We quantified the relative influence of maternal fidelity to feeding grounds and natal fidelity to breeding grounds on the population structure of humpback whales Megaptera novaeangliae based on an ocean-wide survey of mitochondrial (mt) DNA diversity in the North Pacific. For 2193 biopsy samples collected from whales in 10 feeding regions and 8 breeding regions during the winter and summer of 2004 to 2006, we first used microsatellite genotyping (average, 9.5 loci) to identify replicate samples. From sequences of the mtDNA control region (500 bp) we identified 28 unique haplotypes from 30 variable sites. Haplotype frequencies differed markedly among feeding regions (overall F ST = 0.121, Φ ST = 0.178, p < 0.0001), supporting previous evidence of strong maternal fidelity. Haplotype frequencies also differed markedly among breeding regions (overall F ST = 0.093, Φ ST = 0.106, p < 0.0001), providing evidence of strong natal fidelity. Although sex-biased dispersal was not evident, differentiation of microsatellite allele frequencies was weak compared to differentiation of mtDNA haplotypes, suggesting male-biased gene flow. Feeding and breeding regions showed significant differences in haplotype frequencies, even for regions known to be strongly connected by patterns of individual migration. Thus, the influence of migratory fidelity seems to operate somewhat independently on feeding and breeding grounds over an evolutionary time scale. This results in a complex population structure and the potential to define multiple units to conserve in either seasonal habitat.
Genetic sampling for identification of species, subspecies or stock of whales, dolphins and porpoises at sea remains challenging. Most samples have been collected with some form of a biopsy dart requiring a close approach of a vessel while the individual is at the surface. Here we have adopted droplet digital (dd)PCR technology for detection and species identification of cetaceans using environmental (e)DNA collected from seawater. We conducted a series of eDNA sampling experiments during 25 encounters with killer whales, Orcinus orca, in Puget Sound (the Salish Sea). The regular habits of killer whales in these inshore waters allowed us to locate pods and collect seawater, at an initial distance of 200 m and at 15-min intervals, for up to 2 h after the passage of the whales. To optimize detection, we designed a set of oligonucleotide primers and probes to target short fragments of the mitochondrial (mt)DNA control region, with a focus on identification of known killer whale ecotypes. We confirmed the potential to detect eDNA in the wake of the whales for up to 2 h, despite movement of the water mass by several kilometers due to tidal currents. Re-amplification and sequencing of the eDNA barcode confirmed that the ddPCR detection included the "southern resident community" of killer whales, consistent with the calls from hydrophone recordings and visual observations.
The interplay of natural selection and genetic drift, influenced by geographic isolation, mating systems and population size, determines patterns of genetic diversity within species. The sperm whale provides an interesting example of a long-lived species with few geographic barriers to dispersal. Worldwide mtDNA diversity is relatively low, but highly structured among geographic regions and social groups, attributed to female philopatry. However, it is unclear whether this female philopatry is due to geographic regions or social groups, or how this might vary on a worldwide scale. To answer these questions, we combined mtDNA information for 1091 previously published samples with 542 newly obtained DNA profiles (394-bp mtDNA, sex, 13 microsatellites) including the previously unsampled Indian Ocean, and social group information for 541 individuals. We found low mtDNA diversity (π = 0.430%) reflecting an expansion event <80 000 years bp, but strong differentiation by ocean, among regions within some oceans, and among social groups. In comparison, microsatellite differentiation was low at all levels, presumably due to male-mediated gene flow. A hierarchical amova showed that regions were important for explaining mtDNA variance in the Indian Ocean, but not Pacific, with social group sampling in the Atlantic too limited to include in analyses. Social groups were important in partitioning mtDNA and microsatellite variance within both oceans. Therefore, both geographic philopatry and social philopatry influence genetic structure in the sperm whale, but their relative importance differs by sex and ocean, reflecting breeding behaviour, geographic features and perhaps a more recent origin of sperm whales in the Pacific. By investigating the interplay of evolutionary forces operating at different temporal and geographic scales, we show that sperm whales are perhaps a unique example of a worldwide population expansion followed by rapid assortment due to female social organization.
