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.     

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.     

Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucas in the western Nearctic revealed by mitochondrial DNA

The recent evolutionary history, population structure and movement patterns of beluga whales in the western Nearctic were inferred from an analysis of mitochondrial DNA control region sequence variation of 324 whales from 32 locations representing five summer concentration areas in Alaska and north-west Canada. Phylogenetic relationships among haplotypes were inferred from parsimonious networks, and genetic subdivision was examined using haplotypic frequency-based indices and an analysis of variance method modified for use with interhaplotypic distance data. MtDNA relationships were characterized by a series of star-like phylogenies which, when viewed in conjunction with information on haplotype frequency and distribution, suggested a rapid radiation of beluga whales into the western Nearctic following the Pleistocene, and an early divergence of the Beaufort Sea from the Chukchi and Bering Seas subpopulations. Overall nucleotide diversity was low (0.51%) yet all major summering concentrations were significantly differentiated (Φ_ST= 0.33) from one another. Stratification of samples by gender and age from the three northernmost subpopulations suggested that female cohorts from neighbouring subpopulations were more differentiated than males. Further stratification of adult animals by age revealed that older adults were substantially less subdivided among locations than younger adults, particularly for males, suggesting that dispersal, although limited, is biased toward older adult males. Overall, the patterns of mtDNA variation in beluga whales indicated that the summering concentrations are demographically, if not phyletically distinct. Population structure appears to be maintained primarily by natal homing behaviour, while asymmetries in dispersal may be associated with the type of mating system.     

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.     

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.     

Spatiotemporal segregation among summer stocks of beluga (Delphinapterus leucas) despite nuclear gene flow: implication for the endangered belugas in eastern Hudson Bay (Canada)

Migratory connectivity between areas frequented by wide-ranging animals provides crucial information for conservation and management. In and around Hudson Bay (Canada), three stocks of beluga whales (Delphinapterus leucas) are associated with distinct summering areas. We analyzed genetic variation at mtDNA and 13 microsatellite loci among individuals (N > 1400) harvested by 23 Inuit communities to identify mating units and assess temporal and spatial differences in the way stocks use common migratory pathways. Strong structure at mtDNA and a lack of convincing evidence for nuclear genetic differentiation indicate that both males and females adopt distinct migratory routes towards summering grounds while probably interbreeding on wintering grounds. Spatiotemporal variation in stock composition indicates that subsistence hunting targets all three stocks. While representing ca. 5% of belugas in Hudson Bay, the endangered Eastern Hudson Bay stock accounts for 17% of the overall subsistence harvest by Inuit communities of northern Nunavik (Quebec), and ca. 30% of the spring harvest along northeastern Hudson Bay. Despite interbreeding, cultural conservatism of maternally transmitted migration routes seems to prevent the re-establishment of stocks in previously frequented estuaries. This phenomenon supports the current use of demographic population models based on stock composition for developing behavior-based management strategies.     

Sequence variation at the major histocompatibility complex locus DQ beta in beluga whales (Delphinapterus leucas) [published erratum appears in Mol Biol Evol 1995 Nov;12(6):1174]

Genetic variation at the Major Histocompatibility Complex locus DQ beta was analyzed in 233 beluga whales (Delphinapterus leucas) from seven populations: St. Lawrence Estuary, eastern Beaufort Sea, eastern Chukchi Sea, western Hudson Bay, eastern Hudson Bay, southeastern Baffin Island, and High Arctic and in 12 narwhals (Monodon monoceros) sympatric with the High Arctic beluga population. Variation was assessed by amplification of the exon coding for the peptide binding region via the polymerase chain reaction, followed by either cloning and DNA sequencing or single-stranded conformation polymorphism analysis. Five alleles were found across the beluga populations and one in the narwhal. Pairwise comparisons of these alleles showed a 5:1 ratio of nonsynonymous to synonymous substitutions per site leading to eight amino acid differences, five of which were nonconservative substitutions, centered around positions previously shown to be important for peptide binding. Although the amount of allelic variation is low when compared with terrestrial mammals, the nature of the substitutions in the peptide binding sites indicates an important role for the DQ beta locus in the cellular immune response of beluga whales. Comparisons of allele frequencies among populations show the High Arctic population to be different (P < or = .005) from the other beluga populations surveyed. In these other populations an allele, Dele-DQ beta*0101-2, was found in 98% of the animals, while in the High Arctic it was found in only 52% of the animals. Two other alleles were found at high frequencies in the High Arctic population, one being very similar to the single allele found in narwhal.      

