Evolution and the architecture of life

Resum

Darwin aimed, with his theory of descent with modification through natural selection, to account for three biological explananda: the variety of living forms; the complexity of organisms, apparently increasing through the history of life; and adaptedness, or the fit of organisms to their environment. The success of this original research project 150 years after the publication of the Origin is uneven. The Modern Synthesis, unifying Darwinism and genetics, formalizes, through population genetics, the first claim: traits in a population spread, get fixed, are lost and slowly change into new ones according to their fitness and to the strength of selection. On the other hand, population genetics does not make any claim about complexity, let alone about its putative increase. Darwin’s theory is also the only known explanans for adaptedness. The evolutionary mindset known as adaptationism studies species’ traits and provides explanations about their adaptive origin. A mayor limitation of adaptationist explanations is their narrative nature: they cannot be tested. Several models have been proposed to overcome this limitation, from optimization programs to the ambitious Formal Darwinism Project by Alan Grafen. These proposals, however, focus on traits separately, and ignore the complexities of the architecture of organisms. The issue of complexity thus remains either unaddressed (by population genetics) or taken for granted (by adaptationism): the modern synthesis simply claims that complex traits appears from mutations and recombination shaped slowly and incrementally by selection. Complexity comes from a Deus-ex-Machina hidden in the environment. This approach, more and more challenged in the last decades, ignores many phenomena that do seem to affect phenotypic evolution, and that are accounted for by alternative, non-purely selective accounts. Many of them have been collected under the name of Extended Evolutionary Synthesis (Laland et al. 2015). The range of phenomena targeted by these accounts spans from chemical-physical laws, to genetic (e.g. Cherniak & Rodriguez-Esteban 2013, Kimura 1983, Wagner 2015), developmental (e.g. Maynard Smith et al. 1985), systemic (e.g. Kauffman 2000) and neo-Lamarckian mechanisms (e.g. Koonin & Wolf 2009). None of these accounts denies the importance and even preponderance of selection in the history of life, and they rather aim at integrating non-selective phenomena into Neo-Darwinism (a view known as ‘pluralism’). Although criticized by main-stream biology, we believe that pluralistic views and classical Neo-Darwinism can be integrated into a unified vision of evolution that formally accounts for organismal complexity. In the first place, we propose a definition of organismal architecture as form and function, going beyond the adaptationist consideration of organisms as just the sum of their optimised traits. In the second place, we suggest that fitness, being an intrinsically selective measure, should not be used to judge non-selective phenomena. We propose to use robustness instead, and we show how some non-selective forces impact the robustness of phenotypes. Finally, we present a model of evolutionary changes that maps populations as areas in a bi-dimensional space of fitness and robustness, where the effect of selection and of non-selective forces on shape and position of these areas can be tracked. Complexity, interpreted as organismal architecture, thus appears to be the result of several synchronic processes, among which selection plays an important but not always a preponderant role. References Cherniak, C.; Rodriguez-Esteban, R. (2013). Body maps on the human genome. Mol. Cytogenet. 6 (1): 61 Kauffman, S., (2000). Investigations. Oxford University Press. Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press Koonin, E. V., Wolf, Y. I (2009). Is evolution Darwinian or/and Lamarckian? Biology Direct, 4:42 Laland K.N., Uller T., Feldman M.W., Sterelny K., Müller G.B., Moczek A., Jablonka E., Odling-Smee J. (2015). The extended evolutionary synthesis: its structure, assumptions and predictions. Proc. R. Soc. B 282: 20151019 Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., Wolpert, L. (1985). Developmental Constraints and Evolution: A Perspective from the Mountain Lake Conference on Development and Evolution. The Quarterly Review of Biology, (60) 3: 265-287 Wagner, A., (2011), The Origins of Evolutionary Innovations, Oxford University Press