired from one by Brandon Conley (2020). For a similar point, see Matteo Columbo (2020). 7  Schulte’s (2021, sec. 4) suggestion is to restrict fitness-relevant interactions to competition for resources. Garson (2017, 536n6; 2019, 104; 2022, sec. 3) considers this competition requirement but rejects it as too restrictive. 6

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but consider now that hardness is no longer what determines their differential persistence. When the waves slam, the rocks erode by hitting each other, and they will all end up being ground into sand except for those that are able to “shelter” behind bigger rocks present on the beach. The small rocks that are able to occupy shelters, and therefore to differentially persist, have particular shapes that enable them to remain in shelters, and to displace other small rocks, “stealing” their shelters. The small rocks now compete for a resource: shelters behind big rocks. The generalized selected effects theory therefore implies that small rocks have functions in this case, which seems wrong. So the further refined version of the population criterion still does not fully succeed in excluding the clay crystal and rocks-on-beaches cases.8 This, however, does not in itself prove that no further refined version of the population criterion could successfully exclude cases like clay crystals and rocks. Moreover, as some critics have remarked, although the further refinements may make the population response look increasingly ad hoc (Conley, 2020; Bourrat, 2021, sec. 3), there is a line of justification available to Garson for these further refinements. These refinements – i.e., the specification that functions are bestowed only by selection processes operating on populations with sufficiently high connectedness and whose members affect each other’s access to resources – spell out conditions that make selection processes especially powerful in generating complex adaptations. As Pierrick Bourrat (2021) remarks in discussing Garson’s population criterion, selective processes operating on highly connected populations provide a context more conductive to cumulative selection, which is how selection typically generates complex adaptive structures such as hearts and eyes (see also Lewens, 2004, chap. 6). Competition for resources is also sometimes said to favor cumulative selection (Godfrey-Smith, 2009, 51–52; though see Lewens, 2015; Krashniak, 2021).9 So a possible justification for Garson’s population criterion and his further refinements of it is that only items subject to selection processes operating on highly connected populations whose members compete with each other for resources are able to evolve the type of design-like complexity in reference to which functional language seems relevant. In contrast, items subject to selection processes operating on mere sets or on diffuse populations cannot evolve such design-like

 Though, as I noted, Garson was already willing to bite the bullet with respect to the “competing crystals” case (see footnote 5 above), it remains to be seen whether he would also do so with respect to competing rocks. 9  I should note that, although Bourrat and Lewens’ remarks indicate some line of justification for the population criterion and further restrictions of it, they themselves ascribe little relevance to the demarcation of selection processes that bestow bona fide functions and those that do not. Their take on the issue at times comes close to Garson’s graduated interpretation of the connectedness criterion – which ascribes degrees of functionality to items (see above) – but, at other times, comes closer to Millikan’s (1993) bite the bullet response. Bourrat (2021, 64) approvingly quotes Lewens (2004, 128) stating that “[t]rying to discriminate between ‘real’ and merely ‘as-if’ functions is probably a waste of time.” 8

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complexity. Their structures and patterns remain primarily explainable in terms of nonselective physical processes.10 Hence, although the population criterion may still need further refinements, it tallies with what seems to be a central dimension of the concept of function: Functions are borne by structures and patterns that are design-like. Therefore, Garson’s population criterion, and further refinements of it, simply draw the logical implications of the selected effects theory’s basic idea that design-likeness in nature arises from selection processes. If the main reason why items like clay crystals and rocks do not bear functions is that they are not sufficiently design-like to do so, then the population response to cases of this type seems to point in the right direction. In the next section, however, I will discuss another response to cases like clay crystals and rocks – the service response – which will highlight another (and I think more important) reason why items like clay crystals and rocks do not bear functions.

10.3 The Service Response to Clay Crystals and Rocks Another way that proponents of the selected effects theory have dealt with cases like clay crystals and rocks on beaches consists in incorporating a service criterion into their theory (Price, 2001, sec. 2.2; Wakefield, 2005, 884–885; see also Godfrey-­ Smith, 1994, 347–350; Huneman, this volume). Carolyn Price (2001, 35–36) first proposed this type of response to the clay crystals case (see also Price, 1995). She contends that, in general, a trait may have a function only if it replicates itself through a contribution it makes to the operation of some other system. The trait provides a service to that system, and the operation of that system leads to the item’s replication. For instance, my heart has the function of pumping blood because my ancestors’ hearts pumped blood, and this contributed to their reproductive systems’ ability to initiate a sequence of events that led to the production of my heart. Thus, Price claims that items acquire functions not through stand-alone processes of self-replication, but through a “process of preservation through service” (Price, 2001, 36, italics in the original). Price (2001, 38–39) contends that this service criterion for functions excludes cases like clay crystals. Since clay crystals replicate themselves directly and not through contributing to the operation of some other system, seeding other crystals is not a function that they bear. She could likewise argue that, since harder rocks on beaches persist in a stand-alone manner and not through contributing to the operation of some other system, then persisting is not a function that they bear. As Garson  A possible concern with this justification is that it might better be construed as a replacement of the population response by an alternative response focused on design-likeness and its relation to cumulative selection. Garson (2019, 105–106) considers the restriction of functions to products of cumulative selection as an alternative to the population response (suggested to him by David Papineau) and rejects it as overly restrictive. I set these matters aside here and leave it up to proponents of the population and/or cumulative selection response(s) to settle them. 10

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(2016, 54) notes, however, the service response to the clay-crystal counterexample as formulated by Price seems to fail. Since each layer in the crystal contributes to the formation of the next layer, which itself contributes to the formation of another layer, etc., there is a sense in which a crystal layer replicates itself through contributing to another system. Price (2001, 39) considers this objection and proposes to deal with it by adding the further restriction that the contribution to another system by which an item may acquire a function must not amount to bringing that other system into being. Her rationale seems to be that items that bear functions with respect to a system must be produced by that system, and not the other way round. I do not see any particular inconsistency in this response, but I think we can formulate a more appealing and straightforward version of the service response to cases like clay crystals and rocks on beaches. Such a version of the service response can be derived from Peter Godfrey-Smith’s (1994, 347–350) alternative formulation of the service criterion for function (see Wakefield, 2005, 884–885).11 Godfrey-Smith introduces the service criterion while discussing an issue similar to that raised by clay crystals, which arises with respect to selfish DNA and segregation distorter genes. Selfish DNA replicates itself in an organism’s genome and thus proliferates despite having deleterious effects on its carrier organism. Segregation distorter genes promote their own replication by biasing meiosis in a way that increases their own chances of being passed on to the next generation. Selfish DNA’s ability to replicate through an organism’s genome thus partly explains its presence within this genome, and likewise, selection distorter genes’ ability to bias meiosis partly explains their presence within many organisms’ genomes. However, selfish DNA and segregation distorter genes are not usually considered to bear functions with respect to the organisms that carry them (for other discussions of these cases, see Doolittle, 1988; Manning, 1997; Lewens, 2004, 122; Elliott et al., 2014; Garson, 2016, 44–45; 2022; Huneman, this volume). Godfrey-Smith (1994, 349) proposes to deal with these cases by specifying that an item has a function only if it is part of a “larger biologically real system” and is replicated via a contribution it makes to the fitness of that larger system.12 “Biologically real systems,” he specifies, are systems that are units of natural selection, that is, “[i]ndividuals, kin groups and perhaps populations and species.”13 Selfish DNA and segregation distorter genes do not bear functions within their  Another version of the service dimension, which I set aside here, is that advocated by Peter McLaughlin (2001, 99), which relativizes functions to the welfare of a system. I set aside this proposal for reasons similar to those for which, in Sect. 10.2, I set aside Bedau’s value response to cases like clay crystals and rocks (see footnote 4). 12  Godfrey-Smith (1994, 349) notes that his larger system requirement aligns with Robert Brandon’s (1990, 188) notion that a functional item must increase the “relative adaptedness of [its] possessor.” It also lines up with Neander’s (1991, 174) statement that a type of item’s proper function is “that which items of [its] type did to contribute to the inclusive fitness” of ancestors of the organism that carries it, and with Paul Griffiths’ (1993, 412) assertion that “[t]he proper functions of a trait are those effects of the trait which were components of the fitness of ancestors.” 13  Godfrey-Smith (1994, 360n6) assimilates these systems to “interactors” (sensu, e.g., Hull, 1980), but in line with his more recent take on biological individuality, he might perhaps now say that 11

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carrier organisms because they do not replicate themselves through contributing to these organisms’ fitness. The difference between Price and Godfrey-Smith’s proposals is that, in the former, function-bearing items must contribute to any other system (provided it is not one that the function bearer brings into being) whereas, in the latter, these items must contribute to the fitness of an organism, or another biologically real system, of which they are a part (see Garson, 2016, 45). Godfrey-­ Smith’s formulation of the service criterion seems more apt than Price’s for excluding cases like clay crystals and rocks on beaches. Neither clay crystals nor rocks on beaches are part of “biologically real systems,” and neither of them replicates through contributing to the fitness of such systems. Hence, clay crystals and rocks do not bear functions (see Garson, 2016, 54, 60). Godfrey-Smith’s formulation of the service criterion, however, is perhaps too restrictive. Think of the structures that organisms build in their environment and which contribute to their fitness – Richard Dawkins’ (1982) well-known extended phenotypes.14 For instance, consider the nest that a bird builds, or the dam that a group of beavers builds, in part because their ancestors’ construction of similar structures contributed to their fitness. Or consider the galls that gall-wasps create on oak trees, presumably because the creation of such galls has contributed to their ancestors’ fitness (Griffiths, 1993, 416). It would seem equally legitimate to ascribe selected effects functions to such structures with respect to the organisms that create them as to structures that are parts of these organisms. Godfrey-Smith’s formulation of the service criterion should thus be loosened to include such external structures. This can be done by simply removing the requirement that function-bearing items be part of the system to the fitness of which they contribute. An item thus has a selected effects function if it replicates itself through contributing to the fitness of a biologically real system, irrespective of whether the item is part of that system. This formulation of the service criterion preserves the advantage Godfrey-Smith’s formulation has over Price’s. Since it does not relativize functions to any other system, but, more restrictively, to systems of the appropriate type, it does not grant functions to clay crystals. Clay crystals do not proliferate through contributing to the fitness of a biologically real system; hence they do not bear functions. This formulation of the service criterion likewise excludes rocks on beaches as potential function bearers. Rocks on beaches do not persist through contributing to the fitness of a biologically real system; hence they do not bear functions. In a generalized selected effects theory of function of the type Garson advocates, Godfrey-Smith’s restriction of functions to contributions to biologically real systems could be further relaxed to allow for systems that are subject to some selection process other than natural selection to be ones in relation to which items may have these systems are those that realize a sufficiently high degree of Darwinian individuality and/or of metabolic individuality (Godfrey-Smith, 2009, 2013). 14  Of course, Dawkins discusses extended phenotypes in the context of his gene-centrist view of evolution by natural selection and so construes them as phenotypes of genes, but, as Robert Wilson (2005, 128–130) points out, extended phenotypes can also be construed as phenotypes of organisms.

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functions. We could consider such systems as those that are composed of functionally differentiated parts and that persist through the combined activities of these parts. The idea would be that an item can have a selected effects function only with respect to a system composed of parts among which there is some functional division of labor, that is, a system that persists as a result of the combined activities of its parts. An item that produces some effect could hence have a generalized selected effects function in virtue of achieving something in concert with other items that have different effects and that contribute complementarily to the system’s ability to persist.15 Such a characterization of systems in reference to which items can bear functions would still exclude cases like clay crystals and rocks from the (generalized) selected effects theory. Hence, there is an appealing alternative to the population response to cases like clay crystals and rocks on beaches available to proponents of the (generalized) selected effects theory. The alternative consists in specifying that selected effects functions must be effects that promote the occurrence of the items that produce them through a contribution to the fitness (broadly construed) of a functionally differentiated system, that is, a system that is composed of functionally differentiated parts and that persists through the combined activities of these parts. I will henceforth refer to such systems as complexly organized systems. In the next section, I will argue that this service response to cases like clay crystals and rocks on beaches is the most appropriate one.

10.4 The Twofold Character of Function Are there any reasons why selected effects theorists should prefer either the bite the bullet, the population, or the service response to cases like clay crystals and rocks on beaches? To answer this question, I think we must first take a step back and call to mind some general aspects of the pretheoretical concept of function of which theories of function purport to provide a principled account. I submit that a retrospective look at the function debate in the philosophy of biology allows us to identify two basic dimensions of that pretheoretical concept of function. These are the teleological and systemic dimensions of function. I contend that these two dimensions stand out from the function debate as two central components of the concept – if not its two most important components. Attention to these two dimensions helps one to understand the ongoing tension between selected effects and causal role theories throughout the last few decades’ discussions of function.16 The teleological dimension consists in the idea that functions are effects of items that explain the occurrence of these items. It casts functions as features that  This functional differentiation criterion for systems in reference to which items may bear functions is inspired from Matteo Mossio et al. (2009, sec. 4.2). 16  Robert Cummins underlines these two dimensions at the outset of his original exposition and defense of his causal role theory, presenting them as two assumptions under which the (then) 15

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partly account for why their bearers, instead of items with other effects, exist. This dimension is accounted for extremely well by selected effects theories. Effects that items produce because they helped them to persist and/or to reoccur explain those items’ present occurrences. The systemic dimension consists in the idea that functions are contributions of items to the capacities or activities of complexly organized systems. It casts functions as features of items that partly account for how systems of which they are part (or with which they interact) are able to realize certain capacities or activities. This dimension of the pretheoretical concept of function is well accounted for by the various types of causal role theories proposed by philosophers of biology (e.g., Cummins, 1975; Boorse, 1976; Bigelow & Pargetter, 1987).17 The pretheoretical concept of biological function embeds these two dimensions, I submit, because they are jointly present in the paradigmatic cases from which this concept arises, namely, the traits and parts of individual organisms. The idea that some natural items bear functions in a way analogous (though not necessarily identical) to artifacts that humans intentionally create arises primarily with respect to the parts and traits of individual organisms. These traits and parts manifest both the systemic and teleological dimensions: They contribute to the capacities of these organisms and occur because they achieve these contributions. The joint presence of these two dimensions in the paradigmatic case of organisms’ traits and parts may lead one to expect that they will always be jointly present in a given item, but cases like clay crystals and rocks on beaches indicate that they need not be. The converse possibility of items that contribute to the capacities of complexly organized systems, but occur for reasons that have nothing to do with these contributions, can be illustrated with cases of items of their environment that organisms make use of and/ or that contribute to their ability to survive and reproduce, e.g., the mollusk shells used by hermit crabs (Griffiths, 1993, 416; Boorse, 2002, 82) and the oxygen, iron, potassium, and other molecules used in organisms’ metabolism (Gayon, 2013, sec. 4; this volume, sec. 7.2.1). If the above observations are correct, then the pretheoretical concept of function has a twofold character. That is, it embeds two dimensions, which respond to two distinct natural phenomena: items that are remarkable in that their effects promote their own occurrence, and items that are remarkable in that they contribute to the capacities of complexly organized systems. In some (even more remarkable) occurrences, paradigmatically the traits and parts of individual organisms, these two phenomena co-occur (Fig. 10.1). The twofold character of the pretheoretical concept of function admits two possible stances on how one should delimit the class of selected effects functions. A first stance emphasizes the teleological dimension and downplays the systemic “recent philosophical literature on the nature of functional analysis and explanation” had proceeded (see Cummins, 1975, 741). 17  For the purposes of the present discussion, “causal role theories” can be interpreted broadly as including any theory that casts functions as contributions to activities or capacities of systems, including, not only Cummins’ (1975) theory, but also goal contribution theories (e.g., Boorse, 1976) and fitness contribution theories (e.g., Bigelow & Pargetter, 1987).

