- Humpback whales (Megaptera novaeangliae, Borowski 1781) in the North Pacific migrate from mid- to high- latitude summer feeding grounds along the Pacific Rim, including areas off the coasts of the U.S., Canada, Russia and eastern Asia, to tropical breeding grounds each winter along Pacific coasts of Mexico and Central America as well as the offshore islands of Mexico, Hawaii, and Japan. Humpback whales in the North Pacific and elsewhere were reduced to very low numbers during a period of intense commercial exploitation that ended in 1965. As the population recovers in abundance, the range of cultural and genetic diversity that survived the exploitation-driven bottleneck is able to adapt, endure and evolve. My work uses genetic tools and photo identification data to investigate the population dynamics, mitochondrial (mt) DNA control region evolution and potential drivers of a specialized feeding behavior in a recovering subpopulation of humpback whales in the Glacier Bay and Icy Strait (GBIS) sub-region of the southeastern Alaska (SEAK) feeding ground. I first collated and reconciled available DNA profiles (mtDNA control region, 10 microsatellite loci and sex) from 556 individuals using tissue samples collected from 1987 to 2012. Photo identification records associated with 692 of 1,026 total genetic samples collected in SEAK (now archived within the SEAK DNA Register and Tissue Database) corresponded to extensive life-history information, extending back to the early 1970s, as archived within the SEAK Regional Database, curated by the National Park Service (NPS) and University of Alaska, Southeast (UAS).
Changes in population structure in GBIS over 32 years (1973-2005) were investigated in order to determine whether the increase in local abundance was attributable to local fidelity and recruitment or immigration from outside of SEAK. Two temporal strata were defined: 'Founder' individuals identified between 1973-1985 (n = 74, n = 46 with DNA profiles) and 'Contemporary' individuals identified between 2004-2005 (n = 171, n = 114 with DNA profiles). There was no significant genetic differentiation between the strata, indicating that it is unlikely that the population increase within GBIS was due largely to immigration of whales from elsewhere in the North Pacific. However, two additional haplotypes were documented in the Contemporary stratum at low frequency, one of which was previously unreported in the North Pacific (haplotype A8, see below). This relative stability in haplotype frequencies over time argues for strong regional fidelity of the maternal lineages represented in GBIS between 1973 and 1985. After excluding the 42 Contemporary whales with no photo ID record of a mother or genotype available for maternity inference, at least 73.6% (n = 95) of the Contemporary stratum was either a returning Founder or a recruited descendant of a Founder female. Of all genetically confirmed females with genotypes in the Founder stratum, 96% (n = 24) were either represented in the Contemporary stratum, had at least one confirmed descendant in the Contemporary stratum, or both. This high proportion, in addition to the large proportion of the verifiable Contemporary stratum that were either returning Founders or a descendant of a Founder female, provides clear evidence for local fidelity and recruitment to GBIS.
The discovery of the A8 haplotype, which differs by one base pair from a common haplotype referred to as A-, represents an increase in mtDNA diversity for the North Pacific humpback whale from 28 to 29 haplotypes. To investigate the origin of this new haplotype, we re-evaluated n = 1089 electropherograms of n = 710 individuals with A- haplotypes from both the SEAK DNA Register and Tissue Database and the ocean-wide program, SPLASH (Baker et al. 2013). From this review, we identified two individuals with the A8 haplotype (a cow and calf, both sampled in GBIS) and n = 20 individuals with clear heteroplasmy for haplotypes A-/A8. The majority of A-/A8 individuals (n = 15) were sampled in SEAK. Genotype exclusion and likelihood were used to identify one of the heteroplasmic females, #196 (first sighted in SEAK in 1982), as the likely mother of the A8 cow and grandmother of the A8 calf, establishing the inheritance and germ-line fixation of the new haplotype from the parental heteroplasmy. Based on life history records and estimates of pairwise relatedness from microsatellite genotypes, it appears likely that the A-/A8 and the A8 individuals are descendants from a common maternal ancestor one or more generations prior to the three generations documented here.
Humpback whale sociality takes a distinct form in Icy Strait, where whales form large, coordinated groups with repeated membership across several decades. Twenty-one years of group association records (1985-2005, n = 2,204 groups) were used to investigate the hypothesis that kin selection influences membership in large, stable groups. Of the 2204 groups recorded, 113 consisted of 6 or more individuals; a size considered unexpectedly large assuming a Poisson distribution of group size with a mean of 1.7. A total of n = 71 individuals (n = 48 with DNA profiles) were encountered in a large group in at least one year, n = 38 individuals (n = 34 with DNA profiles) were encountered in a large group in at least two years, n = 29 individuals (n = 27 with DNA profiles) were encountered in a large group in at least three years, decreasing to n = 2 individuals (n = 2 with DNA profiles) that were encountered in a large group in at least 20 years. There were no significant differences in mtDNA frequencies between large group feeders and the Founder and Contemporary strata or when compared to whales never encountered in large groups in Icy Strait, indicating that group membership is not predominately passed through one maternal lineage. Sex ratios did not deviate significantly from 1:1 for those feeding in large groups over an increasing number of years, as would be expected if females were actively recruiting offspring into large groups. The average pairwise relatedness for large group feeders was not significantly greater than expected by chance and did not increase for those feeding in large groups over an increasing number of years. Of the 179 known offspring of females encountered in a large group, only 6% were also encountered in a large group in Icy Strait as an adult and only 2.2% in the same large group as their mother. These results indicate that kin selection is not the primary driver of membership in large, stable groups and pose an interesting dynamic in local habitat use: individuals are recruited to GBIS through local maternal fidelity but do not usually associate closely with direct maternal kin.
The extensive collection of DNA profiles now archived with the individual-based data within the SEAK Regional Database allowed us to integrate genetics and photo ID to answer ecologically relevant questions regarding the whales in GBIS. Together, these results demonstrate that GBIS provide habitat for a distinct collection of individuals that exhibit strong fidelity and local recruitment, some of which engage in a highly specialized feeding behavior. Further, GBIS is a local feeding habitat for two individuals with a newly arising North Pacific mtDNA haplotype. These findings reveal local genotypic and cultural variation and highlight the importance of habitat protection for species with fine-scale habitat use and strong fidelity to local migratory destinations.