Adaptive evolution of animal proteins over development: support for the Darwin selection opportunity hypothesis of Evo-Devo

Abstract

Animal morphological diversity is shaped both by adaptation and by developmental constraints. Here we have tested Darwin's "selection opportunity" hypothesis, according to which high evolutionary divergence in late development is due to strong positive selection. We contrasted it to a "developmental constraint" hypothesis, according to which late development is under relaxed negative selection. Indeed, the highest divergence, both at the morphological and molecular levels, is observed late there is a consistent signal that positive selection mainly affects genes and pathways expressed in late embryonic development and in adult. Our results imply that the evolution of embryogenesis is mostly conservative, with most adaptive evolution affecting post-embryonic gene expression, and thus post-embryonic phenotypes. This is consistent with the diversity of environmental challenges to which juveniles and adults are exposed.

Molecular evolution across developmental time reveals rapid divergence in early embryogenesis

“…To date, analyses of molecular evolution have primarily revealed gametic and post-embryonic stages to have fastest rates of evolution in animals and plants (Cutter and Ward 2005;Ellegren and Parsch 2007;Arunkumar et al 2013;Piasecka et al 2013;Liu and Robinson-Rechavi 2018a). Our findings corroborate this result, showing that co-expression modules with peaks in adulthood that are enriched for sperm-related gene function evolve especially rapidly.…”

“…And yet, micro-evolutionary studies demonstrate that a majority of amino acid substitutions in protein coding sequence evolution often accumulate as a result of adaptive evolution in many animals, especially those with large effective population sizes like C. elegans' congeners (Galtier 2016). Genes biased toward expression in adults and gametes are known to show elevated rates of adaptive evolution (Swanson and Vacquier 2002;Arunkumar et al 2013;Liu and Robinson-Rechavi 2018a), but the extent of embryonic adaptive evolution and its implications are less well established. In Drosophila, rapidly-evolving proteins involved in chromatin regulation and genomic conflict are known to play important roles in creating post-zygotic reproductive barriers between species during early development (Presgraves 2010;Maheshwari and Barbash 2011;Cooper et al 2018).…”

“…By contrast, the most famous temporal paradigm derives from embryological observations of a 'phylotypic stage' with greatest phenotypic constraint relative to earlier and later timepoints in development, the 'hourglass model' (Raff 1996;Kalinka and Tomancak 2012). Applications of this idea to molecular data have renewed interest in it beyond morphology for diverse taxa, including C. elegans (Castillo- Davis and Hartl 2002;Cutter and Ward 2005;Levin et al 2012;Zalts and Yanai 2017) and other invertebrates (Davis et al 2005;Cruickshank and Wade 2008;Kalinka et al 2010;Gerstein et al 2014;Levin et al 2016;Liu and Robinson-Rechavi 2018b), vertebrates (Hazkani-Covo et al 2005;Domazet-Loso and Tautz 2010;Irie and Kuratani 2011;Piasecka et al 2013;Liu and Robinson-Rechavi 2018a), and even plants (Quint et al 2012;Drost et al 2015). Different still, population genetics arguments about weaker purifying selection on genes expressed by just one sex, like maternal-effect gene products deposited in eggs, predict disproportionately rapid evolution of such maternallydeposited genes involved in early-embryogenesis of zygotes (Cruickshank and Wade 2008).…”

“…Sexual contests and mate choice drive rapid divergence in morphological ornaments and their genetic underpinnings (Swanson and Vacquier 2002;Ellegren and Parsch 2007), so sexual selection and sexual conflict also predicts faster evolution of sex-biased genes and of genes expressed late in life, to the extent that their development gets specified toward adulthood. The coding sequences of adult-expressed genes do tend to evolve faster than embryonic genes in a number of taxa (Cutter and Ward 2005;Davis et al 2005;Artieri et al 2009;Liu and Robinson-Rechavi 2018a).…”

Developmental constraints on genome evolution in four bilaterian model species

“…Of note, the higher divergence of late development could also be due to stronger adaptive selection, the "Darwin hypothesis" (Artieri et al 2009). This question is independent of the pattern of constraints (early or hourglass) 3 which are the focus of this study, and we explore it in a companion study (Liu and Robinson-Rechavi 2017). Both main models have been supported by recent genomic level studies based on different properties (such as expression divergence, sequence divergence, duplication, or phyletic age), different species, and different analysis methods.…”