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.
During the last 2 centuries, southern right whales Eubalaena australis were hunted to near extinction, and an estimated 150 000 were killed by pre-industrial whaling in the 19th century and illegal Soviet whaling in the 20th century. Here we focus on the coastal calving grounds of Australia and New Zealand (NZ), where previous work suggests 2 genetically distinct stocks of southern right whales are recovering. Historical migration patterns and spatially variable patterns of recovery suggest each of these stocks are subdivided into 2 stocks: (1) NZ, comprising NZ subantarctic (NZSA) and mainland NZ (MNZ) stocks; and (2) Australia, comprising southwest and southeast stocks. We expand upon previous work to investigate population subdivision by analysing over 1000 samples collected at 6 locations across NZ and Australia, although sample sizes were small from some locations. Mitochondrial DNA (mtDNA) control region haplotypes (500 bp) and microsatellite genotypes (13 loci) were used to identify 707 individual whales and to test for genetic differentiation. For the first time, we documented the movement of 7 individual whales between the NZSA and MNZ based on the matching of multilocus genotypes. Given the current and historical evidence, we hypothesise that individuals from the NZ subantarctic are slowly recolonising MNZ, where a former calving ground was extirpated. We also suggest that southeast Australian right whales represent a remnant stock, distinct from the southwest Australian stock, based on significant differentiation in mtDNA haplotype frequencies (F ST = 0.15, p < 0.01; Φ ST = 0.12, p = 0.02) and contrasting patterns of recovery. In comparison with significant differences in mtDNA haplotype frequencies found between the 3 proposed stocks (overall F ST = 0.07, Φ ST = 0.12, p < 0.001), we found no significant differentiation in microsatellite loci (overall
Fidelity to migratory destinations is an important driver of connectivity in marine and avian species. Here we assess the role of maternally directed learning of migratory habitats, or migratory culture, on the population structure of the endangered Australian and New Zealand southern right whale. Using DNA profiles, comprising mitochondrial DNA (mtDNA) haplotypes (500 bp), microsatellite genotypes (17 loci) and sex from 128 individually-identified whales, we find significant differentiation among winter calving grounds based on both mtDNA haplotype (FST = 0.048, ΦST = 0.109, p < 0.01) and microsatellite allele frequencies (FST = 0.008, p < 0.01), consistent with long-term fidelity to calving areas. However, most genetic comparisons of calving grounds and migratory corridors were not significant, supporting the idea that whales from different calving grounds mix in migratory corridors. Furthermore, we find a significant relationship between δ13C stable isotope profiles of 66 Australian southern right whales, a proxy for feeding ground location, and both mtDNA haplotypes and kinship inferred from microsatellite-based estimators of relatedness. This indicates migratory culture may influence genetic structure on feeding grounds. This fidelity to migratory destinations is likely to influence population recovery, as long-term estimates of historical abundance derived from estimates of genetic diversity indicate the South Pacific calving grounds remain at <10% of pre-whaling abundance.
The population structure and mitochondrial (mt) DNA diversity of southern right whales (Eubalaena australis) are described from 146 individuals sampled on 4 winter calving grounds (Argentina, South Africa, Western Australia, and the New Zealand sub-Antarctic) and 2 summer feeding grounds (South Georgia and south of Western Australia). Based on a consensus region of 275 base pairs of the mtDNA control region, 37 variable sites defined 37 unique haplotypes, of which only one was shared between regional samples of the Indo-Pacific and South Atlantic Oceans. Phylogenetic reconstruction of the southern right whale haplotypes revealed 2 distinct clades that differed significantly in frequencies between oceans. An analysis of molecular variance confirmed significant overall differentiation among the 4 calving grounds at both the haplotype and the nucleotype levels (F(ST) = 0.159; Phi(ST) = 0.238; P < 0.001). Haplotype diversity was significantly lower in the Indo-Pacific (h = 0.701 +/- 0.037) compared with the South Atlantic (h = 0.948 +/- 0.013), despite a longer history of exploitation and larger catches in the South Atlantic. In fact, the haplotype diversity in the Indo-Pacific basin was similar to that of the North Atlantic right whale that currently numbers about 300 animals. Multidimensional scaling of genetic differentiation suggests that gene flow occurred primarily between adjacent calving grounds within an ocean basin, with mixing of lineages from different calving grounds occurring on feeding grounds.
