Minke whale genome and aquatic adaptation in cetaceans

Abstract

The shift from terrestrial to aquatic life by whales was a substantial evolutionary event. Here we report the whole-genome sequencing and de novo assembly of the minke whale genome, as well as the whole-genome sequences of three minke whales, a fin whale, a bottlenose dolphin and a finless porpoise. Our comparative genomic analysis identified an expansion in the whale lineage of gene families associated with stress-responsive proteins and anaerobic metabolism, whereas gene families related to body hair and sensory receptors were contracted. Our analysis also identified whale-specific mutations in genes encoding antioxidants and enzymes controlling blood pressure and salt concentration. Overall the whale-genome sequences exhibited distinct features that are associated with the physiological and morphological changes needed for life in an aquatic environment, marked by resistance to physiological stresses caused by a lack of oxygen, increased amounts of reactive oxygen species and high salt levels.

Figure 1. Orthologous gene clusters in the artiodactyl lineage

Shown is a Venn diagram of unique and shared gene families in the minke whale, bottlenose dolphin, cow and pig genomes. The total numbers of gene families are given in parentheses.

Figure 2. Relationship of the minke whale to other mammalian species

(a) Gene family expansion or contraction. The numbers indicate the number of gene families that have expanded (orange) or contracted (blue) since the split from a common ancestor. MYA, million years ago; MRCA, most recent common ancestor. Timelines indicate the divergence times among species, (b) The expanded peroxiredoxin (PRDX) gene family in the whale lineage.

Figure 3. Cetacean-specific amino acid changes in glutathione metabolism-associated genes and haptoglobin

(a) A positively selected gene (GSR) in the bottlenose dolphin is shown in a red rectangle. Genes with cetacean-specific amino acid changes (GSR, GPX2, GGT6, GGT7, ANPEP, ODC1 and GCLC) are shown in blue rectangles. The seven cetacean-specific genes are involved in glutathione metabolism pathways (KEGG pathway map00480). The solid lines indicate direct relationships between enzymes and metabolites. The dashed lines indicate that more than one step is involved in a process, (b) The positions of unique amino acid changes in the crystal structure of the haptoglobin-hemoglobin complex. The haptoglobin protein is shown in a cartoon form; the CCP domain is green, and the SP domain is yellow. Of the ten amino acid changes, eight positions are represented by violet sticks; the other two positions are not displayed because they were not included in the complex structure. Hemoglobin is shown with green sticks, and the CCP domain of the contacting haptoglobin is represented in an electrostatic potential surface model (blue, positive; red, negative; white, neutral). The black dots indicate the polar interaction between His137 of haptoglobin and the terminal carboxylate of hemoglobin.

Figure 4. Estimated whale population size history

T_surf, atmospheric surface air temperature; RSL, relative sea level; 10 m.s.l.e., 10 m sea level equivalent; MW, minke whale; FW, fin whale; BD, bottlenose dolphin; PP, finless porpoise; g, generation time; μ, mutation rate (per site, per year). Minke whale and fin whale data were generated on the basis of comparisons with minke whale scaffolds (“-B” after the species abbreviation) during SNV calling, whereas the bottlenose dolphin and finless porpoise data were generated on the basis of comparisons with the bottlenose dolphin scaffolds (“-T” after the species abbreviation) during SNV calling.