Moira W. Brown

World-wide genetic differentiation of Eubalaena: Questioning the number of right whale species

Few studies have examined systematic relationships of right whales (Eubalaena spp.) since the original species descriptions, even though they are one of the most endangered large whales. Little morphological evidence exists to support the current species designations for Eubalaena glacialis in the northern hemisphere and E. australis in the southern hemisphere. Differences in migratory behaviour or antitropical distribution between right whales in each hemisphere are considered a barrier to gene flow and maintain the current species distinctions and geographical populations. However, these distinctions between populations have remained controversial and no study has included an analysis of all right whales from the three major ocean basins. To address issues of genetic differentiation and relationships among right whales, we have compiled a database of mitochondrial DNA control region sequences from right whales representing populations in all three ocean basins that consist of: western North Atlantic E. glacialis, multiple geographically distributed populations of E. australis and the first molecular analysis of historical and recent samples of E. glacialis from the western and eastern North Pacific Ocean. Diagnostic characters, as well as phylogenetic and phylogeographic analyses, support the possibility that three distinct maternal lineages exist in right whales, with North Pacific E. glacialis being more closely related to E. australis than to North Atlantic E. glacialis. Our genetic results provide unequivocal character support for the two usually recognized species and a third distinct genetic lineage in the North Pacific under the Phylogenetic Species Concept, as well as levels of genetic diversity among right whales world‐wide.

Evaluating the effects of historic bottleneck events: an assessment of microsatellite variability in the endangered, North Atlantic right whale

Commercial exploitation reduced the North Atlantic right whale (Eubalaena glacialis) population from c. 12 000 in the 11th century to around 300 by the 21st century. We examine the effect of this population decline on levels of genetic variation at 16 microsatellite loci and contrast levels of variability to that in a closely related species (E. australis). Of the 13 loci developed from the E. glacialis genome, 100% were polymorphic in E. australis. In contrast, nine loci were polymorphic in E. glacialis and four were fixed. Both allelic diversity (A) and heterozygosity (H) were significantly lower in E. glacialis than E. australis (A = 3.2 ± 2.6 vs. A= 6.9 ± 3.3, P < 0.001; H= 0.31 ± 0.25 vs. H= 0.72 ± 0.23, P < 0.001, respectively). Bottleneck anlayses indicate that the population is in mutation‐drift equilibrium and that a genetic bottleneck did not occur during the most recent decline (18th–20th centuries). Nevertheless, low frequency alleles are relatively uncommon in E. glacialis, suggesting that genetic variability has been reduced in this population. Possible origins of low genetic variability are discussed, including the slow but continual erosion of alleles during the 800‐year period of decline.

Population histories of right whales (Cetacea: Eubalaena) inferred from mitochondrial sequence diversities and divergences of their whale lice (Amphipoda: Cyamus)

Right whales carry large populations of three ‘whale lice’ (Cyamus ovalis, Cyamus gracilis, Cyamus erraticus) that have no other hosts. We used sequence variation in the mitochondrial COI gene to ask (i) whether cyamid population structures might reveal associations among right whale individuals and subpopulations, (ii) whether the divergences of the three nominally conspecific cyamid species on North Atlantic, North Pacific, and southern right whales (Eubalaena glacialis, Eubalaena japonica, Eubalaena australis) might indicate their times of separation, and (iii) whether the shapes of cyamid gene trees might contain information about changes in the population sizes of right whales. We found high levels of nucleotide diversity but almost no population structure within oceans, indicating large effective population sizes and high rates of transfer between whales and subpopulations. North Atlantic and Southern Ocean populations of all three species are reciprocally monophyletic, and North Pacific C. erraticus is well separated from North Atlantic and southern C. erraticus. Mitochondrial clock calibrations suggest that these divergences occurred around 6 million years ago (Ma), and that the Eubalaena mitochondrial clock is very slow. North Pacific C. ovalis forms a clade inside the southern C. ovalis gene tree, implying that at least one right whale has crossed the equator in the Pacific Ocean within the last 1–2 million years (Myr). Low‐frequency polymorphisms are more common than expected under neutrality for populations of constant size, but there is no obvious signal of rapid, interspecifically congruent expansion of the kind that would be expected if North Atlantic or southern right whales had experienced a prolonged population bottleneck within the last 0.5 Myr.

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 ~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.

Real-time reporting of baleen whale passive acoustic detections from ocean gliders

In the past decade, much progress has been made in real-time passive acoustic monitoring of marine mammal occurrence and distribution from autonomous platforms (e.g., gliders, floats, buoys), but current systems focus primarily on a single call type produced by a single species, often from a single location. A hardware and software system was developed to detect, classify, and report 14 call types produced by 4 species of baleen whales in real time from ocean gliders. During a 3-week deployment in the central Gulf of Maine in late November and early December 2012, two gliders reported over 25,000 acoustic detections attributed to fin, humpback, sei, and right whales. The overall false detection rate for individual calls was 14%, and for right, humpback, and fin whales, false predictions of occurrence during 15-min reporting periods were 5% or less. Transmitted pitch tracks--compact representations of sounds--allowed unambiguous identification of both humpback and fin whale song. Of the ten cases when whales were sighted during aerial or shipboard surveys and a glider was within 20 km of the sighting location, nine were accompanied by real-time acoustic detections of the same species by the glider within ±12 h of the sighting time.

Sources and Rates of Errors in Methods of Individual Identification for North Atlantic Right Whales

Abstract Many long-term studies of wildlife populations rely on individual identification based on natural markings or genetic profiling, or both. However, only rarely are these 2 independent data sets systematically compared with each other to estimate the error rates inherent in these studies. Here, >25 years of photo-identification data on the endangered North Atlantic right whale (Eubalaena glacialis) were compared with high-resolution genetic profiles, available for >75% of the individuals in the photo-identification catalog, in order to identify sources and rates of errors associated with both methods of individual identification. The resulting estimates were 0.0308 errors/identification for the photo-identification data, and 0.00121 errors/locus and 0.0327 errors/multilocus profile for the genetic data. These are among the lowest error rates yet reported, and indicate that the approaches used provide reliable means of individual identification for this species. However, despite these low error rates, the large size of the data sets results in a nonnegligible estimated number of errors, indicating that the potential for these errors needs to be incorporated into other analyses that are based on these data. A similar situation likely exists in other long-term studies where, although error rates are assumed to be low, the size of the data set results in a large number of errors that will influence subsequent analyses. Regularly conducting and reporting extensive database comparisons such as this is invaluable for maintaining the integrity of long-term data sets by identifying where sources of error are occurring and how protocols can be improved to lower error rates in the future.

Postcopulatory selection for dissimilar gametes maintains heterozygosity in the endangered North Atlantic right whale

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long-term implications have received little attention. Here, we combined over 25 years of field data with high-resolution genetic data to assess the long-term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long-term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.

DNA profile of a sixteenth century western North Atlantic right whale (Eubalaena glacialis)

Low levels of genetic variability identified within the North Atlantic right whale (Eubalaena glacialis), when compared to the Southern right whale (E. australis) and other large whales, have been suggested to result from population reductions due to whaling. Previous genetic analysis of 218 whale bones from sixteenth century Basque whaling sites in the western North Atlantic revealed only a single right whale bone. We determined the genotypes of 27 microsatellite loci using DNA isolated from this bone. All alleles from the historic specimen occur in the extant western North Atlantic population and both the probability of identity of the specimen and the number of heterozygous loci are similar to that in the extant population. Assessments of how genetically different the historical population might have been suggest genetic characteristics have not changed substantially over four centuries of whaling.