Deterministic shifts in molecular evolution correlate with convergence to annualism in killifishes

Abstract The repeated evolution of novel life histories correlating with ecological variables offer opportunities to test scenarios of convergence and determinism in genetic, developmental, and metabolic features. Here we leverage the diversity of aplocheiloid killifishes, a clade of teleost fishes that contains over 750 species on three continents. Nearly half of these are “annual” or seasonal species that inhabit bodies of water that desiccate and are unfeasible for growth, reproduction, or survival for weeks to months at a time. We present a large-scale phylogenomic reconstruction of aplocheiloid killifish evolution using newly sequenced transcriptomes from all major clades. We show that developmental dormancy (diapause) and annualism have up to seven independent origins in Africa and America. We then measure evolutionary rates of orthologous genes and show that annual life history is correlated with higher d N /d S ratios. Many of these fast-evolving genes in annual species constitute key developmental genes and nuclear-encoded metabolic genes that control oxidative phosphorylation. Lastly, we compare these fast-evolving genes to genes associated with developmental dormancy and metabolic shifts in killifishes and other vertebrates and thereby identify molecular evolutionary signatures of repeated evolutionary transitions to extreme environments.