The impact of past climate change on genetic variation and population connectivity in the Icelandic arctic fox

Previous studies have suggested that the presence of sea ice is an important factor in facilitating migration and determining the degree of genetic isolation among contemporary arctic fox populations. Because the extent of sea ice is dependent upon global temperatures, periods of significant cooling would have had a major impact on fox population connectivity and genetic variation. We tested this hypothesis by extracting and sequencing mitochondrial control region sequences from 17 arctic foxes excavated from two late-ninth-century to twelfth-century AD archaeological sites in northeast Iceland, both of which predate the Little Ice Age (approx. sixteenth to nineteenth century). Despite the fact that five haplotypes have been observed in modern Icelandic foxes, a single haplotype was shared among all of the ancient individuals. Results from simulations within an approximate Bayesian computation framework suggest that the rapid increase in Icelandic arctic fox haplotype diversity can only be explained by sea-ice-mediated fox immigration facilitated by the Little Ice Age.     

Population history and genetic structure of a circumpolar species: the arctic fox

The circumpolar arctic fox Alopex lagopus thrives in cold climates and has a high migration rate involving long-distance movements. Thus, it differs from many temperate taxa that were subjected to cyclical restriction in glacial refugia during the Ice Ages. We investigated population history and genetic structure through mitochondrial control region variation in 191 arctic foxes from throughout the arctic. Several haplotypes had a Holarctic distribution and no phylogeographical structure was found. Furthermore, there was no difference in haplotype diversity between populations inhabiting previously glaciated and unglaciated regions. This suggests current gene flow among the studied populations, with the exception of those in Iceland, which is surrounded by year-round open water. Arctic foxes have often been separated into two ecotypes: 'lemming' and 'coastal'. An analysis of molecular variance suggested particularly high gene flow among populations of the 'lemming' ecotype. This could be explained by their higher migration rate and reduced fitness in migrants between ecotypes. A mismatch analysis indicated a sudden expansion in population size around 118 000 BP, which coincides with the last interglacial. We propose that glacial cycles affected the arctic fox in a way opposite to their effect on temperate species, with interglacials leading to short-term isolation in northern refugia.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 79–89.     

Temporal variability in arctic fox diet as reflected in stable-carbon isotopes; the importance of sea ice

Consumption of marine foods by terrestrial predators can lead to increased predator densities, potentially impacting their terrestrial resources. For arctic foxes (Alopex lagopus), access to such marine foods in winter depends on sea ice, which is threatened by global climate change. To quantify the importance of marine foods (seal carrion and seal pups) and document temporal variation in arctic fox diet I measured the ratios of the stable isotopes of carbon (¹³C/¹²C) in hair of arctic foxes near Cape Churchill, Manitoba, from 1994 to 1997. These hair samples were compared to the stable carbon isotope ratios of several prey species. Isotopic differences between seasonally dimorphic pelage types indicated a diet with a greater marine content in winter when sea ice provided access to seal carrion. Annual variation in arctic fox diet in both summer and winter was correlated with lemming abundance. Marine food sources became much more important in winters with low lemming populations, accounting for nearly half of the winter protein intake following a lemming decline. Potential alternative summer foods with isotopic signatures differing from lemmings included goose eggs and caribou, but these were unavailable in winter. Reliance on marine food sources in winter during periods of low lemming density demonstrates the importance of the sea ice as a potential habitat for this arctic fox population and suggests that a continued decline in sea ice extent will disrupt an important link between the marine and terrestrial ecosystems.     

Vertical distribution of bacteria in arctic sea ice

Abstract Heterotrophic bacteria were enumerated in north polar sea ice cores obtained near Point Barrow, Alaska. Highest concentrations of total and viable bacteria were found in the layer containing the sea ice microbial community identified by the maximum chlorophyll a content. Gas vacuolate bacteria were also found in the sea ice, a discovery which is consistent with their recent report from antarctic sea ice microbial communities. The gas vacuolate bacteria comprised 0.2% or less of the viable bacteria isolated from sea ice cores, lower than concentrations reported for most antarctic samples. Most gas vacuolate isolates from the sea ice cores were pigmented pink, orange, or yellow. An ice core from nearby saline Elson Lagoon contained an inverted sea ice microbial community with highest chlorophyll a concentrations and bacterial counts found in the top 0–20 cm of the ice. This surface layer also contained high numbers (up to 186 bacteria/ml) of a nonpigmented, gas vacuolate, elongated rod-shaped bacterium.     

Rabies and canine distemper in an arctic fox population in Alaska

Two oil field workers were attacked by a rabid arctic fox (Alopex lagopus) in the Prudhoe Bay oil field (Alaska, USA) prompting officials to reduce the local fox population. Ninety-nine foxes were killed during winter 1994. We tested foxes for prevalence of rabies and canine distemper. Exposure to rabies was detected in five of 99 foxes. Of the five, only one fox had rabies virus in neural tissue as determined by the direct fluorescent antibody test. The other four foxes had been exposed to rabies, but had apparently produced antibodies and did not have an active infection. No evidence of canine distemper was detected as determined by the absence of distemper antibodies in serum and distemper virus in neural tissue.     

