Do beluga whales truly migrate? Testing a key trait of the classical migration syndrome.

BACKGROUND: Migration enables organisms to access resources in separate regions that have predictable but asynchronous spatiotemporal variability in habitat quality. The classical migration syndrome is defined by key traits including directionally persistent long-distance movements during which maintenance activities are suppressed. But recently, seasonal round-trip movements have frequently been considered to constitute migration irrespective of the traits required to meet this movement type, conflating common outcomes with common traits required for a mechanistic understanding of long-distance movements. We aimed to test whether a cetacean ceases foraging during so-called migratory movements, conforming to a trait that defines classical migration. METHODS: We used location and dive data collected by satellite tags deployed on beluga whales (Delphinapterus leucas) from the Eastern Beaufort Sea population, which undertake long-distance directed movements between summer and winter areas. To identify phases of directionally persistent travel, behavioural states (area-restricted search, ARS; or Transit) were decoded using a hidden-Markov model, based on step length and turning angle. Established dive profiles were then used as a proxy for foraging, to test the hypothesis that belugas cease foraging during these long-distance transiting movements, i.e., they suppress maintenance activities. RESULTS: Belugas principally made directed horizontal movements when moving between summer and winter residency areas, remaining in a Transit state for an average of 75.4% (range = 58.5-87.2%) of the time. All individuals, however, exhibited persistent foraging during Transit movements (75.8% of hours decoded as the Transit state had ≥ 1 foraging dive). These data indicate that belugas actively search for and/or respond to resources during these long-distance movements that are typically called a migration. CONCLUSIONS: The long-distance movements of belugas do not conform to the traits defining the classical migration syndrome, but instead have characteristics of both migratory and nomadic behaviour, which may prove adaptive in the face of unpredictable environmental change. Such patterns are likely present in other cetaceans that have been labeled as migratory. Examination of not only horizontal movement state, but also the vertical behaviour of aquatic animals during directed movements is essential for identifying whether a species exhibits traits of the classical migration syndrome or another long-distance movement strategy, enabling improved ecological inference.

Comparative embryology of Delphinapterus leucas (beluga whale), Balaena mysticetus (bowhead whale), and Stenella attenuata (pan-tropical spotted dolphin) (Cetacea: Mammalia).

Embryogenesis of cetaceans (whales, dolphins, porpoises) is best known in Stenella attenuata, the pan-tropical spotted dolphin, based on a remarkably complete and well-studied prenatal ontogenetic series. Our study expands understanding of cetacean embryology by adding two additional cetacean taxa: the beluga whale (Delphinapterus leucas, Odontoceti), and the bowhead whale (Balaena mysticetus, Mysticeti). We identify key features that characterize these taxa at specific stages and highlight heterochrony between the odontocetes and mysticetes. The toothed whales are more similar in developmental timing to each other than either is to Balaena. The two odontocete taxa, Stenella and Delphinapterus, share similar developmental trajectories while early Balaena specimens differ from the odontocetes. This developmental variation proves challenging to ascribe to the existing Carnegie staging system. Most notably, flippers, hindlimbs, and flukes all provide morphological traits for characterization within the Carnegie staging system. A presomitic Delphinapterus embryo is also described. This study applies the Carnegie staging system to two more cetacean taxa and forms a framework for future research on cetacean developmental genetics and the modeling of fetal growth.

Origin and expansion of the world's most widespread pinniped: Range-wide population genomics of the harbour seal (Phoca vitulina).

