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.

Keywords: aquatic adaptation; comparative genomics; marine mammals.

Fig. 1.

Phylogeny and population changes of marine mammals. (A) A maximum likelihood phylogenetic tree of 35 marine mammal species and 16 outgroup mammal species. Three lineages of marine mammals are distinguished by columns of different colors: Cetacea (blue), Pinnipedia (green), and Sirenia (red). Red stars represent the species differentiation node mentioned in the main text. (B) Population size history of three lineages of marine mammals. The normalized effective population size (N_e) of each species was estimated using pairwise sequentially Markovian coalescent. The N_e for each group of marine mammals is shown.

Fig. 2.

Structural characteristics and chromosome evolution of marine mammal genomes. (A) Circos plot of representative genomes of marine mammals: sperm whale, Indo-Pacific bottlenose dolphin (IPB dolphin), South American fur seal (SA fur seal), and spotted seal. (B) Genome sizes and transposable element content analysis of representative genomes of marine mammals. We selected three Ruminantia species, three cetacean species, three Canidae species, three pinniped species, an elephant, and a manatee. (C) Chromosome evolution of Cetacea and Pinnipedia. We reconstructed 23 and 19 ancestral chromosomes of Cetacea and Pinnipedia, respectively. The chromosome assignment to ancestral chromosomes is shown by colored bars, Indo-Pacific humpback dolphin (IPH dolphin).

Fig. 3.

Convergent evolution of thermoregulation in marine mammals. (A) Schematic diagram of thermoregulation in marine mammals. Up- or down-regulation of nuclear factor I A (NFIA) affects the cell fate of mesenchymal precursors, the integrity of UCP1 gene affects the fate of brown adipocyte, and the well-developed retia mirabilia in marine mammal aids in the heat transfer to maintain body temperature balance. VSMC, vascular smooth muscle cell; EC, endothelial cell. (B) A unique amino acid change in the NFIA gene of marine mammals. Shared amino acid change are highlighted in blue, IP, Indo-Pacific. (C) A unique amino acid change in the Sema3E gene of cetaceans and pinnipeds. Blue highlighting indicates the shared amino acid change. (D) VISTA sequence conservation plot of the UCP1 gene, using goat (ARS1) as a reference.

Fig. 4.

Various genomic changes potentially related to aquatic adaptations. (A) PG biosynthesis pathway. Genes with roles in the PG biosynthesis pathway have unique amino acid changes (highlighted in blue) in marine mammals. Ser, serine; Xyl, xylose; Gal, galactose; P, phosphorylate and SA, South American. (B) Diagram of genes that specifically change in the deep-diving group is divided into four parts according to the gene functions, highlighting specific mutation genes (SMGs) (orange) and PSGs/REGs (blue).