The Novel Evolution of the Sperm Whale Genome

Abstract

The sperm whale, made famous by Moby Dick, is one of the most fascinating of all ocean-dwelling species given their unique life history, novel physiological adaptations to hunting squid at extreme ocean depths, and their position as one of the earliest branching toothed whales (Odontoceti). We assembled the sperm whale (Physeter macrocephalus) genome and resequenced individuals from multiple ocean basins to identify new candidate genes for adaptation to an aquatic environment and infer demographic history. Genes crucial for skin integrity appeared to be particularly important in both the sperm whale and other cetaceans. We also find sperm whales experienced a steep population decline during the early Pleistocene epoch. These genomic data add new comparative insight into the evolution of whales.

Keywords: cetaceans; genome; sperm whale.

Fig. 1.

—Cetacean-specific losses of protease genes. Proteases that have undergone loss-of-function in sperm whales, specifically, are shown to the left of the phylogeny whereas those that are inferred to be convergent, or inferred to have occurred in ancestral lineages, are mapped on to the phylogeny. Each event is depicted along the branch where loss events have been inferred to occur. Genes expected to impact skin function are colored blue; immune system: purple; blood homeostasis: red; digestion: orange, and those showing convergent loss-of-function as underlined bold. The unique duplication of sperm whale CASP3 is shown above the phylogeny and marked by an asterisk.

Fig. 2.

—Estimated effective population size history and heterozygosity of sperm whales from different ocean basins. Samples are color coded by the key, with blue/green = Pacific, orange/yellow = Indian Ocean, and dark orange = Gulf of Mexico, Atlantic. (A) PSMC reconstruction of effective population size through time by sample (excluding SEY420021031-063, see supplementary material S1, Supplementary Material online), dashed lines represent the estimated start dates for each epoch; (B) Genome wide distribution of heterozygosity for each sample, by contig/scaffold. The Gulf of Mexico sample—characterized by low heterozygosity—is marked by an asterisk where it has the largest number of contigs in a category. The insert emphasizes that this sample has the largest number of contigs with low heterozygosity (<0.0005). Bright yellow in panel (b) is additional Indian ocean sample