Avian phenotypic convergence is subject to low genetic constraints based on genomic evidence

Phenotypic convergence between distinct species provides an opportunity to examine the predictability of genetic evolution. Unrelated species sharing genetic underpinnings for phenotypic convergence suggests strong genetic constraints, and thus high predictability of evolution. However, there is no clear big picture of the genomic constraints on convergent evolution. Genome-based phylogenies have confirmed many cases of phenotypic convergence in birds, making them a good system for examining genetic constraints in phenotypic convergence. In this study, we used hierarchical genomic approaches to estimate genetic constraints in three convergent avian traits: nocturnality, raptorial behavior and foot-propelled diving.

Phylogeny-based hypothesis tests and positive selection tests were applied to compare 16 avian genomes, representing 14 orders, and identify genes with strong convergence signals. We found 43 adaptively convergent genes (ACGs) associated with the three phenotypic convergence cases and assessed genetic constraints in all three cases, from (amino acid) site mutations to genetic pathways. We found that the avian orders shared few site mutations in the ACGs that contributed to the convergent phenotypes, and that these ACGs were not enriched in any genetic pathways. In addition, different pairs of orders with convergent foot-propelled diving or raptorial behaviors shared few ACGs. We also found that closely related orders that shared foot-propelled diving behavior did not share more ACGs than did distinct orders, suggesting that convergence among these orders could not be explained by their initial genomic backgrounds.

Our analyses of three avian convergence events suggest low constraints for phenotypic convergence across multiple genetic levels, implying that genetic evolution is unpredictable at the phylogenetic level of avian order. Ours is one of first studies to apply hierarchical genomic examination to multiple avian convergent cases to assess the genetic constraints in life history trait evolution.