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
Antarctic humpback whales are recovering from near extirpation from commercial whaling. To understand the dynamics of this recovery and establish a baseline to monitor impacts of a rapidly changing environment, we investigated sex ratios and pregnancy rates of females within the Western Antarctic Peninsula (WAP) feeding population. DNA profiling of 577 tissue samples (2010–2016) identified 239 males and 268 females. Blubber progesterone levels indicated 63.5% of the females biopsied were pregnant. This proportion varied significantly across years, from 36% in 2010 to 86% in 2014. A comparison of samples collected in summer versus fall showed significant increases in the proportion of females present (50% to 59%) and pregnant (59% to 72%), consistent with demographic variation in migratory timing. We also found evidence of annual reproduction among females; 54.5% of females accompanied by a calf were pregnant. These high pregnancy rates are consistent with a population recovering from past exploitation, but appear inconsistent with recent estimates of WAP humpback population growth. Thus, our results will help to better understand population growth potential and set a current baseline from which to determine the impact of climate change and variability on fecundity and reproductive rates.
Pilot whales (Globicephala spp.) provide an interesting example of recently diverged oceanic species with a complex evolutionary history. The two species have wide but largely non-overlapping ranges. Globicephala melas (longfinned pilot whale; LFPW) has an antitropical distribution and is found in the cold-temperate waters of the North Atlantic and Southern Hemisphere, whereas Globicephala macrorhynchus (short-finned pilot whale; SFPW) has a circumglobal distribution and is found mainly in the tropics and subtropics. To investigate pilot whale evolution and biogeography, we analysed worldwide population structure using mitochondrial DNA (mtDNA) control region sequences (up to 620 bp) from a variety of sources (LFPW = 643; SFPW = 150), including strandings in New Zealand and Tasmania, and whale-meat products purchased on the markets of Japan and Korea. Phylogenetic reconstructions failed to support a reciprocal monophyly of the two species, despite six diagnostic substitutions, possibly because of incomplete lineage sorting or inadequate phylogenetic information. Both species had low haplotype and nucleotide diversity compared to other abundant widespread cetaceans (LFPW, p = 0.35%; SFPW, p = 0.87%) but showed strong mtDNA differentiation between oceanic basins. Strong levels of structuring were also found at the regional level. In LFPW, phylogeographic patterns were suggestive either of a recent demographic expansion or selective sweep acting on the mtDNA. For SFPW, the waters around Japan appear to represent a centre of diversity, with two genetically-distinct forms, as well as a third population of unknown origin. The presence of multiple unique haplotypes among SFPW from South Japan, together with previously documented morphological and ecological differences, suggests that the southern form represents a distinct subspecies and/or evolutionary significant unit.
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.
Baleen whales are the largest animals that have ever lived. To develop an improved estimation of substitution rate for nuclear and mitochondrial DNA for this taxon, we implemented a relaxed-clock phylogenetic approach using three fossil calibration dates: the divergence between odontocetes and mysticetes approximately 34 million years ago (Ma), between the balaenids and balaenopterids approximately 28 Ma, and the time to most recent common ancestor within the Balaenopteridae approximately 12 Ma. We examined seven mitochondrial genomes, a large number of mitochondrial control region sequences (219 haplotypes for 465 bp) and nine nuclear introns representing five species of whales, within which multiple species-specific alleles were sequenced to account for within-species diversity (1-15 for each locus). The total data set represents >1.65 Mbp of mitogenome and nuclear genomic sequence. The estimated substitution rate for the humpback whale control region (3.9%/million years, My) was higher than previous estimates for baleen whales but slow relative to other mammal species with similar generation times (e.g., human-chimp mean rate > 20%/My). The mitogenomic third codon position rate was also slow relative to other mammals (mean estimate 1%/My compared with a mammalian average of 9.8%/My for the cytochrome b gene). The mean nuclear genomic substitution rate (0.05%/My) was substantially slower than average synonymous estimates for other mammals (0.21-0.37%/My across a range of studies). The nuclear and mitogenome rate estimates for baleen whales were thus roughly consistent with an 8- to 10-fold slowing due to a combination of large body size and long generation times. Surprisingly, despite the large data set of nuclear intron sequences, there was only weak and conflicting support for alternate hypotheses about the phylogeny of balaenopterid whales, suggesting that interspecies introgressions or a rapid radiation has obscured species relationships in the nuclear genome.
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