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Comparative genomics provides insights into the aquatic adaptations of mammals.

ABSTRACT: The ancestors of marine mammals once roamed the land and independently committed to an aquatic lifestyle. These macroevolutionary transitions have intrigued scientists for centuries. Here, we generated high-quality genome assemblies of 17 marine mammals (11 cetaceans and six pinnipeds), including eight assemblies at the chromosome level. Incorporating previously published data, we reconstructed the marine mammal phylogeny and population histories and identified numerous idiosyncratic and convergent genomic variations that possibly contributed to the transition from land to water in marine mammal lineages. Genes associated with the formation of blubber (NFIA), vascular development (SEMA3E), and heat production by brown adipose tissue (UCP1) had unique changes that may contribute to marine mammal thermoregulation. We also observed many lineage-specific changes in the marine mammals, including genes associated with deep diving and navigation. Our study advances understanding of the timing, pattern, and molecular changes associated with the evolution of mammalian lineages adapting to aquatic life.

SUBMITTER: Yuan Y

PROVIDER: S-EPMC8449357 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Comparative genomics provides insights into the aquatic adaptations of mammals.

Yuan Yuan Y Zhang Yaolei Y Zhang Peijun P Liu Chang C Wang Jiahao J Gao Haiyu H Hoelzel A Rus AR Seim Inge I Lv Meiqi M Lin Mingli M Dong Lijun L Gao Haoyang H Yang Zixin Z Caruso Francesco F Lin Wenzhi W da Fonseca Rute R RR Wang Ding D Wang Xianyan X Rasmussen Marianne H MH Liu Mingming M Zheng Jinsong J Zhao Liyuan L Campos Paula F PF Kang Hui H Iversen Maria M Song Yue Y Guo Xinyu X Guo Jiao J Qin Yating Y Pan Shanshan S Xu Qiwu Q Meng Lingfeng L A Yunga Y Liu Shanshan S Lee Simon Ming-Yuen SM Liu Xin X Xu Xun X Yang Huanming H Fan Guangyi G Wang Kun K Li Songhai S

Proceedings of the National Academy of Sciences of the United States of America 20210901 37

The ancestors of marine mammals once roamed the land and independently committed to an aquatic lifestyle. These macroevolutionary transitions have intrigued scientists for centuries. Here, we generated high-quality genome assemblies of 17 marine mammals (11 cetaceans and six pinnipeds), including eight assemblies at the chromosome level. Incorporating previously published data, we reconstructed the marine mammal phylogeny and population histories and identified numerous idiosyncratic and converg ...[more]

PMID: 34503999

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Project description:BackgroundDiversity of hair in marine mammals was suggested as an evolutionary innovation to adapt aquatic environment, yet its genetic basis remained poorly explored. We scanned α-keratin genes, one major structural components of hair, in 16 genomes of mammalian species, including seven cetaceans, two pinnipeds, polar bear, manatee and five terrestrial species.ResultsExtensive gene loss and high pseudogenization rate of α-keratin genes were identified in cetaceans when compared to terrestrial artiodactylans (average number of α-keratins 37.29 vs. 58.33; pseudogenization rate 29.89% vs. 8.00%), especially of hair follicle-specific keratin genes (average pseudogenization rate in cetaceans of 43.88% relative to 3.80% artiodactylian average). Compared to toothed whale, the much more number of intact functional α-keratin genes was examined in the baleen whale that had specific keratinized baleen. In contrast, the number of keratin genes in pinnipeds, polar bear and manatee were comparable to those of their respective terrestrial relatives. Additionally, four keratin genes (K39, K9, K42, and K74) were found to be pseudogenes or lost uniquely in cetaceans and manatees.ConclusionsSpecies-specific evolution of α-keratin gene family identified in the marine mammals might be responsible for their different hair characteristics. Increased gene loss and pseudogenization rate identified in cetacean lineages was likely to contribute to hair-less phenotype to adaptation for complete aquatic environment. However, the fully aquatic manatee still remained the comparable number of intact genes to its terrestrial relative, probably due to its perioral bristles and bristle-like hairs on the oral disk. By contrast, similar evolution pattern of α-keratin gene repertoire in the pinnipeds, polar bear and their terrestrial relatives was likely due to abundant hair to keep warm when they went ashore. Interestingly, some keratin genes were exclusively lost in cetaceans and manatees, likely as a result of convergent hair-loss phenotype to inhabit completely aquatic environment in both groups.

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Comparative genomics provides insights into the aquatic adaptations of mammals.

Publications

Comparative genomics provides insights into the aquatic adaptations of mammals.

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