Statistical approaches to paternity analysis in natural populations and applications to the North Atlantic humpback whale

We present a new method for paternity analysis in natural populations that is based on genotypic data that can take the sampling fraction of putative parents into account. The method allows paternity assignment to be performed in a decision theoretic framework. Simulations are performed to evaluate the utility and robustness of the method and to assess how many loci are necessary for reliable paternity inference. In addition we present a method for testing hypotheses regarding relative reproductive success of different ecologically or behaviorally defined groups as well as a new method for estimating the current population size of males from genotypic data. This method is an extension of the fractional paternity method to the case where only a proportion of all putative fathers have been sampled. It can also be applied to provide abundance estimates of the number of breeding males from genetic data. Throughout, the methods were applied to genotypic data collected from North Atlantic humpback whales (Megaptera novaeangliae) to test if the males that appear dominant during the mating season have a higher reproductive success than the subdominant males.     

Serum chemistry and evidence of renal failure in the North Atlantic fin whale population

Serum electrolytes, urea nitrogen, creatinine, albumin and globulin were studied in fin whales (Balaenoptera physalus) caught by commercial whalers in the North Atlantic (Denmark Strait area). Blood samples were obtained by catchment or cardiac puncture within 5-15 min of death and analyzed using automated spectrophotometric methods and flame photometry. Osmolality was determined for two serum samples by a vapor pressure method. Linear regressions determined for each measured serum variable vs. chase time suggested that pursuit of the whales prior to capture had no substantive effect on measured serum chemistry. As in other cetaceans, serum sodium, chloride, urea nitrogen and osmolality were distinctly higher in the fin whale than in terrestrial mammals. The total concentration of serum proteins, however, was 1.4-1.8 g/dl lower, on average, than reported in small toothed whales, and was similar to that of domesticated animals. One animal in this population showed alterations in serum chemistry which were consistent with renal failure.     

Genetic differentiation among North Atlantic killer whale populations

Population genetic structure of North Atlantic killer whale samples was resolved from differences in allele frequencies of 17 microsatellite loci, mtDNA control region haplotype frequencies and for a subset of samples, using complete mitogenome sequences. Three significantly differentiated populations were identified. Differentiation based on microsatellite allele frequencies was greater between the two allopatric populations than between the two pairs of partially sympatric populations. Spatial clustering of individuals within each of these populations overlaps with the distribution of particular prey resources: herring, mackerel and tuna, which each population has been seen predating. Phylogenetic analyses using complete mitogenomes suggested two populations could have resulted from single founding events and subsequent matrilineal expansion. The third population, which was sampled at lower latitudes and lower density, consisted of maternal lineages from three highly divergent clades. Pairwise population differentiation was greater for estimates based on mtDNA control region haplotype frequencies than for estimates based on microsatellite allele frequencies, and there were no mitogenome haplotypes shared among populations. This suggests low or no female migration and that gene flow was primarily male mediated when populations spatially and temporally overlap. These results demonstrate that genetic differentiation can arise through resource specialization in the absence of physical barriers to gene flow.     

Hydrodynamic design of the humpback whale flipper

The humpback whale (Megaptera novaeangliae) is reported to use its elongate pectoral flippers during swimming maneuvers. The morphology of the flipper from a 9.02-m whale was evaluated with regard to this hydrodynamic function. The flipper had a wing-like, high aspect ratio plan-form. Rounded tubercles were regularly interspersed along the flipper's leading edge. The flipper was cut into 71 2.5-cm cross-sections and photographed. Except for sections near the distal tip, flipper sections were symmetrical with no camber. Flipper sections had a blunt, rounded leading edge and a highly tapered trailing edge. Placement of the maximum thickness placement for each cross-section varied from 49% of chord at the tip to 19% at mid-span. Section thickness ratio averaged 0.23 with a range of 0.20–0.28. The humpback whale flipper had a cross-sectional design typical of manufactured aerodynamic foils for lift generation. The morphology and placement of leading edge tubercles sugges that they function as enhanced lift devices to control flow over the flipper and maintain lift at high angles of attack. The morphology of the humpback whale flipper suggests that it is adapted for high maneuverability associated with the whale's unique feeding behavior. © 1995 Wiley-Liss, Inc.     

