Adaptation and organisms in retrospect : complexifying the picture of the Modenr Synthesis

1. Adaptation and organisms in retrospect: complexifying the picture of the ModenrSynthesis Philippe Huneman IHPST (CNRS/Université Paris I Sorbonne)

2. Nowadays: two critiques of the Modern Synthesisthatconcern adaptation: Critique of adaptationism. not all traits are resulting from natural selection; natural selection is not the exclusive cause of evolutionary change, etc. (Gould-Lewontin, 1979; Godfrey Smith 1996; Lewens 2008) - The active role of organisms: adaptation starts from the activity of organisms: • Phenotypic plasticity (West Eberhardt, 2005): « Genes are followers, not leaders »; • Niche construction (Odling Smee et al. 2003)

3. -> The space of controversies is structured by thesetwo issues – adaptationism, genes vs. organisms.

4. The space of controversies Organisms Not only natural selection (no adptationnism) Gould Genes Mostly natural selection ( adaptationnism) Dawkins • Dawkins • Lyn Mayr • Gould Genes Not only natural selection (no adaptationnism) Lynch Michod Organisms Mostly natural selection ( adaptationnism) Mayr

5. The space of controversies Organisms Not only natural selection (no adaptationnism) Gould Genes Mostly natural selection ( adaptationnism) Dawkins Optimisation line • Dawkins • Lyn Mayr • Gould Genes Not only natural selection (no adaptationnism) Lynch Michod Organisms Mostly natural selection ( adaptationnism) Mayr Organismic line

6. Adaptation and the meaning and role of organisms: a genealogicalenquiry • Question : whatdoesthisowe to the « Modern Synthesis » (as a not necessarilysynthetic set of books, papers, etc.?) • Outline • Evolutionary organicism, then and now • Adaptation and organisms • The MS’stake on organisms • Mayr’s organicism • Population genetics and the Modern Synthese(s)

7. I. Evolutionary organicism, then and now ?

8. I.A Adaptation and organisms

9. A 2 decades-long critique of suborganismic/adaptationist biology • Gould (1983): the « hardening of the Synthesis » • Walsh (2010) The triumph of « suborganismal biology » (= MS) and the recent prospects for « organismal » biology (phenotypic plasticity, adaptivity of organisms)

10. What is crucial : the status of adaptation. (Depew 2010, on the duality (UK /US) of the Synthesis; the « hardening » is the triumph of the former) Receivedview : an adaptation = a (trait) result(ing) from natural selection Challenges : adaptation as changing the environment (Odling-Smee et al. 2003); adaptation as adaptive plasticity (Walsh 2003, 2010, West-Eberhardt...) Oldproblem : how to get the adaptedness of organisms ?

11. Adaptation: Disentangling the conceptual issues • Adaptation as a process, adaptation as a product • Currentist vs historical concepts of adaptations • Traits as adaptations, adaptedness of organisms • Nature of the state; waystowardsit • Adaptations; complex adaptations (Williams 1992) • Explanatory importance (the adaptationist challenge) Issues not related to adaptationnism; yetincluded in all questions about adaptationism.

12. Adaptation as a process, adaptation as a product Physiology products(decreased pulse in altitude)/ processleading to it - > Phenotypic plasticity Genetic product(webbedfeet of ducks) / processleading to it (duckphylogeny)

13. Currentist vs historical concepts of adaptations « X is an adaptation » is a historicalstatement(Brandon 1996, Sober 1984, etc.) (In the case of maintenance questions) adaptation is a currentist concept, i.e. the highest fitness variants in a population (as opposed to origin questions, e.g. paleontology) (Reeve & Sherman 1993)

14. Traits as adaptations/ adaptedorganisms Traits are adaptations. « The expression of conditions of existence, so often insisted on by the illustrious Cuvier, is fully embraced by the principle of natural selection. For natural selection acts by either now adapting the varying parts of each being to its organic and inorganic conditions of life; or by having adapted them during past periods of time: the adaptations being aided in many cases by the increased use or disuse of parts, being affected by the direct action of external conditions of life, and subjected in all cases to the several laws of growth and variation.” Darwin – OS – 6; summary MS – traits are tied to genes (that’swhy natural selection acts on them) But: organisms are « adapted. » Formerly (Cuvier, etc. – see Ospovat 1980)– adaptation was a quantitative property of organisms… Double issue : « Adaptedness » of organisms is involved in fitness, which is explanatoy of adaptation; An organims is a « bundle of adaptations » (Huxley, 1942) ? Or not ? (adaptations can be conflicting; « trade-off » may not be the solution)

15. Whichpathway to adaptation? « Adaptation » connotes a kind of fit; whatdoesproducesuch fit ? (one or severalpathways?) -> externalism vs. (constructive) internalism • The Niche Construction challenge • Is natural selection the cause of adaptation or of itsspreading (Walsh 2003; Sober 1999, Neander 1995, etc.)