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Fig. 10.1  The two distinct natural phenomena to which the teleological and systemic dimensions of function respond, and their intersection: items whose effects promote their own occurrence (left oval), items that contribute to the capacities of complexly organized systems (right oval), and items that have effects that promote their own occurrences through contribution to complexly organized systems (intersection between the two ovals)

dimension. It adopts the view that selected effects are bona fide functions irrespective of whether they promote the occurrence of the items that produce them through contributing to the capacities of complexly organized systems, or whether they do so in a stand-alone manner (Fig.  10.2). What matters is just that the items have effects that (to a sufficient degree) explain their own occurrence. Two varieties of this stance are possible. A first variety takes the most liberal line possible and states that any effect that explains the occurrence of the item that produces it is functional. Thus, all selected effects are bona fide functions, and items like clay crystals and rocks on beaches bear selected effects functions. A second variety takes a more circumspect line and attempts to restrict the class of bona fide functions to cases of selected effects that are similar enough to the paradigm case of the traits and parts of individual organisms. One way to achieve this, as seen in Sect. 10.2 above, is to specify that genuine selected effects functions are effects that explain differential persistence and/or proliferation among members of appropriate types of populations. On this second variety, clay crystals and rocks either do not bear selected effects functions or bear such functions only to a very low degree. These two varieties of the first stance indeed correspond, respectively, to the “bite the bullet” and population responses discussed in Sect. 10.2. A second possible stance on how to delimit the class of selected effects functions given the twofold character of the pretheoretical concept of function incorporates both the teleological and systemic dimensions (Fig. 10.3). It adopts the view that selected effects are bona fide functions only when they promote the occurrence of the items that produce them through a contribution to the (fitness-relevant) capacities of a complexly organized system. This stance thus incorporates into the selected

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Fig. 10.2  First possible stance on how to delimit the class of selected effects functions given the twofold character of the pretheoretical concept of function: Selected effects are bona fide functions irrespective of whether they promote the occurrence of the items that produce them through contributing to the capacities of complexly organized systems, or whether they do so in a stand-­ alone manner

Fig. 10.3  Second possible stance on how to delimit the class of selected effects functions given the twofold character of the pretheoretical concept of function: selected effects are bona fide functions only when they promote the occurrence of the items that produce them through a contribution to the (fitness-relevant) capacities of a complexly organized system

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effects theory the dimension of the pretheoretical concept of function that causal role theories more straightforwardly account for: the idea that functions are contributions to the capacities of complexly organized systems. This stance corresponds to the service response to cases like clay crystals and rocks on beaches presented in Sect. 10.3. The two varieties of the first stance thus set up the self-promotion phenomenon that is tied to the teleological dimension of the pretheoretical concept of function as the essential phenomenon that the selected effects theory must capture and sideline the systemic dimension and the system-contribution phenomenon associated with it. In contrast, the second stance recognizes both the self-promotion phenomenon that is tied to the teleological dimension of the pretheoretical concept of function, and the system-contribution phenomenon that is tied to the systemic dimension, as phenomena that the selected effects theory must capture. I think there is no straightforward conceptual reason to favor either of these two stances. Neither of them can pretend to be more correct than the other on solely conceptual grounds. Although the pretheoretical concept of function includes both a teleological and a systemic dimension, it may turn out that the account of function that offers the most fruitful conceptualization downplays one of these two dimensions.18 The choice, I think, should be a matter of which delimitation of the concept of function best serves the purposes for which it is used in scientific research. Against this background, I contend that selected effects theorists should prefer the service response to cases like clay crystal and rocks on beaches, and the delimitation of the class of selected effects functions that it implies (i.e., the second stance characterized above, see Fig.  10.3). I think so because, by restricting the use of “function” to items that contribute to complexly organized systems, the service response provides better unity between the selected effects theory and the non-­ selected-­effects uses of the concept of function that occur in biology.19 As remarked by many proponents of causal role theories, or of a pluralism about function that leaves room for functions defined along these theories’ lines (e.g., Amundson & Lauder, 1994; Walsh, 1996; Bouchard, 2013), there are many biological contexts

 In this respect, it is interesting to note that when introducing the service criterion, Godfrey-Smith (1994, 349) recognizes that some theorists may prefer sticking to “the simpler analysis,” according to which any self-replicating effect, including those of selfish DNA and segregation distorter genes, is functional. 19  My argument thus presupposes that conceptual unity with regard to the various biological uses of “function” is preferable to the pluralistic line that many selected effect theorists advocate (e.g., Millikan, 1989; Neander, 1991; Godfrey-Smith, 1993), and that the conceptual unification I am proposing is better than the other ones that have been proposed (e.g., Kitcher, 1993; Walsh, 1996; Mossio et  al., 2009). I cannot enter here into the debate over pluralism versus unification with respect to function, but, briefly, I think that the pluralistic line has the implausible implication that many biological uses of “function” that seem to make use of the same concept in fact involve different concepts (on this point, see Hardcastle, 1999, 29; Longy, 2010, 205–206). Moreover, I think that the unificatory line I am proposing, compared to the alternative unificatory lines, better captures the relationship between what I identified above as the teleological and systemic dimensions of function. 18

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and/or biological subdisciplines in which functions are not typically construed as selected effects.20 Examples that have been given are biochemistry, developmental biology, the neurosciences, anatomy, morphology, physiology, ecology, etc. (e.g., Godfrey-Smith, 1993; Amundson & Lauder, 1994; Bouchard, 2013; Caponi, this volume). To be sure, Garson, in recent discussions, provides persuasive arguments that some, and perhaps many, purported examples of non-selected-effects biological uses of “function” might well turn out in the final analysis to be selected effects functions (Garson, 2016, sec. 5.3; Garson, 2019, chap. 9; for a related point, see Neander, 2017, 1150–1151). Nevertheless, it has not yet been established that this applies to all purported cases.21 And more compellingly, there is at least one clear case of a biological subdiscipline in which functions are not typically construed as selected effects: ecology. In ecology, organisms and their populations are often ascribed “ecological functions,” that is, functions with respect to the capacities of the communities and ecosystems that they are a part of. Such ascriptions usually involve no claims that organisms and/or their populations are selected for fulfilling these functions, claims which would seem to hinge on the idea that natural selection customarily operates at the levels of communities and ecosystems (see Dussault, 2018 for a discussion).22 All that is necessary for an organism and/or its population to bear an ecological function is that it contributes to some relevant capacity of a community or ecosystem. For this reason, many philosophers argue that ecological functions consist mainly in (some variety of) causal role functions (e.g., Maclaurin & Sterelny, 2008, sec. 6.2; Odenbaugh, 2010; Gayon, 2013, sec. 6; this volume, sec. 7.2.3; Dussault & Bouchard, 2017).23 A straightforward way to unify selected effects functions with these non-selected-­ effects uses is to construe the former as a subset of all the functions that exist in nature (see Fig. 10.4). Functions are basically contributions of items to the capacities of complexly organized systems, and among these functions, some have the special character of being selected effects functions. Among the two natural phenomena to which the pretheoretical concept of function responds, the system-­ contribution phenomenon to which the above systemic dimension responds is the defining feature of function. The self-promotion phenomenon to which the teleological dimension responds delineates a subclass of functions, one that  Here, by speaking of “biological sub-disciplines,” I do not mean to support any strong form of what Garson (2016, 90; 2019, 142) calls between-discipline pluralism about functions, asserting that biological subdisciplines can be clearly parsed as making use of either a selected effects or a non-selected-effects concept of function. All I am saying is that there are some biological subdisciplines in which the non-selected-effects uses of “function” prevail or are at least frequent. 21  Garson himself does not deny the occurrence of non-selected-effects uses of “function” in biology (see Garson, 2016, 94; 2019, 151). 22  Roberta Millstein (2020) recently proposed a selected effects account of ecological function based in coevolution among species rather than on community- or ecosystem-level selection. For a discussion of Millstein’s proposal and of where it stands with regard to the above dissociation of ecology from selected-effects uses of “function,” see Antoine C. Dussault (2022). 23  Others advocate an account of ecological functions derived from Mossio, Saborido, and Moreno’s (2009) organizational account of function (Nunes-Neto et al., 2014). 20

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Fig. 10.4  A simple way to unify selected effects functions with the non-selected-effects uses of “function” at work in many biological subdisciplines: Functions, basically, are contributions of items to the capacities of complexly organized systems, and among these functions, some have the special character of being selected effects functions. Selected effects functions are therefore only a subset of all the functions that exist in nature

encompasses items whose contribution to a system partly explains their occurrence. These functions are particularly interesting given that the self-promotion phenomenon in which they are involved is a very peculiar one, but they are not all the functions that exist in nature.24 When we adopt this view, selected effects that do not make contributions to complexly organized systems must be regarded as a nonfunctional (in line with the second stance characterized above). I think selected effects theorists should adopt this view because only it seems able to unify selected effects functions with the non-selected-effects uses of “function” that occur in biology. Any alternative to it would, it seems, be unable to unify

 Garson (2016, chap. 6; 2017, 2019) argues that the (generalized) selected effects theory of function is superior to competing accounts because it better captures three features of the concept of function as it is frequently used in biology: It grounds a distinction between functions and accidents, it explains how functions can be normative such that biological items can sometimes be said to be dysfunctional, and it makes functions explanatory of the presence of their bearers. As seen above, however, Garson also recognizes that biologists sometimes use “function” in a way that diverges from the (generalized) selected effects theory (see footnote 21). This, I think, entails that even if we conceded that the (generalized) selected effects theory better captures the three features of function Garson highlights, this would not support the claim that the (generalized) selected effects theory provides a superior account of function in general. This would only support the claim that the (generalized) selected effects theory provides a superior account of the subset of functions that have these three features. 24

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selected effects functions with these non-selected-effects uses. On a first alternative, the selected effects theory would purport to provide an account of a concept of function that denotes all instances of the self-production phenomenon to which the teleological dimension of function is tied, and on a second alternative, it would purport to provide an account of a concept of function that denotes the subset of those instances that are also instances of the system-contribution phenomenon to which the systemic dimension of function is tied. On both alternatives, selected effects theorists would have to (implausibly) claim that the concept of function of which the selected effects theory provides an account is wholly distinct from the one at work in biologists’ non-selected-effects uses of “function.” It is better, I submit, to construe all biological uses as involving one single concept of function, and this can be achieved, it seems, only if we adopt the view that functions, in general, are contributions of items to the capacities of complexly organized systems, and the corollary view that selected effects functions are only a subset of all the functions that exist in nature. This view implies, in line with the second stance characterized above and with the service response, that selected effects are bona fide functions only when they promote the occurrence of the items that produce them through a contribution to the (fitness-relevant) capacities of a complexly organized system. So given the attention it pays to the systemic dimension of function and that attending to this dimension is necessary for unifying selected-effects with non-­ selected-­effects uses of “function,” I contend that the service response to cases like clay crystals and rocks on beaches is the most adequate one. The reason why items like clay crystals and rocks do not bear (generalized) selected effects functions is that functions are, at the very least, contributions to capacities of complexly organized systems. Since functions in general are such contributions, (generalized) selected effects functions in particular must be also. However sophisticated a population response to cases like clay crystals and rocks on beaches might be, it will miss this aspect and therefore remain at best incomplete.

10.5 Conclusion: On the Relation Between Function and Teleology Above, I discussed the family of counterexamples to the (generalized) selected effects theory of function classically epitomized by Bedau’s (1991) case of differentially growing and proliferating clay crystals, and more recently illustrated by Garson’s (2016, 2017, 2019) case of rocks differentially eroding on a beach. I discussed three possible responses to this type of case: the bite the bullet response, the population response, and the service response. I argued that the latter response is the most appropriate one, because it yields better unity between the selected effects theory and the non-selected-effects uses of the concept of function that occur in many biological subdisciplines, such as ecology. This response involves

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incorporating into the selected effects theory the dimension of the pretheoretical concept of function that causal role theories more straightforwardly account for, that is, the idea that functions are contributions to the capacities of complexly organized systems. I called this dimension of the pretheoretical concept of function the systemic dimension, and I argued that a satisfactory version of the selected effects theory should incorporate this dimension, along with the other main dimension of the pretheoretical concept of function that it straightforwardly accounts for, namely, the teleological dimension. A happy implication of the service response to cases like clay crystals and rocks on beaches, and of the service criterion for function associated with it, concerns whether whole organisms can or cannot be ascribed functions. As many theorists of function have remarked (e.g., Godfrey-Smith, 1994, 349; McLaughlin, 2001, 99; Huneman, this volume), it would seem odd to ascribe functions to whole individual organisms themselves, in contrast to their traits and parts, at least when considering them independently of any relation to other systems.25 Organisms seem to potentially bear functions primarily when considered in relation to more encompassing systems to which they contribute, e.g., colonies of eusocial animals (Gayon, 2013, sec. 5; this volume, sec. 7.2.2), and communities or ecosystems (e.g., Dussault, 2018). The service criterion aptly captures this, whereas the population criterion does not. Organisms are paradigm cases of members of populations that meet the standard conditions for natural selection. The population criterion therefore does not prevent organisms from bearing functions, even when taken independently of any relation to other systems. In contrast, the service criterion entails that organisms can bear functions only insofar as they contribute to some higher-level complexly organized system, and therefore that they can bear selected effects functions only on the basis of effects that have been selected on account of their contribution to the fitness of such a system (which would involve selection above the organism level). This, I think, is a further advantage of the service response over the population and the bite the bullet responses. My support of the service response, however, opens up the question of the label by which to designate items, like individual organisms, which do not meet the service criterion, but which are nevertheless involved in selection processes of the appropriate type for the generation of complex adaptations. These items manifest the teleological dimension of function, but not the systemic dimension, and I argued above that such items should not be considered as bearing functions (see Fig. 10.4 above). This contention may seem unappealing given that although these items do not contribute to complexly organized systems, their self-promoting character is a remarkable feature which deserves a special status that the “function” label seems apt to designate. The way to delineate the class of functions I am advocating does not foreclose the possibility of recognizing a special status for these (nontrivially) self-promoting

 See, however, Lewens (2004, 126) for a contrasting take on whole organisms as candidate function bearers. 25

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Fig. 10.5  Relationship between, on the one hand, the “teleological” and the “functional” designators and, on the other hand, items whose effects promote their own occurrence and items that contribute to the capacities of complexly organized systems

items. A basis for my proposal was the observation that the natural phenomena to which the teleological and systemic dimensions of the pretheoretical concept of function respond need not always co-occur (see Sect. 10.4 above). It should therefore be no surprise that, by restricting the class of functions to items that manifest the systemic dimension, my proposal leaves us in need of a label for the class of items that manifest the teleological dimension, but not the systemic one. I submit that these items should simply be labeled teleological or design-like (Fig. 10.5). We can label them as such while insisting that they do not bear functions. We thus get four classes of items. First, we have items that manifest neither the teleological nor systemic dimensions of function (e.g., clay crystals and rocks on beaches). These items are neither functional nor teleological (or only teleological to a very low degree). Second, we have items that manifest the teleological, but not the systemic dimension (e.g., individual organisms). These items are teleological (or design-like), but not functional. Third, we have items that manifest both the teleological and systemic dimensions (e.g., the parts and traits of individual organisms). These items are both functional and teleological (or design-like). And fourth, we have items that manifest the systemic dimension, but not the teleological dimension (e.g., items of their environment used by organisms). These items are functional, but not teleological (or design-like). This, I submit, is a clean and appealing way of parsing items with regard to their possible functional and/or teleological characters (see Table 10.1).

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Table 10.1  The four classes of items yielded by the intersection of the functional/non-functional and teleological/non-teleological distinctions Teleological (or teleological to a high degree) Non-teleological (or teleological to a low degree)

Functional The parts and traits of individual organisms Items of their environment used by organisms

Non-functional Individual organisms, selfish DNA, segregation distorter genes Item like clay crystals and rocks on beaches

Acknowledgments  The author is thankful to Brandon Conley, Justin Garson, and Armand de Ricqlès for helpful comments on previous versions of this manuscript. He also thanks Alice Everly for editing the manuscript. The work for this chapter was supported by a research grant from the Fonds de recherche du Québec – Société et culture (FRQSC, 2018-CH-211053).

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Part III

Structures and Functions in Morphology and Paleontology

Chapter 11

The Problem of Complex Causality at the Origin of the Structure-Function Relationship 1/Generality, 2/The Case of Bone Tissue Armand de Ricqlès and Jorge Cubo Abstract  Beyond consideration of function as a concept, the observation of biological reality allows to discover the occurrence of “structuro-functional complexes,” where the “doing” of living things (processes and their results) is ultimately supported by a specific materiality: the structure. In the first part, we discuss the general issue of structuro-functional complexes and suggest that they are best explained by several orders of causality that should be simultaneously taken into account. In the second part, we apply this approach to explain the variability of bone as a tissue among amniotes. Using new quantitative approaches based on variation partitioning methods, we take simultaneously into account the two non-teleological theories of functions, the systemic and etiologic theories. The test shows, in a quantitative way, the implication of the two types of functional causality and their interactions to account for the segregation of various types of appositional bone tissues among amniotes. We also show that the addition of a third order of explanatory factors to the functional and phylogenetic factors reduces the non-explained fraction of the bone growth rate variation among amniotes. This third factor expresses the architectural component of materials from which organs and tissues are built and deals with the morphogenetic rules of their growth.