FEEDING, SOCIAL AND MIGRATION BEHAVIOR OF BOWHEAD WHALES, BALAENA MYSTICETUS, IN BAFFIN BAY VS. THE BEAUFORT SEA—REGIONS WITH DIFFERENT AMOUNTS OF HUMAN ACTIVITY

This paper compares the behavior of bowhead whales of the Davis Strait/Baffin Bay stock, as observed along the east coast of Baffin Island in 1979–1986, with behavior of the Bering/Chukchi/Beaufort Sea stock observed in the Beaufort Sea in 1980–1986. All data used here were collected during late summer and early autumn in the absence of acute human disturbance. The behavioral repertoires of the two populations were similar. However, quantitative differences were found for whales engaged in all three activities studied: (1) Bowheads feeding in deep water off Isabella Bay, Baffin Island, had longer dives and surfacings, on average, than noted for bowheads feeding in the Beaufort Sea. (2) Among whales socializing in shallow water, we saw sexual interactions more often at Isabella Bay than in the Beaufort Sea. Calls emitted by socializing whales off Baffin Island were similar to those heard in the Chukchi and Beaufort Seas. However, pulsed tonal calls were longer off Baffin Island, and previously undescribed mechanical "crunch" sounds were recorded there near socializing bowheads. (3) During autumn migration, "fluke-out" dives were less common, and dive durations were longer, in the Beaufort Sea than off Baffin Island (P<0.001). Multivariate and other analyses indicated that some but not all differences can be ascribed to regional differences in the natural environment or in whale activities, However, during 1974–1986, Bering/Chukchi/Beaufort bowheads were exposed to more industrial, hunting and other human activity than Davis Strait/Baffin Bay bowheads. The "inconspicuous" behavior during autumn migration in the Beaufort may have been attributable to human activities, but causative links cannot be isolated.     

Gene flow on ice: the role of sea ice and whaling in shaping Holarctic genetic diversity and population differentiation in bowhead whales (Balaena mysticetus)

Sea ice is believed to be a major factor shaping gene flow for polar marine organisms, but it remains unclear to what extent it represents a true barrier to dispersal for arctic cetaceans. Bowhead whales are highly adapted to polar sea ice and were targeted by commercial whalers throughout Arctic and subarctic seas for at least four centuries, resulting in severe reductions in most areas. Both changing ice conditions and reductions due to whaling may have affected geographic distribution and genetic diversity throughout their range, but little is known about range‐wide genetic structure or whether it differed in the past. This study represents the first examination of genetic diversity and differentiation across all five putative stocks, including Baffin Bay‐Davis Strait, Hudson Bay‐Foxe Basin, Bering‐Beaufort‐Chukchi, Okhotsk, and Spitsbergen. We also utilized ancient specimens from Prince Regent Inlet (PRI) in the Canadian Arctic and compared them with modern stocks. Results from analysis of molecular variance and demographic simulations are consistent with recent and high gene flow between Atlantic and Pacific stocks in the recent past. Significant genetic differences between ancient and modern populations suggest PRI harbored unique maternal lineages in the past that have been recently lost, possibly due to loss of habitat during the Little Ice Age and/or whaling. Unexpectedly, samples from this location show a closer genetic relationship with modern Pacific stocks than Atlantic, supporting high gene flow between the central Canadian Arctic and Beaufort Sea over the past millennium despite extremely heavy ice cover over much of this period.     

DISSOLVING STOCK DISCRETENESS WITH SATELLITE TRACKING: BOWHEAD WHALES IN BAFFIN BAY

Nine bowhead whales (Balaena mysticetus) were instrumented with satellite transmitters in West Greenland in May 2002 and 2003. Transmitters were either encased in steel cans or imbedded in floats attached to wires. Transmitters mounted in steel cans had a high initial failure rate, yet those that were successful provided tracking durations up to seven months. Float tags had a low initial failure rate and initially provided large numbers of positions; however, they had deployment durations of only 2–33 d. All tracked whales departed from West Greenland and headed northwest towards Lancaster Sound in the end of May. Three tags with long tracking durations (197–217 d) recorded movements of whales (1 ♂, 2 ♀) into December in 2002 and 2003. All of these individuals remained within the Canadian High Arctic or along the east coast of Baffin Island in summer and early fall. By the end of October, all three whales moved rapidly south along the east coast of Baffin Island and entered Hudson Strait, an apparent wintering ground for the population. One of the whales did not visit Isabella Bay on east Baffin Island, the locality used for abundance estimation from photographic reidentification of individuals. The movements of whales tagged in this study raise critical questions about the assumed stock discreteness of bowhead whales in Foxe Basin, Hudson Strait, and Davis Strait and indicate current estimates of abundance are negatively biased.     

