History of a concept in complexity studies

1. History of a concept in complexity studies The origins of natural design The origins of particularly complex and perfect organs (analogy with artifacts) “There cannot be design without a designer; contrivance, without a contriver; order, without choice” Young Darwin impressed by Paley’s descriptions of “adaptations” Natural Theology, 1802

2. Charles Darwin’s Transmutation Notebooks 1836 - 1839

3. SOME RADICAL DOUBTS… (1837-1838) Imperfection: “When one sees nipple on man’s breast, one does not say some use. So with useless wings under elytra of beetles, born from beetles with wings and modified. If simple creation, surely would have been born without them” (Not. B, Sept. 1837) Evolution is not superiority: “It is absurd to talk of one animal being higher than another. We consider those, where the cerebral structure, or intellectual faculties, most developed, as highest. A bee doubtless would when the instincts were” (Not. B, Sept. 1837) Adaptive contingency of characters: “Chance and unfavourable conditions to parent may become favourable to offspring” (Notebook E, 19 Oct. 1838) “Every species is due to adaptation AND hereditary structure” (Not. B, 1837)

4. The tree (or coral) of life (branching evolution) as description Natural selection (differential survival and reproduction) as explanation Notebook B, July 1837

5. ADAPTATION WITHOUT FINALISM (Notebook E, Dec. 1, 1838) “No adaptation to an end, but adaptation to varying circumstances… owing to external contingencies and relations with other species, not owing to mandate of God” (commenting William Whewell’s “History of the Inductive Sciences” and his idea of a providential adaptation) “Structure is due to external agency and circumstances, without final cause, either in present, or past generation” (Notebook E, Dec. 14 1838)

6. A pessimistic passage in Notebook C, July 1838… “We never may be able to trace the steps by which the organization of the eye, passed from simpler stage to more perfect, preserving its relations. The wonderful power of adaptation given to organization. This really perhaps greatest difficulty to whole theory” (CD) DIFFICULTY: is there any contradiction between continuity of change, by natural selection, and the need of a persistent (even “infinitesimal”) functional advantage?

7. CD is quoting Henri Milne-Edwards (“Histoire naturelle de crustacés”, 1834, paper 1838): “Il est aussi digne de remarque que l’instrument affecté à cet usage insolite n’est pas un organe nouveau introduit ad hoc dans la structure des Crustacés à brachies infèrieures, mais un appendice qui existe dans tous les animaux de cette catégorie, et qui est seulement en partie détourné de sa destination ordinaire et lègérement modifié dans sa conformation pour devenir apte à remplir ses fonctions nouvelles” (in, Notebook E, Oct. 19, 1838)

8. The “five percent of a wing” Problem How can evolution ever make a wing in Darwin’s gradualist and functionalist way if the five percent of a wing cannot possibly provide any benefit for flight? George Mivart’s objection to Darwin (1871): the incompetency of natural selection to account for the incipient stages of useful and complex structures

9. Risky predictions… “To suppose that the eye with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest degree” (CD, Origin, Sixth Edition, 1872, p.)

10. Mivart’s objection: answer 1 GRADUAL IMPLEMENTATION “When it was first said that the sun stood still and the world turned round, the common sense of mankind declared the doctrine false; but the old saying of Vox populi, vox Dei, as every philosopher knows, cannot be trusted in science. Reason tells me, that if numerous gradations from a simple and imperfect eye to one complex and perfect can be shown to exist, each grade being useful to its possessor, as is certainly the case; if further, the eye ever varies and the variations be inherited, as is likewise certainly the case; and if such variations should be useful to any animal under changing conditions of life, then the difficulty of believing that a perfect and complex eye could be formed by natural selection, though insuperable by our imagination, should not be considered as subversive of the theory” (p. 144)

11. Mivart’s objection: answer 2 FUNCTIONAL SHIFT “Natural selection might specialise, if any advantage were thus gained, the whole or part of an organ, which had previously performed two functions, for one function alone, and thus by insensible steps greatly change its nature. … Again, two distinct organs, or the same organ under two very different forms, may simultaneously perform in the same individual the same function, and this is an extremely important means of transition. In all such cases one of the two organs might readily be modified and perfected so as to perform all the work, being aided during the progress of modification by the other organ; and then this other organ might be modified for some other and quite distinct purpose, or be wholly obliterated” (p. 147)