A. de Ricqlès Collège de France, Muséum National d’Histoire Naturelle, CNRS Centre de Recherche en Paléontologie– Paris (CR2P, UMR 7207), Paris, France e-mail: [email protected] J. Cubo (*) Sorbonne Université, Muséum National d’Histoire Naturelle, CNRS, Centre de Recherche en Paléontologie – Paris (CR2P, UMR 7207), Paris, France e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_11

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11.1 General Issue, Problematics As practitioners of biology, it seems difficult to us to reason on Function as a general, abstract concept, set aside of any context. Conversely, the observation of biological reality leads us to discover, at every level of biological integration, the occurrence of structuro-functional complexes, where the “doing” of living things is always supported by a given materiality: the structure (de Ricqlès, 2008). Biological structures, as observable material objects with precise compositional, size, shape, and energy characteristics, have specific properties which derive, with a very strong level of necessity, from the laws of physico-chemistry, geometry and topology (e.g. length to volume ratios). One may thus say that the functions of structures are emerging properties of them, derived from their own constitution. The precise relationship between the existing structure and the function(s) it fulfils (performance) may thus be understood, in terms of causality, by the analysis of the structure’s properties, the functions of which being only their emerging necessary consequences. In fine, it is entirely in physico-chemical terms that the structuro-­ functional interactions within the living organisms would be described and could be understood. Another condition must be added to the preceding one – it is to respect the temporality imperative. Putting one explicitly out of the quantic domain of elementary particles in order to stay in our “macroworld,” one can admit that cause always precedes effect. To explain, to give account of, it is thus always to come back up from effects to causes; in other words, to offer a retrodiction which can be, hopefully, challenged by an experimental test, or, in the case of historical sciences, by a congruence (or consiliency) test, for instance. In this context, it is clear that any finalistic explanation of the structure-function relationship violates the temporality condition and cannot be accepted. Finally, a third condition of the explanation should be taken into account – it is the structure of temporality itself. It is one thing to account for a molecular modification in nanoseconds at a synaptic level, another one to explain the sub-speciation starting from a founding population in a hundred or thousand generations. One may at once extract a consequence from these views: in the analysis of causality, it will be necessary to set apart a synchronic from a diachronic causality. As a first approximation, the synchronic causality manifests itself within the living organism, it is typically the one studied by physiology. The diachronic causality, on the contrary, is linked to “time steps,” which overpass individual life and deal with populations, species, or even supra-specific phylogenetic entities (clades). For example, because of their intrinsic character states (autapomorphies), clades may react in specific ways to environmental changes, leading them to new radiations or to extinction. Thus, one sees at once what could be at least a partial interpretation of the “final causes” problem: wouldn’t that be an ordinary causality problem, the resolution of which is mistakenly addressed at a non-relevant “time step”? In a famous paper published in 1961, Ernst Mayr has focused on what we have called here synchronic vs. diachronic times, demonstrating that this distinction meets two different explanatory regimes in biology: a biology of proximal causes on one hand and a biology

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of historical or ultimate causes on the other hand. Proximal causes are those at work within the living organism. Historical causes account for the data by reference to the evolutionary history of the organisms. The biology of proximal causes is a functional biology, biology of ultimate causes is an evolutionary biology (Gayon, 2006). Those two biologies are useful to account for the structuro-functional relationships but it is worth to emphasize that, because of their different relationships to time, their epistemological regimes are different. Functional biology, physiology being a typical example, is an experimental science, very close of physico-chemical sciences by its methods: they are nomological sciences, i.e. seeking a-temporal laws as general as possible. Demonstration of the evidence is rooted in the experimental practice, repeatability and testing being of paramount importance. Evolutionary biology, which may be exemplified by paleontology, is, on the contrary, a paleoetiological (or idiopathic) science, namely a science that studies “what has happened once”; in other words, the domain of historical sciences. In such fields, demonstration of the evidence cannot generally rely on experimental tests but rather relies on the accumulation of circumstantial evidences which converge (consiliency (or congruence) tests). It is thus a biology largely based on the comparative method (Martins, 2000). This method allows to show correlations and to suggest inferences, but it generally cannot, alone, bring evidence for a causality, this faculty being generally restricted to the domain of experimental sciences. That point reached, we observe that the explanation of the structuro-functional relationship in biology is intrinsically complex because it should combine two components: functionalism and historicism, whose epistemological regimes notoriously differ, especially in the methods bringing the demonstration of the evidence. In its traditional aspects, the Synthetic Theory of Evolution takes into account, after Mayr (1961), explanations relevant to both historicism and functionalism, even if, in practice, one point of view generally dominates the other, according to the various scientists’ approaches and traditions. For instance, for the pure systematist, especially the phylogeneticist, hence practitioner of historicism, every functional adaptation of a terminal taxon (species) to local conditions (namely its intrinsic, not shared derived character states or autapomorphies) blurs the phylogenetic signal. On the contrary, for the pure functionalist, such as the physiologist, every characteristic imposed by a common phylogenetic ancestry (hence, derived character states, but shared by every co-descendants of a proximate and exclusive ancestor, or synapomorphies) appears as a constraint, likely to restrain an optimal adaptation to the function. Starting in 1970, Adolf Seilacher and his “ Konstructionmorphologie” school have added an important supplementary element to this already complex issue (Cubo, 2004; Briggs, 2017). They consider that the characteristics of any biological entity are not governed by two, but by three general orders of causal factors: phylogenetic, adaptive and architectural. Those three orders of causality, respectively renamed historical, functional and structural by Gould (2002), form the summits of what has been named the “Seilacher’s triangle”. With the “architectural” summit of the causal triangle, Seilacher formally reintroduces in modern Biology a structuralist causal factor, formerly well developed in the older, pre-Darwinian European

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Biology, with Etienne Geoffroy Saint-Hilaire and Richard Owen. Following the rising to power of the Darwinian approach, this structuralist point of view became progressively outmoded. Accordingly, a whole “internalist” view of the structuration of the organism became neglected by a purely “externalist” view where natural selection took paramount importance (Gould & Lewontin, 1979). Structuralists focus on self-organizing morphogenetical properties of biological materials, on topological constraints and on biophysical rules of growth under weak genetic control, thus reintroducing problematics formerly developed by Russell (1916) and, above all, d’Arcy Thompson (1917). Following Seilacher’s lead, Gould has vigorously advocated for the reintroduction of such structuralist points of view, alongside the historical and functional factors of biological causality already taken into account by the orthodox Modern Synthesis (2002). Nevertheless, and up to now, the point of view of Seilacher and Gould, although recognized as intellectually satisfactory, has remained of little use in practice. Biological explanations of the structuro-­ functional relationships remain most often restricted either to historicism, to functionalism, or even to structuralism, each of them being exclusively taken into account, according to the intellectual and methodological traditions of the scientists.

11.2 The Case of Bone Tissue A striking example of the interpretative dead-ends stemming from this intellectual partitioning is offered by the biological interpretation of the variability of bone as a tissue. Each explanatory point of view, phylogenetic, functional or structural, has produced an enormous specialized literature, each one most often totally disconnected from the two other points of view (Cubo, 2004; Cubo et al., 2008). A more synthetic consideration of the data had nevertheless led to the belief that this variability of bone as a tissue results from a complex determinism, which simultaneously integrates phylogenetic, functional and structural components (de Ricqlès, 1975–1978). But, up to now, a methodological tool allowing to go beyond this qualitative point of view was not at hand. Such a tool is now available, and we give herewith an example of its use, precisely on the issue of the complex determinism of the structuro-functional relationship of bone as a tissue among amniotes (i.e. all tetrapod (four-limbed) vertebrates with an amniotic egg, namely chelonians (turtles), squamates (lizards, snakes), crocodilians, birds and mammals of the common language). For this purpose, we have developed new quantitative approaches, based on variation partitioning methods (Cubo et al., 2008) with the aim of taking simultaneously into account the two non-teleological theories of function currently available, namely the systemic and etiologic theories (Gayon, 2006). Our approach is based on the Desdevises method (Desdevises et al., 2003) and allows partitioning of a given phenotypic trait (character) between a fraction exclusively explained by the systemic concept of function (“pure” functional fraction), a fraction exclusively explained by the etiologic concept of function (“pure” historical or phylogenetic fraction), a fraction simultaneously explained by the two factors and an unexplained fraction.

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The “Etiologic concept” suggests that a function is a selected effect because it has improved the fitness during the phylogenetic history of the lineage whose extant representative(s) express that function (Gayon, 2006). It fits well to the biology of ultimate causes or evolutionary biology (Mayr, 1961). Cubo et al. (2008) offer the hypothesis that a change in the bone growth rate (taken as the dependent variable) is in part produced by the phylogenetic position of the taxa among amniotes (a historical variable with an explanatory power) because, during phylogenesis, various clades within the evolutionary radiation of the amniotes have increased their fitness by developing different “growth strategies,” some of them linked to low or moderate growth rates (chelonians, squamates, crocodilians) others linked to high to very high growth rates (mammals, birds). The “systemic concept” suggests that a function is an emerging ability of a system stemming from the more elementary abilities within the system (Gayon, 2006). It fits well to the biology of proximal causes (Mayr, 1961) or mechanistics (Autumn et al., 2002): they produce a change in an object from a state one at time one to a state two at time two. Cubo et al. (2008) offer the hypothesis that a change in bone growth rate (taken as the dependent variable) is in part produced by a change in resting metabolism (a functional variable with an explanatory power) because the production of new tissues at high rates require high activity of protein synthesis and catabolism, which are energetically costly (Nagy, 2005). According to this hypothesis, growth of chelonians, lizards and crocodiles is restricted by their low metabolic rates which would act as a constraint preventing those organisms to reach very high growth rates. Cubo et al. (2008) tested those hypotheses by partitioning the variation of bone growth rate within a sample of amniotes according to the following fractions: (1) a “pure” functional fraction (which one may view as meeting the systemic concept of function) exclusively explained by the resting metabolic rate, (2) a “pure” phylogenetic fraction (which one may view as meeting the etiologic concept of function) and (3) a fraction simultaneously explained by the two factors (see Fig. 11.1). The test effectively demonstrates, in a quantitative way, the implication of the two types of functional causality and their interactions to account for the segregation of various types of appositional bone tissues among amniotes (Cubo et al., 2008). It is interesting to note that, within a cladistic framework, the “pure” functional component agrees with the concept of autapomorphy at the species level, the “pure” historical component agrees with the concept of synapomorphies without any clear functional significance, and the functional component that overlaps with the historical component agrees with the cladistic concept of synapomorphy with functional significances. We have also shown (Cubo et al., 2008) that the addition of a third explanatory factor to the functional and phylogenetic factors considered above could reduce the non-explained fraction of the bone growth rate variation among amniotes. This third factor expresses the architectural or structural component (sensu Seilacher, 1970) and deals with the properties and characteristics of materials from which organs and tissues are built, and with the morphogenetic rules of their growth (Cubo, 2004; Briggs, 2017). For bone, growth occurs by accretion, namely the new bone deposit which will become mineralized necessarily occurs on bone-free surfaces, because

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Fig. 11.1  Components of the variation of a dependent variable (square) explained by the phylogeny (historial component), a functional factor, and a structural factor (the three circles). Each component (circle) has a “pure fraction” and fractions that overlap either with another factor or with the two other factors

once mineralized, the bone already laid down cannot contribute to growth anymore. Growth of bone, because of its additive-accretionary mode linked to mineralization, strongly departs from the multiplicative (or intususseptional) growth of soft tissues because it acts as a topological-constructional constraint, limiting the maximal rates of growth that can be reached. Some amniotes, especially mammals and birds, have evolved growth processes which circumvent, in part, this structural constraint on growth. Growth takes place not only at the periphery of the bone cortex (centrifugal growth) but also, and simultaneously, on intracortical free surfaces lining cavities: this is the centripetal deposit giving rise to the “primary” or addition osteons. Actually, growth becomes biphasic: at first, a light scaffolding of bone is laid down, leaving extensive cavities, which are filled in, later on, by the primary osteons. Significantly, organisms (birds and mammals) which routinely show the demise of this “constructional constraint” are also those which have the highest resting metabolic rates (higher, roughly by an order of magnitude, to those of crocodiles, lizards and chelonians). The fact that some clades of fossil amniotes (dinosaurs, pterosaurs, etc.) show phenotypic characteristics of their bone tissues very similar to those associated with high growth rates and elevated metabolism among extant ones strongly suggests that those groups had already developed those high rates themselves (de Ricqlès, 1975–1978). Whatever it may be, the method of variation partitioning already allows to analyze quantitatively, in the case of bone apposition, the complex causality of the structuro-functional relationship in an evolutionary context (Cubo et al., 2008). Some scientists have used the method of variation partitioning to quantify the microevolutionary component of the etiological concept of function (Diniz-Filho

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and Bini 2008; Piras et  al. 2009). In this context, adaptations are understood as character-states offering a higher evolutionary fitness than other character-states for the same environment (Martins, 2000). In such approaches, natural selection indeed appears as the efficient mechanism of evolutionary change and phylogenetic and structural factors as constraints modulating its action.

References Autumn, K., Ryan, M. J., & Wake, D. B. (2002). Integrating historical and mechanistic biology enhances the study of adaptation. The Quarterly Review of Biology, 2002(77), 383–408. Briggs, D. E. G. (2017). Seilacher, Konstruktions-Morphologie, Morphodynamics, and the evolution of form. The Journal of Experimental Zoology (Molecular and Developmental Evolution), 00B, 1–10. https://doi.org/10.1002/jez.b.22725 Cubo, J. (2004). Pattern and process in constructional morphology. Evolution & Development, 6(3), 131–133. Cubo, J., Legendre, P., de Ricqlès, A., Montes, L., de Margerie, E., Castanet, J., & Desdevises, Y. (2008). Phylogenetic, functional and structural components of variation in bone growth rate in Amniots. Evolution & Development, 10, 217–227. de Ricqlès, A. (1975–1978). Recherches paléohistologiques sur les os longs des tétrapodes. VII: sur la classification, la signification fonctionnelle et l’histoire des tissus osseux des tétrapodes (1975–1978): (1) Structures, Annales de Paléontologie, 61, 51–129; (2) Fonctions, id, 62, 71–126, id, 63, 33–56, id, 63, 133–160; (3) Evolution, id, 64, 85–111, id, 64, 153–184. de Ricqlès, A. (2008). Travaux de la chaire de Biologie historique et Évolutionnisme. Annuaire du Collège de France 2007–2008, 108e année, 2008, 357–364. Desdevises, Y., Legendre, P., Azouzi, L., & Morand, S. (2003). Quantifying phylogenetically structured environmental variation. Evolution, 57, 2647–2652. Diniz-Filho, J.-A. F., & Bini, L.-M. (2008). Macroecology, global change and the shadow of forgotten ancestors. Global Ecology and Biogeography, 17, 11–17. Gayon, J. (2006). Do biologists need the concept of function? A philosophical perspective. Comptes Rendus Palevol, 2006(5), 479–487. Gould, S.  J. (2002). The structure of evolutionary theory. Belknap Press Harvard University (M. Blanc, French Trans., Paris, Gallimard, 2006). Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the panglossian paradigm: A critique of the adaptationist program. Proceedings of the Royal Society of London B, 205, 581–598. Martins, E. P. (2000). Adaptation and the comparative method. Trends in Ecology and Evolution, 15, 296–299. Mayr, E. (1961). Cause and effect in biology. Science, 134, 1501–1506. Nagy, K. A. (2005). Field metabolic rate and body size. The Journal of Experimental Biology, 208, 1621–1625. https://doi.org/10.1242/jeb.01553 Piras, P., Teresi, L., Buscalioni, A.  D., & Cubo, J. (2009). The shadow of forgotten ancestors differently constrtains the fate of Alligatoroidea and Crocodyloidea. Global Ecology and Biogeography, 2009(18), 30–40. Russell, E. S. (1916). Form and function. Londres, J. Murray. (new impr. University of Chicago Press, 1982). Seilacher, A. (1970). Arbeitskonzept zur konstruktions-morphologie. Lethaia, 3, 393–396. Thompson, D.’. A. W. (1917). On growth and form. Cambridge University Press.

Chapter 12

Structure, Function and Evolution of the Middle Ear of Extant and Extinct Vertebrates: Paleobiological and Phylogenetic Interpretations Michel Laurin Abstract  The study of the middle ear function is more difficult in extinct than in extant taxa, but a good understanding of middle ear evolution cannot be gained without consideration of the extinct taxa, which outnumber extant ones by a ratio of approximately one hundred to one. Functional inference can be of two types: qualitative and quantitative. In the case of the middle ear, qualitative inference can bear on the presence or absence of a tympanum, whereas quantitative inference would consist in estimating hearing performance or frequency range of sensitivity, among other possibilities. Inferring the history of the tetrapod middle ear is further complicated by uncertainties about the origin of extant amphibians (among lepospondyls or temnospondyls). According to the traditional scenario, most temnospospondyls had a tympanum, and given that this group is often assumed to be ancestral to lissamphibians, gymnophionans and urodeles have long been thought to have lost the tympanic middle ear. Evidence is presented that temnospondyls and the first lissamphibians lacked a tympanum and that lepospondyls, from which lissamphibians probably derive, lacked a tympnum. Thus, the anuran tympanum must have appeared in the Permian or Triassic. The ancestors of gymnophionans and urodeles appear never to have possessed a tympanum.

