Genomics reveals the role of admixture in the evolution of structure among sperm whale populations within the Mediterranean Sea.

In oceanic ecosystems, the nature of barriers to gene flow and the processes by which populations may become isolated are different from the terrestrial environment, and less well understood. In this study we investigate a highly mobile species (the sperm whale, Physeter macrocephalus) that is genetically differentiated between an open North Atlantic population and the populations in the Mediterranean Sea. We apply high-resolution single nucleotide polymorphism (SNP) analysis to study the nature of barriers to gene flow in this system, assessing the putative boundary into the Mediterranean (Strait of Gibraltar and Alboran Sea region), and including novel analyses on structuring among sperm whale populations within the Mediterranean basin. Our data support a recent founding of the Mediterranean population, around the time of the last glacial maximum, and show concerted historical demographic profiles in both the Atlantic and the Mediterranean. In each region there is evidence for a population decline around the time of the founder event. The largest decline was seen within the Mediterranean Sea where effective population size is substantially lower (especially in the eastern basin). While differentiation is strongest at the Atlantic/Mediterranean boundary, there is also weaker but significant differentiation between the eastern and western basins of the Mediterranean Sea. We propose, however, that the mechanisms are different. While post-founding gene flow was reduced between the Mediterranean and Atlantic populations, within the Mediterranean an important factor differentiating the basins is probably a greater degree of admixture between the western basin and the North Atlantic and some level of isolation between the western and eastern Mediterranean basins. Subdivision within the Mediterranean Sea exacerbates conservation concerns and will require consideration of what distinct impacts may affect populations in the two basins.

Runs of homozygosity in killer whale genomes provide a global record of demographic histories.

Runs of homozygosity (ROH) occur when offspring inherit haplotypes that are identical by descent from each parent. Length distributions of ROH are informative about population history; specifically, the probability of inbreeding mediated by mating system and/or population demography. Here, we investigated whether variation in killer whale (Orcinus orca) demographic history is reflected in genome-wide heterozygosity and ROH length distributions, using a global data set of 26 genomes representative of geographic and ecotypic variation in this species, and two F1 admixed individuals with Pacific-Atlantic parentage. We first reconstructed demographic history for each population as changes in effective population size through time using the pairwise sequential Markovian coalescent (PSMC) method. We found a subset of populations declined in effective population size during the Late Pleistocene, while others had more stable demography. Genomes inferred to have undergone ancestral declines in effective population size, were autozygous at hundreds of short ROH (<1 Mb), reflecting high background relatedness due to coalescence of haplotypes deep within the pedigree. In contrast, longer and therefore younger ROH (>1.5 Mb) were found in low latitude populations, and populations of known conservation concern. These include a Scottish killer whale, for which 37.8% of the autosomes were comprised of ROH >1.5 Mb in length. The fate of this population, in which only two adult males have been sighted in the past five years, and zero fecundity over the last two decades, may be inextricably linked to its demographic history and consequential inbreeding depression.

Expanding protected areas to encompass the conservation of the endangered common dolphin (Delphinus delphis) in the Alboran Sea.

The Natura 2000 network is the centerpiece of the European Union conservation strategy to safeguard priority species and habitats. The question of whether other co-occurring species of conservation concern may also benefit from this network, however, remains largely unknown. Here, we used a systematic approach (MARXAN) for i) evaluating if the current Natura 2000 network in the Alboran Sea (western Mediterranean Sea), initially proposed to protect the common bottlenose dolphin (Tursiops truncatus) and priority habitats, is also spatially protecting the endangered common dolphin (Delphinus delphis), and ii) identifying additional marine areas that should be protected to reach adequate conservation targets for the common dolphin. While the current Natura 2000 network encompass ca. 22% of predicted abundances for common dolphins, this percentage might be enhanced by protecting coastal areas nearby the Strait of Gibraltar. However, dolphins and fisheries largely overlap spatially nearby the coastline, and only segregate in offshore areas that represent the marginal distribution of the species. Thus, conservation decision-makers must achieve a trade-off between cetacean conservation and fisheries by combining an area-based approach (i.e., new protected areas close to the Strait of Gibraltar) together with a basin-wide threat-based approach (e.g., regulation of fisheries).

Wait your turn, North Atlantic fin whales share a common feeding ground sequentially.

Highly migratory marine species pose a challenge for the identification of management units due to the absence of clear oceanographic barriers. The population structure of North Atlantic fin whales has been investigated since the start of whaling operations but is still the subject of an ongoing scientific debate. Here we measured stable isotopes of carbon, nitrogen and oxygen in skin samples collected from 151 individuals from western Iceland, Galicia (NW Spain), the Azores archipelago and the Strait of Gibraltar (SoG). We found spatiotemporal differences in stable isotope ratios suggesting that fin whales sampled in these four areas may share a common feeding ground within the Northeast Atlantic at different times during the year. Our results also suggest that SoG whales use this common feeding ground in summer but exploit Mediterranean resources during the winter months, further supporting the existence of a limited but current exchange of individuals between these two basins.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Diet of bottlenose dolphins (Tursiops truncatus) from the Gulf of Cadiz: Insights from stomach content and stable isotope analyses.

