Group structure and kinship in beluga whale societies.

Evolutionary explanations for mammalian sociality typically center on inclusive-fitness benefits of associating and cooperating with close kin, or close maternal kin as in some whale societies, including killer and sperm whales. Their matrilineal structure has strongly influenced the thinking about social structure in less well-studied cetaceans, including beluga whales. In a cross-sectional study of group structure and kinship we found that belugas formed a limited number of distinct group types, consistently observed across populations and habitats. Certain behaviours were associated with group type, but group membership was often dynamic. MtDNA-microsatellite profiling combined with relatedness and network analysis revealed, contrary to predictions, that most social groupings were not predominantly organized around close maternal relatives. They comprised both kin and non-kin, many group members were paternal rather than maternal relatives, and unrelated adult males often traveled together. The evolutionary mechanisms that shape beluga societies are likely complex; fitness benefits may be achieved through reciprocity, mutualism and kin selection. At the largest scales these societies are communities comprising all ages and both sexes where multiple social learning pathways involving kin and non-kin can foster the emergence of cultures. We explore the implications of these findings for species management and the evolution of menopause.

Persistent Mü̈llerian duct syndrome in a beluga whale Delphinapterus leucas.

This case study describes a persistent Mü̈llerian duct syndrome (PMDS), a rare form of XY disorder of sex development (DSD), in a mature (>15 yr) beluga whale Delphinapterus leucas. The phenotypically and genetically male beluga whale had both Mü̈llerian (paramesonephric) and Wolffian (mesonephric) duct derivatives. A mild hydrometra was present. Gross and histological analyses indicated the testes were atrophied. Histopathologic findings in the testes also included fibrosis in addition to ductus deferens ductular dilation, epididymal ductular dilation, lymphoplasmacytic balanitis, uterine glandular atrophy, and endometrial fibrosis. DSDs are rarely reported in cetaceans, and PMDS has never been described in a cetacean.

Positive selection in coding regions and motif duplication in regulatory regions of bottlenose dolphin MHC class II genes.

The vertebrate immune response is mediated through highly adaptive, quickly evolving cell surface receptors, the major histocompatibility complex (MHC). MHC molecules bind and present a diverse array of pathogenic molecules and trigger a cascade of defenses. Use of MHC variation as a marker for population health has also evolved quickly following advances in sequencing methods. We applied a combination of traditional and next generation sequencing methodology to characterize coding (peptide binding region) and regulatory (proximal promoter) sequence variation in MHC Class II DQA and DQB genes between estuarine and coastal populations of the bottlenose dolphin, Tursiops truncatus, an apex predator whose health status is indicative of anthropogenic impacts on the ecosystem. The coding regions had 10 alleles each at DQA and DQB; the promoters had 6 and 7 alleles at DQA and DQB, respectively with variation within key regulatory motifs. Positive selection was observed for the coding regions of both genes while both coding and promoter regions exhibited geographic differences in allele composition that likely indicates diversifying selection across habitats. Most notable was the discovery of a complete duplication of a 14-bp T-box motif in the DQA promoter. Four class II promoter regions (DQA, DQB, DRA, DRB) were characterized in species from four cetacean families (Delphinidae, Monodontidae, Lipotidae, and Physeteridae) and revealed substantial promoter structural diversity across this order. Peptide binding regions may not be the only source of adaptive potential within cetacean MHC for responding to pathogenic threats. These findings are the first analysis of cetacean MHC regulatory motifs, which may divulge unique immunogenetic strategies among cetaceans and reveal how MHC transcriptional control continues to evolve. The combined MHC regulatory and coding data provide new genetic context for distinct vulnerability profiles between coastal and estuarine populations, which are key concerns for health and risk management.

Bridging immunogenetics and immunoproteomics: Model positional scanning library analysis for Major Histocompatibility Complex class II DQ in Tursiops truncatus.

The Major Histocompatibility Complex (MHC) is a critical element in mounting an effective immune response in vertebrates against invading pathogens. Studies of MHC in wildlife populations have typically focused on assessing diversity within the peptide binding regions (PBR) of the MHC class II (MHC II) family, especially the DQ receptor genes. Such metrics of diversity, however, are of limited use to health risk assessment since functional analyses (where changes in the PBR are correlated to recognition/pathologies of known pathogen proteins), are difficult to conduct in wildlife species. Here we describe a means to predict the binding preferences of MHC proteins: We have developed a model positional scanning library analysis (MPSLA) by harnessing the power of mixture based combinatorial libraries to probe the peptide landscapes of distinct MHC II DQ proteins. The algorithm provided by NNAlign was employed to predict the binding affinities of sets of peptides generated for DQ proteins. These binding affinities were then used to retroactively construct a model Positional Scanning Library screen. To test the utility of the approach, a model screen was compared to physical combinatorial screens for human MHC II DP. Model library screens were generated for DQ proteins derived from sequence data from bottlenose dolphins from the Indian River Lagoon (IRL) and the Atlantic coast of Florida, and compared to screens of DQ proteins from Genbank for dolphin and three other cetaceans. To explore the peptide binding landscape for DQ proteins from the IRL, combinations of the amino acids identified as active were compiled into peptide sequence lists that were used to mine databases for representation in known proteins. The frequency of which peptide sequences predicted to bind the MHC protein are found in proteins from pathogens associated with marine mammals was found to be significant (p values <0.0001). Through this analysis, genetic variation in MHC (classes I and II) can now be associated with the binding repertoires of the expressed MHC proteins and subsequently used to identify target pathogens. This approach may be eventually applied to evaluate individual population and species risk for outbreaks of emerging diseases.

Migratory culture, population structure and stock identity in North Pacific beluga whales (Delphinapterus leucas).

The annual return of beluga whales, Delphinapterus leucas, to traditional seasonal locations across the Arctic may involve migratory culture, while the convergence of discrete summering aggregations on common wintering grounds may facilitate outbreeding. Natal philopatry and cultural inheritance, however, has been difficult to assess as earlier studies were of too short a duration, while genetic analyses of breeding patterns, especially across the beluga's Pacific range, have been hampered by inadequate sampling and sparse information on wintering areas. Using a much expanded sample and genetic marker set comprising 1,647 whales, spanning more than two decades and encompassing all major coastal summering aggregations in the Pacific Ocean, we found evolutionary-level divergence among three geographic regions: the Gulf of Alaska, the Bering-Chukchi-Beaufort Seas, and the Sea of Okhotsk (Φst = 0.11-0.32, Rst = 0.09-0.13), and likely demographic independence of (Fst-mtDNA = 0.02-0.66), and in many cases limited gene flow (Fst-nDNA = 0.0-0.02; K = 5-6) among, summering groups within regions. Assignment tests identified few immigrants within summering aggregations, linked migrating groups to specific summering areas, and found that some migratory corridors comprise whales from multiple subpopulations (PBAYES = 0.31:0.69). Further, dispersal is male-biased and substantial numbers of closely related whales congregate together at coastal summering areas. Stable patterns of heterogeneity between areas and consistently high proportions (~20%) of close kin (including parent-offspring) sampled up to 20 years apart within areas (G = 0.2-2.9, p>0.5) is the first direct evidence of natal philopatry to migration destinations in belugas. Using recent satellite telemetry findings on belugas we found that the spatial proximity of winter ranges has a greater influence on the degree of both individual and genetic exchange than summer ranges (rwinter-Fst-mtDNA = 0.9, rsummer-Fst-nDNA = 0.1). These findings indicate widespread natal philopatry to summering aggregation and entire migratory circuits, and provide compelling evidence that migratory culture and kinship helps maintain demographically discrete beluga stocks that can overlap in time and space.