12.1 Introduction Studying middle ear function in extant vertebrates is difficult because the ear is a delicate structure. Middle ear activity can be detected either through a measure of the tympanum (ear drum) motion through laser interferometry, or through a M. Laurin (*) CR2P, UMR 7207, CNRS/MNHN/UPMC, Muséum National d’Histoire Naturelle, Bâtiment de Géologie, Paris, France e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_12

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measure of neuron activity (electrical action potential) in the inner ear, which is an obligatory link between the middle ear and the brain (Werner et al., 2002, 2008). Such studies are difficult enough. Nevertheless, studying middle ear function in ancient vertebrates is much more difficult because it cannot be studied directly through measurements of the two types evoked above. It rests on an integration of studies of the middle ear function of extant vertebrates and on our meager knowledge of the structure of the middle (and more rarely, internal) ear and systematic position of the relevant fossils. Obviously, paleobiological inferences about hearing abilities in early vertebrates are much more uncertain than observations about hearing performance in extant vertebrates. There are two basic types of paleobiological inferences. The first is qualitative inference, such as determining the presence or absence of a tympanum in an extinct taxon. This can be based on the presence of discrete osteological characters, such as an otic notch, or on quantitative data, such as the diameter of the stapes. The second, the quantitative inference, could bear on the sensitivity of the ear, or on the frequency at which it is most sensitive, for instance. It is based essentially on quantitative data, such as (in the case of hearing ability) stapes size, skull dimensions, and estimated tympanum size (if present), but it can also incorporate qualitative data. Generally, quantitative inference can be attempted only if qualitative inference is fairly easy. As we will see, in the case of the middle ear of Paleozoic vertebrates, even the qualitative inference is difficult (there are controversies about the presence of a tympanum in several taxa). Thus, this contribution will focus mostly on qualitative inference, but a few general comments on quantitative inference will also be given. Studying the evolution of middle ear function in long-extinct taxa is even more difficult and gives results less precise than paleobiological inference, because our indirect knowledge about this evolution rests on the data evoked above (observations on extant taxa, paleobiological inferences and the systematic position of extinct taxa), but the uncertainties affecting all the source data combine to make evolutionary inferences about functional characters highly uncertain and mathematically (or statistically) complex. This can be illustrated through a simple hypothetical example. Suppose that we want to know the difference in performance between two species and that this performance is 0.6 ± 0.05 and 0.8 ± 0.05. The difference in performance between both species is then about 0.2, but the uncertainty about this value is greater than 0.05. If we want to know the evolutionary rate of the character, the situation is worse still, because suppose that both species are extant and that they diverged from a last common ancestor 12.5 ± 2.5 Ma. The evolutionary rate will then be 0.0008/Ma, but this value has a greater uncertainty because both the difference between species and their divergence data have associated uncertainty. The uncertainty thus increases with the level or complexity of the inference. Inferring an evolutionary rate is one of the worst-case scenarios because this is one of the highest-­level inferences that could be attempted (the farthest from observations), though such rates are normally inferred by comparing dozens of species, not just a single pair, which should minimize variance of the estimates. However, most quantitative paleobiological inferences bear on the simpler problem of estimating the

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value of a character in a hypothetical ancestor (Laurin, 2004) or in some extinct species (Laurin et al., 2004; Quémeneur et al., 2013), rather than on evolutionary rates. The latter are inferred mostly as intermediate steps in molecular dates (Sanderson, 2002; Britton et al., 2007), which are also inferred with much uncertainty (Shaul & Graur, 2002; Graur & Martin, 2004; Britton, 2005; Marjanovic & Laurin, 2007; Pyron, 2011). Thus, when all sources of uncertainty affecting paleobiological inferences are considered (and functional inferences about ancient species are all paleobiological inferences), it is easy to understand why many paleontologists were not interested in this topic until fairly recently. Nevertheless, this chapter attempts to tackle the challenge of inferring middle ear function in Paleozoic vertebrates.

12.2 Principles of Paleobiological Inference The most direct and general method to draw a paleobiological inference consists in building inference models from extant taxa in which a relationship between a function of interest and structural (normally skeletal) attributes can be established. Thus, by using quantitative data on bone microanatomy, we can, using logistic regressions (Laurin et al., 2004) or discriminant analyses (Kriloff et al., 2008; Quémeneur et al., 2013), build inference models about the lifestyle (aquatic, amphibious or terrestrial; this is a qualitative inference). Through cross-validations, it is even possible to assess the success rate of such models, although this rate is valid only on the extant taxa sampled; the actual success rate, when applying it to Paleozoic taxa, must be lower. It is also possible to use simple or multiple linear regressions to build quantitative inference models if the characters of interest are continuous and if they have a normal distribution. Thus, Pouydebat et al. (2008) built models to infer the relative frequency of various kinds of grasping behaviors, such as the precision grip that some authors attributed only to humans. In fact, a large array of statistical methods can be used for paleobiological inferences. Returning to hearing, sophisticated models to infer the hearing acuity of odontocete cetaceans have been built (Hemilä et al., 1999). Qualitative inference models (such as for the presence or absence of a tympanum) have generally not been formulated mathematically, but they have nevertheless been applied to infer the presence of a tympanum (Laurin, 1998). The precision or performance of an inference model must decrease whenever we apply it outside the clade within which the relationships between the variables were studied and as the geological age of the taxa to which we apply it increases. Thus, the studies by Laurin et al. (2004) and Kriloff et al. (2008) were based on 46 lissamphibian and 98 tetrapod species (plus the Devonian tristichopterid sarcopterygian Eusthenopteron), respectively. These inference models are thus probably most reliable within lissamphibians and tetrapodomorphs, respectively (Fig. 12.1). These are the clades within which inference is fully justified. Witmer (1995) initially drew attention to this problem (under the name “extant phylogenetic bracket”) in a slightly different context; he was trying to reconstruct structures that generally do

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Fig. 12.1  Extant phylogenetic bracket and tetrapodomorph phylogeny. If an inference model is based on extant tetrapods (amniotes and lissamphibians), the clade within which inferences are fully justified is the crown-group, as shown in the figure. The sampling used by Kriloff et al. (2008) also included a tristichopterid (the taxon at the extreme left), so in their case, valid inferences could be drawn in most tetrapodomorphs (which include all taxa shown here)

not fossilize in extinct species, mainly based on parsimony, the phylogeny, and the distribution of these structures in extant vertebrates. Nevertheless, a similar reasoning applies to inferences drawn from models built from extant taxa and from continuous or discrete characters (Laurin et al., 2004). The reason is simple: a correlation between two characters may be strong in a clade, but weak or inexistent in another, because organisms evolve and all are different, contrary to atoms and other simple entities studied in chemistry or physics. Furthermore, the structures or mechanisms involved are often only analogous, not homologous, which may limit the scope of inference models. Thus, as we will see, even though the stapes (the main middle ear ossicle in most tetrapods) is homologous in all tetrapods, the tympanum is not; it obviously appeared multiple times. Thus, since the tympanum of anurans (frogs and toads) is not homologous with that of mammals, and since the middle ear architecture differs (there is a single ossicle in anurans, but three in mammals), an inference model designed for anurans would work poorly if applied to mammals. This is one of the reasons why there are very few universal laws in biology, contrary to chemistry and physics. An alternative to paleobiological inference models is optimizing characters on evolutionary trees. These optimizations can be obtained through various methods, such as standard parsimony (Swofford & Maddison, 1987) or maximum likelihood (Felsenstein, 1973) for discrete characters or squared-change parsimony (Maddison, 1991) for quantitative characters. In the last case, confidence intervals can be calculated through phylogenetic independent contrasts (Felsenstein, 1985). Contrary to

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inference models, which are mostly used for extinct species represented by fossils, optimizations are mostly used to infer properties of hypothetical ancestors that have (for the most part) left no trace in the fossil record, but an alternative strategy could be envisioned (Canoville & Laurin, 2010). Thus, the body size of the first amniote was inferred (with confidence intervals) using data on the body size of 107 species of early (Devonian to Middle Permian) stegocephalians (as limbed vertebrates will be called throughout this chapter; see Laurin, 1998 for the nomenclature), with seven reference phylogenies (to incorporate some uncertainty concerning topology and branch lengths), through squared-change parsimony and phylogenetic independent contrasts (Laurin, 2004). The main limitation of this approach is that if the relevant data are available only on extant taxa, uncertainty is directly proportional to the geological age of the hypothetical taxon for which we want to draw the inference. However, this method has the advantage that it is applicable even in the complete absence of fossils, which broadens its field of potential applications to taxa lacking a fossil record or to characters that do not fossilize, for which the model-­ based methods are inapplicable. Thus, Garland et al. (1997) inferred osmotic concentration of blood plasma of various hypothetical ancestors of amniotes. The evolution of this character is impossible to study through the fossil record because no osteological or histological correlates are known. The rest of this paper will deal with inferring the evolutionary history of the structure and (especially) function of the ear. Now that the methodological limits have been briefly discussed, the next step, before discussing ear evolution, is to discuss ear structure.

12.3 Main Parts of the Ear The ear includes three parts: the inner ear  – the oldest, the middle ear,  and the external ear. The internal ear exists in all craniates (the smallest clade that includes hagfishes, lampreys, and gnathostomes). Thus, its origin harks back at least to the Ordovician (more than 444 Ma), if not the Early Cambrian (more than 488 Ma), if we accept the interpretation given to some fossils devoid of a mineralized skeleton (Shu et al., 1999, 2003). Its initial function mostly involved equilibrium and detection of movements of the animal. It initially had only two semi-circular canals (the horizontal semi-circular canal is unique to gnathostomes). Its role in hearing increased slowly in evolution and became important mostly in terrestrial vertebrates (even though one group of teleosts convergently acquired a good hearing). The middle ear appeared by the transformation of the suspensorium, which is involved in linking the jaw to the rest of the skull. The hyomandibular, which braces the jaw against the braincase in most gnathostomes, lost this role in some stegocephalians, became more slender, and acquired a role in the transmission of sounds between the tympanum and the inner ear. Once thus transformed, we call it a stapes, even though it is the same element. The middle ear acquired a role in hearing mostly after the fenestra ovalis appeared in the Devonian (Fig. 12.2), because this allowed

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Fig. 12.2 Evolution of the three parts of the ear in the relevant systematic framework. Abbreviations: E. a. external ear, Ma million years ago

the vibrations of the stapes to be transmitted directly to the inner ear fluid (in the perilymphatic system). The tympanum (Fig. 12.3), which allowed drastic improvements in hearing high-frequency air-borne sounds, like most animal vocalizations, appeared several times, starting in the Late Carboniferous. Finally, the external ear, which funnels the sounds toward the tympanum, is unique to mammals. It must thus have appeared between 180 Ma and 315 Ma ago, because the former is the approximate divergence time between monotremes and therians, and the latter is the appearance date of synapsids (Fig. 12.2).

12.4 Middle Ear Structure and Function in Extant Vertebrates Among aquatic vertebrates, hearing poses no special challenge; sound waves can easily pass from the environment to the inner ear because both are filled with water. The low hearing acuity of most primitively aquatic vertebrates is thus surprising (it is presumably partly compensated by the lateral line organ, which detects movements in water), but it is not linked with physical constraints, as shown by the excellent hearing of cetaceans. Nevertheless, the hearing acuity of our first amphibious ancestors must have been still worse in air than in water. Indeed, in air, sound waves, in the absence of a mechanism to amplify their force, are mostly reflected at the interface between air and water (which makes up most of our body) because of the

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Fig. 12.3  Middle ear structure of the gecko (squamate) Ptychodactylus guttatus. (Modified from Laurin (2010: fig. 6.9), which is itself modified from Werner and Igic (2002))

tremendous density difference between both environments (water is about 1000 times more dense than air, as measured at sea level on Earth). Furthermore, the lateral line organ does not work in air (its ciliated cells must bathe in an aqueous solution to work). The loss of functionality of both of these sensory organs in air must have contributed to the selective pressures that resulted in the appearance, multiple times in terrestrial vertebrate evolution, of a tympanic middle ear. Such an ear must have been fairly useful to detect approaching prey or predators, and later, this facilitated the appearance of vocalizations (vertebrates lacking a tympanum do not sing because songs are typically directed at conspecific individuals, so there is no point if they cannot hear). In such an ear (Fig. 12.3), sounds received at the tympanum are transmitted to one or three ossicles that carry the vibrations to the internal ear, through the fenestra ovalis. Two mechanisms contribute to amplifying the force of sound waves. The first is the ratio between the surface of the tympanum and that of the fenestra ovalis, which varies between 10:1 and 40:1, approximately. The second is a system of in and out levers (composed of the cartilaginous extra-columella in squamates, the “columella” being a synonym of “stapes” frequently used for reptiles) that decreases the amplitude of motion but increases the force by the same ratio (fairly variable, but often around four times). The combination of both mechanisms results in a force amplification of a factor of about 40–160 times, which

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allows sound waves to enter the inner ear and stimulate its neuromasts (ciliated sensory cells). It should be noted that the appearance of the tympanic middle ear was not unavoidable. Various extant terrestrial tetrapods lack one, which does not imply that they are completely deaf. Thus, snakes hear low-frequency sounds transmitted by the ground (such as the noise produced by an animal when it walks). These sounds are transmitted to the lower jaw when the head of the snake rests on the ground; they then pass to the quadrate (a bone of the primitive upper jaw that articulates with the lower jaw), then to the stapes, and, finally, to the inner ear. In urodeles, which also lack a tympanum, similar sounds are detected through the forelimbs; they are then transmitted to the opercularis muscle, which extends from the suprascapula to the operculum (an ossicle located between the stapes and the fenestra ovalis in batrachians). From the operculum, sounds enter the inner ear through the perilymphatic fluid. The tympanic middle ear disappeared in various terrestrial vertebrates, such as snakes, a few other squamate taxa, Sphenodon (Laurin, 1991), and various anurans (Laurin, 2010). Evolution is thus clearly neither linear nor irreversible.

12.5 Ear Evolution The fenestra ovalis appeared in the Late Devonian, as shown by its presence in Acanthostega and Ichthyostega, which were nevertheless primitively aquatic. It derives from the older vestibular fontanelle, but it acquired a new role after the proximal articulation of the stapes shifted there. In Acanthostega, the main role of the stapes and the fenestra ovalis may not have been hearing (Clack, 1994). However, the stapes of Ichthyostega was apparently involved in underwater hearing (Clack et al., 2003), a unique phenomenon among Paleozoic stegocephalians. Throughout the Paleozoic, the stapes retained its bracing role in mandibular suspension in most stegocephalians, as shown by its robustness in the first temnospondyls, embolomeres, amphibians (“lepospondyls”), and most amniotes. The presence of a slender stapes and the retention of an otic notch suggest that a tympanum had appeared in seymouriamorphs. The tympanum is also present in anurans, and it probably appeared three times in amniotes: once in diapsids (Laurin, 1991), a second time in parareptiles (Müller & Tsuji, 2007), and a third time in synapsids, the total clade that includes mammals (Allin, 1975). There have been, for more than a decade, two linked controversies about the function and evolution of the middle ear of Paleozoic stegocephalians. First, does the absence of a tympanum in gymnophionans and urodeles result from a loss (Fig. 12.4a), as suggested by some studies, or is it primitive (Fig. 12.4b)? Second, did some temnospondyls possess a tympanum, as suggested by some authors (Bolt & Lombard, 1985) but contested by others (Laurin & Soler-Gijón, 2006), and if so, is this structure homologous (synapomorphic) with that of anurans? This second question is both important to understand early middle ear evolution, and difficult to answer because the affinities of temnospondyls are debated; they are often

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Fig. 12.4  Hypotheses about middle ear volution in stegocephalians. A, ancient hypothesis that is still accepted by several authors; B, more recent hypothesis (Laurin, 1998). Abbreviations: Dev Devonian, Jur Jurassic, Mis Mississippian, Pen Pennsylvanian, Per Permian, Tri Triassic

considered as the stem of lissamphibians (Ruta & Coates, 2007), but this has been contested (Vallin & Laurin, 2004; Pawley, 2006; Marjanovic & Laurin, 2013). The systematic position of temnospondyls and the origin of lissamphibians remain hotly debated topics (Anderson et al., 2008; Marjanovic & Laurin, 2013), so we will not dwell on this point. The functional interpretation of the temnospondyl middle ear appears to be easier to determine. It seems likely that most (if not all) temnospondyls lacked a tympanum. Several reasons justify this conclusion. In many cases, the proximal end of the stapes is sutured, if not fused, to the edges of the fenestra ovalis, whereas the distal end contacts the ventral edge of the tabular (Laurin, 1998). The stapes is nearly always much more robust than in extant tetrapods that possess a tympanum, and in the temnospondyl Iberospondylus, an otic lamelle completely occluded the otic notch and would thus have been interposed between the stapes and the tympanum (Laurin & Soler-Gijón, 2006). Furthermore, several temnospondyls possessed a lateral line organ, which implies an aquatic lifestyle generally incompatible with the presence of tympanum, which tends to be lost in secondarily aquatic tetrapods, such as cetaceans (Nummela et al., 1999). Several authors have nevertheless asserted that temnospondyls possessed a tympanum, presumably partly because anurans are generally considered to be descendants of temnospondyls, a hypothesis compatible with some (Ruta & Coates, 2007; Anderson et  al., 2008) but not all recent phylogenetic analyses (Vallin & Laurin, 2004; Pawley, 2006; Marjanovic & Laurin, 2009). Arguments supporting

