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

Abstract

BackgroundUnderstanding 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.ResultsWe 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3810-7) contains supplementary material, which is available to authorized users.

Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies

“…Finally, our novel results are consistent with a recently published independent analysis of gene expression in San Salvador pupfishes that identified many of the same genes we found divergently expressed between specialists (Lencer et al. ). We examined this dataset using the same significance thresholds for differentially expressed genes as described in Lencer et al.…”

“…We measured expression across 22,183 genes with greater than two read counts out of 24,383 total genes annotated for the Cyprinodon variegatus assembly (NCBI, C. variegatus Annotation Release 100 (Lencer et al. )).…”

Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation

“…Moreover, recent work by Lencer et al. () shows that the scale‐eater significantly overexpresses insulin‐like growth factor binding proteins, strongly implicating such growth factors in this divergent morphology of the jaw.…”

“…Sampling from several hypersaline lakes/ponds on San Salvador, Martin & Wainwright (,,) described clear trophic (Martin & Wainwright, ; Martin, ) and genetic divergence (Martin & Feinstein, ; Lencer et al. ) among these three species. The widespread C. variegatus , thought to have given rise to this small species flock, enjoys a broad geographic distribution spanning from Maine to the West Indies (Hoese & Moore, ) and Venezuela (Turner et al.…”

“…), to date there have been no functional morphological descriptions for radiations of Cyprinodon (but see Lencer et al. for an ontogenetic analysis). Although there are published data on the rapid rate of morphological evolution within key feeding structures (Martin & Wainwright, ; Martin, ), detailed reports of how such morphological changes may have led to trophic specialization are rare (Lencer et al.…”