12. Mivart’s objection: answer 1+2 PRE-ADAPTATION “The illustration of the swimbladder in fishes is a good one, because it shows us clearly the highly important fact that an organ originally constructed for one purpose, namely, flotation, may be converted into one for a widely different purpose, namely, respiration. The swimbladder has, also, been worked in as an accessory to the auditory organs of certain fishes. All physiologists admit that the swim bladder is homologous, or "ideally similar" in position and structure with the lungs of the higher vertebrate animals: hence there is no reason to doubt that the swim bladder has actually been converted into lungs, or an organ used exclusively for respiration” (p. 148) Flexibility Redundancy Structure/Function

13. PRE-ADAPTATION (Ernst Mayr): continuity in differential reproductive success, not in the same function • CURRENT USE not always => HISTORICAL ORIGIN • SUB-OPTIMALITY of adaptation (CONSTRAINTS) “Natural selection tends only to make each organic being as perfect as, or slightly more perfect than, the other inhabitants of the same country with which it comes into competition. And we see that this is the standard of perfection attained under nature. Natural selection will not produce absolute perfection, nor do we always meet, as far as we can judge, with this high standard under nature” (p. 163) “I am convinced that Natural Selection has been the most important, but not the exclusive, means of modification” (CD, Origin, p. 4)

14. XX Century vulgata: ADAPTATIONISM (strong) • A) power of natural selection as an optimizing agent, at the genetic level • - B) breaking an organism into unitary "traits" and proposing an adaptive story for each one considered separately • - C) Trade-offs among competing selective demands exert the only brake upon perfection (non-optimality is thereby rendered as a result of adaptation as well)

15. A “PANGLOSSIAN” PARADIGM? (Gould-Lewontin, 1979) Criticisms: • 1) SELECTION ACTING ON CONSTRAINTS • 2) DISTINCTION BETWEEN CURRENT UTILITY AND REASONS FOR ORIGIN • 3) INFALSIFICABILITY OF ADAPTIVE STORIES • 4) failure to consider adequately such competing themes as random fixation of alleles, production of non-adaptive structures by developmental correlation with selected features (allometry, pleiotropy, material compensation, mechanically forced correlation) and current utility as an epiphenomenon of nonadaptive structures. - Coming back to Darwin…

16. Daniel Dennett’s “Reverse Engineering” (Darwin’s dangerous idea) EXPLANATORY ADAPTATIONISM • Not only adaptations in nature, but adaptations explain evolution • Adaptive problems in the past adaptations evolved to solve them • Evolutionary problem-solving based on the universal “darwinian algorithm” Hypothesis of optimality

17. “QUIRKY FUNCTIONAL SHIFT” Exaptation: a missing term in the science of form (S.J. Gould, E. Vrba, 1982) • APTATION: any features now contributing to fitness • - AD-APTATION: a feature directly crafted for a current utility by natural selection • - EX-APTATION: a feature coopted for a current utility following an origin for a different function, or for not function at all. “Exaptation”: character useful (aptus) as a consequence of (ex) its form

18. 1941 - 2002 “To paraphrase Mr. Huxley in a famous context, I am prepared to go to the stake for exaptation; for this new term stands in important contrast with adaptation, defining a distinction at the heart of evolutionary theory, and also plugging an embarassing hole in our previous lexicon for basic processes in the history of life” (S.J. Gould, “The Structure of Evolutionary Theory”, 2002, p. 1234)

19. Process Character Usage Darwinian Function Darwinian Effect THE END OF ADAPTATIONISM - A NEW TAXONOMY OF FITNESS (Gould-Vrba 1982; Gould, 2002) Natural Selection shapes the character for a current use Adaptation A character, previously shaped by natural selection for a particular function (an adaptation), is coopted for a new use Exaptation 1 (by cooptation) preadaptation A character whose origin cannot be ascribed to the direct action of Natural Selection (a non-aptation), is coopted for a current use Structural Effect Exaptation 2 (by nonaptation)