The ecological role of species can vary among populations depending on local and regional differences in diet. This is particularly true for top predators such as the bottlenose dolphin (Tursiops truncatus), which exhibits a highly varied diet throughout its distribution range. Local dietary assessments are therefore critical to fully understand the role of this species within marine ecosystems, as well as its interaction with important ecosystem services such as fisheries. Here, we combined stomach content analyses (SCA) and stable isotope analyses (SIA) to describe bottlenose dolphins diet in the Gulf of Cadiz (North Atlantic Ocean). Prey items identified using SCA included European conger (Conger conger) and European hake (Merluccius merluccius) as the most important ingested prey. However, mass-balance isotopic mixing model (MixSIAR), using δ13C and δ15N, indicated that the assimilated diet consisted mainly on Sparidae species (e.g. seabream, Diplodus annularis and D. bellottii, rubberlip grunt, Plectorhinchus mediterraneus, and common pandora, Pagellus erythrinus) and a mixture of other species including European hake, mackerels (Scomber colias, S. japonicus and S. scombrus), European conger, red bandfish (Cepola macrophthalma) and European pilchard (Sardina pilchardus). These contrasting results highlight differences in the temporal and taxonomic resolution of each approach, but also point to potential differences between ingested (SCA) and assimilated (SIA) diets. Both approaches provide different insights, e.g. determination of consumed fish biomass for the management of fish stocks (SCA) or identification of important assimilated prey species to the consumer (SIA).

Insecticide pyrethroids in liver of striped dolphin from the Mediterranean Sea.

Pyrethroid pesticides were analysed in liver of striped dolphin (Stenella coeruleoalba) from the Alboran Sea (south of Spain, Mediterranean Sea). The occurrence and bioaccumulation of pyrethroid insecticides in marine mammal tissues from the northern hemisphere had never been determined before. Pyrethroids were detected in 87% of the specimens with a mean total concentration of 300 ng g-1 lw ±â€Š932 (range 2.7-5200 ng g-1 lw). Permethrin and tetramethrin were the main contributors to the pyrethroid profiles, with enantiospecific accumulation for the first and isomer specific accumulation for the latter. Bioaccumulation of pyrethroids was unlike that of persistent organic pollutants (POPs), as pyrethroid concentrations were not correlated to the maturity stage of the specimens. Concentrations slightly increased from calves to juveniles, whereas juveniles presented similar concentrations to adults. Metabolization of pyrethroids after achieving sexual maturity might account for this pattern.

PCB pollution continues to impact populations of orcas and other dolphins in European waters.

Organochlorine (OC) pesticides and the more persistent polychlorinated biphenyls (PCBs) have well-established dose-dependent toxicities to birds, fish and mammals in experimental studies, but the actual impact of OC pollutants on European marine top predators remains unknown. Here we show that several cetacean species have very high mean blubber PCB concentrations likely to cause population declines and suppress population recovery. In a large pan-European meta-analysis of stranded (n = 929) or biopsied (n = 152) cetaceans, three out of four species:- striped dolphins (SDs), bottlenose dolphins (BNDs) and killer whales (KWs) had mean PCB levels that markedly exceeded all known marine mammal PCB toxicity thresholds. Some locations (e.g. western Mediterranean Sea, south-west Iberian Peninsula) are global PCB "hotspots" for marine mammals. Blubber PCB concentrations initially declined following a mid-1980s EU ban, but have since stabilised in UK harbour porpoises and SDs in the western Mediterranean Sea. Some small or declining populations of BNDs and KWs in the NE Atlantic were associated with low recruitment, consistent with PCB-induced reproductive toxicity. Despite regulations and mitigation measures to reduce PCB pollution, their biomagnification in marine food webs continues to cause severe impacts among cetacean top predators in European seas.

Individual improvements and selective mortality shape lifelong migratory performance.

Billions of organisms, from bacteria to humans, migrate each year and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1-27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic.