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the presence of a tympanum in temnospondyls now appear weaker than before, partly because of the recent rejection of the old idea that the otic notch was always associated with a tympanum. That idea supported the presence of a tympanum in temnospondyls because most have a well-developed otic notch. However, recent studies showed that a well-developed otic notch can be associated with a massive stapes (e.g., Clack, 1983) that could not be efficient in high-frequency air-borne sound transmission. In addition to recent phylogenetic arguments (e.g., Marjanovic & Laurin, 2013), anatomical considerations militate against this hypothesis. The most decisive, the fusion between the stapes and the neurocranium and the resulting absence of mobility of the stapes, were contested by Bolt and Lombard (1985) for five reasons. We will now examine these arguments. The first reason is that, according to Bolt and Lombard (1985), the stapes is often only sutured to the neurocranium, which would have allowed some mobility. Given that temnospondyls had undetermined (open) growth (Steyer et al., 2004), as most vertebrates (except for mammals and birds), most skull elements remained separated from each other by sutures throughout ontogeny. This does not necessarily imply that motion was possible; it was surely absent in most cases, as demanded by simple mechanical considerations. The frequent preservation of the stapes in its anatomical position (Lombard & Bolt, 1988; personal observation) suggests a coossification with the braincase. The second reason invoked by Bolt and Lombard (1985) is that the interpretation of a fusion between the stapes and the neurocranium in some (but not all) temnospondyls rests on the absence of observation of a suture (a proof resting on negative evidence). It is true that negative proofs are inherently weak, but this is the only kind of proof that we can expect to find by visual inspection of fossils, so rejecting such evidence would lead to rejecting the possibility of testing the presence of a tympanum in extinct vertebrates. The third reason is that, according to Bolt and Lombard (1985), the absence of fusion is the prevailing condition in temnospondyls. The objections raised above apply here. Furthermore, absence of fusion is frequent mostly in small individuals that were probably immature, and mostly in Permo-Carboniferous taxa. Among most Triassic temnospondyls (Schoch, 2000) and in some Permian temnospondyls well-represented by mature individuals, such as Eryops (Sawin, 1941), fusion is often observed. The fourth argument is that “Buettneria,” a Triassic temnospondyl now called Koskinodon (Mueller, 2007), is supposed to have a mobile articulation between the ventral part of the stapedial footplate and the neurocranium. This is probably an exception, a juvenile character, or a pedomorphic attribute. Bolt and Lombard’s (1985: 90) last argument is that a mobile stapes ventrally articulated with the braincase is a configuration comparable with that of anurans. This argument falls if temnospondyls are stem-tetrapods (Vallin & Laurin, 2004; Pawley, 2006), or simply if Lissamphibia is monophyletic, because the stapes of urodeles and gymnophionans differs drastically from that of anurans. This brief review suggests that temnospondyls lacked a tympanum. If the eardrum was nevertheless present, the auditory acuity of temnospondyls must have decreased drastically when the stapes fused to the neurocranium in ontogeny. This

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phenomenon, unknown in extant tetrapods possessing a tympanum (except for pathological cases associated with loss of hearing) would be illogical given that temnospondyl larvae were aquatic (Schoch, 2009) and thus lacked a need or an opportunity to use the tympanum, whereas the adults, often more terrestrial, would have lost the capacity to hear high-frequency air-borne sounds.

12.6 Discussion Despite the several sources of uncertainty discussed above, rapid progress in comparative and evolutionary biology, particularly in phylogenetics (Goloboff et al., 2003; Swofford, 2003), in molecular dating (Rambaut & Bromham, 1998; Sanderson, 2002; Thorne & Kishino, 2002; Britton et  al., 2007; Ronquist et  al., 2012; Sauquet, 2013) and in paleontological dating (Josse et al., 2006; Marjanovic & Laurin, 2007, 2008; Wilkinson & Tavaré, 2009; Sterli et al., 2013) and 3D imaging (e.g., Lemierre et  al., 2021) should quickly result in substantial progress in paleobiological inferences in the next few years. This progress should have a major impact on our understanding of functional morphology (and hence, of functions) in extinct taxa. Given that extinct species outnumber extant ones by a factor of at least 100:1, this should drastically improve our understanding of the living world. Hearing in temnospondyls will probably be better understood once their systematic position is resolved, and once the otic morphology is better described. In the meantime, we must limit ourselves to a qualitative inference (the absence of a tympanum). There would be no point in applying quantitative inference models to determine more accurately hearing acuity, because the latter depends strongly on the presence of a tympanum, which remains contentious. Middle ear evolution can be briefly and tentatively outlined, according to the suggestions made above (Fig. 12.4b). The first stegocephalians apparently lacked a tympanum. This structure may have appeared in a few temnospondyls (although only in a small minority of species, and even this remains to be convincingly demonstrated) and probably appeared in seymouriamorphs. Among amniotes, it appeared at least three times (in synapsids, parareptiles, and diapsids). Among amphibians, the tympanum is found only among anurans. The older hypothesis that the anuran tympanum derives from a similar structure in temnospondyls is poorly supported by evidence, even though it remains popular among paleontologists.

References Allin, E.  F. (1975). Evolution of the mammalian middle ear. Journal of Morphology, 147(4), 403–437. Anderson, J. S., Reisz, R. R., Scott, D., Fröbisch, N. B., & Sumida, S. S. (2008). A stem batrachian from the Early Permian of Texas and the origin of frogs and salamanders. Nature, 453(7194), 515–518.

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Sterli, J., Pol, D., & Laurin, M. (2013). Incorporating phylogenetic uncertainty on phylogeny-­ based paleontological dating and the timing of turtle diversification. Cladistics, 29(3), 233–246. https://doi.org/10.1111/j.1096-­0031.2012.00425.x Steyer, J.-S., Laurin, M., Castanet, J., & de Ricqlès, A. (2004). First histological and skeletochronological data on temnospondyl growth: palaeoecological and palaeoclimatological implications. Palaeogeography Palaeoclimatology Palaeoecology, 206, 193–201. Swofford, D.  L. (2003). PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates. Swofford, D.  L., & Maddison, W.  P. (1987). Reconstructing ancestral character states under Wagner parsimony. Mathematical Biosciences, 87, 199–229. Thorne, J.  L., & Kishino, H. (2002). Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology, 51(5), 689–702. Vallin, G., & Laurin, M. (2004). Cranial morphology and affinities of Microbrachis, and a reappraisal of the phylogeny and lifestyle of the first amphibians. Journal of Vertebrate Paleontology, 24(1), 56–72. https://doi.org/10.1671/5.1 Werner, Y. L., & Igic, P. G. (2002). The middle ear of gekkonoid lizards: Interspecific variation of structure in relation to body size and to auditory sensitivity. Hearing Research, 167, 33–45. Werner, Y. L., Igic, P. G., Seifan, M., & Saunders, J. C. (2002). Effects of age and size in the ears of gekkonomoph lizards: Middle-ear sensitivity. The Journal of Experimental Biology, 205, 3215–3223. Werner, Y. L., Montgomery, L. G., Seifan, M., & Saunders, J. C. (2008). Effects of age and size in the ears of gekkotan lizards: Auditory sensitivity, its determinants, and new insights into tetrapod middle-ear function. European Journal of Phycology, 456(5), 951–967. Wilkinson, R. D., & Tavaré, S. (2009). Estimating primate divergence times by using conditioned birth-and-death processes. Theoretical Population Biology, 75(4), 278–285. Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In J. J. Thomason (Ed.), Functional morphology in vertebrate paleontology (pp. 19–33). Cambridge University Press.

Part IV

Attributions of Function in Experimental Biology

Chapter 13

The History of Integration: From Spencer to Sherrington and Later Jean-Claude Dupont

Abstract Integration is now very successful in the field of life sciences: neuroscience, physiology, and a whole part of biology claim to be “integrative.” The term appears in the titles of scientific journals: Integrative Biology, Integrative and Comparative Biology, OMICS: A Journal of Integrative Biology, etc. However, this situation results from a complex genealogy. Initially mathematical like the notion of function, the concept penetrated into the field of life sciences in the second half of the nineteenth century. Its history meets simultaneously Herbert Spencer’s evolutionism and Claude Bernard’s physiology. It will take a more specific meaning in John Hughlings Jackson’s, David Ferrier’s, and especially Charles Scott Sherrington’s neurologies. The following contesting of the Sherringtonian paradigm will not prevent the development of the notion in general physiology at John Barcroft’s instigation. We suggest here investigating the successive rectifications of the concept of integration, which every time express a different vision of the body and successively a strategy to be adopted to elucidate its physiology.

13.1 Introduction The notion of integration is now very successful in the field of life sciences: neuroscience, physiology, and a whole part of biology claims to be “integrative.” The term appears in the titles of new scientific journals as well as new versions of old publications, such as the venerable AJP (1898), henceforth Regulatory, Integrative and Comparative Physiology (Table 13.1). What are the historical roots of the concept of integration? What epistemological meaning can we give to this extension? How does it relate to the biological use of the concept of function? J.-C. Dupont (*) Professeur des Universités, Centre d’histoire des sociétés, des sciences et des conflits (CHSSC-EA 4289), Université de Picardie Jules Verne, UFR de sciences humaines et sociales et philosophie, Pôle Citadelle, Amiens, France e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_13

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Table 13.1  List of life science periodicals whose title refers to “integration” Some titles American Journal of Physiology. Regulatory, Integrative and Comparative Physiology = Am J Physiol Regul Integr Comp Physiol Communicative and Integrative Biology = Commun Integr Biol Comparative Biochemistry and Physiology: Part A, Molecular & Integrative Physiology = Comp Biochem Physiol, Part A Mol Integr Physiol Continues Comparative Biochemistry and Physiology. Part A, Physiology Frontiers in Integrative Neuroscience = Front Integr Neurosci Functional & Integrative Genomics = Funct Integr Genomics Omics : A Journal of Integrative Biology = OMICS Continues: Microbial & Comparative Genomics. Integrative and Comparative Biology = Integr Comp Biol Integrative Biology : Quantitative Biosciences from Nano to Macro = Integr Biol (Camb) Integrative Zoology = Integr Zool Journal of Integrative Plant Biology = J Integr Plant Biol Integrative Cancer Therapies = Integr Cancer Ther Journal of the Society for Integrative Oncology = J Soc Integr Oncol Continue : Journal of Cancer Integrative Medicine Integrative Psychiatry = Integr Psychiatry Homeostasis in Health and Disease : International Journal Devoted to Integrative Brain Functions and Homeostatic Systems = Homeost Health Dis Continues : Activitas Nervosa Superior. Integrative Physiological And Behavioral Science = Integr Physiol Behav Sci Continues: Pavlovian Journal Of Biological Science Integrative Phychological and Behavioral Science = Integr Phychol Behav Sci Continues : Intergrative Physiological and Behavioral Science Journal of Integrative Neuroscience = J Integr Neurosci

Start publishing 1977

Country USA

2008

USA

1998

USA

2007

Switzerland

2000

Germany

2002

USA

2002

England

2009

England

2006

Australia

2005

China

2002

USA

2005

Canada

1983

USA

1991

Czech Republic

1991

USA

2007

USA

2002

England (continued)

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Table 13.1 (continued) Some titles Integrative Medicine : Integrating Conventional and Alternative Medicine = Integr Med Chinese Journal of Integrative Medicine = Chin J Integr Med Zhong xi yi jie he xue bao = Journal of Chinese Integrative Medicine = Zhong Xi Yi Jie He Xue Bao

Start publishing 1998

Country USA

2003

China

2003

China

13.2 The Evolutionary Integration The concept of integration, like that of function, is at first mathematical. It extended over the nineteenth century with the general meaning of annexation of an element in a set, or insertion of a part in a whole. Later it was still extended to the scientific language of economics, ecology, psychoanalysis, and then computer science and sociology. In the field of biology, Herbert Spencer has introduced the term “integration” in a very specific meaning. Spencer defines life as equilibrium between internal forces and external forces, or as a set of adaptive relations: “the continual adjustment of the internal relations to external relations” (Spencer, 1885, vol. I: 293). Spencer described the evolution of these connections and of these correspondences between the environment and the organism, from the least developed organisms to the man. They extend in space and time; they grow in specialization, in generalization, in complexity. They undergo then coordination, and finally integration. Under the influence of the environment, superior, more definite, and complex forms group the elements that were in an individual state in lower forms. As a result of integration and differentiation, parts and functions become increasingly dependent on each other, and organic forms become more complex. Mind itself emerges from the successive phases of the progress of life, which represents at the same time the development of intelligence. It is worth remembering that for Spencer, integration has an evolutionist connotation, and not simply an evolutionary one. Integration can only be conceived in the framework of the physical and mental evolution. Integration affecting mental evolution, nerve centers play a role, which is to realize increasingly complex coordination. Though the exact role of the nerve centers in the integration was fairly obscure, and though the integration exceeded the strict framework of neurology, Spencer’s very specific and very speculative concept of integration allowed to conceive hereditary functional transformations and to derive in a phylogenetic point of view all the cognitive and affective functions from the reflexes. Reflexes became instinct, memory, reason, feelings, will. All mental states were initially imperfect

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automatic acts. At the biological level, psychic reorganization and passage to the automatism corresponded to the passage of the nervous fluid through ways and definite canals. Because these changes were heritable, one were witnessing progress of intelligence to an ever greater adaptation to increasingly complex environments.

13.3 The Neurological Appropriation of Integration By doing so derive all functions of intelligence from simple reflexes, Spencer brings back Johannes Müller and Ivan Sechenov. He is in the lineal heir of the British tradition of the organic theorists of the mental functions: David Hartley, Erasmus Darwin, James Mill, and Alexander Bain, whose inspiration is associationism. This tradition continued abroad with Ribot, and beyond the Atlantic Ocean notably with William James. Spencer hence incarnates the physiological turn of the psychology, trying to think mental functions using the model of sensorimotricity. Numerous neurologists who admitted a debt to Spencer reused the concept of integration: Brown-Sequard, John Hughlings Jackson, and David Ferrier. Spencer became the common theoretical reference to the whole British neurology till Sherrington. Before integration became a general physiological concept, neurophysiology indeed more especially appropriated it. But this appropriation came along with a rectification. Integration was deprived of a part of the attributes of Spencerian evolutionism. The concept was detached from the Spencerism as a system, by keeping a more or less evolutionary connotation. Integration became more prosaically the process by which the action of the nervous system contributed essentially to unify the expressions of the activity of the individual, and in particular the sensorimotor activity. It remained to specify the action of the nerve centers. There were in this regard significant differences between Brown-Sequard, Jackson, Ferrier, and Sherrington. The idea of integration was present among these authors. But except for Sherrington, the concept was not developed systematically. It was rather a background for their research program. For example, the most important work of Charles Eduard Brown-Sequard concerned the crossing of the sensory nervous ways in the marrow: a hemisection of the marrow produced a paralysis on the side of the section and an anesthesia on the other side. Symptoms were the result of a combination of the two types of elementary activities of the central nervous system (Brown-Séquard, 1882). Sherrington has admitted Brown-Sequard’s influence on the idea of a double action in the cerebral cortex, excitation and inhibition. With hindsight, more generally the concept of “final common pathway,” the autonomy of the marrow, and even the concept of integrative action could be extensions of Brown-Sequard’s ideas. According to John Hughlings Jackson, integration was carried out on each hierarchical level of the central nervous system. Jackson described the psychic system as a hierarchy of levels corresponding to the evolutionary history of the brain. This history was reflected in ontogenesis: this reminded Spencer, but also

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Haeckel. Evolution went from organized, automatic lower centers toward less organized, voluntary higher centers. Dissolution went in opposite direction. It was visible in the attacks of the nervous system and results in the abolition of the function of higher centers and in the exaltation of the function of the underlying centers (Jackson, 1884). Ribot applied this concept of dissolution to amnesia and the theorists of the aphasia too. The stimulation of the cerebral cortex, resumption of Fritsch and Hitzig, and the techniques of ablation allowed him to draw up a cortical map of the sensorimotor functions of various types of vertebrates, particularly the monkey. The experiments of ablation in animal suggested him the hypothesis that the frontal lobes could support a psychological function, the selection, and the inhibition of ideas in competition, which is a characteristic activity of attention and intelligence (Ferrier, 1876). Ferrier’s experimental analyses contributed to give stronger physiological bases to sensorimotor activity, and Sherrington recognized that, and he dedicated his famous book The Integrative Action of the Nervous System to Ferrier. Ferrier reinforced the idea that it was possible to build a functional psychology from sensorimotor data, that is, to connect mental functions with a cerebral cortex described in sensorimotor terms, with psychological units constituted by sensations and by associated movements (which became later stimuli and associated responses). Basically, this inspiration derived from Bain and Spencer.