16. Whichpathway to adaptation? (Cc)NC vs. Natural selection (earthworms) • Niche construction • Natural selection

17. Adaptation and complexity Complex adaptation is a problem (eye, bats radar, vertebrate immune system, etc.); but many adaptations are notcomplex (e.g. fur colour etc.). Link: The criterion of adaptation = complexity. (Paley, quoted in Williams 1992; « exquisitecontrivances »: Gardner 2009) Evolutionary biology may be determinedeither by an interest in complex adaptations (Dawkins’ problem) or by a question about in the pervasiveness of adaptations (but what are the criteria?)

18. Explanatory relevance -> what is the main explanatoryproject of evolutionary biology ? Adaptations ? Complex adaptations ? Not justadaptation (but diversity; or unity in diversity, etc.)? Lewontin 1971: « Evolutionary theory explains adaptation and diversity in the living world. ». • Are all explananda compatibles? • Is the explanation of diversity (resp. Unity in diversity), deducible from the explanation of adaptation ? (Darwin’sfinches)

19. On my theory, unity of type is explained by unity of descent. The expression of conditions of existence, so often insisted on by the illustrious Cuvier, is fully embraced by the principle of natural selection. For natural selection acts by either now adapting the varying parts of each being to its organic and inorganic conditions of life; or by having adapted them during past periods of time: the adaptations being aided in many cases by the increased use or disuse of parts, being affected by the direct action of external conditions of life, and subjected in all cases to the several laws of growth and variation. Hence, in fact, the law of the Conditions of Existence is the higher law; as it includes, through the inheritance of former variations and adaptations, that of Unity of Type.

20. Alternative view Natural selection Plasticity/NC Developmental constraints Adaptation Adaptive radiation Diversity Unity

21. Adaptation as a multilayered concept

22. summarizing… The MS (or supposedso…) view: an adaptation is a result of natural selection; adaptedness of organismsresults from the set of adaptations (« bundles of adaptations »); adaptation is historical (monism) or we can admit currentist concept (pluralism); adaptation explainedleads to explainingother explananda; adaptations may be complex or not (neutral) – but complex adaptations are (one of ) the BigProblem(s) Challenge : the « fit » within adaptation results from somethingelsethan selection; itinvolvesorganisms; the traits as adaptations can’tgive us adaptedness of organisms; the explananda of EB are not all yielded by the explanation of adpatation, whichmaynot be the main important thing; complex adaptations are not THE problem of evo bio.

23. -> Challenging the conception of adaptation in MS leads to thinkingdifferently about organisms and theirrole in producing adaptation, as well as diversity and evolution. But : different from what?.... Claim – thiswas an issue within the MS.

24. I.B ORGanicism, another MS take on adaptation

25. But: organismic critique is not new Indeeditwas a crucial moment in the consolidation/ aftermath of the MS: Ernst Mayr, “Where Are We?” Cold Spring Harbor Symposium on Quantitative Biology 24 (1959): 1–14. Ernst Mayr, “Cause and Effect in Biology” Science 134 (1961): 1501–06; Theodosius Dobzhansky, “Biology, Molecular and Organismic,” American Zoologist 4 (1964): 443–52. Sewall Wright, “Gene and Organism,” The American Naturalist 87, no. 832 (1953): 5–18. George Gaylord Simpson, “The Status of the Study of Organisms,” American Scientist 50, (1962): 36–45. case of Waddington left aside here Is this a last stage of the MS ? A first round of interpretation ?

26. Organicism, 60s. • The level of organicism is emphasized as proper to biology • Especiallyagainst the rise of Molecular Biology

27. Arguments by Wright (levels) and Mayr (2 causes) werecruciallyinfluential …

28. Essential idea, 1. • Biology is hierarchised. Reduction, in Nagel’ssense (Dobzhansky, Mayr cite Nagel 1961) does not work. Each level is not deducible from the precedings

29. Wright, 1953

30. Mayr 1955 • Critique of « beanbaggenetics » One- or two-loci model are unable to capture the complexity of causal interactions in evolutionary dynamics

31. Evolutionary thinking is holistic and interactionist - Dobzhansky • “Talking about traits as though they were independent entities is responsible for much confusion in biological and especially in evolutionary thought” (1970, 65). • “A change in the genotype alters the reaction norm, and some of the alterations may enable the new genotype to produce a harmonious response where the ancestral has been a failure … Selection deals not with the genotype as such, but with its dynamic properties, its reaction norm, which is the sole criterion of fitness in the struggle for existence.” (1937, 170).

