Increased rate of hair keratin gene loss in the cetacean lineage

Abstract

BackgroundHair represents an evolutionary innovation that appeared early on mammalian evolutionary history, and presumably contributed significantly to the rapid radiation of the group. An interesting event in hair evolution has been its secondary loss in some mammalian groups, such as cetaceans, whose hairless phenotype appears to be an adaptive response to better meet the environmental conditions. To determine whether different repertoire of keratin genes among mammals can potentially explain the phenotypic hair features of different lineages, we characterized the type I and II clusters of alpha keratins from eight mammalian species, including the hairless dolphin and minke whale representing the order Cetacea.ResultsWe combined the available genomic information with phylogenetic analysis to conduct a comprehensive analysis of the evolutionary patterns of keratin gene clusters. We found that both type I and II gene clusters are fairly conserved among the terrestrial mammals included in this study, with lineage specific gene duplication and gene loss. Nevertheless, there is also evidence for an increased rate of pseudogenization in the cetacean lineage when compared to their terrestrial relatives, especially among the hair type keratins.ConclusionsHere we present a comprehensive characterization of alpha-keratin genes among mammals and elucidate the mechanisms involved in the evolution of this gene family. We identified lineage-specific gene duplications and gene loss among the Laurasiatherian and Euarchontoglires species included in the study. Interestingly, cetaceans present an increased loss of hair-type keratin genes when compared to other terrestrial mammals. As suggested by the ‘less-is-more’ hypothesis, we do not rule out the possibility that the gene loss of hair-type keratin genes in these species might be associated to the hairless phenotype and could have been adaptive in response to new selective pressures imposed by the colonization of a new habitat. Our study provides support for the idea that pseudogenes are not simply ‘genomic fossils’ but instead have adaptive roles during the evolutionary process.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-869) contains supplementary material, which is available to authorized users.

Comparative genomics analyses of alpha-keratins reveal insights into evolutionary adaptation of marine mammals

“…Previous studies characterized KRTAP gene repertoire in 22 mammals and found that gene family repertoire expansion, contraction, and pseudogenization were related to hair diversities in mammals [ 13 ]. In addition, an increase rate of hair keratin genes loss and pseudogenization were examined in two cetacean species when compared with fur terrestrial relatives, which was suggested to be associated with cetacean hairless phenotype [ 14 ]. However, previous studies only determined in one or two cetacean species could not provide comprehensive insight into genetic basis of hair diversities in marine mammals.…”

Genes lost during the transition from land to water in cetaceans highlight genomic changes involved in aquatic adaptations

“…To detect gene-inactivating mutations, we employed a comparative approach that makes use of genome alignments to search for mutations that disrupt the protein's reading frame (stop codon mutations, frameshifting insertions or deletions, deletions of entire exons) and mutations that disrupt splice sites (36). We excluded olfactory receptor and keratin-associated genes since losses in these large gene families have previously been reported (18,19,24,25). This resulted in a set of 85 genes that exhibit shared inactivating mutations in odontocetes and mysticetes, most of which have not been reported before (Table S1).…”

“…In addition to patterns of positive selection, the loss (inactivation) of protein-coding genes is associated with derived cetacean traits. For example, cetaceans have lost a large number of olfactory and vomeronasal receptors, olfactory signal transduction genes, taste receptors, and hair keratin and epidermal genes (17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27). Furthermore, all or individual cetacean lineages lost the ketone body synthesizing enzyme HMGCS2 (28), the sebaceous glandexpressed MC5R gene (29), the non-shivering thermogenesis gene UCP1 (30), the protease KLK8 that plays distinct roles in the skin and hippocampus (31), short-and longwave sensitive opsin genes (32,33), and the antiviral genes MX1 and MX2 (34).…”

Peer Review #1 of "The dopamine receptor D5 gene shows signs of independent erosion in toothed and baleen whales (v0.1)"

“…Reductive episodes have been widely documented across the tree of life contributing to organismal divergence and physiological and morphological adaptation to environmental cues (Albalat & Canestro, 2016;Braun, 2003;Jeffery, 2009;Olson, 1999). In agreement, gene loss mechanisms seem pervasive in lineages that endured drastic habitat transitions in the course of evolution, such as Cetacea, entailing niche-specific adaptations (Huelsmann et al, 2019;Lachner et al, 2017;Lopes-Marques et al, 2019b;McGowen et al, 2014;Nery et al, 2014;Sharma et al, 2018;Strasser et al, 2015). Thus, our findings suggest that these species are natural KOs for this dopamine receptor and might offer valuable insights into the mechanisms of some forms of essential hypertension.…”