Population genomics of the white-beaked dolphin (Lagenorhynchus albirostris): Implications for conservation amid climate-driven range shifts.

Climate change is rapidly affecting species distributions across the globe, particularly in the North Atlantic. For highly mobile and elusive cetaceans, the genetic data needed to understand population dynamics are often scarce. Cold-water obligate species such as the white-beaked dolphin (Lagenorhynchus albirostris) face pressures from habitat shifts due to rising sea surface temperatures in addition to other direct anthropogenic threats. Unravelling the genetic connectivity between white-beaked dolphins across their range is needed to understand the extent to which climate change and anthropogenic pressures may impact species-wide genetic diversity and identify ways to protect remaining habitat. We address this by performing a population genomic assessment of white-beaked dolphins using samples from much of their contemporary range. We show that the species displays significant population structure across the North Atlantic at multiple scales. Analysis of contemporary migration rates suggests a remarkably high connectivity between populations in the western North Atlantic, Iceland and the Barents Sea, while two regional populations in the North Sea and adjacent UK and Irish waters are highly differentiated from all other clades. Our results have important implications for the conservation of white-beaked dolphins by providing guidance for the delineation of more appropriate management units and highlighting the risk that local extirpation may have on species-wide genetic diversity. In a broader context, this study highlights the importance of understanding genetic structure of all species threatened with climate change-driven range shifts to assess the risk of loss of species-wide genetic diversity.

Don't mind if I do: Arctic humpback whales respond to winter foraging opportunities before migration.

Migration patterns are fundamentally linked to the spatio-temporal distributions of prey. How migrating animals can respond to changes in their prey's distribution and abundance remains largely unclear. During the last decade, humpback whales (Megaptera novaeangliae) used specific winter foraging sites in fjords of northern Norway, outside of their main summer foraging season, to feed on herring that started overwintering in the area. We used photographic matching to show that whales sighted during summer in the Barents Sea foraged in northern Norway from late October to February, staying up to three months and showing high inter-annual return rates (up to 82%). The number of identified whales in northern Norway totalled 866 individuals by 2019. Genetic sexing and hormone profiling in both areas demonstrate a female bias in northern Norway and suggest higher proportions of pregnancy in northern Norway. This may indicate that the fjord-based winter feeding is important for pregnant females before migration. Our results suggest that humpback whales can respond to foraging opportunities along their migration pathways, in some cases by continuing their feeding season well into winter. This provides an important reminder to implement dynamic ecosystem management that can account for changes in the spatio-temporal distribution of migrating marine mammals.

Strong and lasting impacts of past global warming on baleen whales and their prey.

Global warming is affecting the population dynamics and trophic interactions across a wide range of ecosystems and habitats. Translating these real-time effects into their long-term consequences remains a challenge. The rapid and extreme warming period that occurred after the Last Glacial Maximum (LGM) during the Pleistocene-Holocene transition (7-12 thousand years ago) provides an opportunity to gain insights into the long-term responses of natural populations to periods with global warming. The effects of this post-LGM warming period have been assessed in many terrestrial taxa, whereas insights into the impacts of rapid global warming on marine taxa remain limited, especially for megafauna. In order to understand how large-scale climate fluctuations during the post-LGM affected baleen whales and their prey, we conducted an extensive, large-scale analysis of the long-term effects of the post-LGM warming on abundance and inter-ocean connectivity in eight baleen whale and seven prey (fish and invertebrates) species across the Southern and the North Atlantic Ocean; two ocean basins that differ in key oceanographic features. The analysis was based upon 7032 mitochondrial DNA sequences as well as genome-wide DNA sequence variation in 100 individuals. The estimated temporal changes in genetic diversity during the last 30,000 years indicated that most baleen whale populations underwent post-LGM expansions in both ocean basins. The increase in baleen whale abundance during the Holocene was associated with simultaneous changes in their prey and climate. Highly correlated, synchronized and exponential increases in abundance in both baleen whales and their prey in the Southern Ocean were indicative of a dramatic increase in ocean productivity. In contrast, the demographic fluctuations observed in baleen whales and their prey in the North Atlantic Ocean were subtle, varying across taxa and time. Perhaps most important was the observation that the ocean-wide expansions and decreases in abundance that were initiated by the post-LGM global warming, continued for millennia after global temperatures stabilized, reflecting persistent, long-lasting impacts of global warming on marine fauna.

Autumn movements of fin whales (Balaenoptera physalus) from Svalbard, Norway, revealed by satellite tracking.