Abstract. Superpopulation capture-recapture models are useful for estimating the abundance of long-lived, migratory species because they are able to account for the fluid nature of annual residency at migratory destinations. Here we extend the superpopulation POPAN model to explicitly account for heterogeneity in capture probability linked to reproductive cycles (POPAN-s). This extension has potential application to a range of species that have temporally variable life stages (e.g., non-annual breeders such as albatrosses and baleen whales) and results in a significant reduction in bias over the standard POPAN model. We demonstrate the utility of this model in simultaneously estimating abundance and annual population growth rate (k) in the New Zealand (NZ) southern right whale (Eubalaena australis) from 1995 to 2009. DNA profiles were constructed for the individual identification of more than 700 whales, sampled during two sets of winter expeditions in 1995-1998 and 2006-2009. Due to differences in recapture rates between sexes, only sex-specific models were considered. The POPAN-s models, which explicitly account for a decrease in capture probability in non-calving years, fit the female data set significantly better than do standard superpopulation models (DAIC . 25). The best POPAN-s model (AIC) gave a superpopulation estimate of 1162 females for 1995-2009 (95% CL 921, 1467 and an estimated annual increase of 5% (95% CL À2%, 13%). The best model (AIC) gave a superpopulation estimate of 1007 males (95% CL 794, 1276) and an estimated annual increase of 7% (95% CL 5%, 9%) for 1995-2009. Combined, the total superpopulation estimate for 1995-2009 was 2169 whales (95% CL 1836, 2563). Simulations suggest that failure to account for the effect of reproductive status on the capture probability would result in a substantial positive bias (þ19%) in female abundance estimates.
Reconstructing the history of exploited populations of whales requires fitting a trajectory through at least three points in time: (i) prior to exploitation, when abundance is assumed to be at the maximum allowed by environmental carrying capacity; (ii) the point of minimum abundance or 'bottleneck', usually near the time of protection or the abandonment of the hunt; and (iii) near the present, when protected populations are assumed to have undergone some recovery. As historical abundance is usually unknown, this trajectory must be extrapolated according to a population dynamic model using catch records, an assumed rate of increase and an estimate of current abundance, all of which have received considerable attention by the International Whaling Commission (IWC). Relatively little attention has been given to estimating minimum abundance (N(min)), although it is clear that genetic and demographic forces at this point are critical to the potential for recovery or extinction of a local population. We present a general analytical framework to improve estimates of N(min) using the number of mtDNA haplotypes (maternal lineages) surviving in a contemporary population of whales or other exploited species. We demonstrate the informative potential of this parameter as an a posteriori constraint on Bayesian logistic population dynamic models based on the IWC Comprehensive Assessment of the intensively exploited southern right whales (Eubalaena australis) and published surveys of mtDNA diversity for this species. Estimated historical trajectories from all demographic scenarios suggested a substantial loss of mtDNA haplotype richness as a result of 19th century commercial whaling and 20th century illegal whaling by the Soviet Union. However, the relatively high rates of population increase used by the IWC assessment predicted a bottleneck that was implausibly narrow (median, 67 mature females), given our corrected estimates of N(min). Further, high levels of remnant sequence diversity (theta) suggested that pre-exploitation abundance was larger than predicted by the logistic model given the catch record, which is known to be incomplete. Our results point to a need to better integrate evolutionary processes into population dynamic models to account for uncertainty in catch records, the influence of maternal fidelity on metapopulation dynamics, and the potential for inverse density dependence (an 'Allee effect') in severely depleted populations.
Historically, the range of the southern right whale (SRW) included winter calving grounds around the North and South Islands (mainland) of New Zealand (NZ) and in the NZ subantarctic Auckland and Campbell Islands. Due to extensive whaling in the 19th and 20th centuries, no SRW was seen around mainland NZ for nearly four decades (1928–1963). Here we present evidence for the regular use of the mainland NZ wintering ground, presumably from a remnant population that persisted in the NZ subantarctic Auckland and Campbell Islands. SRWs have been sighted every year around mainland NZ since 1988, with 125 sightings during the focus of this work: from 2003 to 2010. There were 28 cow‐calf pairs sighted around mainland NZ from 2003 to 2010, compared with 11 sightings from 1991 to 2002. Furthermore, two females, identified by DNA profiles, were sighted with calves around mainland at 4 yr intervals: the first evidence of female site fidelity to the mainland NZ calving ground. Individual identification from photographs of natural markings and DNA profiles provided information on within‐year movements and residency around the mainland, and further evidence for exchange between the mainland and subantarctic wintering grounds. Despite these promising signs, the distribution of NZ SRWs remains primarily concentrated in the NZ subantarctic.
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.
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