13.4 The Combinatory Integration But the man who renewed the concept of nervous integration was Charles Scott Sherrington. Sherrington especially used the concept of integration in the sense of complex combination of multiple signals, capable of integrating messages at a medullary level, so as to realize a coordination of suitable responses. He gave to the term integration a special connotation, not an evolutionist connotation in the sense of Spencer, although the adaptive connotation was preserved, but rather a combinative dimension, of calculation, computational, as we would say today. Sherrington’s genius would consist in the fact that it gave empirical bases to the concept at neurological level. The Integrative Action of the Nervous System, published in Sherrington, 1906, is the result of 15  years of experimental researches. Beyond a simple way of conduction, Sherrington described the activity of the marrow as that of a mechanics of precision, possessing a perfect functional unity. He explained coordination in the simple reflexes, the interaction between the reflexes, and compound reflexes resulting from simultaneous and successive combinations. Sherrington conceived the locomotion of mammals, as the perfect fitting of a set of reflexes. Essential concepts were final common path and reciprocal innervation: the motor neuron receives the multiple sensory afferences that join (summation) or oppose (inhibition). Coordination supposes the mutual innervation of the antagonistic muscles. It also supposes the presence of intercalated neurons in the medullary

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segments and between the segments, that is to say in the various stages or levels of the spinal cord. The term synapse was introduced to name interneuron connections. Control exerted by overlying structures, shown on the decerebrate preparation (decerebrate rigidity), supposed a functional hierarchy between the centers where integration was realized. These findings resulted from the application of a rigorous methodology as follows: to identify an elementary behavior, to determine a priori the minimal neurological components necessary for this behavior; to look for the evidence of the existence of these components. It was this very robust methodology that led to the postulate of the synapse. What is finally Sherrington’s profound originality in the physiological thought? We can summarize the characteristics of Sherrington’s neural integration as follows: 1. First, spinal reflex is conceived as a unitary basic model, the functional unit of the integration. 2. This power of integration is a medullary capacity of calculation. The nervous system becomes a computing system corresponding sensory events to motor responses, according to a logic for which he tries to decipher. Sherrington would have proposed something as a calculation of the reflex, describing a series of elementary operations from which every determined behavior could be generated. He imagines more and more complex circuits, basing on a binary logic (of excitation and inhibition), an algebra in + and −. We know the realization that his pupil Eccles will give to this algebra, by recording the excitatory postsynaptic potentials (EPSP) and inhibitory postsynaptic potentials (IPSP) with intracellular techniques. 3. The clarification of conditions and the neurological means of the integration of functions raise the important question of the general purpose of integrative function. Naturally, this purpose is adaptation. Reflexes are plastic reactions continually adapted to the environment. Sherrington describes in the two final chapters of The Integrative Action the analysis of the receptive fields, exteroceptive and interoceptive fields, and the analysis of the interface of the organism and the environment, which he places in the process of the evolution. He develops there a true philosophy of organism and at the same time a biology of behavior, based on integration.

13.5 Progresses and Corrections of the Neural Integration Sherrington’s contribution had decisive epistemological implications on the problem of the function. While Marshall Hall conceived reflex as a stereotypical functional reaction, Eduard Pflüger regarded it as a functional, local, and adequate response. This adaptive function of the reflex was an appearance of intelligence, of psychic activity. Pflüger spoke about “medullary soul,” because he conceived with trouble the function as an expression of pure mechanism.

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Pflüger became aware of this epistemological problem and tempted the first to formalize reference to the function in physiology. He formulated the famous “law of teleological causality” (1877): the origin of a need in a living organism is also the origin of the means of satisfying the need. In the case of the pupil: “The need here is for the correct degree of excitation of the optic nerve, in the way more suitable for acute perception. Thus the excitation of the optic nerve itself must control the width of the pupil” (Pflüger, 1877, p. 78). However, it remained difficult to see the reflex as both an unconscious mechanism, as a purely local phenomenon already, and as a phenomenon suitable for purpose. Sherrington then had designed the reflex as a unit of functional integration. Sherrington made the reflex dependent on the activity of the nervous system. By there, he removed from the reflex the status of local phenomenon. The reflex became a simple functional unit of nervous integration, and consequently the discussions relating to the dependence on the central nervous system, and to the conscious or intelligent “nature” of the reflex, became less relevant. By making reflex a unit of functional integration, participating in the functioning of the whole nervous system in an adaptive direction, Sherrington marked a further step, beyond Pflüger, toward the mechanistic debunking of the function. Consequently, reflex became essentially a functioning to be deciphered, independently of the epistemological problem of the function. The epistemological problem of the function was no more directly associated to the reflex, because it is deferred at the more global level of the organism. Moreover, the reflex function was maintained in the evolutionary framework. Therefore, neurophysiologists could focus easily on mechanisms. However, the concept of integration was quickly challenged. The essential criticism was that the nervous system according to Sherrington remained a too passive entity, in line with Spencer. The nervous system initiated nothing on his own authority, spontaneously. Reflexes were the units of organization both of the nervous system and behavior, in particular motor function. So sequential behavior as walking was a chain of reflexes, in which every element involved the following one automatically. But the adequacy of the model of the reflex to explain all the behaviors was criticized. Additional “extra-reflexive” mechanisms were necessary, particularly to explain sequential behavior as walking. Several mechanisms were proposed for the control of motricity, which constitute rectifications of the Sherrington’s conceptions. Thomas Graham Brown, a pupil of Sherrington, supported on the basis of surgical experiments that the motor function of the cat was not explained by the coordination of reflexes and the sensory input. It was connected to a central, medullary rhythmic activity (Graham Brown, 1914). We can quote also Erik von Holst and Horst Mittelstaedt, and their principle of reafference: any movement controlled at central level causes an afferent signal (reafference) starting from the peripheral receptors (von Holst & Mittelstaedt, 1950). The behavior can even be structured hierarchically, as supports it Paul Weiss. Weiss sets that the walking results from the activity of a higher nerve center, which executes specific plans. Afferences only modify and control actions, adapting them to circumstances (Weiss, 1941).

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A dispute maybe more fundamental resulted from the physiology of the action, in particular from the Russian schools. Russians started from a contesting of Pavlov, but also indirectly of Sherrington when they supported that reflexes were not the organizational basic elements of the behavior. A physiology of the action took the place of a physiology of the reaction, putting forward the activity of centers. Pyotr Anokhin replaced the concept of simple reflex action by the notion of a system controlled by the results of its own actions, what allowed complex adaptive actions (Anokhin, 1974). One finds also in Nicholas Bernstein this notion of sanctioning afference. But it becomes only one of the functions of a comparator: another one is corrective (Bernstein, 1967).

13.6 The Regulatory Integration The mechanisms of neural integration have thus become much more complex than Sherrington imagined. Despite the neurological contestation of Sherrington’s ideas, the concept of integration extended in biology. However, the concept of integration referred to a wider and less specific physiological meaning, which did not correspond anymore either to Spencer’s meaning or completely to Sherrington’s meaning or even to post-Sherringtonian meanings. It referred to a more traditional meaning, connected with the idea of regulation. It was because integration was not dissociable of the fundamental idea of regulation, which was more than a simple reflex and which was consubstantial with the physiology, that integration remained anchored in the physiology. If the integration of parts produced order of the whole, that supposed mechanisms of reactions to modifications of the environment. In other words, for that integration was possible, it was necessary to include reflex in a vaster functional system that it becomes the element of a regulation. Reflex was according to Pflüger an agent of regulation, “a mechanism of preservation of the constancy of a function” (e.g., pupillary reflex maintained correct vision). The function was already the determining cause of regulating mechanisms. But this returns us more especially to Claude Bernard. According to Claude Bernard (1878, 9th lecture), integration referred at the same time to integrality (completeness) but also to integrity. Claude Bernard did not use the term integration but that of “redintegration,” namely, action that brought a thing back to its first integrity. The redintegration was the action by which an organism regenerates amputated or necrosed part. In this embryological conception, integration already took a regulating connotation. Of course, Claude Bernard’s integration referred to another system of well-known notions. If integrative spirit was inherent to Claude Bernard’s physiology, it was by virtue of the preservation of “the unity of the conditions of life in the internal environment (milieu intérieur).” The concept of constancy of the internal environment supposed the idea of a regulation, ensured with nervous and humoral mechanisms. The elucidation of these mechanisms constituted a considerable research program for the physiology of correlations, which

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was concerned with the autonomic nervous system and with humoral agents of correlation, hormones, and neuromediators. The famous Cambridge School of Physiology, to which Sherrington did not belong, but where he studied, introduced a good part of these works. But what was common to Claude Bernard and to Sherrington was the concern of thinking integration at the various levels of organization. Integration according to Sherrington concerned the neuron. It concerned the cell in general for C. Bernard. It was at first the cellular theory that makes for Claude Bernard the relation of the part in the whole a relation of integration. The biological history of integration would have really started with Claude Bernard, and maybe with Kölliker and his idea of a cellular physiology, continued by Sherrington at the level of the neuron. Although Claude Bernard did not use the term, it was rather integration in Bernard’s meaning than the integration in Sherrington’s meaning, too limited to nervous area, which was converted to general physiological concept. According to Joseph Barcroft, for example, each physiological adaptation maintained constancy of the internal environment due to an integration of parallel or antagonist mechanisms (1934). From the beginning, it was the goal of classical physiology, which in this sense could only be integrative, to identify experimentally the basic interactions of integration. Under Bernard’s impetus, the study of the physiological integration penetrated all levels of biological organization, from the molecule to the organism.

13.7 Toward the “Integrative” Biology? Physiology has thus historically individualized through the two concepts of integration and regulation. In addition to these fundamental concepts, other conceptual tools were developed very early to try to understand the complexity of biological organization. The theory of levels of integration was defended by Joseph Needham (1937) and later by Alex Novikoff (1945) and James K. Feibleman (1954). It was discussed by theorists of biology like Ludwig von Bertalanffy, John H.  Woodger, Paul Weiss, Conrad H.  Waddington, etc.. The notion of integration removes an arbitrary element in the concept of level of organization: each level includes the lower by the emerging properties that organize its constituent levels. The effort focuses on each passage between levels of integration. Experimental strategies aim to integrate description mechanisms between different levels (Craver, 2002; Craver & Darden, 2001, 2005). If biology is affirmed in part now “integrative,” it is primarily in response to its recent history. The new informatics tool has enriched several possible approaches. For some, it is only the use of bioinformatics and massive heterogeneous data of the post-­ genomic (“horizontal” integration). Others are investigating the passage levels of basic organization to more complex levels (“vertical” integration). It is possible

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finally to focus on the implementation of knowledge about a particular species (model organisms) to a broader set of species (“transversal integration”) (Passioura, 1979, Pigliucci, 2003, Wake, 2003). Ultimately, it is sometimes expected this “new” integrative biology is a holistic understanding of biological phenomena mathematically modeled with the prospect of a life, curiously recalling the mathematical origin of the concept of integration (Chauvet, 2004).

13.8 Conclusion Claude Bernard thought the idea of integration consubstantial with the notion of function: “La fonction est une série d’actes ou de phénomènes groupés, harmonisés en vue d’un résultat déterminé. Pour l’exécution de la fonction intervient l’activité d’une multitude d’éléments anatomiques ; mais la fonction n’est pas la somme brutale des activités élémentaires de cellules juxtaposées ; ces activités composantes se continuent les unes par les autres ; elles sont harmonisées, concertées, de manière à concourir à un résultat commun. C’est ce résultat entrevu par l’esprit qui fait le lien et l’unité de ces phénomènes composants, qui fait la fonction” (Bernard, 1878: 9th lecture). In the history of physiology, the concept of integration undergoes successive corrections, which every time expressed a conception of the organism, and a special design of its functioning as an organized whole. The concept of functional integration has its own history, inseparable but distinct from history of special biological functions. The idea of integration evolves further in its relationship to the function. It is according to Claude Bernard closely linked to the concept of integrity of the organism and to the regulation of functions. It binds from Spencer to the notion of evolution. From Sherrington, the integration keeps this evolutionary connotation, but it binds to the notion of computation or functional combinatorics, in a meaning specifically linked to the history of neurophysiology. Today, the concept of integration precludes the simple to the complex linked to the operation of an organized system. The term “systems biology” is preferred to that of integrative biology in the English-speaking world. There is some convergence between the master plans that govern the general approach of physiologists and the systemic approach functions in the philosophy of biology. Yet the notion of integration still retains its historical evolutionary connotation. It supports the same tension as the notion of function between systemic and etiological theory and has the same dimensions, normative and teleological, which are the result of its history. To be regretted or not, this trivialization of the term integration reflects a background process: the evolution of biology toward still finer description of functional architectures and toward understanding of increasingly integrated functions.

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References Anokhin, P.  K. (1974). Biology and neurophysiology of conditioned reflexes and their role in adaptive behaviour. Pergamon. Barcroft, J. (1934). Features in the architecture of physiological functions. The McMillan Company. Bernard, C. (1878). Leçons sur les phénomènes de la vie communs aux animaux et aux végétaux (p. 1966). Vrin. Bernstein, N. A. (1967). The coordination and regulation of movement. Pergamon Press. Brown-Séquard, C.  E. (1882). Recherches expérimentales et cliniques sur l’inhibition et la dynamogénie. Masson. Chauvet, G. (2004). The mathematical nature of the living world. The power of integration. World scientific publishing company. Craver, C. (2002). Interlevel experiments, multilevel mechanisms in the neuroscience of memory. Philosophy of Science (Supplement), 69, S83–S97. Craver, C., & Darden, L. (2001). Discovering mechanisms in neurobiology: The case of spatial memory. In P.  Machamer, R.  Grush, & P.  McLaughlin (Eds.), Theory and method in the neurosciences (pp. 112–137). University of Pittsburgh Press. Craver, C.  F., & Darden, L. (2005). Introduction: Mechanisms then and now. Mechanisms in Biology (special issue) Studies in History and Philosophy of Biological and Biomedical Sciences, 36, 233–244. Feibleman, J. K. (1954). Theory of integrative levels. British Journal for the Philosophy of Science, 5, 59–66. Ferrier, D. (1876). The functions of the brain. Elder Smith. Graham Brown, T. (1914). On the nature of the fundamental activity of the nervous centers; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. Journal of Physiology (London), 48, 18–46. Jackson, J.  H. (1884). The Croonian lectures on the evolution and dissolution of the nervous system. The British Medical Journal, 1, 591–593, 660–663, 703–707. Needham, J. (1937). Integrative levels: A revaluation of the idea of progress. Herbert Spencer Lecture, Oxford University. In Time: The refreshing river: Essays and Addresses, 1932–1942 (pp. 233–272). Allen and Unwin, 1943. Novikoff, A. B. (1945). The concept of integrative levels and biology. Science, 101, 209–215. Passioura, J. B. (1979). Accountability, philosophy and plant physiology. Search, 10, 347–350. Pflüger, E. (1877). Die teleologische Mechanik der lebendigen Natur. Pflügers Archiv der gesamte Physiologie, 15, 57–103. Pigliucci, M. (2003). From Molecules to Phenotypes? The Promise and Limits of Integrative Biology. Basic and Applied Ecology 4: 297–306. Sherrington, C. S. (1906). The integrative action of the nervous system. A. Constable. Spencer, H. (1885). The principles of psychology. Longman. Von Holst, E., & Mittelstaedt, H. (1950). Das Reafferenzprinzip. Wechselwirkung zwischen Zentralnervensystem und Peripherie. Naturwissenchaften, 37, 464–476. Wake, M.  H. (2003). What is integrative biology? Integrative and Comparative Biology, 43, 239–241. Weiss, P. (1941). Self-differentiation on the basic pattern of coordination. Comparative Psychology Monographs, 17, 1–96.

Chapter 14

Assigning Functions to Individual Macromolecules: A Complex History That Reflects the Transformations of Biology Michel Morange

Abstract  The assignment of elementary functions to biological macromolecules, and in particular to proteins, plays a major role in contemporary biology. One may see therein a natural tendency: once researchers focused their efforts on the characterization of macromolecules, from the 1930s onward, the functions hitherto ascribed to organs or cells were transferred to macromolecules. This “logical” presentation, however, overlooks the historical dynamic that transiently placed functional macromolecules center stage and which, more recently, has questioned this view. Here, I consider successively the circumstances of the birth and development of the notion of macromolecular function and then, from the 1960s, its extension and attendant difficulties. We shall see that divergent tendencies coexist today in biology and that the well-defined assignment of functions to macromolecules accompanies the tendency to “raise” the function to the supramolecular level.

