Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation

Beluga whales ( Delphinapterus leucas ) in North American waters migrate seasonally between wintering areas in broken pack ice and summering locations in estuaries and other open water areas in the Arctic and sub-Arctic. Results from our previous investigation of beluga whale mitochondrial DNA (mtDNA) revealed genetic heterogeneity among beluga from different summering locations that was interpreted as representing a high degree of summering site philopatry. However, mtDNA is maternally inherited and does not reflect mating that may occur among beluga from different summering locations in wintering areas or during annual migrations. To test the possibility that breeding occurs among beluga from different summering locations, genetic variability at five nuclear DNA (nDNA) microsatellite loci was examined in the same animals tested in the mtDNA study. Beluga samples ( n = 640) were collected between 1984 and 1994 from 24 sites across North America, mostly during the summer. Whales from the various sites were categorized into eight summering locations as identified by mtDNA analysis, as well as four hypothesized wintering areas: Bering Sea, Hudson Strait (Hudson Strait, Labrador Sea, southwest Davis Strait), Baffin Bay (North Water, east Davis Strait), and St Lawrence River. Microsatellite allele frequencies indicated genetic homogeneity among animals from summering sites believed to winter together but differentiation among whales from some of the wintering areas. In particular, beluga from western North America (Bering Sea) were clearly distinguished from beluga from eastern North America (Hudson Strait, Baffin Bay, and St Lawrence River). Based upon the combined data set, the population of North American beluga whales was divided into two evolutionarily significant units. However, the population may be further subdivided into management units to reflect distinct groups of beluga at summering locations.     

Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation

Beluga whales ( Delphinapterus leucas ) in North American waters migrate seasonally between wintering areas in broken pack ice and summering locations in estuaries and other open water areas in the Arctic and sub-Arctic. Results from our previous investigation of beluga whale mitochondrial DNA (mtDNA) revealed genetic heterogeneity among beluga from different summering locations that was interpreted as representing a high degree of summering site philopatry. However, mtDNA is maternally inherited and does not reflect mating that may occur among beluga from different summering locations in wintering areas or during annual migrations. To test the possibility that breeding occurs among beluga from different summering locations, genetic variability at five nuclear DNA (nDNA) microsatellite loci was examined in the same animals tested in the mtDNA study. Beluga samples ( n = 640) were collected between 1984 and 1994 from 24 sites across North America, mostly during the summer. Whales from the various sites were categorized into eight summering locations as identified by mtDNA analysis, as well as four hypothesized wintering areas: Bering Sea, Hudson Strait (Hudson Strait, Labrador Sea, southwest Davis Strait), Baffin Bay (North Water, east Davis Strait), and St Lawrence River. Microsatellite allele frequencies indicated genetic homogeneity among animals from summering sites believed to winter together but differentiation among whales from some of the wintering areas. In particular, beluga from western North America (Bering Sea) were clearly distinguished from beluga from eastern North America (Hudson Strait, Baffin Bay, and St Lawrence River). Based upon the combined data set, the population of North American beluga whales was divided into two evolutionarily significant units. However, the population may be further subdivided into management units to reflect distinct groups of beluga at summering locations.     

Sequence variation at the major histocompatibility complex DRB loci in beluga (Delphinapterus leucas) and narwhal (Monodon monoceros)

 The variation at loci with similarity to DRB class II major histocompatibility complex loci was assessed in 313 beluga collected from 13 sampling locations across North America, and 11 narwhal collected in the Canadian high Arctic. Variation was assessed by amplification of exon 2, which codes for the peptide binding region, via the polymerase chain reaction, followed by either cloning and DNA sequencing or single-stranded conformation polymorphism analysis. Two DRB loci were identified in beluga: DRB1, a polymorphic locus, and, DRB2, a monomorphic locus. Eight alleles representing five distinct lineages (based on sequence similarity) were found at the beluga DRB1 locus. Although the relative number of alleles is low when compared with terrestrial mammals, the amino acid variation found among the lineages is moderate. At the DRB1 locus, the average number of nonsynonymous substitutions per site is greater than the average number of synonymous substitutions per site (0.0806 : 0.0207, respectively;P<0.01). Most of the 31 amino acid substitutions do not conserve the physiochemical properties of the residue, and 21 of these are located at positions implicated as forming pockets responsible for the selective binding of foreign peptide side chains. Only DRB1 variation was examined in 11 narwhal, revealing a low amount of variation. These data are consistent with an important role for the DRB1 locus in the cellular immune response of beluga. In addition, the ratio of nonsynonymous to synonymous substitutions is similar to that among primate alleles, arguing against a reduction in the balancing selection pressure in the marine environment. Two hypotheses may explain the modest amount of Mhc variation when compared with terrestrial mammals: small population sizes at speciation or a reduced neutral substitution rate in cetaceans. Received: 15 July 1997 / Revised: 24 March 1998     

