Ancient and modern DNA track temporal and spatial population dynamics in the European fallow deer since the Eemian interglacial.

Anthropogenic factors have impacted the diversity and evolutionary trajectory of various species. This can be through factors such as pressure on population size or range, habitat fragmentation, or extensive manipulation and translocation. Here we use time-calibrated data to better understand the pattern and processes of evolution in the heavily manipulated European fallow deer (Dama dama). During the Pleistocene, fallow deer had a broad distribution across Europe and were found as far north as Britain during the Eemian interglacial. The last glacial period saw fallow deer retreat to southern refugia and they did not disperse north afterwards. Their recolonisation was mediated by people and, from northern Europe and the British Isles, fallow deer were transported around the world. We use ancient and modern mitochondrial DNA (mtDNA) and mitogenomic data from Eemian Britain to assess the pattern of change in distribution and lineage structure across Europe over time. We find founder effects and mixed lineages in the northern populations, and stability over time for populations in southern Europe. The Eemian sample was most similar to a lineage currently in Italy, suggesting an early establishment of the relevant refuge. We consider the implications for the integration of anthropogenic and natural processes towards a better understanding of the evolution of fallow deer in Europe.

A global cline in a colour polymorphism suggests a limited contribution of gene flow towards the recovery of a heavily exploited marine mammal.

Evaluating how populations are connected by migration is important for understanding species resilience because gene flow can facilitate recovery from demographic declines. We therefore investigated the extent to which migration may have contributed to the global recovery of the Antarctic fur seal (Arctocephalus gazella), a circumpolar distributed marine mammal that was brought to the brink of extinction by the sealing industry in the eighteenth and nineteenth centuries. It is widely believed that animals emigrating from South Georgia, where a relict population escaped sealing, contributed to the re-establishment of formerly occupied breeding colonies across the geographical range of the species. To investigate this, we interrogated a genetic polymorphism (S291F) in the melanocortin 1 receptor gene, which is responsible for a cream-coloured phenotype that is relatively abundant at South Georgia and which appears to have recently spread to localities as far afield as Marion Island in the sub-Antarctic Indian Ocean. By sequencing a short region of this gene in 1492 pups from eight breeding colonies, we showed that S291F frequency rapidly declines with increasing geographical distance from South Georgia, consistent with locally restricted gene flow from South Georgia mainly to the South Shetland Islands and Bouvetøya. The S291F allele was not detected farther afield, suggesting that although emigrants from South Georgia may have been locally important, they are unlikely to have played a major role in the recovery of geographically more distant populations.

Hybridization in bottlenose dolphins-A case study of Tursiops aduncus × T. truncatus hybrids and successful backcross hybridization events.

The bottlenose dolphin, genus Tursiops is one of the best studied of all the Cetacea with a minimum of two species widely recognised. Common bottlenose dolphins (T. truncatus), are the cetacean species most frequently held in captivity and are known to hybridize with species from at least 6 different genera. In this study, we document several intra-generic hybridization events between T. truncatus and T. aduncus held in captivity. We demonstrate that the F1 hybrids are fertile and can backcross producing apparently healthy offspring, thereby showing introgressive inter-specific hybridization within the genus. We document that female F1 hybrids can reach sexual maturity at 4 yr and 3 mo of age, and can become pregnant and give birth before being fully weaned. The information presented has implications for understanding hybrid reticulation among cetacean species and practical implications for captive facilities housing either Tursiops species or hybrids thereof.

Cryptic lineage differentiation among Indo-Pacific bottlenose dolphins (Tursiops aduncus) in the northwest Indian Ocean.

Phylogeography can provide insight into the potential for speciation and identify geographic regions and evolutionary processes associated with species richness and evolutionary endemism. In the marine environment, highly mobile species sometimes show structured patterns of diversity, but the processes isolating populations and promoting differentiation are often unclear. The Delphinidae (oceanic dolphins) are a striking case in point and, in particular, bottlenose dolphins (Tursiops spp.). Understanding the radiation of species in this genus is likely to provide broader inference about the processes that determine patterns of biogeography and speciation, because both fine-scale structure over a range of kilometers and relative panmixia over an oceanic range are known for Tursiops populations. In our study, novel Tursiops spp. sequences from the northwest Indian Ocean (including mitogenomes and two nuDNA loci) are included in a worldwide Tursiops spp. phylogeographic analysis. We discover a new 'aduncus' type lineage in the Arabian Sea (off India, Pakistan and Oman) that diverged from the Australasian lineage ∼261 Ka. Effective management of coastal dolphins in the region will need to consider this new lineage as an evolutionarily significant unit. We propose that the establishment of this lineage could have been in response to climate change during the Pleistocene and show data supporting hypotheses for multiple divergence events, including vicariance across the Indo-Pacific barrier and in the northwest Indian Ocean. These data provide valuable transferable inference on the potential mechanisms for population and species differentiation across this geographic range.