14.1 Introduction […] I am astonished to see how… molecular biologists respond to the questions of molecular biology. The behaviour of macromolecules is extraordinarily surprising, and yet, on reading what biologists typically publish, one has the impression that they find that there’s nothing more natural. In the replication of DNA, in the way the double helix splits and its two strands unwind and enter different cells, and so on, in all this they only see the work of enzymes, which they believe explain everything. (Thom, 1983: 131)

René Thom’s critique underscores the major role that the assignment of elementary functions to biological macromolecules, and in particular to proteins, plays in contemporary biology. One may see therein a natural tendency: once researchers focused their efforts on the characterization of macromolecules, from the 1930s onward, the functions hitherto ascribed to organs or cells were transferred to M. Morange (*) Institut d’histoire et de philosophie des sciences et des techniques, UMR 8590, Université Paris 1, Paris, France © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_14

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macromolecules. This “logical” presentation, however, overlooks the historical dynamic that transiently placed functional macromolecules center stage and which, more recently, has questioned this view. Here, I consider successively the circumstances of the birth and development of the notion of macromolecular function and then, from the 1960s, its extension and attendant difficulties. We shall see that divergent tendencies coexist today in biology and that the well-defined assignment of functions to macromolecules accompanies the tendency to “raise” the function to the supramolecular level.

14.2 Birth and Development of the Notion of Macromolecular Function The transformation of physiology into physiological chemistry and then into biochemistry has progressively led to functions formerly ascribed to the cell, or to its living structure, protoplasm, being assigned instead to macromolecules, which replace this hitherto ill-defined structure. Pasteur considered that metabolic functions require a living cell. Right at the end of the nineteenth century, Büchner opined that a cellular extract can accomplish the same functions. Biochemists in the first half of the twentieth century were of the opinion that a battery of enzymes acting sequentially accounts for all metabolic functions – the synthesis or degradation of a metabolic compound. Each of the enzymes involved is responsible for one of the basic steps of these metabolic functions and so, in a way, for a basic function. This “descent” of function finds an independent parallel in heredity. Following Mendel, organisms were broken down into traits transmitted independently by factors later dubbed genes. The “function” of genes was to ensure the “reproduction” of these traits. In 1941, George Beadle and Edward Tatum (1941) established the reality and generality of a relation already proposed before them by many biologists: each gene corresponds to an enzyme, and each enzyme corresponds to a gene. This relation fitted well with the increasing role ascribed to genes and enzymes in the writings of biologists. It justified the idea that any gene (and its product) has a basic function, which is to accelerate greatly, and thereby enable, a particular chemical reaction. The first geneticists, like Edward B. Lewis, who attempted to pinpoint and explain the role of genes in embryonic development, agreed with this outlook: the genes involved in embryonic development control the specific chemical reactions of this process (Lewis, 1951). This assignment of basic functions to proteins (and to enzymes) can be justified both systemically and etiologically. The overall system comprises all the chemical reactions in the synthesis or degradation of a metabolite, while each enzyme is one of the components of this system. In the 1950s, ideas were put forward to explain how metabolic pathways were able to lengthen and how this extension conferred a selective advantage on the organisms in which it occurred. Suppose, for example,

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that the ancestral organism found in its environment a compound B and that the appearance of enzyme 1 enables transformation of compound B into compound C, which is essential for cellular survival but is scarce in the environment. Suppose now that, in the environment, compound B has become rare, whereas another molecule, A, is abundant. The organism that, again, “invents” enzyme 2, which can convert A into B, will have a definite selective advantage compared with organisms solely able to use B. This type of scenario – which is hard to demonstrate and so is largely hypothetical  – explains the progressive emergence of complex metabolic functions and justifies the selective advantage conferred by the invention of each new step and hence of the enzyme underpinning it.

14.3 Extension and Difficulties Associated with the Notion of Macromolecular Function Even at the time it was proposed, it was clear that the one gene-one enzyme hypothesis could not be applied to all genes and, hence, to all proteins. The so-called structural proteins, which ensure the cohesion of tissues and cells, had already been described. Likewise, antibodies, which are important for the immune response, are proteins with no enzymatic functions. These exceptions to the general model were cases apart and were deemed to be of secondary importance and not to be involved in the most fundamental mechanisms of living organisms. Paradoxically, it was progress in molecular description that led to the discovery of new functions but also, progressively, to the fading of the very notion of macromolecular function. In 1952, Hodgkin and Huxley interpreted nerve impulses as the transient passage of ions through the membrane of nerve cells (Hodgkin & Huxley, 1952). The pores or channels allowing the passage of these ions were identified as proteins, before the structure of these proteins was described and used to explain their function as channels (Trumpler, 1997; Doyle et al., 1998). Also, the capacity of small proteins, hormones, and growth factors to bind to cell membranes, thereby inducing morphological or metabolic transformations, was explained by the presence on the cell surface of receptors, which were gradually identified as proteins. Structural characterization of these receptors explained how a ligand binding to the outside of the membrane can trigger a series of transformations within the cell. In 1961, François Jacob and Jacques Monod distinguished two classes of genes, so-called structural genes that enable the synthesis of proteins with various functions, particularly enzymatic, and regulatory genes whose products have the sole function of regulating the expression of structural genes (Jacob & Monod, 1961). Jacob and Monod found these two types of functions to be so different that they initially thought that the product of a regulatory gene was an RNA, which is chemically distinct from the product of structural genes, as can be seen from the formalism they used to represent the molecules in Fig. 6 of their article.

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This identification of the product of regulatory genes as RNA can be viewed as a mistake, which was quickly corrected in the years that followed, or as an anticipation of the increasing part played by regulatory RNAs in contemporary biology (, Morange2008). The highlighting of these two new functions, those of receptors and of regulators of transcription, was not only an extension of the notion of macromolecular function but also the start of a seemingly inexorable process leading to the reconsideration of this notion. The characterization of receptors led to that of the pathways that conduct the signals of the cell membrane to their intracellular targets. Two of the characteristics of the components of these signaling pathways  – their number and their lack of specificity (they often belong to several different pathways) – made it hard to assign precise functions. In addition, while some proteins forming these pathways and networks have enzymatic functions, others serve only as “adaptors,” that is, they connect other components of the same pathways. The adaptor has a “borderline basic” function which is hardly distinguishable from the overall function of the system. Discoveries concerning the proteins that regulate gene expression raised the same difficulties. Far from being specific to a regulation like the first regulatory proteins characterized, most, particularly in the most complex organisms, have a regulatory power that is limited but which concerns a large number of genes coding for proteins with highly diverse intracellular functions. Specific regulation emerges from the combination of these nonspecific regulators. So, the function of these transcription factors is very hard to define! The difficulty is even greater for the more recently discovered RNA regulators, which are the subject of much current research and whose inhibitory effect is minimal but whose targets are legion. In the process called annotation, which follows genome sequencing and which consists in assigning an elementary function to each gene, biologists had to resign themselves to establishing what they call an ontology, which is much more complex than they would have liked. Three functions are attributed to each gene: a basic function, e.g., enzymatic; a global function, such as participation in a regulatory network; and a localization function corresponding to the positioning of the protein in the cell. It is pointless to focus upon the heterogeneous nature of this ontology and particularly on the tension between the basic function, which is often reduced to few elements, and the overall function, which is the process in which the elementary component participates. If the systemic justification of the assignment of functions to proteins (macromolecules) is brought into question, the etiological justification is also undermined. Be they transcription factors or elementary components in networks, their function has varied during evolution. Involved at first in a single process, they have been successively recruited during the evolution of living organisms to perform other, sometimes quite distinct, functions. The etiological justification of basic functions is often very hard! The tinkering of evolution blurs roles (Jacob, 1977).

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14.4 Current Divergent Tendencies The difficulties described above have only increased in recent years. The limits of the functional assignment of elementary proteins (and of genes) have been amply demonstrated by gene inactivation or knockout experiments made possible by advances in the 1980s (Morange, 1998). The functions revealed by these experiments – the consequences of the inactivation – did not correspond to the functions until then assigned to these genes and proteins. The demonstration of transcriptional regulatory networks and of protein interaction networks using post-genomic technologies led to a function being attributed to these networks, or to parts thereof, and not to their elementary components. Function emerges from the dynamic of these systems formed by dozens or hundreds of macromolecules. The basic functions of the components are no more than an unspecified part of an overall process. Despite these upheavals, the notion of macromolecular function nonetheless persists, for various very distinct reasons. The first reason is that not everything in a cell or an organism is a network! And a good many networks have basic functions. Metabolic pathways have been incorporated into a metabolic network, but each enzyme therein is responsible, in most cases, for a particular reaction. As in the 1940s, there were already numerous exceptions to the one gene-one protein hypothesis, and representation in networks does not account for the function of many macromolecules (Morange, 2004). It is as if there are two permissible attitudes: assign functions at a basic or at a global level. This is an impossible choice analogous to the alternation of themata that Gerald Holton evokes to account for the transformations of scientific theories (Holton, 1978). The pendulum today has swung to the side of overarching explanations, whereas its equilibrium position would doubtless be halfway between the two extremes. But there is another reason why the notion of macromolecular function refuses to go away. It is that, unlike the ignorance berated by René Thom, molecular biologists today have the explanation of the demiurgeous power of proteins and enzymes (Morange, 2005). The structural description of these macromolecules explains the functions they are capable of accomplishing in cells. One of the most illustrative examples is that of the ion channels involved in the propagation of nerve impulses. The channels have three remarkable functional characteristics: they are specific to a particular ion; they open upon propagation of a nerve impulse; and this opening is transient. These three characteristics are explicable in terms of structure (Doyle et  al., 1998). The capacity of macromolecules, generally proteins, to behave as nanomachines – an expression increasingly used to designate their functioning – is explained by their structure. Each of these nanomachines contains mechanisms underpinned by interrelated structural elements, the relative movements of which explain their function. In attributing basic functions to biological macromolecules, progress made in explaining molecular mechanisms compensates greatly for the difficulties engendered by the rise of the systemic vision.

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Even the notions of tinkering and recruitment should be handled with care (Morange, 2003), as the particular physical and chemical characteristics of a macromolecule are what enables it to perform different tasks. The notion of macromolecular function may be fading, but it will not disappear altogether. As with all tinkering, that of evolution respects the functional characteristics of the component parts it assembles. Finally, there are two additional justifications for assigning functions to macromolecular components, to proteins and RNA. The first, of little worth, is the tendency criticized by the English biologist Peter Lawrence to value the macromolecules to which the research scientist has devoted years of work (Lawrence, 2001). This justification carries little weight because if technology, as is the case today, can reveal systemic organization, it is this organization which almost automatically for the same reason takes pride of place. The second justification, which is much more fundamental, draws strength from the history, or rather the prehistory, of the evolution of living organisms. The reproduction of macromolecules is achieved through a “piece by piece” mechanism. One may imagine, as have Manfred Eigen et al. (1981) and Stuart Kauffman (1993), that the reproduction of the first macromolecules was the result of functioning in a complex network. Be that as it may, at a precise moment in the evolutionary history of life, no doubt for reasons of fidelity, this reproduction became individual. Each molecule, each RNA or protein, is reproduced from a particular genetic structure. Even if these individual genetic structures are organized within chromosomes, they retain a large degree of independence. In the case of proteins, the rule of correspondence between the nucleotide sequence and the amino acid sequence – the genetic code – makes the synthesized product, in spite of particular processes like editing and differential splicing, independent of the other genetic structures. The strong link between individual macromolecules and basic functions is also inscribed in this “frozen accident” of the evolutionary history of living forms. These divergent and virtually irreconcilable tendencies no doubt explain why a third approach is favored by many research scientists: the search for an intermediate level, that of modules, above individual macromolecules, so that it is reasonable to ascribe functions to them, but sufficiently close to these macromolecules so that the structural explanation can play its full part (Hartwell et al., 1999). This is a category necessary for understanding, because it allows large networks to be broken down into more easily studied parts, but also for practical reasons: “synthetic biologists” seek to alter living forms so that they acquire new functions by using these modules in an organism called a “chassis.” These modules then would be very useful – if they exist – but they seem to be more the artificial reification of a need than a natural category of the world. The module of the developmental biologist is not that of the molecular geneticist or that of the protein chemist (Mitchell, 2006).

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The assignment of functions to macromolecules is therefore partial, is incomplete, and seemingly can neither be abandoned nor extended. This halfway house perhaps reflects an intermediate stage in the history of life. Increasingly efficient adaptation of organisms to their environment and their increasing complexification can only be achieved, slowly and with difficulty, by surpassing the state of the fledgling organism: holistic functioning resulting from the addition of distinct macromolecular functions.

References Beadle, G., & Tatum, E.  L. (1941). Genetic control of biochemical reactions in Neurospora. Proceedings of the National Academy of Sciences of the United States of America, 27, 499–506. Doyle, D.  A., et  al. (1998). The structure of the potassium channel: Molecular basis of K+ conduction and selectivity. Science, 280, 69–77. Eigen, M., Gardiner, W., Schuster, P., & Winkler-Oswatitsch, R. (1981). The origin of genetic information (Vol. 244, pp. 78–94). Scientific American. Hartwell, L. H., Hopfield, J. J., Leibler, S., & Murray, A. W. (1999). From molecular to modular cell biology. Nature, 402, C47–C52. Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology, 117, 500–544. Holton, G. (1978). The scientific imagination: Case studies. Cambridge University Press. Jacob, F. (1977). Evolution and tinkering. Science, 196, 1161–1166. Jacob, F., & Monod, J. (1961). Genetic regulatory mechanisms in the synthesis of proteins. Journal of Molecular Biology, 3, 318–356. Kauffman, S. A. (1993). The origin of order: Self-organization and selection in evolution. Oxford University Press. Lawrence, P. (2001). Science or alchemy? Nature Reviews/Genetics, 2, 139–141. Lewis, E.  B. (1951). Pseudoallelism and gene evolution. Cold Spring Harbor Symposia on Quantitative Biology, 16, 159–171. Mitchell, S. D. (2006). Essay review: Modularity – More than a buzz word? Biological Theory, 1, 98–101. Morange, M. (1998). La part des gènes. Odile Jacob. Morange, M. (2003). Remettre un peu d’ordre physico-chimique dans l’exubérance fonctionnelle du vivant. Médecine/Sciences, 19, 643–644. Morange, M. (2004). La part des gènes: Évolutions récentes. In P.  Pharo (Ed.), L’homme et le vivant (pp. 301–313). Fayard. Morange, M. (2005). Les secrets du vivant: Contre la pensée unique en biologie. La Découverte. Morange, M. (2008). Regulation of gene expression by non-coding RNAs: The early steps. Journal of Biosciences, 33, 327–331. Thom, R. (1983). Paraboles et catastrophes: Entretiens sur les mathématiques, la science et la philosophie. Flammarion. Trumpler, M. (1997). Converging images: Techniques of intervention and forms of representation of sodium-channel proteins in nerve cell membranes. Journal of the History of Biology, 30, 5.

Chapter 15

Function, Functioning, Multifunctionality: Genetics of Development and Evolution Charles Galperin

Abstract  In this two-part study, I shall first examine the initial foundations of developmental genetics in the works of Edward B.  Lewis. The earliest models based on the relation one gene–one function gave us the idea of functioning, that is, the linking of functions in a chain leading to the final observable phenotype. The second part shows that the conception of models was to be completely modified with the multifunctionality of genes and proteins. I will then indicate three consequences. The first echoes François Jacob’s lesson (Science 196:1161–1166, 1977): “The hierarchy in the complexity of objects is thus accompanied by a series of restrictions and limitations. At each level, new properties may appear which impose new constraints on the system.” In evolutionary perspectives this translates as the “successive recruitment of a gene to produce increasing multifunctionality.” The second consequence is the necessity of new models and thereby for new analytical tools, such as, as Joram Piatigorsky (Gene sharing and evolution: the diversity of protein functions. Harvard University Press, Cambridge, MA, 2007) illustrates, a “network analysis” that “concerns simultaneous changes in the expression of many genes and can predict new functional associations.” The third consequence is that evolutionary diversification is based on a strongly preserved molecular cluster that allows to produce the most varied forms in organisms. The multifunctionality of genes and proteins offers new models that will shed light on this paradox and allow to penetrate more deeply into the relations between, on the one hand, the complexity of genes and their regulation and, on the other, the complexity of development and evolution.