The harbour seal (Phoca vitulina) is the most widely distributed pinniped, occupying a wide variety of habitats and climatic zones across the Northern Hemisphere. Intriguingly, the harbour seal is also one of the most philopatric seals, raising questions as to how it colonized its current range. To shed light on the origin, remarkable range expansion, population structure and genetic diversity of this species, we used genotyping-by-sequencing to analyse ~13,500 biallelic single nucleotide polymorphisms from 286 individuals sampled from 22 localities across the species' range. Our results point to a Northeast Pacific origin of the harbour seal, colonization of the North Atlantic via the Canadian Arctic, and subsequent stepping-stone range expansions across the North Atlantic from North America to Europe, accompanied by a successive loss of genetic diversity. Our analyses further revealed a deep divergence between modern North Pacific and North Atlantic harbour seals, with finer-scale genetic structure at regional and local scales consistent with strong philopatry. The study provides new insights into the harbour seal's remarkable ability to colonize and adapt to a wide range of habitats. Furthermore, it has implications for current harbour seal subspecies delineations and highlights the need for international and national red lists and management plans to ensure the protection of genetically and demographically isolated populations.

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.

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.

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.

Crossing to safety: dispersal, colonization and mate choice in evolutionarily distinct populations of Steller sea lions, Eumetopias jubatus.

Population growth typically involves range expansion and establishment of new breeding sites, while the opposite occurs during declines. Although density dependence is widely invoked in theoretical studies of emigration and colonization in expanding populations, few empirical studies have documented the mechanisms. Still fewer have documented the direction and mechanisms of individual transfer in declining populations. Here, we screen large numbers of pups sampled on their natal rookeries for variation in mtDNA (n = 1106) and 16 microsatellite loci (n = 588) and show that new Steller sea lion breeding sites did not follow the typical paradigm and were instead colonized by sea lions from both a declining (Endangered) population and an increasing population. Dispersing individuals colonized rookeries in the distributional hiatus between two evolutionarily distinct (Φ¯(st) = 0.222, R¯(st) = 0.053, K = 2) metapopulations recently described as separate subspecies. Hardy-Weinberg, mixed-stock and relatedness analysis revealed levels of interbreeding on the new rookeries that exclude (i) assortative mating among eastern and western forms, and (ii) inbreeding avoidance as primary motivations for dispersal. Positive and negative density dependence is implicated in both cases of individual transfer. Migration distance limits, and conspecific attraction and performance likely influenced the sequence of rookery colonizations. This study demonstrates that resource limitation may trigger an exodus of breeding animals from declining populations, with substantial impacts on distribution and patterns of genetic variation. It also revealed that this event is rare because colonists dispersed across an evolutionary boundary, suggesting that the causative factors behind recent declines are unusual or of larger magnitude than normally occur.

Lacaziosis in bottlenose dolphins Tursiops truncatus along the coastal Atlantic Ocean, Florida, USA.

This study represents the first systematic study of lacaziosis (lobomycosis) in bottlenose dolphins Tursiops truncatus in the Atlantic Ocean along the east-central coast of Florida, USA. Lacaziosis is a chronic infection of the skin caused by the fungus Lacazia loboi, which affects only dolphins and humans. Previous studies have shown a high prevalence (6.8 to 12.0%) of lacaziosis in resident dolphins from the adjacent Indian River Lagoon Estuary (IRL), where the disease is endemic. We examined the prevalence of lacaziosis in this coastal area using photo-identification data collected between 2002 and 2008 to determine the prevalence of lacaziosis in coastal dolphins using photographic methodology shown to have high sensitivity and specificity in prior research. The prevalence of skin lesions compatible with lacaziosis estimated from photographic data was 2.1% (6/284), approximately 3 times lower than that described for the estuarine population using similar methods. To exclude potential bias introduced by differences in study duration and survey effort among areas, an 18 mo period when effort was most equal (January 2006 to June 2007) was chosen for statistical comparison. The prevalence of lacaziosis estimated from photographic data was significantly lower (3.8%: n = 6/160) in the Atlantic Ocean compared to the IRL (12.0%: n = 20/167) (risk ratio = 3.19, 95% CI 1.32 to 7.75, p < 0.01 by chi-square analysis). The lower prevalence of lacaziosis in dolphins found in the Atlantic Ocean and the overall lack of movement of dolphins between these habitats suggests that environmental conditions within the estuary may favor viability of L. loboi, and/or that immune compromise in resident estuarine dolphins is a precursor to the disease.