32. Essential idea, 2. (Mayr). • What’sproper to biology is evolutionary style explanations. (« ultimate ») • « Nothing in biology makessense etc. » (Dobzhansky 1964.) Explanatory thesis

33. The strategy. (1) + (2) = the proper biological (= evolutionary) level is organism (and beyond). MAYR Notice : curiously, evolutionary explanation and organicism are tied (whereas, one couldthinkthat evolutionary explanations are level-independent) • A first reason : genes are too close to chemistry (via molecular biology) • A second reason : critique of geneticatomism(as misleading abstraction); interactionism: concretecomplexityoccursat the organismic level In biology, a second kind of explanation may be added to the first, or reductionist explanation, made in terms of physical, chemical and mechanical principles. This second form of explanation, which can be called compositionist in contrast to reductionist, is in terms of adaptive usefulness of structures and processes to the whole organism and to the species of which it is a part, and still further, in terms of ecological function in which the species occurs. (Simpson 1964)

34. II.2. Mayr’s organicism

35. Mayr ? “It is hard to exaggerate the significance of Mayr's defense of the proximate/ultimate distinction in establishing philosophy of biology as a legitimate special area of inquiry” (Beatty 1994) Most quoted author in Hull’s classical « What philosophy of biology is not ? » (19 occurrences)

36. Critique of geneticatomism Twopolemic stances: 1942-53, downplay the role of geneticists in the founding of modern evolutionary biology 1955-later (after the discovery of DNA): vindicate the specificity of evolutionary biology againstmolecular biology

37. Historical sketch of MS by Mayr « Several historians have mistakenly thought that this synthesis within genetics had solved all the problems of Darwinism. That assumption, however, failed to take account of an important gap. One of the two major branches of evolutionary biology, the study of the origin of biodiversity, had been left out of the major treatises of Fisher, Haldane, and Wright. Actually, unknown to these geneticists, the problems of the origin of biodiversity had already been solved in the 1920s by several European naturalists, most important among them, Moritz Wagner, Karl Jordan, Poulton, Chetverikov and Stresemann. Thus, evolutionary biology around 1930 found itself in a curious position. It faced two major seemingly unsolved problems: the adaptive changes of populations and the origin of biodiversity. Two large and very active groups of evolutionists worked on these problems. One of these groups consisted of the population geneticists. As summarized in the works of Fisher, Haldane, and Wright, this group had solved the problem of gradual evolution of populations through natural selection. But they had not made any contribution to the problem of how species arise (speciation) - that is, to the problem of the origin of biodiversity. The other group of evolutionists consisted of the naturalists taxonomists.”

38. The two explananda of evolution : adaptation, diversity (notice how itdiffers from Dobzhansky, quotedabove) About Systematics and the origins of species (1942): “The real objective of my volume was to explain a whole set of phenomena,—such as species and speciation, as the effects of selection on populations, as the role of geography at the level of species and populations, and as the role of species in macroevolution,— that were omitted in the accounts of the geneticists or that were based on the findings of the systematists, such as in the volumes of Dobzhansky, Timoféeff-Ressovsky and Huxley”

39. “It is now understood that evolution consists in two major processes, the changes (usually adaptational) of populations in time, and the multiplication of species in space that is the origin of new organic diversity.The latter process, more often called speciation, has been clouded with confusion ever since 1859. Darwin in his early unpublished writings (1837 to 1844) had come to the conclusion that geographic isolation was a necessary prerequisite for speciation and that therefore allopatricspeciation was the prevailing, if not the only, form of speciation (Kottler1978; Sulloway1979). However, by 1859 when he published the Origin, Darwin had concluded that sympatric speciation, the splitting of a single population without geographic isolation, was at least equally common.” Mayr, JHB paper on Weissmann, 1985