Translated from French by Catherine Porter. Charles Galperin (1929–2019). C. Galperin (*) (deceased) Institut d’histoire et de philosophie des sciences et des techniques (CNRS/Université Paris 1/Ecole Normale Supérieure), Paris, France © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 J. Gayon et al. (eds.), Functions: From Organisms to Artefacts, History, Philosophy and Theory of the Life Sciences 32, https://doi.org/10.1007/978-3-031-31271-7_15

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15.1 Introduction Genetics is a discipline that has successfully used abstractions to attack many of the most important problems of biology, including the study of evolution and how animals and plants develop. (Lewis, 1995, 247)

Edward B. Lewis offered this characterization of his discipline in the lecture he gave when he was awarded the Nobel Prize in 1995. Evoking Thomas Hunt Morgan (1866–1945), who received the same prize in 1933, he recalled some of the astonishing discoveries that had been made since Drosophila was introduced into the field of genetics in 1910: [T]o mention only a few: that the genes (Mendel’s factors) are arranged in a linear order and can be placed on genetic maps, that they mutate in forward and reverse directions, that they can exist in many forms, or alleles, and that their functioning can depend on their position. (Lewis, 1995, 247)

Lewis continued: “The concept of the gene is one of the most powerful abstractions in biology and one of great utility. For many years the gene could be satisfactorily defined as a unit within which genetic recombination, or crossing over, does not occur” (Lewis, 1995, 248). Conceived in this way, the unit tended to correspond to unity of function. Later, it would be necessary to use a “complementation” test promoted by Lewis. Howard D. Lipshitz, author of a comprehensive book on Lewis’s life and work, states for his part that “genetics is a discipline that is based on operational definitions. Thus, it is technically limited by the operations that are performed” (Lipshitz, 2004 (2007), 4). This crucial observation keeps us from abandoning experimental procedures, which always have to accompany the heuristic aspect of concepts and their significations. Hence the two faces of our discipline, which is too familiar to astonish us but which decidedly warrants astonishment: with its high degree of experimental refinement and theoretical construction, it is at once operational and inventive of concepts and abstract models. One final consideration, to circumscribe my project. Unlike philosophical analyses, which are interesting in their own right, studies that bear on function (or functions) in no way respond to the question of what it means to attribute a function or functions to an object, organ, or artificial tool (Bigelow & Pargetter, 1987). The gene and its function are one and the same. A gene exists only through its function or functions. As Joram Piatigorsky says, “without expression, a gene is reduced to a simple sequence of inert nucleotides with an unrecognizable potential of one sort or another, perhaps appropriately considered a ‘non-gene gene’” (Piatigorsky, 2007, 52). The operational nature of the definition of the gene confers on it not only the property of being revisable, but that of being “comprehensive,” that is, open to new experimental conditions and to new theoretical problems. In this two-part study, I shall first examine the initial foundations of genetic analysis in the work of Edward B. Lewis; then I shall make some observations on the multifunctionality of genes and proteins.

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15.2 Edward B. Lewis and the Initial Foundations of Genetic Analysis in Development 15.2.1 The Potential of Genetic Analysis and the Function of a Gene In 1925, as Howard Lipshitz notes, “Sturtevant’s key observation was that the phenotype of flies carrying two B mutations is dependent on their position relative to each other on homologous chromosomes: if two B mutations are present on the same chromosome but the other chromosome carries the wild-type alleles (B B/+) then these flies have somewhat smaller eyes than those that carry one mutant allele on each homolog (B/B).” And Lipshitz goes on to summarize: “The implication of this result was that the function of a gene is dependent on its position relative to its neighbors, hence the term ‘position effect’” (Lipshitz, 2004 (2007), 28). In his own summary of his 1925 study, Sturtevant noted that the changes in the number of facets of the fly’s eyes in all possible combinations of the Bar series— “round, infrabar, bar, double-infrabar, bar-infrabar, double-bar”—showed that “two genes lying in the same chromosome are more effective on development than are the same two genes when they lie in different chromosomes” (Sturtevant, 1925, 146, emphasis added). The other series of studies that strongly influenced Lewis’s interpretations was that of Calvin B. Bridges (1889–1938). In a historical article he devoted to Bridges, Lewis noted that Bridges left it to others to discover recombination within a gene as well as the existence of a group of closely linked and functionally related genes. He nevertheless contributed the cytological foundation that made it possible to call into question the concept of multiple alleles, a question that dominated research on the nature of genes for more than 40 years. “Multiple alleles had been supposed to represent changes in a single original gene, and there were two criteria for their recognition: they occupied the same locus in the chromosome and were not separable by crossing over; and their heterozygote (trans type) was mutant with respect to their common recessive phenotype, since neither carried the wild-type allele of the other” (Sturtevant, 1966, 89–90). The situation would change when it could be shown that a crossing-over could be produced in what had been viewed as individual genes. This was to be the case in the 1940s with the Star and Lozenge mutations (Oliver, 1940; Oliver & Green, 1944). In an article published in 1935, Bridges had “called attention to duplication-­ like structures in the salivary gland chromosomes of wild-type larvae” of Drosophila. In particular, he interpreted numerous double banded structures, or “doublets,” as two duplicated bands fused along their edges. Their structure suggests that they are reverse (ABBA), rather than direct (ABAB) repeats of single bands. Bridges’ cytological evidence for such repeats combined with Sturtevant’s demonstration of position effect suggested that multiple alleles of a given gene might in some cases be resolvable into two or more repeated genes that acted like one because of a position effect. (Lewis, 1995, 249)

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Multiple alleles might then reflect the duplication of loci and imply their disjunction. Between 1939 and 1945, when Lewis sought to recombine the mutants affecting the fly’s eye, the S (Star) mutation and its allele, rebaptized asteroid (Ast), he succeeded in finding recombinants through a real tour de force (Schmitt, 2004, 481). He showed that in the cis configuration (S ast/++) the eyes are normal, whereas in the trans configuration (S+/+ast) the eyes are almost absent (ibid.). With the position effect and the recombination of S and ast, Lewis had what he needed for the cis-trans test. The usual presentation of the test is as follows. When two recessive mutations a and b show similar phenotypes, if the cis configuration a b/++ reveals a wild phenotype, the trans configuration (a+/b+) offers a mutant phenotype. In this case, a and b belong to the same gene. If, on the contrary, the trans configuration presents a wild phenotype, there is said to be complementation; a and b belong to different genes. Lipshitz emphasizes that this presentation neglects the subtleties of the phenotypes between the two extremes. The choice of distinct phenotypes “was central to Lewis’ later analyses of the bithorax series of mutations” (Lipshitz, 2004 (2007), 30). “The cis-trans test provides a purely genetic method of defining a unit of function” (Lewis, 1967, 19; emphasis added). In 1957, Seymour Benzer had defined this unit as a “cistron.” The test of “complementation” offered a method for recognizing whether the a and b mutants fell within the same “cistron” or in different “cistrons.” In this operational context, a gene and a cistron were merged. The position effect existing between the S and ast loci was thus interpreted by Lewis “as a function of their repeat nature and the very short distance between them, both genetically and cytologically speaking” (Lewis, 1945, 164). The conclusion of the 1945 study was striking, especially for those of us familiar with Lewis’s contribution to the genetics of development. The probable frequency of these repeats suggested that “multiple allelic series may be resolved into duplicate loci which act, by reason of a position effect, as a developmental unit” (Lewis, 1945, 165). Functional unity and developmental unity were beginning to merge. In 1952, Lewis noted that, in recent years, “several cases had been found in which non-allelic genes give a positive phenotypic test for allelism by virtue of a position effect” (Lewis, 1952, 953). For these cases, he introduced the term “position pseudoalleles.” The term pseudo-allelic had been introduced by Barbara McClintock (1944). Lewis extended his analysis of position pseudoalleles to mutants involving Drosophila bristles, Stubble (Sb) and stubbloid (sbd). The three mutations discussed in the 1951 paper affected the thoracic segments and the first abdominal segment, bithorax (bx), Bithorax-like (Bxl), and bithoraxoid (bxd); finally, the white (w) and apricot (apr) pseudoalleles changed the eye color of the fly. The discussion in the 1952 article is very interesting for my purposes, because it allows us to move from the notion of function to that of functioning. When Lewis cites the genes apr+ and w+, he sees more than a functional difference: “a position effect is present” (Lewis, 1952, 960). The difference between the two genes is striking: in apr+/+w (the trans configuration), the phenotype is pinkish, and in the cis configuration (apr w/++), the phenotype is red, the wild-type eye color.

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The model that followed was inspired by the biochemical pathways that gave rise to the hypothesis of one gene–one enzyme (Horowitz, 1950). The model “suggests that a mutant gene on one of the loci blocks, or impairs the functioning of, the normal allele of the gene at the other locus, when both are present in the same chromosome, as in the heterozygote apr+/+w” (Lewis, 1952, 959); in contrast, one cannot detect phenotypically any alteration in the functioning of the different wild-type alleles when they are present in the same chromosome. The simplest assumption is that the effect is one-way; that is, that the mutant gene apr impairs the functioning of w+, or that w impairs that of apr+. This leads to a simple model in which one of the genes controls a step A→B, and the other a step B→C, in a biochemical reaction chain of the type: A→B→C. The position effect can then be assumed to result from a failure of substance B to diffuse readily from one chromosome to the other so that the chain of reactions in one of the chromosomes of the heterozygote is carried out more or less independently of the chain in the homologous chromosome. (Lewis, 1952, 959)

15.2.2 What Is a New Genetic Function in Evolution? The problems connected with gene duplication, a phenomenon supported by cytological data, were not recent, nor was the examination of their possible consequences for evolution (Taylor & Raes, 2004). Thus, A. S. Serebrowsky (1938), studying the achaete-scute series (a mutation that affects Drosophila bristles, whose genes are closely linked on the X chromosome), thought that after duplication a gene could influence multiple aspects of a phenotype and as a result multiple functions could be envisaged. Hermann J. Muller, who had recognized the duplication of the scute gene, considered the evolutionary consequences, just as Bridges had: “the redundant loci will come to have divergent mutations, and so gradually will become more differentiated, until they can finally be regarded as quite non-homologous genes” (Muller, 1935, 360). Bridges recalled that in his first report to the meeting of the American Association for the Advancement of Science in 1918, he had emphasized that “the main interest in duplications lay in their offering a method for evolutionary increase in lengths of chromosomes with identical genes which could subsequently mutate separately and diversify their effects” (Bridges, 1935, 64). The idea was thus an old one and, as it were, familiar. “Our underlying thesis will be that in those instances of pseudoallelism in which there is evidence for close functional similarity among the component genes we may come close to seeing the direct results of a process which produces new genes” (Lewis, 1951, 159). Thus in 1951 Lewis began by recognizing that the new genes stemmed from pre-existing ones. This process can take place in two steps: (1) the duplication of a particular gene or its repetition and (2) the formation in one of the two (or more) genes of a mutation towards a new function. This will result in what can be called “a new gene” (Lewis, 1951, 159). The mutation resides in a new “product” different from the one that was created earlier, that is, “the old function” of the original gene. An a priori theoretical argument follows.

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“We believe,” Lewis writes, “that it will generally be necessary to postulate the first step involving gene duplication because of the following a priori considerations regarding the immediate fate of a new gene”: A gene which mutates to a new function should, in general, lose its ability to produce its former immediate product, or suffer an impairment in that ability. Since it is unlikely that this old function will usually be an entirely dispensable one from the standpoint of the evolutionary survival of the organism, it follows that the new gene will tend to be lost before it can be tried out, unless, as a result of establishment of a duplication, the old gene has been retained to carry out the old function. (Lewis, 1951, 159)

Lewis was able to draw on Bridges’s intuitions as well as on direct cytological data in which the duplications are frequently “repetitions of adjacent genes.”

15.2.3 The First Models: Levels of Development in the “Bithorax” Series Even when Lewis refers to examples in which the members of a series of pseudoalleles are so many steps in a series of chemical reactions, he proceeds to consider models, that is, more abstract schemes. Thus he distinguishes between two types of schemes, competitive and sequential. In the first, the immediate products A and B of each of the genes a and b result from the action of the latter on a common substance S (Lewis, 1951, 162): a+



b+

A←S → B The second scheme is the following: a+



b+

S → A→ B

Lewis always preferred the second scheme. It provided him with a relatively simple working hypothesis to apply to the cases he had at hand. It also represented “a progressive process such as is needed for any general theory for the origin of new gene functions” (Lewis, 1951, 162). Finally, this scheme accounted better for the polarity of the sequences. The bithorax mutant, discovered by Bridges in 1915, “is characterized by a more or less complete change of the normal metathorax into a segment like the normal mesothorax” (Bridges & Morgan, 1923, 138). This first homeotic mutant was to inaugurate a 50-year history of studies on the topic (Lewis, 1995). In 1919, Bridges found a similar mutant, which he named bithoraxoid (bxd). This mutant transforms the first segment of the abdomen into a third thoracic segment. Analysis by crossing-­ over revealed a third mutant, Bithorax-like (Bxl), which occupies a distinct locus between bx and bxd. It was later renamed Ultrabithorox (Ubx) (Lindsley & Zimm, 1992).

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“This analysis provided a number of cis and trans genotypes that exhibited position effects” (Lewis, 1995, 252). The analysis was facilitated by distinct phenotypes. Thus, in what Lewis called “the bithorax phenotype” (Lewis, 1951, 165), the anterior portion of the metathorax comes to resemble the anterior portion of the mesothorax; the posterior portion of the metathorax remains unchanged. Another complex is that of the “bithoraxoid phenotype,” which “can be observed in the bxd homozygote or in the Bxl + / + bxd heterozygote. Here, “the posterior portion of the metathorax comes to resemble the posterior portion of the mesothorax, the anterior metathorax remaining unchanged. At the same time, there is always a thoracic-like modification of the first abdominal segment.” Lewis draws attention to “one of the most striking results . . . which is the occasional production of a pair of first abdominal legs” (Lewis, 1951, 165) (Fig. 15.1). Lewis’s 1951 article is quite remarkable, and it is doubly pertinent to my demonstration. First, it consecrates the search for a general functional model; then it inscribes phenotypical transformations in levels of development. Finally, for genetic analysis, which in 1951 relied essentially on crossing-over, it associates the relation one gene–one function with models of functioning. Lewis views the effects of the bx mutant as a change in the metathoracic level of development, which can be represented as (L – mt), towards a mesothoracic level (L – ms). This can take place in the anterior portion of the metathorax and even in the corresponding part of the first abdominal segment (L  – ab). Lewis adopts an embryological and phylogenetic viewpoint in which he follows R. E. Snodgrass’s treatise on the ancestral origin of insects with two pairs of wings, such as the wellknown phenotype of the homozygotes, abx, bx3, and pbx (Snodgrass, 1935; Lewis, 1995).

Fig. 15.1  A drawing of the thorax and first-abdominal (AB1) segment of Drosophila melanogaster. Only the outlines of the prothorax (PR), mesothorax (MS), and metathorax (MT) are shown. The haltere or dorsal appendage of the metathorax is drawn in heavy outline. The shaded areas represent the regions defined in the text as the posterior mesothorax and posterior metathorax. (Greatly modified from Zalokar, 1947) (Lewis, 1951, 166)

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A model that would bring together all the transformations of a pseudoallele series could be constructed, Lewis insists, by assuming that the three genes control successively related reaction steps according to either of the following two schemes: bx +

Bxl +

bxd +

Bxl +

bx +

bxd +

1) S → A → B → C , or 2) S → A → B → C where a reduction in amount of substance, C, is assumed to lead towards a bithoraxoid phenotype, and a reduction in the amount of B or A towards a bithorax phenotype. Stated in another way, the postulated substances will be assumed to control levels of development, already defined above, according to the following scheme: AorB

c

( L − ms ) → ( L − mt ) → ( L − ab )

(Lewis, 1951, 167)

Lipshitz points out that Lewis introduced two key concepts in 1951. “First, he introduces the idea that the bithorax series pseudoalleles controls the [developmental] ‘level’ . . . of subsegments of the fly. Second, he begins to consider the meaning of position effects and developmental control in abstract terms” (Lipshitz, 2004 (2007), 18). We must also note what Lewis called a “genetic model” in opposition to the functional interpretation proposed by Pontecorvo (1952a, b). In the genetic model, the one adopted at that point by Lewis, “each of the component genes of the series acts as a functional unit in the modern sense—namely, as an agent controlling a single, specific gene” (Lewis, 1955, 87). In Pontecorvo’s interpretation, in contrast, “the mutants at the different pseudoallelic loci are alterations at different sites of a single functional unit” (Lewis, 1955, 73). Lewis saw once again in Pontecorvo the hypothesis of multiple alleles that he had at least partially discredited (Fig. 15.2). Most of the genetic complexity of the bithorax complex resides in the multiple regulatory regions and not in the proteins whose spatial and temporal expression they control” (Lipshitz, 2007, 40–41). To demonstrate this, it was necessary to wait for the molecular analysis of the complex (White & Wilcox, 1984; Beachy et  al., 1985). “Lewis’ genetic model was wrong in postulating that each genetic function (bx, bxd, etc.) encodes a distinct substance” (Lipshitz, 2007, 41). Similarly, the pseudoallele series was not constituted by the number of genes coding for proteins that he had discovered. “Instead, the BX-C was shown to consist of three homeodomain-protein coding genes—fewer in number than Lewis had postulated, although clearly related by tandem duplication—along with nearly a dozen cis-regulatory regions, each represented by one of Lewis’ genes (Lipshitz, 2007, 305).

Whatever corrections may still be to come, this genetic analysis of functions was a necessary stage for which Lewis always remained a little nostalgic (Lewis, 1995).

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Fig. 15.2  The postulated gene-controlled reactions at the site of the chromosomes (represented as two parallel lines) in the four possible genotypic arrangements of three mutant and three normal alleles of the bithorax pseudoallelic series. The symbols < and