Selection on different genes with equivalent functions: the convergence story told by Hox genes along the evolution of aquatic mammalian lineages

Abstract

Background: Convergent evolution has been a challenging topic for decades, being cetaceans, pinnipeds and sirenians textbook examples of three independent origins of equivalent phenotypes. These mammalian lineages acquired similar anatomical features correlated to an aquatic life, and remarkably differ from their terrestrial counterparts. Whether their molecular evolutionary history also involved similar genetic mechanisms underlying such morphological convergence nevertheless remained unknown. To test for the existence of convergent molecular signatures, we studied the molecular evolution of Hox genes in these three aquatic mammalian lineages, comparing their patterns to terrestrial mammals. Hox genes are transcription factors that play a pivotal role in specifying embryonic regional identity of nearly any bilateral animal, and are recognized major agents for diversification of body plans.

Results: We detected few signatures of positive selection on Hox genes across the three aquatic mammalian lineages and verified that purifying selection prevails in these sequences, as expected for pleiotropic genes. Genes found as being positively selected differ across the aquatic mammalian lineages, but we identified a substantial overlap of their developmental functions. Such pattern likely resides on the duplication history of Hox genes, which probably provided different possible evolutionary routes for achieving the same phenotypic solution.

Conclusions: Our results indicate that convergence occurred at a functional level of Hox genes along three independent origins of aquatic mammals. This conclusion reinforces the idea that different changes in developmental genes may lead to similar phenotypes, probably due to the redundancy provided by the participation of Hox paralogous genes in several developmental functions.

Keywords: Cetaceans; Hox genes; Molecular evolution; Pinnipeds; Positive selection; Sirenians.

Fig. 1

Tree topology used to conduct the analyses of variable ω among lineages; tree assembled from published literature [77, 78]

Fig. 2

The ω values for Hox genes in cetaceans, pinnipeds, sirenian and average value for the remaining mammals (solid line) derived from the two-ratio model. Asterisks indicate those Hox genes statistically inferred as evolving under positive selection or those having significantly higher evolutionary rates

Fig. 3

Hox genes evolving under positive selection in cetaceans, pinnipeds and sirenians, coupled with their functions