The Cyprinodon variegatus genome reveals gene expression changes underlying differences in skull morphology among closely related species

Ezra S. Lencer, Wesley C. Warren, Richard Harrison, Amy R. McCune

Understanding the genetic and developmental origins of phenotypic novelty is central to the study of biological diversity. In this study we identify modifications to the expression of genes at four developmental stages that may underlie jaw morphological differences among three closely related species of pupfish (genus Cyprinodon) from San Salvador Island, Bahamas. Pupfishes on San Salvador Island are trophically differentiated and include two endemic species that have evolved jaw morphologies unlike that of any other species in the genus Cyprinodon. We find that gene expression differs significantly across recently diverged species of pupfish. Genes such as Bmp4 and calmodulin, previously implicated in jaw diversification in African cichlid fishes and Galapagos finches, were not found to be differentially expressed among species of pupfish. Instead we find multiple growth factors and cytokine/chemokine genes to be differentially expressed among these pupfish taxa. These include both genes and pathways known to affect craniofacial development, such as Wnt signaling, as well as novel genes and pathways not previously implicated in craniofacial development. These data highlight both shared and potentially unique sources of jaw diversity in pupfish and those identified in other evolutionary model systems such as Galapagos finches and African cichlids. We identify modifications to the expression of genes involved in Wnt signaling, Igf signaling, and the inflammation response as promising avenues for future research. Our project provides insight into the magnitude of gene expression changes contributing to the evolution of morphological novelties, such as jaw structure, in recently diverged pupfish species.