Insight into animal movements is essential for understanding habitat use by individuals as well as population processes and species life-history strategies. In this study, we instrumented 25 fin whales with ARGOS satellite-transmitters in Svalbard, Norway, to study their movement patterns and behaviour (Area Restricted Search (ARS), transiting or unknown) during boreal autumn/early winter. Ten of the whales stayed in the tagging area (most northerly location: 81.68°N) for their entire tracking periods (max 45 days). The other 15 whales moved in a south-westerly direction; the longest track ended off the coast of northern Africa (> 5000 km from the tagging location) after 96 days. The whales engaged in ARS behaviour intermittently throughout their southward migrations. During transit phases the whales moved quickly; one individual maintained an average horizontal speed of 9.3 km/h (travelling 223 km per day) for a period of a week. This study documents that: (1) some fin whales might remain at high latitudes during winter; (2) the whales that do migrate probably feed along the way; (3) they can maintain high transiting speed for long periods and; (4) one breeding area for this species is likely located in deep, warm water some 100 km west of Morocco.

Fin whale (Balaenoptera physalus) mitogenomics: A cautionary tale of defining sub-species from mitochondrial sequence monophyly.

The advent of massive parallel sequencing technologies has resulted in an increase of studies based upon complete mitochondrial genome DNA sequences that revisit the taxonomic status within and among species. Spatially distinct monophyly in such mitogenomic genealogies, i.e., the sharing of a recent common ancestor among con-specific samples collected in the same region has been viewed as evidence for subspecies. Several recent studies in cetaceans have employed this criterion to suggest subsequent intraspecific taxonomic revisions. We reason that employing intra-specific, spatially distinct monophyly at non-recombining, clonally inherited genomes is an unsatisfactory criterion for defining subspecies based upon theoretical (genetic drift) and practical (sampling effort) arguments. This point was illustrated by a re-analysis of a global mitogenomic assessment of fin whales, Balaenoptera physalus spp., published by Archer et al. (2013), which proposed to further subdivide the Northern Hemisphere fin whale subspecies, B. p. physalus. The proposed revision was based upon the detection of spatially distinct monophyly among North Atlantic and North Pacific fin whales in a genealogy based upon complete mitochondrial genome DNA sequences. The extended analysis conducted in this study (1676 mitochondrial control region, 162 complete mitochondrial genome DNA sequences and 20 microsatellite loci genotyped in 380 samples) revealed that the apparent monophyly among North Atlantic fin whales reported by Archer et al. (2013) to be due to low sample sizes. In conclusion, defining sub-species from monophyly (i.e., the absence of para- or polyphyly) can lead to erroneous conclusions due to relatively "trivial" aspects, such as sampling. Basic population genetic processes (i.e., genetic drift and migration) also affect the time to the most recent common ancestor and hence the probability that individuals in a sample are monophyletic.

Whole genome resequencing reveals diagnostic markers for investigating global migration and hybridization between minke whale species.

BACKGROUND: In the marine environment, where there are few absolute physical barriers, contemporary contact between previously isolated species can occur across great distances, and in some cases, may be inter-oceanic. An example of this can be seen in the minke whale species complex. Antarctic minke whales are genetically and morphologically distinct from the common minke found in the north Atlantic and Pacific oceans, and the two species are estimated to have been isolated from each other for 5 million years or more. Recent atypical migrations from the southern to the northern hemisphere have been documented and fertile hybrids and back-crossed individuals between both species have also been identified. However, it is not known whether this represents a contemporary event, potentially driven by ecosystem changes in the Antarctic, or a sporadic occurrence happening over an evolutionary time-scale. We successfully used whole genome resequencing to identify a panel of diagnostic SNPs which now enable us address this evolutionary question. RESULTS: A large number of SNPs displaying fixed or nearly fixed allele frequency differences among the minke whale species were identified from the sequence data. Five panels of putatively diagnostic markers were established on a genotyping platform for validation of allele frequencies; two panels (26 and 24 SNPs) separating the two species of minke whale, and three panels (22, 23, and 24 SNPs) differentiating the three subspecies of common minke whale. The panels were validated against a set of reference samples, demonstrating the ability to accurately identify back-crossed whales up to three generations. CONCLUSIONS: This work has resulted in the development of a panel of novel diagnostic genetic markers to address inter-oceanic and global contact among the genetically isolated minke whale species and sub-species. These markers, including a globally relevant genetic reference data set for this species complex, are now openly available for researchers interested in identifying other potential whale hybrids in the world's oceans. The approach used here, combining whole genome resequencing and high-throughput genotyping, represents a universal approach to develop similar tools for other species and population complexes.

Investigating population genetic structure in a highly mobile marine organism: the minke whale Balaenoptera acutorostrata acutorostrata in the North East Atlantic.

