Aim: Species living in a shared environment face similar selective pressures and often evolve adaptive divergence to avoid competition. Quantifying phenotypic divergence and its genetic parallelism among sympatric species is important for understanding of ecologically moderated biodiversity. Here we integrate ecologic, phenotypic and genomic datasets to study to what extent three sympatrically snowfinches (Montifringilla adamsi, Pyrgilauda ruficollis and Onychostruthus taczanowskii) differ in their adaptations in order to co-exist in a shared environment.

Location: Qinghai-Tibetan Plateau

Methods: We used principal component analysis to summarize and compare environmental and phenotypic divergence. We compared phenotypes relevant to body and beak sizes (n=68) because they are indicators of niche and food segregation, thus critical for establishing co-existence of sympatric birds. We used comparative genomics (n=33) to identify genetic loci that are highly divergent between species as well as loci unique for each of species. Using vector analyses, we integrated correlation and permutation to quantify parallelism between phenotypic and genetic divergences.

Results: We found that body and beak sizes are significantly different among three snowfinches. The phenotypic differentiations are greater in species that share similar ecological conditions than in those that do not. We showed that genes related to developmental process are over-represented within highly divergent genomic regions and unique genetic loci of each species. We found that the extent of phenotypic divergence between snowfinch pairs is more strongly correlated with the magnitude of divergence in developmental genes than in the whole-genome.

Main Conclusions: Adaptive divergence of sympatric snowfinches is highly constrained on developmental genes. As this genetic divergence is strongly correlated with divergence of the traits related to segregation in niche and food resources, this correlation reflects either causal effects or indirect consequences of ecological mediated changes. Our study provides novel insights into the mechanisms underlying evolutionary versatility and ecological success among sympatric species.