Abstract

Since ecomorphologists have started to use explicit and taxonomically-broad frameworks in studies on the relationships between form, behavior, ecology and phylogeny they have consistently reported - often against their expectations - 1) that phylogeny is a better predictor of anatomy than ecology is, and 2) many cases of etho-eco-morphological mismatches. It is puzzling that such mismatches occur frequently in an evolutionary process that often leads to macroevolutionary trends and in which organisms are said to be optimally/almost optimally 'designed' for the habitats they inhabit. Organic Nonoptimal Constrained Evolution (ONCE), a new perspective on biological evolution that is proposed here, addresses this apparent paradox, based on an extensive compilation of empirical data and broader evolutionary ideas, from Aristotle to current Evo-Devo. According to ONCE, by taking behavioral choices, and subsequently due to their behavioral persistence related to behavioral/ecological inheritance, organisms as diverse as bacteria, plants and animals help to construct their own niches and are thus the central, active players in their evolutionary history. The highly constrained character of organic evolution, including developmental constraints as well as the crucial role played by behavioral persistence, can dramatically limit the occurrence of new behavioral shifts and thus the responses to external (e.g., environmental) changes, often resulting in etho-eco-morphological mismatches and eventually in evolutionary dead-ends that may lead to extinction.

Highlights

  • In the last few years, numerous papers—most written by ecomorphologists to identify correlations between ecology and anatomy—consistently reveal eco-morphological mismatches in which form is, for instance, much more strongly related to phylogeny than to the current ecological habitats

  • The common occurrence of such mismatches was not at all expected in the light of the works of many Neo-Darwinists— those subscribing to an adaptationist framework—and, for that matter, even of Darwin himself, who famously stressed how the morphology of the Galapagos finches seems to be beautifully optimized for the specific habitats in which they live

  • Olson recognized that within this context, adaptationism was mainly a synonym of externalism, with natural selection, and in particular the external environment, playing a central role in morphological macroevolution, Neo-Darwinists stressed the importance of other factors in evolution, e.g., genetic drift and gene flow

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Summary

Rui Diogo *

Reviewed by: Pedro Martinez, University of Barcelona, Spain Emanuele Serrelli, Freelance, Italy. According to ONCE, by taking behavioral choices, and subsequently due to their behavioral persistence related to behavioral/ecological inheritance, organisms as diverse as bacteria, plants and animals help to construct their own niches and are the central, active players in their evolutionary history. Darwinian (external) natural selection plays mainly a secondary - but still crucial - role in biological evolution, for instance helping to direct major evolutionary trends by selecting those random mutations that are advantageous within the context of the new, constructed niches. The highly constrained character of organic evolution, including developmental constraints as well as the crucial role played by behavioral persistence, can dramatically limit the occurrence of new behavioral shifts and the responses to external (e.g., environmental) changes, often resulting in etho-eco-morphological mismatches and eventually in evolutionary dead-ends that may lead to extinction

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