Despite no obvious barrier to gene flow, historical environmental processes and ecological specializations can lead to genetic differentiation in highly mobile animals. Ecotypes emerged in several large mammal species as a result of niche specializations and/or social organization. In the North-West Atlantic, two distinct bottlenose dolphin (Tursiops truncatus) ecotypes (i.e. 'coastal' and 'pelagic') have been identified. Here, we investigated the genetic population structure of North-East Atlantic (NEA) bottlenose dolphins on a large scale through the analysis of 381 biopsy-sampled or stranded animals using 25 microsatellites and a 682-bp portion of the mitochondrial control region. We shed light on the likely origin of stranded animals using a carcass drift prediction model. We showed, for the first time, that coastal and pelagic bottlenose dolphins were highly differentiated in the NEA. Finer-scale population structure was found within the two groups. We suggest that distinct founding events followed by parallel adaptation may have occurred independently from a large Atlantic pelagic population in the two sides of the basin. Divergence could be maintained by philopatry possibly as a result of foraging specializations and social organization. As coastal environments are under increasing anthropogenic pressures, small and isolated populations might be at risk and require appropriate conservation policies to preserve their habitats. While genetics can be a powerful first step to delineate ecotypes in protected and difficult to access taxa, ecotype distinction should be further documented through diet studies and the examination of cranial skull features associated with feeding.

As main meal for sperm whales: plastics debris.

Marine debris has been found in marine animals since the early 20th century, but little is known about the impacts of the ingestion of debris in large marine mammals. In this study we describe a case of mortality of a sperm whale related to the ingestion of large amounts of marine debris in the Mediterranean Sea (4th published case worldwide to our knowledge), and discuss it within the context of the spatial distribution of the species and the presence of anthropogenic activities in the area that could be the source of the plastic debris found inside the sperm whale. The spatial distribution modelled for the species in the region shows that these animals can be seen in two distinct areas: near the waters of Almería, Granada and Murcia and in waters near the Strait of Gibraltar. The results shows how these animals feed in waters near an area completely flooded by the greenhouse industry, making them vulnerable to its waste products if adequate treatment of this industry's debris is not in place. Most types of these plastic materials have been found in the individual examined and cause of death was presumed to be gastric rupture following impaction with debris, which added to a previous problem of starvation. The problem of plastics arising from greenhouse agriculture should have a relevant section in the conservation plans and should be a recommendation from ACCOBAMS due to these plastics' and sperm whales' high mobility in the Mediterranean Sea.

The role of synchronized swimming as affiliative and anti-predatory behavior in long-finned pilot whales.

Synchronized swimming in cetaceans has been hypothesized to play a role in affiliative processes as well as anti-predatory responses. We compared observed variation in synchronized swimming at two research sites in relation to disturbance exposure to test these two hypotheses. This study describes and quantifies pair synchronization in long-finned pilot whales at the Strait of Gibraltar, Spain and Cape Breton, Canada. Synchronization differed depending on the behavioral state and the response is different in the two sites leading to the conclusion that environment can shape the occurrence and magnitude of certain behaviors. We also analyzed intra-population variations in synchronization among 4 social units of Pilot whales in the Strait of Gibraltar and the results of this study confirmed the affiliative role of synchronization and highlighted an influence of disturbance on synchronization. We can conclude that synchronization is a common behavior in long-finned pilot whales that allow for close proximity and rapid coordinated response of individuals, with the multiple functions of showing affiliation and reacting to disturbance.

Mitogenomic phylogenetic analyses of the Delphinidae with an emphasis on the Globicephalinae.

BACKGROUND: Previous DNA-based phylogenetic studies of the Delphinidae family suggest it has undergone rapid diversification, as characterised by unresolved and poorly supported taxonomic relationships (polytomies) for some of the species within this group. Using an increased amount of sequence data we test between alternative hypotheses of soft polytomies caused by rapid speciation, slow evolutionary rate and/or insufficient sequence data, and hard polytomies caused by simultaneous speciation within this family. Combining the mitogenome sequences of five new and 12 previously published species within the Delphinidae, we used Bayesian and maximum-likelihood methods to estimate the phylogeny from partitioned and unpartitioned mitogenome sequences. Further ad hoc tests were then conducted to estimate the support for alternative topologies. RESULTS: We found high support for all the relationships within our reconstructed phylogenies, and topologies were consistent between the Bayesian and maximum-likelihood trees inferred from partitioned and unpartitioned data. Resolved relationships included the placement of the killer whale (Orcinus orca) as sister taxon to the rest of the Globicephalinae subfamily, placement of the Risso's dolphin (Grampus griseus) within the Globicephalinae subfamily, removal of the white-beaked dolphin (Lagenorhynchus albirostris) from the Delphininae subfamily and the placement of the rough-toothed dolphin (Steno bredanensis) as sister taxon to the rest of the Delphininae subfamily rather than within the Globicephalinae subfamily. The additional testing of alternative topologies allowed us to reject all other putative relationships, with the exception that we were unable to reject the hypothesis that the relationship between L. albirostris and the Globicephalinae and Delphininae subfamilies was polytomic. CONCLUSION: Despite their rapid diversification, the increased sequence data yielded by mitogenomes enables the resolution of a strongly supported, bifurcating phylogeny, and a chronology of the divergences within the Delphinidae family. This highlights the benefits and potential application of large mitogenome datasets to resolve long-standing phylogenetic uncertainties.

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.