Genetic variation of the St. Lawrence beluga whale population assessed by DNA fingerprinting

Recent surveys suggest that the endangered St. Lawrence beluga ( Delphinapterus leucas ) population is not recovering significantly despite 20 years of protection. Dead individuals that have been autopsied show high levels of tumours and infections. This situation could be a result of pollution, loss of genetic variation, inbreeding depression or a combination of these factors. Analyses of DNA fingerprints from St. Lawrence belugas with three minisatellite probes (Jeffreys 33.6, 33.15 and M13) indicate a reduced level of genetic variation compared to Beaufort Sea animals. The average band-sharing between individuals of the St. Lawrence beluga population for the three probes (0.534, 0.573 and 0.478, respectively) was significantly higher than that of the Beaufort Sea beluga population (0.343, 0.424, 0.314, respectively). Higher levels of mean allele frequency in the St. Lawrence belugas (0.33 vs. 0.21) suggest that this population is composed of individuals which are related. Inbreeding depression could therefore be a factor in the lack of recovery of the St. Lawrence beluga population.     

Panmictic population structure in the hooded seal (Cystophora cristata)

Two putative populations of hooded seals (Cystophora cristata) occur in the North Atlantic. The Greenland Sea population pup and breed on the pack ice near Jan Mayen ('West Ice') while the Northwest Atlantic population is thought to pup in the Davis Strait, in the Gulf of St. Lawrence (the 'Gulf'), and off southern Labrador or northeast Newfoundland (the 'Front'). We used microsatellite profiling of 300 individuals at 13 loci and mitochondrial DNA sequencing of the control region of 123 individuals to test for genetic differentiation between these four breeding herds. We found no significant genetic differences between breeding areas, nor evidence for cryptic nor higher level genetic structure in this species. The Greenland Sea breeding herd was genetically most distant from the Northwest Atlantic breeding areas; however, the differences were statistically nonsignificant. Our data therefore suggest that the world's hooded seals comprise a single panmictic genetic population.     

Preliminary analysis of mitochondrial DNA variation in a southern feeding group of eastern North Pacific gray whales

Although the majority of eastern North Pacific(ENP) gray whales migrate to feeding grounds inthe Bering and Chukchi Seas, some terminate themigration in more southerly areas such asBritish Columbia (BC). Long-term sightingstudies in Clayoquot Sound (CS), BC, indicatethat approximately 35–50 individuals exhibitlong-term fidelity to this site. To determinethe sex composition (based on genetic sexing)of CS gray whales and to assess whethermatrilineal site-fidelity occurs in CS, wecollected skin biopsy samples from 16 CSindividuals (`residents') and 41 samples fromother areas (representative of the overallpopulation in the ENP: `non-residents'). Atotal of 27 polymorphic sites defined 24haploytpes among the 57 samples sequenced forHV1 of the mtDNA control region. Thenucleotide and haplotype diversities of thesesamples were 0.017 (SE = 0.0012) and 0.94(SE = 0.0019), respectively. Neighbor-joininganalysis revealed five lineages each of whichcontained haplotypes that were observed in bothresidents and non-residents. Residents did notdiffer significantly from non-residents, and nosignificant sex-ratio bias was found. Thesedata suggest a level of diversity that isinconsistent with a severe historicalbottleneck, and given the available samplesize, do not indicate matrilineally directedfidelity to Clayoquot Sound.     

Genetic structure of the beaked whale genus Berardius in the North Pacific,with genetic evidence for a new species

There are two recognized species in the genus Berardius, Baird's and Arnoux's beaked whales. In Japan, whalers have traditionally recognized two forms of Baird's beaked whales, the common “slate‐gray” form and a smaller, rare “black” form. Previous comparison of mtDNA control region sequences from three black specimens to gray specimens around Japan indicated that the two forms comprise different stocks and potentially different species. We have expanded sampling to include control region haplotypes of 178 Baird's beaked whales from across their range in the North Pacific. We identified five additional specimens of the black form from the Aleutian Islands and Bering Sea, for a total of eight “black” specimens. The divergence between mtDNA haplotypes of the black and gray forms of Baird's beaked whale was greater than their divergence from the congeneric Arnoux's beaked whale found in the Southern Ocean, and similar to that observed among other congeneric beaked whale species. Taken together, genetic evidence from specimens in Japan and across the North Pacific, combined with evidence of smaller adult body size, indicate presence of an unnamed species of Berardius in the North Pacific.     

