Traits shared among distantly related lineages are indicators of common evolutionary constraints, at the ecological, physiological or molecular level. Here, we show that the vertebral stripe, a cryptic color pattern, has evolved hundreds of times in the evolutionary history of anurans (frogs and toads) and is favored in terrestrial habitats. Using a genome-wide association study, we demonstrate that variation near the Agouti signaling protein gene (ASIP) is responsible for the different vertebral stripe phenotypes in the African grass frog Ptychadena robeensis. RNAseq and real-time quantitative PCR revealed that differential expression of the gene and an adjacent long non-coding RNA is linked to patterning in this species. Surprisingly, and although the stripe phenotypes are shared with closely related species, we found that the P. robeensis alleles are private to the species and unlikely to evolve under long-term balancing selection, thus indicating that the vertebral stripe phenotypes result from parallel evolution within the group. Our findings demonstrate that this cryptic color pattern evolved rapidly and recurrently in terrestrial anurans, and therefore constitutes an ideal system to study repeated evolution.
SummaryTraits shared among distantly related lineages are indicators of common evolutionary constraints, at the ecological, physiological or molecular level. The vertebral stripe is a color pattern that is widespread across the anuran phylogeny. Despite its prevalence in the order, surprisingly little is known about the genetic basis and evolutionary dynamic of this color pattern. Here we combine histology, genome- and transcriptome-wide analyses with order-scale phylogenetic comparative analyses to investigate this common phenotype. We show that the vertebral stripe has evolved hundreds of times in the evolutionary history of anurans and is selected for in terrestrial habitats. Using the Ethiopian Ptychadena radiation as a model system, we demonstrate that variation at the ASIP gene is responsible for the different vertebral stripe phenotypes. Alleles associated to these phenotypes are younger than the split between closely related Ptychadena species, thus indicating that the vertebral stripe results from parallel evolution within the group. Our findings demonstrate that this widespread color pattern evolves rapidly and recurrently in terrestrial anurans, and therefore constitute an ideal system to study repeated evolution.
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