Mating ecology of beluga (Delphinapterus leucas) and narwhal (Monodon monoceros) as estimated by reproductive tract metrics

Narwhal and beluga whales are important species to Arctic ecosystems, including subsistence hunting by Inuit, and little is understood about their mating ecology. Reproductive tract metrics vary across species in relation to mating strategy, and have been used to infer mating ecology. Reproductive tracts from beluga and narwhal were collected between 1997 and 2008 from five beluga stocks and two narwhal stocks across the Canadian Arctic. Tract length for males and females, relative testes mass for males, and tusk length for male narwhal were measured. We assessed variation relative to species, body size, stock, maturity, and season. Significant variation was found in testes mass across month and stock for beluga, and no significant difference between stock or date of harvest for narwhal. Beluga had significantly larger testes relative to body size than narwhal, suggesting they were more promiscuous than narwhal. A significant relationship was found between narwhal tusk length and testes mass, indicating the tusk may be important in female mate choice. No significant differences were found between narwhal and beluga reproductive tract length for males or females. The mating systems suggested for narwhal and belugas by our results mean the two species may respond differently to climate change.     

Bone fluoride concentrations in beluga whales from Canada

Beluga whales (Delphinapterus leucas) from the St. Lawrence Estuary have been reported to have dental and bone abnormalities. To determine whether these lesions could be caused by high exposure to fluorides, we measured bone fluoride levels in eight beluga whales stranded on the shores of the St. Lawrence Estuary (Quebec, Canada), and in nine beluga whales killed by Inuit hunters in the Hudson Bay (North Western Territories, Canada). In both groups, fluoride concentrations were higher than those found in terrestrial mammals intoxicated by fluorides. Unexpectedly, fluoride concentration was significantly higher in beluga whales from the Hudson Bay (mean +/- SD: 10.365 +/- 1.098 ppm) than in beluga whales from the St. Lawrence Estuary (4.539 +/- 875 ppm) and was positively correlated with age in the latter population. Differences in diet might explain the differences in fluoride concentrations found between these two populations.     

A genetic analysis of the beluga whale Delphinapterus leucas (Cetacea: Monodontidae) from summer aggregations in the Russian Far East

The genetic structure of four summer aggregations of the Beluga Whale, Delphinapterus leucas, in Sakhalin Bay and Udskaya Bay, off the western coast of Kamchatka in the Sea of Okhotsk and in the Anadyr Estuary of the Bering Sea was analyzed through nucleotide sequencing of the mtDNA control region and detection of the allelic composition of nine microsatellite loci in nuclear DNA. It has been shown that each of the aggregations features a unique set of maternal lines, which indicates a high degree of philopatry in this species. Beluga whales of the Anadyr Estuary are genetically isolated from those of the Sea of Okhotsk. Beluga whales of the summer aggregations of Sakhalin Bay and those from Udskaya Bay share a common gene pool and belong to a single population, while the whales that summer off western Kamchatka with great consistency may be attributed to a different population. Comparison of nucleotide sequences of the mtDNA in beluga whales from various waters of the Russian Far East and North America allowed us to propose a hypothesis about how the structure of beluga whale populations formed in the North Pacific during the postglacial period.     