Autumn movements, home ranges, and winter density of narwhals (Monodon monoceros) tagged in Tremblay Sound, Baffin Island

Seven narwhals (Monodon monoceros) were instrumented with satellite transmitters in Tremblay Sound, northeast Canada in August 1999. The whales were tracked for 5-218 days with positions received until 17 March 2000. All whales stayed in the fjord system where they were tagged until the end of August. Three whales went northwest visiting adjacent fjords before moving south, together with the three other whales, along the east coast of Baffin Island. The narwhals arrived on the wintering ground in northern Davis Strait in late October. Speed and range of movements declined once the wintering ground was reached. Dive depths increased from summer to autumn, and reached at least 1,500 m. Late summer and winter kernel home ranges were approximately 3,400 km² and 12,000 km², respectively. The relative abundance of whales on the wintering ground was 936 narwhals. Assuming that the home range defines the winter distribution of the stock, an estimated 5,348 narwhals (corrected for perception and availability bias) were present in this area.     

The phylogeographic pattern of mitochondrial DNA variation in the Dall's porpoise Phocoenoides dalli

We used 11 restriction endonucleases to study mtDNA variation in 101 Dall's porpoises Phocoenoides dalli from the Bering Sea and western North Pacific. There was little phylogeographic patterning among the 34 mtDNA haplotypes identified in this analysis, suggesting a strong historical connection among populations across this region. Nonetheless, mtDNA variation does not appear to be randomly distributed in this species. Both G_ST and AMOVA uncovered significant differences in the distribution of mtDNA variation between the Bering Sea and western North Pacific populations. These mtDNA results, coupled with differences in allozyme variation and parasite infestation, support the demographic distinctiveness of Bering Sea and western North Pacific stocks of Dall's porpoise. The lack of a strong phylogeographic orientation of mtDNA haplotypes within the Dall's porpoise is similar to the pattern reported in other vertebrates such as coyotes, blackbirds, chickadees, marine catfish, and catadromous eels. Like Dall's porpoise, these species are broadly distributed, and have large populations linked by moderate to high levels of gene flow. However, the more complex, deeply branched phylogenetic network of mtDNA haplotypes within Dall's porpoise, relative to these other vertebrates, suggests important differences between these species in the forces shaping mtDNA variation. One such force is the effective size of female populations, which appears to have been comparatively large and stable in Dall's porpoise.     

Autumn migration and wintering of northern fulmars (<Emphasis Type="Italic">Fulmarus glacialis</Emphasis>) from the Canadian high Arctic

Five northern fulmars (Fulmarus glacialis) were tracked by satellite transmitters from their breeding colony in the Canadian high Arctic (Cape Vera, Devon Island, NT) to their wintering grounds in the northwest Atlantic Ocean. In both 2004 and 2005, fulmars left northern Baffin Bay in mid- to late September, and migrated south to Davis Strait in less than 1 week, after which movements were erratic. In October and November, the birds were widely distributed, but by December through March, they tended to remain in the Labrador Sea between 50 and 55°N. Average flight speed was 35 km/h with a maximum of 64 km/h, and over their entire transmission periods, the five traveled on average 84 km/day. Our work suggests that the North Atlantic northern fulmar population may be panmictic in winter, with the Labrador Sea as a key wintering site for fulmars from high Arctic Canada.     

Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis

Intraspecific genetic variation of Echinococcus multilocularis, the etiologic agent of human alveolar echinococcosis, has been evaluated among 76 geographic isolates from Europe, Asia and North America by using sequence data of mitochondrial and nuclear DNA. Relatively low genetic variation was found only in the mitochondrial DNA sequence consisting of 3 protein-coding genes. Pairwise divergence among the resultant 18 haplotypes ranged from 0.03 to 1.91%. Phylogenetic trees and parsimony network of these haplotypes depicted a geographic division into European, Asian and North American clades, but 1 haplotype from Inner Mongolia was unrelated to other haplotypes. The coexistence of the Asian and North American haplotypes could be seen, particularly on the St. Lawrence Island in the Bering Sea. These data suggest an evolutionary scenario in which distinct parasite populations derived from glacial refugia have been maintained by indigenous host mammals. The nuclear DNA sequence for the immunodominant B cell epitope region of ezrin/radixin/moesin-like protein (elp) was extremely conservative, indicating that the elp antigen is available for immunodiagnosis in any endemic areas.