Convergent evolution of noncoding elements associated with short tarsus length in birds

Abstract

Background: Convergent evolution is the independent evolution of similar traits in unrelated lineages across the Tree of Life. Various genomic signatures can help identify cases of convergent evolution at the molecular level, including changes in substitution rate in the same genes or gene networks. In this study, utilizing tarsus measurements of ~ 5400 species of birds, we identify independent shifts in tarsus length and use both comparative genomic and population genetic data to identify convergent evolutionary changes among focal clades with shifts to shorter optimal tarsus length. Results: Using a newly generated, comprehensive and broadly accessible set of 932,467 avian conserved non-exonic elements (CNEEs) and a whole-genome alignment of 79 birds, we find strong evidence for convergent acceleration in short-tarsus clades among 14,422 elements. Analysis of 9854 protein-coding genes, however, yielded no evidence of convergent patterns of positive selection. Accelerated elements in short-tarsus clades are concentrated near genes with functions in development, with the strongest enrichment associated with skeletal system development. Analysis of gene networks supports convergent changes in regulation of broadly homologous limb developmental genes and pathways. Conclusions: Our results highlight the important role of regulatory elements undergoing convergent acceleration in convergent skeletal traits and are consistent with previous studies showing the roles of regulatory elements and skeletal phenotypes.