Genetic analysis of population structure of tusk in the North Atlantic

To study the population structure of tusk Brosme brosme in the North Atlantic, samples from six fishing grounds were collected: St Kilda; Storegga; Faroe Islands; Rockall bank; Davis Strait and East Greenland. In addition two samples from the Norwegian coast; Kragerø and Øygarden, were included. Nine enzymes and haemoglobin were analysed by starch gel and agar gel electrophoresis. In addition isoelectric focusing (IEF) was carried out. At least 22 loci were represented. Polymorphisms were shown in eight loci and average heterozygosity was found to be about 0.05. Highest heterozygosity was found in haemoglobin analysed by Smithies buffer pH 8.6. Malate dehydrogenase ( MDH-2 ) analysed in IEF (pH 3.5-9.5), and haemoglobin were found as valuable tools for studies of stock structure in tusk. In the Greenland samples only one of the MDH-2 heterozygotes was found, while in the East Atlantic both the observed heterozygotes were more frequent. The frequencies of the the Hb * b allele were about 0.40 and 0.70 in the samples from east and west Atlantic respectively.     

Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo-identification data with high-resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource- and/or mate-defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until approximately 15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.     

Population spatial structuring on the feeding grounds in North Atlantic humpback whales (Megaptera novaeangliae)

Population spatial structuring among North Atlantic humpback whales Megaptera novaeangliae on the summer feeding grounds was investigated using movement patterns of identified individuals. We analysed the results from an intensive 2-year ocean-basin-scale investigation resulting in 1658 individuals identified by natural markings and 751 individuals by genetic markers supplemented with data from a long-term collaborative study with 3063 individuals identified by natural markings. Re-sighting distances ranged from <1 km to >2200 km. The frequencies ( F ) of re-sighting distances ( D ) observed in consecutive years were best modelled by an inverse allometric function ( F =6631 D ^−1.24, r ²=0.984), reflecting high levels of site fidelity (median re-sighting distance <40 km) with occasional long-distance movement (5% of re-sightings >550 km). The distribution of re-sighting distances differed east and west of 45°W, with more long-distance movement in the east. This difference is consistent with regional patterns of prey distribution and predictability. Four feeding aggregations were identified: the Gulf of Maine, eastern Canada, West Greenland and the eastern North Atlantic. There was an exchange rate of 0.98% between the western feeding aggregations. The prevalence of long-distance movement in the east made delineation of possible additional feeding aggregations less clear. Limited exchange between sites separated by as little as tens of kilometres produced lower-level structuring within all feeding aggregations. Regional and temporal differences in movement patterns reflected similar foraging responses to varying patterns of prey availability and predictability. A negative relationship was shown between relative abundance of herring and sand lance in the Gulf of Maine and humpback whale movement from the Gulf of Maine to eastern Canada.     

G-banded karyotype and ideogram for the North Atlantic right whale (Eubalaena glacialis)

Published cytogenetic data for extant cetacean species remain incomplete. In a review of the literature, we found karyotypic information for 6 of the 13 tentatively recognized species of the suborder Mysticeti (baleen whales). Among those yet to be described is the critically endangered North Atlantic right whale (Eubalaena glacialis). Herein, we describe and propose a first-generation G-banded karyotype and ideogram for this species (2n = 42), obtained from peripheral blood chromosome preparations from a stranded male calf. This information may prove useful for future genetic mapping projects and for interspecific and intraspecific genomic comparisons by techniques such as zoo-FISH.     

Ecological,morphological and genetic divergence of sympatric North Atlantic killer whale populations

Ecological divergence has a central role in speciation and is therefore an important source of biodiversity. Studying the micro‐evolutionary processes of ecological diversification at its early stages provides an opportunity for investigating the causative mechanisms and ecological conditions promoting divergence. Here we use morphological traits, nitrogen stable isotope ratios and tooth wear to characterize two disparate types of North Atlantic killer whale. We find a highly specialist type, which reaches up to 8.5 m in length and a generalist type which reaches up to 6.6 m in length. There is a single fixed genetic difference in the mtDNA control region between these types, indicating integrity of groupings and a shallow divergence. Phylogenetic analysis indicates this divergence is independent of similar ecological divergences in the Pacific and Antarctic. Niche‐width in the generalist type is more strongly influenced by between‐individual variation rather than within‐individual variation in the composition of the diet. This first step to divergent specialization on different ecological resources provides a rare example of the ecological conditions at the early stages of adaptive radiation.     

Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale

Cultural transmission, the social learning of information or behaviors from conspecifics, is believed to occur in a number of groups of animals, including primates, cetaceans, and birds. Cultural traits can be passed vertically (from parents to offspring), obliquely (from the previous generation via a nonparent model to younger individuals), or horizontally (between unrelated individuals from similar age classes or within generations). Male humpback whales (Megaptera novaeangliae) have a highly stereotyped, repetitive, and progressively evolving vocal sexual display or "song" that functions in sexual selection (through mate attraction and/or male social sorting). All males within a population conform to the current version of the display (song type), and similarities may exist among the songs of populations within an ocean basin. Here we present a striking pattern of horizontal transmission: multiple song types spread rapidly and repeatedly in a unidirectional manner, like cultural ripples, eastward through the populations in the western and central South Pacific over an 11-year period. This is the first documentation of a repeated, dynamic cultural change occurring across multiple populations at such a large geographic scale.     

Orientation behaviour of leatherback sea turtles within the North Atlantic subtropical gyre

Leatherback sea turtles (Dermochelys coriacea) travel thousands of kilometres between temperate feeding and tropical breeding/over-wintering grounds, with adult turtles able to pinpoint specific nesting beaches after multi-year absences. Their extensive migrations often occur in oceanic habitat where limited known sensory information is available to aid in orientation. Here, we examined the migratory orientation of adult male, adult female and subadult leatherbacks during their open-ocean movements within the North Atlantic subtropical gyre by analysing satellite-derived tracks from fifteen individuals over a 2-year period. To determine the turtles'' true headings, we corrected the reconstructed tracks for current drift and found negligible differences between current-corrected and observed tracks within the gyre. Individual leatherback headings were remarkably consistent throughout the subtropical gyre, with turtles significantly oriented to the south-southeast. Adult leatherbacks of both sexes maintained similar mean headings and showed greater orientation precision overall. The consistent headings maintained by adult and subadult leatherbacks within the gyre suggest use of a common compass sense.     

Historical influences dominate the population genetic structure of a sedentary marine fish,Atlantic wolffish (Anarhichas lupus), across the North Atlantic Ocean

Genetic variation was assessed in Atlantic wolffish, Anarhichas lupus, across the North Atlantic Ocean using microsatellite and amplified fragment length polymorphism (AFLP) markers. Despite unusual life history attributes such as large benthic eggs, large larvae, a limited pelagic stage and relatively sedentary adults, which suggest potential for strong population structure, range‐wide F_ST values were comparable to other marine fishes (≤0.035). Nevertheless, both significant genetic differentiation among regions and isolation by distance were observed, suggesting limited dispersal in this species. AFLP loci, evaluated on a subset of samples, revealed slightly higher F_ST values, but similar patterns of differentiation and isolation‐by‐distance estimates, compared to microsatellites. The genetic structure of Atlantic wolffish has likely been shaped by its post‐glacial history of recolonization, North Atlantic current patterns and continuity of habitat on continental shelves.     

Spondylitis in a humpback whale (Megaptera novaeangliae) from the southeast Pacific

A 7.25 m long male humpback whale (Megaptera novaeangliae) with spondylitis was found beached on August 13, 1994 at Ancon, Ecuador (2 degrees 23' S, 80 degrees 47' W). The condition involved at least 11 vertebrae, 7 lumbar (L4 to L11) and 4 caudal (Ca1 to Ca4). Partial fusion of vertebrae was observed as a result of intervertebral bony proliferation, likely impeding full motion. The relatively young age of this specimen and the severity of the deformities suggest an infectious, rather than degenerative, process. The gross findings are most consistent with some type of spondyloarthritis. Although this condition has previously been identified in a number of cetacean species, the pathogenesis, population impact and ecologic implications have not been fully assessed. This is the third case described for humpback whales and the first for a humpback whale from the SE Pacific.     

