Graduate Thesis Or Dissertation
 

The influence of social structure and molecular evolution on genetic diversity in the sperm whale (Physeter macrocephalus)

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  • The sperm whale (Physeter macrocephalus) shows some of the most derived characteristics of any mammal: a large body size, large brain, complex social organization and a capacity for deep foraging dives that few other marine mammals can match. Despite a history of exploitation that removed hundreds of thousands of individuals, the sperm whale population remains relatively abundant in comparison with other large whale species. Given this abundance, and the sperm whale's matrifocal social organization, it is surprising that previous research found that mitochondrial DNA control region (mtDNA CR) diversity in sperm whales is extremely low and population structure is relatively limited within oceans. This dissertation addresses several questions spanning evolutionary and ecological time scales, including whether the low levels of mtDNA CR diversity and differentiation seen in the sperm whale have been limited by sample size and geographic scope in previous studies; how sperm whale genetic diversity is partitioned at several hierarchical levels; and hypotheses explaining the low mtDNA CR diversity. To achieve this, I generated DNA profiles representing 557 individuals from circum-equatorial regions, strandings around the coasts of New Zealand, Samoa and Oregon, and biopsy samples from the Gulf of Mexico. DNA genotypes constructed from these samples (mtDNA CR, sex, 13 microsatellite loci), and mtDNA information from 1,167 previously published samples, indicated a high degree of mtDNA CR differentiation within the previously un-sampled Indian Ocean (FST 0.314, p < 0.001). The level of differentiation seen was similar to that found with the marginal seas of the Atlantic i.e. the Gulf of Mexico and the Mediterranean (FST 0.469, p < 0.001). In contrast, levels of mtDNA differentiation seen in the Pacific were much lower (FST 0.061, p < 0.001). Microsatellite differentiation was much less marked for all three oceans, consistent with tests indicating male-biased dispersal and gene flow. In addition to regional differentiation, significant differentiation was seen among social groups. However, the magnitude of this differentiation differed by ocean. Hierarchical mtDNA analyses showed that in the Pacific, 'social group' explained more variance than geographic region. In contrast, in the Indian Ocean, regions explained more variance than social group. In the Atlantic, the number of social groups within regions was too limited to make conclusions. Social group was the only level that explained significant variation in microsatellite allele frequencies in any ocean. Increased relatedness within social groups does not appear to explain the microsatellite differentiation. Instead, the likely explanation is different breeding males consorting with different female-dominated social groups. mtDNA differentiation seen among social groups appears to be driven by ‘lenient matrilineality', where 38% of groups were strictly matrilineal, and a further 25% of groups were comprised of more than one matriline, but fewer matrilines than expected by chance. However, the levels of matrilineality are too low to be consistent with the previously proposed hypothesis of a selective sweep linked with maternal cultural innovations as an explanation for low mtDNA diversity in the sperm whale. To examine alternative hypotheses for low mtDNA diversity, next-generation sequencing (454 and Illumina) was used to sequence mitogenomes for 17 Pacific Ocean sperm whale samples, with other cetacean mitogenomes compiled from the literature. Using these mitogenomes, no evidence of slow substitution rates were found in the mtDNA CR or protein-coding genes of the mitogenome that could explain the low diversity. In addition, the mtDNA CR had the highest diversity of the entire mitogenome and showed genealogical patterns concordant with the rest of the mitogenome. This discounts mtDNA CR-specific constraints as the cause of low mtDNA CR diversity. To investigate the remaining hypotheses of a selective sweep, population bottleneck or expansion, 8 nuclear loci (~12,000 bp) were sequenced for 22 sperm whales (Pacific and Gulf of Mexico), and compared to 10 New Zealand pygmy sperm whales (Kogia breviceps). The results were inconsistent with a selective sweep and showed instead low diversity across both mtDNA and nuclear DNA, in comparison to the higher levels of genetic diversity in the pygmy sperm whale and other cetacean species. Demographic reconstructions showed the sperm whale to have had a stable, but small, population size for much of historical time. This suggests a recent population expansion is responsible for the low mtDNA (and nuclear DNA) diversity in the sperm whale. The inferred timing of the expansion corresponds with expansions in squid species (the primary prey of the sperm whale), and explains shared mtDNA haplotypes between oceans. Since this expansion, the marked philopatry shown by female sperm whales at various hierarchical levels ranging from social groups (e.g. lenient matrilineality) to broader geographic scales, has led to maternally-mediated genetic drift driving striking differences in mtDNA haplotype frequencies between social groups, regions, and oceans.
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