Strong population structure in a species manipulated by humans since the Neolithic: the European fallow deer (Dama dama dama).

Species that have been translocated and otherwise manipulated by humans may show patterns of population structure that reflect those interactions. At the same time, natural processes shape populations, including behavioural characteristics like dispersal potential and breeding system. In Europe, a key factor is the geography and history of climate change through the Pleistocene. During glacial maxima throughout that period, species in Europe with temperate distributions were forced south, becoming distributed among the isolated peninsulas represented by Anatolia, Italy and Iberia. Understanding modern patterns of diversity depends on understanding these historical population dynamics. Traditionally, European fallow deer (Dama dama dama) are thought to have been restricted to refugia in Anatolia and possibly Sicily and the Balkans. However, the distribution of this species was also greatly influenced by human-mediated translocations. We focus on fallow deer to better understand the relative influence of these natural and anthropogenic processes. We compared modern fallow deer putative populations across a broad geographic range using microsatellite and mitochondrial DNA loci. The results revealed highly insular populations, depauperate of genetic variation and significantly differentiated from each other. This is consistent with the expectations of drift acting on populations founded by small numbers of individuals, and reflects known founder populations in the north. However, there was also evidence for differentiation among (but not within) physically isolated regions in the south, including Iberia. In those regions we find evidence for a stronger influence from natural processes than may be expected for a species with such strong, known anthropogenic influence.

Post-glacial habitat release and incipient speciation in the genus Delphinus.

The role of ecological and changing environmental factors in the radiation of species diversity is a fundamental question in evolutionary biology. Of particular interest is the potential for these factors to determine the boundary between what we would consider differentiation among populations and incipient speciation. Dolphins in the genus Delphinus provide a useful test case, exhibiting morphological variation in beak length, coloration and body size across their wide geographic distribution, and in particular among coastal and more pelagic habitats. Two species have been proposed, D. delphis and D. capensis, but morphologically similar allopatric populations are not monophyletic, indicating that the mostly coastal 'long-beaked' D. capensis form is not a single globally distributed species. However, the sympatric populations in the Eastern North Pacific currently designated as these two species are both morphologically and genetically differentiated. Here we use microsatellite DNA and mitochondrial DNA markers to investigate the evolutionary mechanisms that led to this incipient speciation event. We used coalescent and assignment methods to investigate the timing and extent of reproductive isolation. Our data indicate that although there is some level of on-going gene flow, the putative species found in the Eastern North Pacific are reciprocally monophyletic. The timing of isolation appears to be associated with regional changes in paleoceanographic conditions within the Holocene timeframe.

Population differentiation in the context of Holocene climate change for a migratory marine species, the southern elephant seal.

Understanding observed patterns of connectivity requires an understanding of the evolutionary processes that determine genetic structure among populations, with the most common models being associated with isolation by distance, allopatry or vicariance. Pinnipeds are annual breeders with the capacity for extensive range overlap during seasonal migrations, establishing the potential for the evolution of isolation by distance. Here, we assess the pattern of differentiation among six breeding colonies of the southern elephant seal, Mirounga leonina, based on mtDNA and 15 neutral microsatellite DNA markers, and consider measures of their demography and connectivity. We show that all breeding colonies are genetically divergent and that connectivity in this highly mobile pinniped is not strongly associated with geographic distance, but more likely linked to Holocene climate change and demographic processes. Estimates of divergence times between populations were all after the last glacial maximum, and there was evidence for directional migration in a clockwise pattern (with the prevailing current) around the Antarctic. We discuss the mechanisms by which climate change may have contributed to the contemporary genetic structure of southern elephant seal populations and the broader implications.

Phylogenomics of the killer whale indicates ecotype divergence in sympatry.

For many highly mobile species, the marine environment presents few obvious barriers to gene flow. Even so, there is considerable diversity within and among species, referred to by some as the 'marine speciation paradox'. The recent and diverse radiation of delphinid cetaceans (dolphins) represents a good example of this. Delphinids are capable of extensive dispersion and yet many show fine-scale genetic differentiation among populations. Proposed mechanisms include the division and isolation of populations based on habitat dependence and resource specializations, and habitat release or changing dispersal corridors during glacial cycles. Here we use a phylogenomic approach to investigate the origin of differentiated sympatric populations of killer whales (Orcinus orca). Killer whales show strong specialization on prey choice in populations of stable matrifocal social groups (ecotypes), associated with genetic and phenotypic differentiation. Our data suggest evolution in sympatry among populations of resource specialists.

