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Cetaceans are unique in being the only mammals completely adapted to an aquatic environment. This adaptation has required complex changes and sometimes a complete restructuring of physiology, behavior and morphology. Identifying genes that have been subjected to selection pressure during cetacean evolution would greatly enhance our knowledge of the ways in which genetic variation in this mammalian order has been shaped by natural selection. Here, we performed a genome-wide scan for positive selection in the dolphin lineage. We employed models of codon substitution that account for variation of selective pressure over branches on the tree and across sites in a sequence. We analyzed 7,859 nuclear-coding ortholog genes and using a series of likelihood ratio tests (LRTs), we identified 376 genes (4.8%) with molecular signatures of positive selection in the dolphin lineage. We used the cow as the sister group and compared estimates of selection in the cetacean genome to this using the same methods. This allowed us to define which genes have been exclusively under positive selection in the dolphin lineage. The enrichment analysis found that the identified positively selected genes are significantly over-represented for three exclusive functional categories only in the dolphin lineage: segment specification, mesoderm development and system development. Of particular interest for cetacean adaptation to an aquatic life are the following GeneOntology targets under positive selection: genes related to kidney, heart, lung, eye, ear and nervous system development.
Introduction
A central goal in evolutionary biology is to understand the relative contribution of the different evolutionary forces in the origin of new species. The answer to this long-standing question has often been framed in terms of the relative contribution of natural selection to extant patterns of genetic variation. In particular, there has been great interest in detecting genes or genomic regions under positive selection since these provide evidence for adaptive changes in protein function. Identifying genes with a signature of adaptive evolution could shed light on the type of genetic variation that contributes to the origin of phenotypic diversity, and to which extent positive selection plays a major role in evolutionary change.
With the increasing availability of genome sequences and sophisticated analytical tools, the interest in finding targets of positive selection has increased in the last decade. In mammals most of the studies are focused on understanding the genetic changes that occurred during human ancestry, and have identified several genes that show strong evidence of positive selection, including those related to immunity, sensory perception, reproduction and host-pathogen interactions [1]–[7].
From all known mammalian lineages, the evolutionary history of cetaceans is one of the most eloquent examples of extensive adaptations to meet new environmental conditions [8]. The macroevolutionary transition from a fully terrestrial quadruped to an obligate aquatic form involved extensive changes in the morphological, physiological and behavioral systems [9]. These changes likely resulted from selective pressures for new genotypes that were better suited to the novel environments. Paleontological evidence indicates a series of transformations from more terrestrial to more aquatic lifestyle as we move from the most ancestral (represented by the Pakicetus from the early Eocene of Pakistan, about 50 million years ago [9]) to the most recent species. These transitions have affected most of the cetacean biological systems and allowed them to diversify to different aquatic habitats, dispersing across the world's oceans, and into estuaries and even rivers [10].
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