Matriarchal genetic population structure of North American beluga whales Delphinapterus leucas (Cetacea: Monodontidae)

The North American beluga whale Delphinapterus leucas population has been divided into a number of putative geographical stocks based upon migration routes and areas of summer concentration. Nucleotide sequences of the mitochondrial DNA (mtDNA) control region were used to assess whether these geographical stocks are genetically distinct. Beluga whale samples from 25 sites were collected primarily from aboriginal subsistence hunts across North America from 1984 to 1994. Thirty-nine mtDNA haplotypes were identified in 628 beluga samples. No differences were found in the distribution of haplotypes between male and female beluga whales at any sampling site. These haplotypes segregated into two distinct assemblages in both a haplotype network and a neighbour-joining tree. The haplotype assemblages had a geographically disjunct distribution that suggests postglacial recolonization of the North American Arctic from two different refugia.
An analysis of molecular variance based on haplotype relationships and frequency indicated genetic heterogeneity among beluga whale summering groups ( P ≤ 0.001). Sequence divergence estimates between sampling sites also indicated geographical differentiation, particularly between samples taken at east Hudson Bay or St Lawrence River and the western or central Arctic. The results of this study show a high degree of philopatry to specific summering areas by this highly mobile animal.     

Allelic and haplotype variation of major histocompatibility complex class II DRB1 and DQB loci in the St Lawrence beluga (Delphinapterus leucas)

In order to assess levels of major histocompatibility complex (Mhc) variation within the St Lawrence beluga (Delphinapterus leucas) the variation at the beluga Mhc DRB1 class II locus was assessed by single-strand conformation polymorphism (SSCP) analysis of the peptide-binding region for 313 whales collected from 13 sampling locations across North America. In addition, samples from west Greenland and the St Lawrence were also typed at the DQB locus, allowing comparison to a previous study and assessment of linkage disequilibrium of alleles at the two loci. Comparisons of DRB1 and DQB allele frequencies among all sampling locations indicated genetic structure (α < 0.005). Most of this structure resulted from differences between the different wintering groups. Significant genetic structure (α = 0.05) exists among each pair of the following groups at both the DRB1 and DQB loci; St Lawrence, Hudson Strait, Bering Sea, Cunningham Inlet, and Davis Strait (minus Cunningham Inlet), except the St Lawrence and Hudson Strait for the DQB locus. In the St Lawrence population, six of the eight DRB1 alleles are present representing all five known allelic lineages. Evidence of linkage disequilibrium between the DRB1 and DQB is present in two sampling locations, the St Lawrence and Nuussuaq (α = 0.05). Analysis of probable DRB1–DQB haplotypes among groups of beluga suggests a haplotype reduction in the St Lawrence.     

Age structure, growth, mortality, and density of belugas (Delphinapterus leucas) in the Canadian Arctic: responses to environment?

Environmental constraints on life-history traits are expected to increase with seasonality in resources such as food and appropriate breeding habitat. Seasonality is highest at polar latitudes, where environmental constraints can be stronger than biotic factors, such as density and its effect on intraspecific competition. In this study, the age structure, body-length distribution, mortality, and density were studied and compared among five beluga populations of the Canadian Arctic: eastern Beaufort Sea (EBS), Baffin Bay (BB), Cumberland Sound (CS), western (WHB), and eastern Hudson (EHB) Bay, to test the prediction that density-dependent effects on these life-history traits should be inversely related to latitude. Growth, but not mortality, showed a significant positive relationship with latitude. Winter density also increased with winter latitude, consistent with the prediction of greater risk of mortality associated with density-independent effects, such as ice entrapment in winter. Age distributions differed among populations, with animals harvested at the highest-latitude population (EBS) being the oldest and attaining the longest adult body lengths, compared to lower-latitude populations (WHB and EHB). The latitudinal variation in growth, adult body size, and winter density is congruent with the hypothesis that environmental seasonality may impose stronger constraints on life-history traits of beluga with increasing latitude.     

