Identifying molecular evolutionary rate shifts accompanying dietary transitions in mammals
Authors: Wynn Meyer 1; Kathleen Foley 1,2; Simon Gajewski 1; Oluwafunmbi Ojo 1; Irene Kaplow 3; Daniel Schäffer 3; Maria Chikina 4; Andreas Pfenning 3; Zoonomia Consortium
Affiliations: 1) Lehigh University, Bethlehem, PA; 2) University of Iowa, Iowa City, IA; 3) Carnegie Mellon University, Pittsburgh, PA; 4) University of Pittsburgh, Pittsburgh, PA
Keywords: Comparative genomics & genome evolution
Mammals display striking contrasts in diet, particularly between species that eat other animals almost exclusively and those that predominantly eat plants. These dietary specializations have evolved multiple times independently within the mammalian phylogeny, providing an opportunity to identify molecular evolutionary signatures associated with these convergent phenotypes. Such signatures can implicate genes involved in mammalian adaptation to distinct diets. We here implement a robust computational method to identify associations between relative rates of molecular evolution in coding sequences and dietary phenotype across branches of the mammalian phylogeny, representing 71 strictly carnivorous or herbivorous species. We test for these associations at 14,883 protein coding genes for which high quality alignments are available from the Zoonomia Project. Overall, we find that substantially more genes evolve rapidly in herbivorous lineages relative to carnivorous lineages than the opposite pattern (evolving more rapidly in carnivorous lineages). By implementing a false discovery rate correction for multiple testing, we find strong correlations between diet and the relative evolutionary rates of multiple large axonemal dynein heavy chain genes, driven by rapid evolution among many members of fully herbivorous clades. When we implement phylogenetic simulations and permutations to account for non-independence in phenotype throughout the tree, we find a different set of genes as most strongly associated with dietary phenotype, driven by large convergent shifts in molecular evolutionary rates on internal branches representing phenotype transitions. Among these results, we find an enrichment of more rapid evolution in herbivores among genes expressed in the human thyroid and brain, specifically the cerebellar hemisphere and frontal cortex. Two of the genes with the strongest phylogeny-corrected signatures of rapid evolution in response to herbivory have previously been implicated in adipogenesis. While relaxation of selective constraint may explain some convergent shifts in evolutionary rates, particularly for genes evolving rapidly in all lineages in herbivorous clades, the strong signatures of convergent rate shifts on internal branches more likely represent changing fitness optima in response to dietary change. The genes we have identified with these signatures thus represent strong candidates for targets of adaptation to herbivorous diets in mammals.