Genomic signatures associated with transitions to viviparity in Cyprinodontiformes

Abstract

The transition from oviparity to viviparity has occurred independently over 150 times across vertebrates, presenting one of the most compelling cases of phenotypic convergence. However, whether the repeated, independent evolution of viviparity is driven by redeployment of similar genetic mechanisms and whether these leave a common signature in genomic divergence remains largely unknown. Whilst recent investigations into the evolution of viviparity have demonstrated striking similarity among the genes and molecular pathways involved across disparate vertebrate groups, quantitative tests for genome-wide convergent have provided ambivalent answers. Here, we investigate the potential role of molecular convergence during independent transitions to viviparity across an order of ray-finned freshwater fish (Cyprinodontiformes). We assembled de novo genomes and utilized publicly-available genomes of viviparous and oviparous species to test for molecular convergence across both coding and non-coding regions. We found no evidence for an excess of molecular convergence in amino acid substitutions and in rates of sequence divergence, implying independent genetic changes are associated with these transitions. However, both statistical power and biological confounds could constrain our ability to detect significant correlated evolution. We therefore identified candidate genes with potential signatures of molecular convergence in viviparous Cyprinodontiformes lineages. Motif-enrichment and gene ontology analyses suggest transcriptional changes associated with early morphogenesis, brain development and immunity occurred alongside the evolution of viviparity. Overall, however, our findings indicate that independent transitions to viviparity in these fish is not strongly associated with an excess of molecular convergence, but a few genes show convincing evidence of convergent evolution.