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

Abstract

BackgroundConvergent 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0682-4) contains supplementary material, which is available to authorized users.

Lineage-specific evolution of bitter taste receptor genes in the giant and red pandas implies dietary adaptation

“…Similar results have been found in chimpanzees and humans, where although the 2 species shared variable taste sensitivity to bitter compounds mediated by phenylthiocarbamide receptor variants, the molecular basis of the variation has arisen twice, independently, in the 2 species (Wooding et al 2006). This phenomenon has been suggested as convergence occurred at a functional level of genes (Nery et al 2016). The find ings presented in this study provide us with new insight into the molecular basis of evolutionary adaptation in giant and red pandas to dietary shift, and support previous discoveries that bitter taste receptor genes have evolved independently in mammals in response to dietary specialization (Wooding et al 2006;Jiang et al 2012;Li & Zhang 2014;Risso et al 2017).…”

Evolutionary changes of Hox genes and relevant regulatory factors provide novel insights into mammalian morphological modifications

“…Taking the functional overlap of different Hox genes into account, the adaptive molecular signatures of these 2 genes in whales and pinnipeds may also suggest a different evolutionary route to the similar limb morphologies in whales and pinnipeds. This seems to conform to the assumption that the phenotypic convergence of marine mammals may be achieved through the selection of different Hox genes with equivalent functions proposed by Nery et al (2016). However, Nery et al (2016) nority of positive selection of Hox genes with overlapping functions in marine mammals, which seemed to be insufficiently cogent case with respect to the remarkable convergent phenotypic traits of marine mammals.…”

“…This seems to conform to the assumption that the phenotypic convergence of marine mammals may be achieved through the selection of different Hox genes with equivalent functions proposed by Nery et al (2016). However, Nery et al (2016) nority of positive selection of Hox genes with overlapping functions in marine mammals, which seemed to be insufficiently cogent case with respect to the remarkable convergent phenotypic traits of marine mammals. In addition, the parallel amino acid substitution of Hoxd12 was identified between the whales and the manatee.…”

“…Parallel amino acid substitutions of Hox proteins have been identified in marine mammals, such as pinnipeds and manatee sharing one site separately at Hoxa2 and Hoxc10, which might be considered as molecular evidence for their convergent streamlined shape. Furthermore, it has been reported that similar gene function may also lead to convergent phenotypes in unrelated taxa (Nery et al 2016). Our results have detected the adaptive molecular signatures of Hoxb9 in whales and pinnipeds, and Hoxd12 in whales.…”

Accelerated Evolution of Limb-Related Gene Hoxd11 in the Common Ancestor of Cetaceans and Ruminants (Cetruminantia)

“…Abbreviations for taxonomy are "Pe" (Perissodactyla), "Ca" (Carnivora), "Ch" (Chiroptera), "La" (Lagomorpha) and "Af" (Afrosoricida). further evidences that different Hox genes are important for the diversified morphologies during mammalian evolution (Liang et al 2013;Nery et al 2016;Li et al 2018). Considering that Hoxd11 is more specifically involved in carpal and tarsal bone development (Davis and Capecchi 1994;Koyama et al 2010), we conducted a molecular evolutionary study of this gene to determine whether evolution of Hoxd11 might explain the bone number variations in Cetruminantia.…”