Larger body size leads to greater female beluga whale ovarian reproductive activity at the southern periphery of their range

Identification of phenotypic characteristics in reproductively successful individuals provides important insights into the evolutionary processes that cause range shifts due to environmental change. Female beluga whales (Delphinapterus leucas) from the Baffin Bay region (BB) of the Canadian Arctic in the core area of the species’ geographic range have larger body size than their conspecifics at the southern range periphery in Hudson Bay (HB). We investigated the mechanism for this north and south divergence as it relates to ovarian reproductive activity (ORA = total corpora) that combines morphometric data with ovarian corpora counted from female reproductive tracts. Our study aim was to assess the relative influence of age and body size of female beluga whale on ORA in the two populations. Female beluga whale ORA increased more quickly with age (63% partial variation explained) in BB than in HB (41%). In contrast, body length in HB female beluga whales accounted for considerably more of the total variation (12% vs. 1%) in ORA compared to BB whales. We speculate that female HB beluga whale ORA was more strongly linked with body length due to higher population density resulting in food competition that favors the energetic advantages of larger body size during seasonal food limitations. Understanding the evolutionary mechanism of how ORA varies across a species’ range will assist conservation efforts in anticipating and mitigating future challenges associated with a warming planet.     

Population-specific home ranges and migration timing of Pacific Arctic beluga whales (Delphinapterus leucas)

Two populations of beluga whales (Delphinapterus leucas), the Eastern Beaufort Sea (BS) and Eastern Chukchi Sea (ECS), make extensive seasonal migrations into the Pacific Arctic. However, the extent to which these populations overlap in time and space is not known. We quantified distribution and migration patterns for BS and ECS belugas using daily locations from whales tracked with satellite-linked transmitters. Home ranges and core areas in summer (July and August) and in each month (July–November), daily displacement, dispersal from core areas, and autumn migration timing were estimated. Distinct summer and fall distribution patterns and staggered autumn migration timing were identified for BS and ECS whales. Summer home ranges for each population had less than 10 % overlap. Monthly home ranges were also relatively distinct between populations except in September (up to 88 % home range overlap). A distinct east–west shift in focal area use occurred in September that persisted into October, with the two populations essentially switching longitudinal positions. Highest daily displacements occurred during the migratory period in September for BS whales and October for ECS whales, further indicating westward fall migration was offset between populations. Sexual segregation of males and females within a population also varied monthly. Autumn migration timing as well as differences in spatial and temporal segregation between BS and ECS beluga populations may be a result of maternally driven philopatry and population-specific adaptations to dynamically available resources. Our results contribute to the management of these populations by identifying seasonal area use and differences in migration patterns.     

Beluga whale ecology: a concern of freshwater biologists?

SUMMARY. 1. Churchill estuary beluga whales displayed their highest densities in freshwater habitat, suggesting preferential use.
2. Whale densities in freshwater were as high as 350 animals km⁻² and represented over one tenth of the estimated Hudson Bay population.
3. Future environmental assessments of hydroelectric development in northern Manitoba, Canada, must consider the effects on the beluga whales.     

Population genetic structure and evolutionary history of North Atlantic beluga whales (Delphinapterus leucas) from West Greenland, Svalbard and the White Sea

Population structure in many Arctic marine mammal species reflects a dynamic interplay between physical isolating mechanisms and the extent to which dispersal opportunities are met. We examined variation within mtDNA and eight microsatellite markers to investigate population structure and demographic history in beluga whales in the North Atlantic. Genetic heterogeneity was observed between Svalbard and West Greenland that reveals limited gene flow over ecological time scales. Differentiation was also recorded between Atlantic belugas and two previously studied populations in the North Pacific, the Beaufort Sea and Gulf of Alaska. However, Bayesian cluster analysis of the nDNA data identified two population clusters that did not correspond to the respective ocean basins, as predicted, but to: (1) Arctic (Svalbard–White Sea–Greenland–Beaufort Sea) and (2) Subarctic (Gulf of Alaska) regions. Similarly, the deepest phylogeographic signal was between the Arctic populations and the Gulf of Alaska. Fitting an isolation-with-migration model yielded genetic abundance estimates that match census estimates and revealed that Svalbard and the Beaufort Sea likely diverged 7,600–35,400 years ago but have experienced recurrent periods with gene flow since then, most likely via the Russian Arctic during subsequent warm periods. Considering current projections of continued sea ice losses in the Arctic, this study identified likely routes of future contact among extant beluga populations, and other mobile marine species, which have implications for genetic introgression, health, ecology and behavior.     