Inferring the number of genetically distinct populations and their levels of connectivity is of key importance for the sustainable management and conservation of wildlife. This represents an extra challenge in the marine environment where there are few physical barriers to gene-flow, and populations may overlap in time and space. Several studies have investigated the population genetic structure within the North Atlantic minke whale with contrasting results. In order to address this issue, we analyzed ten microsatellite loci and 331 bp of the mitochondrial D-loop on 2990 whales sampled in the North East Atlantic in the period 2004 and 2007-2011. The primary findings were: (1) No spatial or temporal genetic differentiations were observed for either class of genetic marker. (2) mtDNA identified three distinct mitochondrial lineages without any underlying geographical pattern. (3) Nuclear markers showed evidence of a single panmictic population in the NE Atlantic according STRUCTURE's highest average likelihood found at K = 1. (4) When K = 2 was accepted, based on the Evanno's test, whales were divided into two more or less equally sized groups that showed significant genetic differentiation between them but without any sign of underlying geographic pattern. However, mtDNA for these individuals did not corroborate the differentiation. (5) In order to further evaluate the potential for cryptic structuring, a set of 100 in silico generated panmictic populations was examined using the same procedures as above showing genetic differentiation between two artificially divided groups, similar to the aforementioned observations. This demonstrates that clustering methods may spuriously reveal cryptic genetic structure. Based upon these data, we find no evidence to support the existence of spatial or cryptic population genetic structure of minke whales within the NE Atlantic. However, in order to conclusively evaluate population structure within this highly mobile species, more markers will be required.

Hybrids between common and Antarctic minke whales are fertile and can back-cross.

BACKGROUND: Minke whales are separated into two genetically distinct species: the Antarctic minke whale found in the southern hemisphere, and the common minke whale which is cosmopolitan. The common minke whale is further divided into three allopatric sub-species found in the North Pacific, southern hemisphere, and the North Atlantic. Here, we aimed to identify the genetic ancestry of a pregnant female minke whale captured in the North Atlantic in 2010, and her fetus, using data from the mtDNA control region, 11 microsatellite loci and a sex determining marker. RESULTS: All statistical parameters demonstrated that the mother was a hybrid displaying maternal and paternal contribution from North Atlantic common and Antarctic minke whales respectively. Her female fetus displayed greater genetic similarity to North Atlantic common minke whales than herself, strongly suggesting that the hybrid mother had paired with a North Atlantic common minke whale. CONCLUSION: This study clearly demonstrates, for the first time, that hybrids between minke whale species may be fertile, and that they can back-cross. Whether contact between these species represents a contemporary event linked with documented recent changes in the Antarctic ecosystem, or has occurred at a low frequency over many years, remains open.

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.

Migration of Antarctic minke whales to the Arctic.

The Antarctic minke whale (Balaenoptera bonaerensis), and the common minke whale found in the North Atlantic (Balaenoptera acutorostrata acutorostrata), undertake synchronized seasonal migrations to feeding areas at their respective poles during spring, and to the tropics in the autumn where they overwinter. Differences in the timing of seasons between hemispheres prevent these species from mixing. Here, based upon analysis of mitochondrial and microsatellite DNA profiles, we report the observation of a single B. bonaerensis in 1996, and a hybrid with maternal contribution from B. bonaerensis in 2007, in the Arctic Northeast Atlantic. Paternal contribution was not conclusively resolved. This is the first documentation of B. bonaerensis north of the tropics, and, the first documentation of hybridization between minke whale species.

Nuclear and mitochondrial markers reveal distinctiveness of a small population of bottlenose whales (Hyperoodon ampullatus) in the western North Atlantic.

Small populations at the edge of a species' distribution can represent evolutionary relics left behind after range contractions due to climate change or human exploitation. The distinctiveness and genetic diversity of a small population of bottlenose whales in the Gully, a submarine canyon off Nova Scotia, was quantified by comparison to other North Atlantic populations using 10 microsatellites and mitrochondrial DNA (mtDNA) control region sequences (434 bp). Both markers confirmed the distinctiveness of the Gully (n = 34) from the next nearest population, off Labrador (n = 127; microsatellites -F(ST)= 0.0243, P < 0.0001; mtDNA -Phi(ST) = 0.0456, P < 0.05). Maximum likelihood microsatellite estimates suggest that less than two individuals per generation move between these areas, refuting the hypothesis of population links through seasonal migration. Both males and females appear to be philopatric, based on significant differentiation at both genomes and similar levels of structuring among the sexes for microsatellites. mtDNA diversity was very low in all populations (h = 0.51, pi = 0.14%), a pattern which may be due to selective sweeps associated with this species' extreme deep-diving ecology. Whaling had a substantial impact on bottlenose whale abundance, with over 65 000 animals killed before the hunt ceased in the early 1970s. Genetic diversity was similar among all populations, however, and no signal for bottlenecks was detected, suggesting that the Gully is not a relic of a historically wider distribution. Instead, this unique ecosystem appears to have long provided a stable year-round habitat for a distinct population of bottlenose whales.