Hundreds of Genes Experienced Convergent Shifts in Selective Pressure in Marine Mammals

Abstract

Mammal species have made the transition to the marine environment several times, and their lineages represent one of the classical examples of convergent evolution in morphological and physiological traits. Nevertheless, the genetic mechanisms of their phenotypic transition are poorly understood, and investigations into convergence at the molecular level have been inconclusive. While past studies have searched for convergent changes at specific amino acid sites, we propose an alternative strategy to identify those genes that experienced convergent changes in their selective pressures, visible as changes in evolutionary rate specifically in the marine lineages. We present evidence of widespread convergence at the gene level by identifying parallel shifts in evolutionary rate during three independent episodes of mammalian adaptation to the marine environment. Hundreds of genes accelerated their evolutionary rates in all three marine mammal lineages during their transition to aquatic life. These marine-accelerated genes are highly enriched for pathways that control recognized functional adaptations in marine mammals, including muscle physiology, lipid-metabolism, sensory systems, and skin and connective tissue. The accelerations resulted from both adaptive evolution as seen in skin and lung genes, and loss of function as in gustatory and olfactory genes. In regard to sensory systems, this finding provides further evidence that reduced senses of taste and smell are ubiquitous in marine mammals. Our analysis demonstrates the feasibility of identifying genes underlying convergent organism-level characteristics on a genome-wide scale and without prior knowledge of adaptations, and provides a powerful approach for investigating the physiological functions of mammalian genes.

Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms

“…Our work on rhodopsin builds on previous studies finding evidence of convergent selection pressures at the molecular level between species that display convergent morphological adaptions to shared ecological variables (Chikina et al. ; Rubin and Moreau ; Partha et al. ).…”

“…Recent comparative studies suggest that estimating gene‐specific evolutionary rates as convergent shifts in d N / d S relative to dissimilar outgroups can help identify candidate genes involved in mediating molecular convergence in phenotypically convergent species (Chikina et al. ; Rubin and Moreau ; Partha et al. ).…”

Their loss is our gain: regressive evolution in vertebrates provides genomic models for uncovering human disease loci

“…Direct searches for specific genes can allow for testing of specific hypotheses, but genome-wide scans have the potential to uncover additional genes that may not have been previously considered. For instance, modelling the evolution of thousands of genes across the genomes of numerous mammals has uncovered signals of relaxed selection related to marine adaptations 56. Similarly, such an approach can be applied to disease-mimicking phenotypes to find similar signals of relaxed selection, and presumably pseudogenisation, of genes.…”

Convergent vomeronasal system reduction in mammals coincides with convergent losses of calcium signalling and odorant‐degrading genes

“…In this context, the inactivation of protein‐coding, also referred to as gene loss, has recently received more and more attention (Albalat & Canestro, ; Sharma et al, ). The inactivation or loss of protein‐coding genes reflects adaptations to diverse ecological niches including the change to a subterranean or aquatic habitat (Chikina, Robinson, & Clark, ; Ehrlich et al, ; Huelsmann et al, ; Kishida, Kubota, Shirayama, & Fukami, ; Lopes‐Marques et al, ; Nery, Arroyo, & Opazo, ; Partha et al, ; Prudent, Parra, Schwede, Roscito, & Hiller, ; Sharma et al, ) and various nutrition strategies that range from carnivory, herbivory, insectivory to frugivory (Hecker, Sharma, & Hiller, ; Huelsmann et al, ; Jiang et al, ; Kim et al, ; Liu et al, ; Lopes‐Marques et al, ; Sharma et al, ). Hence, studying the inactivation of protein‐coding genes constitutes a promising approach to gain further insights into evolutionary ecology.…”