Influence of Holocene environmental change and anthropogenic impact on the diversity and distribution of roe deer.

Extant patterns of population structure and levels of diversity are a consequence of factors that vary in both space and time. Our objective in this study is to investigate a species that has responded to both natural and anthropogenic changes in ways that have shaped modern populations and provide insight into the key processes. The roe deer (Capreolus capreolus) is one of the two species of deer native to Britain. During the last glacial maximum (LGM), the British habitat was largely under ice and there was a land bridge to mainland Europe. As the Earth warmed during the early Holocene, the land bridge was lost. Subsequent hunting on the British mainland left the southern region extirpated of roe deer, whereas a refugial population remained in the north. Later reintroductions from Europe led to population expansion, especially in southern United Kingdom. Here, we combine data from ancient and modern DNA to track population dynamics and patterns of connectivity, and test hypotheses about the influence of natural and anthropogenic environmental change. We find that past expansion and divergence events coincided with a warming environment and the subsequent closure of the land bridge between Europe and the United Kingdom. We also find turnover in British roe deer haplotypes between the late-Holocene and modern day that have likely resulted from recent human disturbance activities such as habitat perturbation, overhunting and restocking.

Atypical panmixia in a European dolphin species (Delphinus delphis): implications for the evolution of diversity across oceanic boundaries.

Despite the scarcity of geographical barriers in the ocean environment, delphinid cetaceans often exhibit marked patterns of population structure on a regional scale. The European coastline is a prime example, with species exhibiting population structure across well-defined environmental boundaries. Here we undertake a comprehensive population genetic study on the European common dolphin (Delphinus delphis, based on 492 samples and 15 loci) and establish that this species shows exceptional panmixia across most of the study range. We found differentiation only between the eastern and western Mediterranean, consistent with earlier studies, and here use approximate Bayesian computations to explore different scenarios to explain the observed pattern. Our results suggest that a recent population bottleneck likely contributed significantly to the differentiation of the Eastern Mediterranean population (in Greek waters). This interpretation is consistent with independent census data that suggest a sharp population decline in the recent past. The implication is that an unperturbed population may currently show panmixia across the full study range. This exception to the more typical pattern of population structure seen for other regional dolphin species (and for common dolphin populations elsewhere in the world) suggests particular ecological or life-history traits distinct to this species in European waters.

Phenotypic and genetic divergence among harbour porpoise populations associated with habitat regions in the North Sea and adjacent seas.

Determining the mechanisms that generate population structure is essential to the understanding of speciation and the evolution of biodiversity. Here, we investigate a geographical range that transects two habitat gradients, the North Sea to North Atlantic transition, and the temperate to subpolar regions. We studied the harbour porpoise (Phocoena phocoena), a small odontocete inhabiting both subpolar and temperate waters. To assess differentiation among putative populations, we measured morphological variation at cranial traits (N = 462 individuals) and variation at eight microsatellite loci for 338 of the same individuals from Norwegian, British and Danish waters. Significant morphological differentiation reflected the size of the buccal cavity. Porpoises forage in relatively shallow waters preying mainly on benthic species in British and Danish waters, and on mesopelagic and pelagic fish off the coast of Norway. We suggest that the observed differentiation may be explained by resource specialization and either adaptation or developmental responses to different local habitats.

Environmental factors associated with genetic and phenotypic divergence among sympatric populations of Arctic charr (Salvelinus alpinus).

The mechanisms by which phenotypic and genetic divergence may occur among sympatric, conspecific populations have been widely discussed but are still not well understood. Possible mechanisms include assortative mating based on morphology or variation in the reproductive behaviour of phenotypes, and both have been suggested to be relevant to the differentiation of salmonid populations in post-glacial lakes. Here, we studied Arctic charr (Salvelinus alpinus) in Windermere, where putative populations are defined by spatial and temporal variation in spawning. Genetic differentiation was assessed based on nine microsatellite loci, and phenotypic variation was assessed from morphometric characters. We test hypotheses about the relative role of morphology, spawning season and spawning habitat in the evolution of genetic divergence among these populations. Distinct from other lake systems, we find that both morphological and genetic differentiation are restricted primarily to one of two interconnecting basins, that genetic and morphological differentiation are decoupled in this lake and that both phenotype and environment have changed over the last 20 years. The implication is that breeding habitat plays a primary role in isolating populations that differentiate by drift and that phenotypically plastic changes, potentially related to foraging specializations, have either become secondarily decoupled from the genetically defined populations or were never fundamental in driving the evolution of genetic diversity in the Windermere system.

Genetic panmixia and demographic dependence across the North Atlantic in the deep-sea fish, blue hake (Antimora rostrata).