Microsatellite genetic distances between oceanic populations of the humpback whale (Megaptera novaeangliae)

Mitochondrial DNA haplotypes of humpback whales show strong segregationbetween oceanic populations and between feeding grounds within oceans, butthis highly structured pattern does not exclude the possibility ofextensive nuclear gene flow. Here we present allele frequency data for fourmicrosatellite loci typed across samples from four major oceanic regions:the North Atlantic (two mitochondrially distinct populations), the NorthPacific, and two widely separated Antarctic regions, East Australia and theAntarctic Peninsula. Allelic diversity is a little greater in the twoAntarctic samples, probably indicating historically greater populationsizes. Population subdivision was examined using a wide range of measures,including Fst, various alternative forms of Slatkin's Rst, Goldstein andcolleagues' delta mu, and a Monte Carlo approximation to Fisher's exacttest. The exact test revealed significant heterogeneity in all but one ofthe pairwise comparisons between geographically adjacent populations,including the comparison between the two North Atlantic populations,suggesting that gene flow between oceans is minimal and that dispersalpatterns may sometimes be restricted even in the absence of obviousbarriers, such as land masses, warm water belts, and antitropical migrationbehavior. The only comparison where heterogeneity was not detected was theone between the two Antarctic population samples. It is unclear whetherfailure to find a difference here reflects gene flow between the regions ormerely lack of statistical power arising from the small size of theAntarctic Peninsula sample. Our comparison between measures of populationsubdivision revealed major discrepancies between methods, with littleagreement about which populations were most and least separated. We suggestthat unbiased Rst (URst, see Goodman 1995) is currently the most reliablestatistic, probably because, unlike the other methods, it allows forunequal sample sizes. However, in view of the fact that these alternativemeasures often contradict one another, we urge caution in the use ofmicrosatellite data to quantify genetic distance.     

Mitochondrial DNA diversity of the Southwestern Atlantic humpback whale (Megaptera novaeangliae) breeding area off Brazil, and the potential connections to Antarctic feeding areas

In the Southwestern Atlantic Ocean, humpback whales migrate every winter to the Brazilian coast for breeding and calving in the Abrolhos Bank. This breeding stock represents the remnants of a larger population heavily exploited during the beginning of the 20th century. Despite its relevance to conservation efforts, the degree of current genetic variation and the migratory relationship with Antarctic feeding areas for this population are still largely unknown. To examine these questions, we sequenced ∼400 bp of the mitochondrial DNA control region from samples taken off the Brazilian coast (n = 171) and near the Antarctic Peninsula (n = 77). The genetic variability of the Brazilian humpback whale breeding population was high and similar to that found in other Southern Hemisphere breeding grounds. Phylogenetic analysis suggested the existence of a new mitochondrial clade that exists at low frequency among Southern Hemisphere populations. Direct comparison between the Brazilian and the Colombia breeding populations and the Antarctic Peninsula feeding population showed no genetic differentiation between this feeding region and the Colombian breeding area or between feeding Areas I and II near the Antarctic Peninsula. In contrast, these populations were genetically distinct from the Brazilian population. Two humpback whales sampled off South Georgia Islands, in the Scotia Sea, shared identical haplotypes to whales from Brazil. Our results, supported by photo-identification and satellite telemetry data, suggest that the main feeding area of the Southern Hemisphere humpback whale population is likely to be located near the South Georgia/South Sandwich Islands area and not in the Antarctic Peninsula.     

Migratory behaviour and otolith chemistry suggest fine-scale sub-population structure within a genetically homogenous Atlantic Cod population

The question whether temperate marine fishes typically consist of self-sustaining populations or “open” populations still remains unresolved. At the heart of this population connectivity problem lays the nature of the stock separation mechanisms. Fish populations could be segregated either by environmental forcing, accompanied with opportunistic recruitment of juveniles to spawning areas, or by philopatric behaviours (i.e., inclination of an individual to return to or remain in its natal area). Here we report three, partly independent, studies on Atlantic Cod (Gadus morhua) stock separation in the Kattegat and Öresund (eastern North Sea): characterisation of spawning aggregations with genetic markers, tagging experiments, and analysis of chemical constituents in otolith cores of recaptured fish that could be linked to a specific spawning site. While the genetic investigation showed no population segregation, the observed migratory patterns indicated three separate spawning sites at close distances. The natal dependence on the choice of spawning site was tested by measuring the contents of various trace elements in the otolith core of recaptured tagged fish. Quantification of the trace elements: Ba, Br, Co, Cr, Cu, Fe, Mn, Mo, Ni, Sr, Ti, and Zn expressed as ratios to Ca were obtained using scanning micro PIXE. These results indicated that natal origin could be differentiated between spawning sites, supporting the hypothesis that natal homing is an important stock separating mechanism even over short distances (<100 km).