Winter distribution and migrations of beluga whales (<Emphasis Type="Italic">Delphinapterus leucas</Emphasis>) in the White Sea based on satellite tracking data

Based on satellite tracking of eight beluga whale males in the White Sea, their habitats in the autumn, winter, and spring periods have been identified. A correlation between the distribution of beluga whales, ice dynamics, and migration of Atlantic salmon has been revealed. It has been found than beluga whale males do not leave the White Sea during the entire ice period. The results obtained confirm the hypothesis that the White Sea population of beluga whales is isolated.     

Killer whale (Orcinus orca) predation in a multi-prey system

Predation can regulate prey numbers but predator behaviour in multiple-prey systems can complicate understanding of control mechanisms. We investigate killer whale (Orcinus orca) predation in an ocean system where multiple marine mammal prey coexist. Using stochastic models with Monte-Carlo simulations, we test the most likely outcome of predator selection and compare scenarios where killer whales: (1) focus predation on larger prey which presumably offer more energy per effort, (2) generalize by feeding on prey as encountered during searches, or (3) follow a mixed foraging strategy based on a combination of encounter rate and prey size selection. We test alternative relationships within the Hudson Bay geographic region, where evidence suggests killer whales seasonally concentrate feeding activities on the large-bodied bowhead whale (Balaena mysticetus). However, model results indicate that killer whales do not show strong prey specialization and instead alternatively feed on narwhal (Monodon monoceros) and beluga (Delphinapterus leucas) whales early and late in the ice-free season. Evidence does support the conjecture that during the peak of the open water season, killer whale predation can differ regionally and feeding techniques can focus on bowhead whale prey. The mixed foraging strategy used by killer whales includes seasonal predator specialization and has management and conservation significance since killer whale predation may not be constrained by a regulatory functional response.     

Summer diet of beluga whales inferred by fatty acid analysis of the eastern Beaufort Sea food web

Beluga whales (Delphinapterus leucas) are the most abundant odontocetes in Arctic waters and are thus thought to influence food web structure and function. The diet of the Beaufort Sea beluga population is not well known, partly due to the inherent difficulty of observing feeding behaviour in Arctic marine cetaceans. To determine which prey items are critical to the Beaufort Sea beluga diet we first examine and describe the Mackenzie Delta and Beaufort Sea food web using fatty acid analyses. Fatty acid profiles effectively partitioned prey items into groups associated with their habitat and feeding ecology. Next, the relative contribution of various prey items to beluga diet was investigated using fatty acids. Finally, beluga diet variability was examined as a function of body size, a known correlate of habitat use. Beluga appeared to feed predominantly on Arctic cod (Boreogadus saida) collected from near shore and offshore regions. Size related dietary differences suggested larger sized beluga preferred offshore Arctic cod given the shared high levels of long chain monounsaturates, whereas smaller sized beluga appeared to feed on prey in their near shore habitats that included near shore Arctic cod. The presence of Arctic cod groups in shallow near shore and deep offshore habitats may facilitate the behavioural segregation of beluga habitat use as it relates to their size and resource requirements. Given Arctic cod are a sea ice associated fish combined with the accelerated sea ice loss in this region, beluga whales may need to adapt to new dietary regimes.     

Distribution of beluga whales (Delphinapterus leucas) in the Russian Arctic seas according to the results of expedition aboard RV Mikhail Somov, September–November 2010