40. What’s the trouble with population genetics ?? Speciationappearswhengeneticenvironment of the genes change (e.g. atboundaries of territories). (« Change of environment and speciation » (1954)) • This assumes that the effect of genes is (organsims- and gene-contextual) dependent. • Usual PG models (atomistic etc.) are not realistic • Whatcausallyaccounts for speciation are changes in reproductive barrierswhichimplywholegenotypes and organismic behaviour

41. Consequences « Population » is not exemplarilyrepresented by population genetics! A population is indeed biological : itreproducesitselfthrough the reproduction of someorganisms. « In the study of biological species one deals with biological populations. (…) Only a small fraction of any biological population reproduces, because not everyindividual in a population survives up to the reproductive age and reproducessuccessfully. This is true on the average of onlytwo of the total number of a prenatal pair in a sexuallyreproductingspecies. » (« What is a species and whatit is not », Phil Sci 1996) From the viewpoint of diversity questions, the causal consistency of population is due to organisms (and not genes)

42. Consequences, 2 -> Population genetics does not exemplify the evolutionary style of explanation: “Evolutionary biology dealing with highly complex systems [not genes, PH]operated by historically evolved genetic programs, must pursue a very different strategy of research in order to provide explanations. Its most productive method is the comparative method, for which the taxonomists have laid the foundation. Indeed I can hardly think of a evolutionary problem that has not developed out of some findings of taxonomy.” (“the role of systematics in biology”)

43. Hence Mayr rejects the textbookdefinition of evolution as « changes in allelefrequencies in a population ». • “Evolution is not a change in gene frequencies, as is claimed so often, but the maintenance (or improvement) of adaptedness and the origin of diversity. Changes in gene frequency are a result of such evolution, not its cause.” (Mayr 1997, 2093). • Mayr wouldsubscribe to Walsh’sideathatitprovidsesonly a shadow (« pseudo-process » sensu Salmon) of the evolutionary process. • This is not at all the MS targeted by Walsh, Muller, Gerhardts and Kirschner, West-Eberhardt etc. • Defining a version of MS -> role of population genetics (viz. the result/causediff.).

44. II. (the speculative part…) ii. Population genetics and the versions of Modern Synthesis

45. Claim 1, weak. Population genetics is central in evolutionary biology becauseitmathematicallyexplainswhy evolution by NS is possible (eg Gayon 1998) (assumingparticularinheritance) • Claim 2, strong. Population geneticsprovides the fine-grainedknowledge of the processof evolution as a population level phenomenon (Hamilton, Maynard-Smith, Williams, Price, Grafen, Michael Lynch, etc.)

46. The call for an extended MS oftenrejects 2. Especially : « PG is not a causalknowledge of evolution. » The issue : is PG a statistical or a causal understanding of evolutionary dynamics ??

47. A parallel in quantitative genetics • Lande-Arnold 1983, measurement of selection on correlatedcharacters (i=1….n) • G = variance-covariance matrix of breeding values • P-1 s = set of partial regression of relative fitnesses on characters (Corresponds to univariatebreeder’sequation R=hs)

48. Major idea:Grepresents how the genic architecureconstrains the response to selection • Yet major problems to get causal explanations out of it (Pigliucci 2005; Barton and Turelli 1989).

49. Back: Twoviews of PGstatistical / causal • Abstract away from causes in general • The content is pure maths (Price equ.) and statistics • Hence causes have to be plugged in from the outside • They are the causes of fitness (pertaining to ecology, physiology, etc.) • It is not the core of MS but has instrumental value • What causes evolution is differentialreplication, which is the explanandum of PG • Hence PG captures the process of Natural Selection • Thereforeit is the core of evolutionary theory • And e.g. grounds itsmethodology (FTNS -> optimisation methods).

50. Fisher’stake on PG. The statement of the principle of Natural Selection in the form of a theorem determining the rate of progress of a species in fitness to survive (this term being used for a well-defined statistical attribute of the population), together with the relation between this rate of progress and its standard error, puts us in a position to judge of the validity of the objection which has been made, that the principle of Natural Selection depends on a succession of favourable chances. The objection is more in the nature of an innuendo than of a criticism, for it depends for its force upon the ambiguity of the word chance, in its popular uses. The income derived from a Casino by its proprietor may, in one sense, be said to depend upon a succession of favourable chances, although the phrase contains a suggestion of improbability more appropriate to the hopes of the patrons of his establishment. It is easy without any very profound logical analysis to perceive the difference between a succession of favourable deviations from the laws of chance, and on the other hand, the continuous and cumulative action of these laws. It is on the latter that the principle of Natural Selection relies. (Fisher GTNS, 1930, 37.)