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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.

Split hand/foot malformation (SHFM) is a rare limb abnormality with clefting of the fingers and/or toes. For many individuals, the genetic etiology is unknown. Through whole-exome and targeted sequencing, we detected three novel variants in a gene encoding a transcription factor, PRDM1, that arose de novo in families with SHFM or segregated with the phenotype. PRDM1 is required for limb development; however, its role is not well understood and it is unclear how the PRDM1 variants affect protein function. Using transient and stable overexpression rescue experiments in zebrafish, we show that the variants disrupt the proline/serine-rich and DNA-binding zinc finger domains, resulting in a dominant-negative effect. Through gene expression assays, RNA sequencing, and CUT&RUN in isolated pectoral fin cells, we demonstrate that Prdm1a directly binds to and regulates genes required for fin induction, outgrowth and anterior/posterior patterning, such as fgfr1a, dlx5a, dlx6a and smo. Taken together, these results improve our understanding of the role of PRDM1 in the limb gene regulatory network and identified novel PRDM1 variants that link to SHFM in humans.

To understand the origins of novelty and the evolution of biological diversity, it is important to investigate the processes that generate phenotypic variation from genotypic variation. A number of path-breaking studies have revealed the genetic basis for phenotypic differences between distantly related taxa, but how qualitative change is produced during the early stages of divergence is largely unexplored. Here, we focus on striking differences in jaw morphology exhibited by three closely related sympatric pupfish species (genus Cyprinodon) from San Salvador Island, Bahamas as a basis for investigating the genetic sources of morphological variation in recently diverged species. San Salvador Island pupfish are trophically diverse and display derived jaw morphologies distinct from any other species in the genus. We illustrate these qualitative morphological differences between species with 3D-reconstructed CT-images and camera lucida drawings of the skulls of wild-caught fish. Quantitative data representing the size of individual bony skull elements in wild fish show how qualitatively novel morphologies arise as a consequence of changes to the size and shape of individual skull elements, particularly the dentary, premaxilla, and maxilla bones associated with the oral jaws. Consistent with these comparative data is that the growth rate of individual bony skull elements, measured on a developmental time series of lab-reared fish, differs between species. Our data provide a critical foundation for future studies developing San Salvador Cyprinodon pupfishes as a model system to understand the evolution and development of novel morphologies at the species level. J. Morphol. 277:935-947, 2016. © 2016 Wiley Periodicals, Inc.

How modification of gene expression generates novel traits is key to understanding the evolutionary process. We investigated the genetic basis for the origin of the piscine gas bladder from lungs of ancestral bony vertebrates. Distinguishing these homologous organs is the direction of budding from the foregut during development; lungs bud ventrally and the gas bladder buds dorsally.