Data on the distribution of marine mammals, including beluga whales (Delphinapterus leucas Pallas, 1766), in the Arctic are scarce because of various causes and conditions, including the vast expanses of the region, its poor accessibility, severe climate, long polar night, and high cost of research. Nevertheless, the results of aerial observations during ice reconnaissance and onboard observations during sea voyages (Kleinenberg et al., 1964; Geptner et al., 1976; Belikov, Boltunov, and Gorbunov, 2002; Belikov and Boltunov, 2002; Ezhov, 2005; Matishov and Ognetov, 2006; Biologiya i okeanografiya??, 2007; Lukin and Ognetov, 2009) have provided a general idea of the distribution pattern of beluga whales in the Russian Arctic seas. More detailed data concern the distribution of these whales in the White Sea, where aerial surveys of the water area were performed previously and have been resumed in recent years (Nazarenko et al., 2008; Glazov et al., 2010, 2011). The relevant data on the Barents, Kara, Laptev, and East Siberian seas are much poorer. In the summer (ice-free) period, beluga whales concentrate in coastal waters. They have been recorded most frequently off Franz Josef Land, Novaya Zemlya, Vaygach Island, and in Czech Bay in the Barents Sea; in Baydaratskaya Bay, Gulf of Ob, and Yenisei Gulf in the Kara Sea; off the northeastern coast of Taimyr and in estuaries of the Anabar, Olenyok, and Lena rivers in the Laptev Sea; and in the estuaries of the Indigirka (where the whales come from the west) and the Kolyma and Ked??ma rivers (where they come from the east) in the East Siberian Sea. The amount of information obtained in other seasons is very limited. In autumn, mass migration of beluga whales from the Kara Sea to the Barents Sea have been recorded in the Karskie Vorota Strait and off Cape Zhelaniya in the north of Novaya Zemlya. In winter, almost no records of these whales have been made in the Kara, Laptev, and East Siberian seas. These data are based on previous observations and have practically not been complemented in recent years.     

Biomarkers of DNA damage in marine mammals.

Certain environmental contaminants found in marine mammals have been shown to cause DNA damage and cancer. The micronuclei (MN), sister chromatid exchange (SCE) and/or chromosome aberration (CA) assays were used to assess baseline (spontaneous) levels of DNA damage in blood lymphocytes of individuals of the relatively healthy and lightly contaminated Arctic beluga whale (Delphinapterus leucas), Sarasota Bay, FL, bottlenose dolphin (Tursiops truncatus) and Northwestern Atlantic grey (Halichoerus grypus) and harp (Phoca groenlandicus) seal populations. MN cell (MNC) frequencies ranged between 2 and 14/1000 binucleated (BN) cells and were statistically similar between species. In bottlenose dolphins, MNC frequency was correlated with age and was significantly higher in females than in males. No intraspecific variation in MNC frequency was found in beluga whales. Intraspecific variation was not tested in seals due to the small sample size. Frequencies of SCEs and total CAs, excluding gaps, ranged, respectively, between 1 and 15 SCE(s)/per cell and 4-6 CAs/100 cells in beluga whales. SCE and CA frequencies did not vary with age or sex in beluga whales. The MN, SCE and CA assays were found to be practical tools for the detection of DNA damage in marine mammals and could be used in the future to compare DNA damage between relatively lightly and highly contaminated populations.     

Sequence variation and gene duplication at MHC DQB loci of baiji (Lipotes vexillifer), a Chinese river dolphin

The major histocompatibility complex (MHC) is a fundamental part of the vertebrate immune system, and the high variability in many MHC genes is thought to play an important role in the recognition of parasites. Baiji (Lipotes vexillifer) is one of the most endangered species in the world. Its wild population has declined to fewer than 100 individuals and has a very high risk of becoming extinct in the near future. In this study we present a first step in the molecular characterization of a DQB-like locus of baiji by nucleotide sequence analysis of the polymorphic exon 2 segments. In the examined 172 bp sequences from a group of 18 incidentally captured or stranded individuals, 48 variable sites were determined and 43 alleles were identified, many of which were represented by only one clone. Three to seven alleles were found in each individual, suggesting gene duplications. No deletion, insertion, or exceptional stop codon was detected, suggesting these alleles function in vivo. Phylogenetic reconstruction using neighbor joining grouped the 43 alleles into two distinct lineages, differing by seven nucleotides and four amino acids. Substitutions of amino acids tend to be clustered around sites postulated to be responsible for selective peptide recognition. In the peptide-binding region (PBR) of the DQB locus, the average number of nonsynonymous substitutions per site is greater than that of synonymous substitutions per site (0.1962 versus 0.0256, respectively). Nucleotide and amino acid sequences both showed a relatively high level of similarity (nucleotides 90.6%; amino acids 80.6%) to those of beluga whale (Delphinapterus leucas) and narwhal (Monodon monoceros). The high level of baiji MHC polymorphism revealed in the present study has not been reported in other cetaceans and could be a consequence of the small baiji population adapting to freshwater with a relatively high level of pathogens.