20. Ichthyosaurus

21. TAXONOMY OF THE EXAPTIVE POOL as structural basis of “evolvability” in life’s history (S.J. Gould, 2002) A – Inherent potentials (unexploited) B – Available things (“spandrels”) B1) As architectural consequences (structural and non-adaptive origin) B2) As historical unemployments (historical, non-adaptive origin) (ex. vestigia) B3) As invisible introductions (historical, non-adaptive origin) (ex. neutral drifts, founder effects)

22. The Spandrels of San Marco A character whose origin cannot be ascribed to the direct action of Natural Selection (a non-aptation), could be coopted for a current use

23. Imperfections in human physiology • Due to: • Previous adaptations • Selective trade-offs • Exaptations • Spandrels and vestigia

24. The Five Percent of a Wing Problem - 2011 Archaeopteryxlithographica Solnhofen, 1861 (Richard Owen) ADAPTIVE STORIES? Protowings? Transitional stages?

25. Dinosaurs with plumage? 1996-2006: AMNH of NY A) Arboreal Theory(for gliding in tree-dwelling ancestors) B) Cursorial Theory(from running terrestrial dinosaurs) C) Wing-assisted incline running in avian ancestors (Dial, Randall, Dial, BioScience, 56, n. 5, May 2006) Anyway: Exaptation (type 1) of avian flight Velociraptor mongoliensis with Mononykus olecranus

26. “A firm step from water to land” (Nature, 440, April 2006) Tiktaalik roseae – Ellesmere Island, Nunavut, Arctic Canada (Shubin, Daeschler, Jenkins, Nature, 440, 2006) Tetrapods 359 M Single intermediate fossil? Missing link? 365 M What is the right pattern for vertebrate transition from water to land? Fishes 385 M Classic picture Devonian–Carboniferous: LINEAR ANAGENESIS?

27. Cladogram of the pectoral fins of taxa on the tetrapod stem Life in shallow water • Multiple adaptive solutions (different combinations of “retained” and “modern” characters) • Exaptation fins-limbs • Not always the present is the key for the past (Henry Gee)

28. EVO-DEVO: HOX-MUTATIONS IN PHYLOGENY - Same Hox genes for the entire animal kingdom - Nat. Selection and Dev. Constraints - Traits without adaptation (structural effects) Evolution and bricolage: functional shifts and cooptations

29. Extensive application of exaptation today • Palaeontology (primary/secondary adaptations) • Evo-Devo (selection on developmental constraints) • Genetics (molecular cooptations; symbioses) • Multilevel selection (adaptations at one level could be exaptations at another) • Niche construction (the active role of organisms shaping the frame of selective pressures; triggers for new niches) • Evolution of unselfish behaviours (selective triggers and then exaptations; or exaptations and then selective reinforcement) • Human evolution (evolution of mind; cultural evolution) • Evolutionary psychology (where the strong adaptationist approach is more and more failing) • Theoretical biology and complexity (“adjacent possible”)

30. What exaptation does not mean: • A CONFUTATION OF THE AGENCY OF NATURAL SELECTION IN EVOLUTION, but: a) trade-offs between functions and structures; b) non-adaptive structures. • 2) A BREAK IN THE CONTINUITY OF EVOLUTIONARY PROCESSES (it could allow major and rapid novelties, but without statements about “saltations” in evolution) • 3) THE “AD HOC” HYPOTHESIS WHEN ALL THE OTHER ONES FAILED (exaptation needs observative and experimental supporting data) • 4) A UNIVERSAL EVOLUTIONARY PROCESS (but: a prominent “pattern” in a pluralistic framework of evolutionary processes)

31. AN EXTENDED NEO-DARWINIAN SYNTHESIS Understanding the phenotype (phenotypic plasticity, macroevolution, origins of form) Advances of Neo-Darwinism (population genetics, drift, speciation) New views on inheritance (epigenetic inherit., niche inherit.) Evo-Devo (innovation, modularity, evolvability) Selection and adaptation reformed (neutralism, multilevel selection, niche construction, exaptation) The evolution of the structure of Neo-Darwinian Research Program