The efficient investment of resources and effort into conservation strategies depends on the accurate identification of management units. At the same time, understanding the processes by which population structure evolves requires an understanding of the conditions under which panmixia may exist. Here, we study a species with an unusual, apparently sex-biased pattern of distribution, and test the hypothesis that distribution processes associated with this pattern (for example, congregating at a single dominant spawning site or periodic mixing during reproduction) could lead to panmixia over a large geographic range. Using 13 microsatellite markers, we compared 393 blue hake (Antimora rostrata) from 11 sample sites across a geographic range of over 3000 km, and found no evidence of population structure. We estimated current effective population size and found it to be large (~15,000) across the sampled area. In addition, we used simulation models to test expectations about demographic correlation among populations and our ability to detect relevant levels of gene flow. All data were consistent with the interpretation of long-range panmixia.

Social cohesion among kin, gene flow without dispersal and the evolution of population genetic structure in the killer whale (Orcinus orca).

In social species, breeding system and gregarious behavior are key factors influencing the evolution of large-scale population genetic structure. The killer whale is a highly social apex predator showing genetic differentiation in sympatry between populations of foraging specialists (ecotypes), and low levels of genetic diversity overall. Our comparative assessments of kinship, parentage and dispersal reveal high levels of kinship within local populations and ongoing male-mediated gene flow among them, including among ecotypes that are maximally divergent within the mtDNA phylogeny. Dispersal from natal populations was rare, implying that gene flow occurs without dispersal, as a result of reproduction during temporary interactions. Discordance between nuclear and mitochondrial phylogenies was consistent with earlier studies suggesting a stochastic basis for the magnitude of mtDNA differentiation between matrilines. Taken together our results show how the killer whale breeding system, coupled with social, dispersal and foraging behaviour, contributes to the evolution of population genetic structure.

Development of 10 microsatellite loci in the ling (Molva molva).

We developed primers for two dinucleotide and eight tetranucleotide microsatellite loci in a marine fish, the ling (Molva molva). All markers were obtained from partial genomic DNA libraries and characterized in 55 unrelated individuals from one putative population. The number of alleles ranged from five to 24 (average 10.5) per locus, and the observed heterozygosity ranged from 0.218 to 0.981 (average 0.643). No loci amplified in two other gadoid species tested, the Atlantic cod (Gadus morhua) and the tusk (Brosme brosme).

Ancient human mtDNA genotypes from England reveal lost variation over the last millennium.

We analysed the historical genetic diversity of human populations in Europe at the mtDNA control region for 48 ancient Britons who lived between ca AD 300 and 1000, and compared these with 6320 modern mtDNA genotypes from England and across Europe and the Middle East. We found that the historical sample shows greater genetic diversity than for modern England and other modern populations, indicating the loss of diversity over the last millennium. The pattern of haplotypic diversity was clearly European in the ancient sample, representing each of the modern haplogroups. There was also increased representation of one of the ancient haplotypes in modern populations. We consider these results in the context of possible selection or stochastic processes.

Holocene elephant seal distribution implies warmer-than-present climate in the Ross Sea.

We show that southern elephant seal (Mirounga leonina) colonies existed proximate to the Ross Ice Shelf during the Holocene, well south of their core sub-Antarctic breeding and molting grounds. We propose that this was due to warming (including a previously unrecognized period from approximately 1,100 to 2,300 (14)C yr B.P.) that decreased coastal sea ice and allowed penetration of warmer-than-present climate conditions into the Ross Embayment. If, as proposed in the literature, the ice shelf survived this period, it would have been exposed to environments substantially warmer than present.

Phylogeography and alpha taxonomy of the common dolphin (Delphinus sp.).

The resolution of taxonomic classifications for delphinid cetaceans has been problematic, especially for species in the genera Delphinus, Tursiops and Stenella. The frequent lack of correspondence between morphological and genetic differentiation in these species raises questions about the mechanisms responsible for their evolution. In this study we focus on the genus Delphinus, and use molecular markers to address questions about speciation and the evolution of population structure. Delphinus species have a worldwide distribution and show a high degree of morphological variation. Two distinct morphotypes, long-beaked and short-beaked, have been considered different species named D. capensis and D. delphis, respectively. However, genetic differentiation between these two forms has only been demonstrated in the Pacific. We analysed samples from eight different geographical regions, including two morphologically defined long-beaked form populations, and compared these with the eastern North Pacific populations. We found high differentiation among the populations described as long-beaked instead of the expected monophyly, suggesting that these populations may have evolved from independent events converging on the same morphotype. We observed low genetic differentiation among the short-beaked populations across a large geographical scale. We interpret these phylogeographical patterns in the context of life history and population structure in related species.