Incorporating non-equilibrium dynamics into demographic history inferences of a migratory marine species.

Understanding how dispersal and gene flow link geographically separated the populations over evolutionary history is challenging, particularly in migratory marine species. In southern right whales (SRWs, Eubalaena australis), patterns of genetic diversity are likely influenced by the glacial climate cycle and recent history of whaling. Here we use a dataset of mitochondrial DNA (mtDNA) sequences (n = 1327) and nuclear markers (17 microsatellite loci, n = 222) from major wintering grounds to investigate circumpolar population structure, historical demography and effective population size. Analyses of nuclear genetic variation identify two population clusters that correspond to the South Atlantic and Indo-Pacific ocean basins that have similar effective breeder estimates. In contrast, all wintering grounds show significant differentiation for mtDNA, but no sex-biased dispersal was detected using the microsatellite genotypes. An approximate Bayesian computation (ABC) approach with microsatellite markers compared the scenarios with gene flow through time, or isolation and secondary contact between ocean basins, while modelling declines in abundance linked to whaling. Secondary-contact scenarios yield the highest posterior probabilities, implying that populations in different ocean basins were largely isolated and came into secondary contact within the last 25,000 years, but the role of whaling in changes in genetic diversity and gene flow over recent generations could not be resolved. We hypothesise that these findings are driven by factors that promote isolation, such as female philopatry, and factors that could promote dispersal, such as oceanographic changes. These findings highlight the application of ABC approaches to infer the connectivity in mobile species with complex population histories and, currently, low levels of differentiation.

First Direct Evidence for Natal Wintering Ground Fidelity and Estimate of Juvenile Survival in the New Zealand Southern Right Whale Eubalaena australis.

Juvenile survival and recruitment can be more sensitive to environmental, ecological and anthropogenic factors than adult survival, influencing population-level processes like recruitment and growth rate in long-lived, iteroparous species such as southern right whales. Conventionally, Southern right whales are individually identified using callosity patterns, which do not stabilise until 6-12 months, by which time the whale has left its natal wintering grounds. Here we use DNA profiling of skin biopsy samples to identify individual Southern right whales from year of birth and document their return to the species' primary wintering ground in New Zealand waters, the Subantarctic Auckland Islands. We find evidence of natal fidelity to the New Zealand wintering ground by the recapture of 15 of 57 whales, first sampled in year of birth and available for subsequent recapture, during winter surveys to the Auckland Islands in 1995-1998 and 2006-2009. Four individuals were recaptured at the ages of 9 to 11, including two females first sampled as calves in 1998 and subsequently resampled as cows with calves in 2007. Using these capture-recapture records of known-age individuals, we estimate changes in survival with age using Cormack-Jolly-Seber models. Survival is modelled using discrete age classes and as a continuous function of age. Using a bootstrap method to account for uncertainty in model selection and fitting, we provide the first direct estimate of juvenile survival for this population. Our analyses indicate a high annual apparent survival for juveniles at between 0.87 (standard error (SE) 0.17, to age 1) and 0.95 (SE 0.05: ages 2-8). Individual identification by DNA profiling is an effective method for long-term demographic and genetic monitoring, particularly in animals that change identifiable features as they develop or experience tag loss over time.

Maximum likelihood estimation for model Mt,α for capture-recapture data with misidentification.

We investigate model Mt,α  for abundance estimation in closed-population capture-recapture studies, where animals are identified from natural marks such as DNA profiles or photographs of distinctive individual features. Model Mt,α  extends the classical model Mt  to accommodate errors in identification, by specifying that each sample identification is correct with probability α and false with probability 1-α. Information about misidentification is gained from a surplus of capture histories with only one entry, which arise from false identifications. We derive an exact closed-form expression for the likelihood for model Mt,α  and show that it can be computed efficiently, in contrast to previous studies which have held the likelihood to be computationally intractable. Our fast computation enables us to conduct a thorough investigation of the statistical properties of the maximum likelihood estimates. We find that the indirect approach to error estimation places high demands on data richness, and good statistical properties in terms of precision and bias require high capture probabilities or many capture occasions. When these requirements are not met, abundance is estimated with very low precision and negative bias, and at the extreme better properties can be obtained by the naive approach of ignoring misidentification error. We recommend that model Mt,α  be used with caution and other strategies for handling misidentification error be considered. We illustrate our study with genetic and photographic surveys of the New Zealand population of southern right whale (Eubalaena australis).

Accounting for female reproductive cycles in a superpopulation capture-recapture framework.

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-tau). 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 (lamda) 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-tau 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 (deltaAIC > 25). The best POPAN-tau model (AIC) gave a super-population estimate of 1162 females for 1995-2009 (95% CL 921, 1467) and an estimated annual increase of 5% (95% CL--2%, 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 (+19%) in female abundance estimates.

How few whales were there after whaling? Inference from contemporary mtDNA diversity.

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.

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.

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.