What influences the worldwide genetic structure of sperm whales (Physeter macrocephalus)?

The interplay of natural selection and genetic drift, influenced by geographic isolation, mating systems and population size, determines patterns of genetic diversity within species. The sperm whale provides an interesting example of a long-lived species with few geographic barriers to dispersal. Worldwide mtDNA diversity is relatively low, but highly structured among geographic regions and social groups, attributed to female philopatry. However, it is unclear whether this female philopatry is due to geographic regions or social groups, or how this might vary on a worldwide scale. To answer these questions, we combined mtDNA information for 1091 previously published samples with 542 newly obtained DNA profiles (394-bp mtDNA, sex, 13 microsatellites) including the previously unsampled Indian Ocean, and social group information for 541 individuals. We found low mtDNA diversity (π = 0.430%) reflecting an expansion event <80 000 years bp, but strong differentiation by ocean, among regions within some oceans, and among social groups. In comparison, microsatellite differentiation was low at all levels, presumably due to male-mediated gene flow. A hierarchical amova showed that regions were important for explaining mtDNA variance in the Indian Ocean, but not Pacific, with social group sampling in the Atlantic too limited to include in analyses. Social groups were important in partitioning mtDNA and microsatellite variance within both oceans. Therefore, both geographic philopatry and social philopatry influence genetic structure in the sperm whale, but their relative importance differs by sex and ocean, reflecting breeding behaviour, geographic features and perhaps a more recent origin of sperm whales in the Pacific. By investigating the interplay of evolutionary forces operating at different temporal and geographic scales, we show that sperm whales are perhaps a unique example of a worldwide population expansion followed by rapid assortment due to female social organization.

Kinship of long-term associates in the highly social sperm whale.

The evolution of stable social groups can be promoted by both indirect and direct fitness benefits. Sperm whales (Physeter macrocephalus) are highly social, with a hierarchical social structure based around core groups of adult females and subadults, a rare level of complexity among mammals. We combined long-term satellite tracking (ranging from 11 to 607 days) of 51 individual sperm whales with genetic kinship analysis to assess the pattern of kin associations within and among coherent social units. Unlike findings for other species with similar social structure, we find no consistent correlation between kinship and association apart from close associations between two pairs of first-order relatives. A third pair of first-order relatives did not associate, and overall, the mean relatedness was the same within as among social groups. However, social behaviour can also be promoted by ecological factors such as resource dispersion. We assessed putative foraging behaviour during travel from the satellite-tracking data, which suggested that prey resources were dispersed and unpredictable, a condition that could promote living in groups.

Female philopatry in coastal basins and male dispersion across the North Atlantic in a highly mobile marine species, the sperm whale (Physeter macrocephalus).

The mechanisms that determine population structure in highly mobile marine species are poorly understood, but useful towards understanding the evolution of diversity, and essential for effective conservation and management. In this study, we compare putative sperm whale populations located in the Gulf of Mexico, western North Atlantic, Mediterranean Sea and North Sea using mtDNA control region sequence data and 16 polymorphic microsatellite loci. The Gulf of Mexico, western North Atlantic and North Sea populations each possessed similar low levels of haplotype and nucleotide diversity at the mtDNA locus, while the Mediterranean Sea population showed no detectable mtDNA diversity. Mitochondrial DNA results showed significant differentiation between all populations, while microsatellites showed significant differentiation only for comparisons with the Mediterranean Sea, and at a much lower level than seen for mtDNA. Samples from either side of the North Atlantic in coastal waters showed no differentiation for mtDNA, while North Atlantic samples from just outside the Gulf of Mexico (the western North Atlantic sample) were highly differentiated from samples within the Gulf at this locus. Our analyses indicate a previously unknown fidelity of females to coastal basins either side of the North Atlantic, and suggest the movement of males among these populations for breeding.