From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe

The capercaillie inhabits a continuous range in large parts of the Palearctic boreal forest, but is patchily distributed in temperate Europe. An ongoing population decline, largely related to human land use changes, has been most pronounced in central and western Europe, where some local populations have become extinct. In this study, we document the genetic differentiation of capercaillie populations at different stages along a gradient of spatial structuring from high connectivity (continuous range in the boreal forest) to a metapopulation systems (Alps) and recent (central Europe) and historic (Pyrenees) isolation. Four hundred and sixty individuals from 14 sample sites were genotyped at 10 polymorphic microsatellite loci to assess genetic structure and variation of capercaillie populations across its European range. As expected, differentiation was least pronounced within the continuous range in the boreal forest. Within the metapopulation system of the Alps, differentiation was less than among the isolated populations of central Europe (Black Forest, Fichtelgebirge, Thuringia, Vosges). In the long-isolated population of the Pyrenees, and the recently isolated populations of central Europe, genetic diversity was significantly reduced compared with the Alps and boreal forest. Our results agree with the concept of a gradual increase in genetic differentiation from connectivity to isolation, and from recent to historic isolation. Anthropogenic habitat deterioration and fragmentation thus not only leads to range contractions and extinctions, but may also have significant genetic and evolutionary consequences for surviving populations. To maintain high levels of genetic variation in species in fragmented habitats, conservation should aim at securing connectivity between spatially distinct populations.     

Sea ice occurrence predicts genetic isolation in the Arctic fox

Unlike Oceanic islands, the islands of the Arctic Sea are not completely isolated from migration by terrestrial vertebrates. The pack ice connects many Arctic Sea islands to the mainland during winter months. The Arctic fox (Alopex lagopus), which has a circumpolar distribution, populates numerous islands in the Arctic Sea. In this study, we used genetic data from 20 different populations, spanning the entire distribution of the Arctic fox, to identify barriers to dispersal. Specifically, we considered geographical distance, occurrence of sea ice, winter temperature, ecotype, and the presence of red fox and polar bear as nonexclusive factors that influence the dispersal behaviour of individuals. Using distance-based redundancy analysis and the BIOENV procedure, we showed that occurrence of sea ice is the key predictor and explained 40-60% of the genetic distance among populations. In addition, our analysis identified the Commander and Pribilof Islands Arctic populations as genetically unique suggesting they deserve special attention from a conservation perspective.     

Strong genetic population structure in the boring giant clam, Tridacna crocea, across the Indo-Malay Archipelago: implications related to evolutionary processes and connectivity

Even though the Indo-Malay Archipelago hosts the world's greatest diversity of marine species, studies on the genetic population structure and gene flow of marine organisms within this area are rather rare. Consequently, not much is known about connectivity of marine populations in the Indo-Malay Archipelago, despite the fact that such information is important to understand evolutionary and ecological processes in the centre of marine biodiversity. This study aims to investigate the genetic population structure of the boring giant clam, Tridacna crocea . The analysis is based on a 456-bp fragment of the cytochrome oxidase I gene from 300 individuals collected from 15 localities across the Indo-Malay Archipelago. Tridacna crocea shows a very strong genetic population structure and isolation by distance, indicating restricted gene flow between almost all sample sites. The observed Φ_ST-value of 0.28 is very high compared to other studies on giant clams. According to the pronounced genetic differences, the sample sites can be divided into four groups from West to East: (i) Eastern Indian Ocean, (ii) Java Sea, (iii) South China Sea, Indonesian throughflow, as well as seas in the East of Sulawesi, and (iv) Western Pacific. This complex genetic population structure and pattern of connectivity, characterised by restricted gene flow between some sites and panmixing between others can be attributed to the geological history and prevailing current regimes in the Indo-Malay Archipelago.     

High population connectivity across the Indo-Pacific: Congruent lack of phylogeographic structure in three reef fish congeners

We used the mitochondrial control region and a comparative approach to study the genetic population structure of two surgeonfishes, Naso brevirostris and Naso unicornis, across their Indo-central Pacific ranges. Our purpose was to compare our results with those of a previous study of Naso vlamingii [Klanten, S.O., van Herwerden, L., Choat J.H., 2007. Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar. Biol. 150, 659-670] another widely distributed Indo-central Pacific Naso species. We found no evidence of a barrier to gene flow between the Indian and Pacific Oceans for either species, consistent with what was shown for N. vlamingii. Overall, both target species lacked spatial population partitions and probably have complex patterns of gene flow on several spatial scales. Despite the lack of geographic population structure distinct clades were observed in N. brevirostris, similar to those found in N. vlamingii. Coalescence times for intraspecific clades of N. brevirostris and N. vlamingii approximate each other, suggesting parallel evolutionary histories. A bimodal mismatch distribution in N. brevirostris indicates that a biogeographic barrier separated N. brevirostris populations sometime during its species history. Naso unicornis, in contrast, lacked genetic structure of any kind, although it has what could represent a single surviving clade. Congruent lack of spatial population structure among all three species suggest that such patterns are not due to stochastic processes of DNA mutation and are most likely driven by ecological and environmental factors.     

Biophysical connectivity explains population genetic structure in a highly dispersive marine species

Connectivity, the exchange of individuals among locations, is a fundamental ecological process that explains how otherwise disparate populations interact. For most marine organisms, dispersal occurs primarily during a pelagic larval phase that connects populations. We paired population structure from comprehensive genetic sampling and biophysical larval transport modeling to describe how spiny lobster (Panulirus argus) population differentiation is related to biological oceanography. A total of 581 lobsters were genotyped with 11 microsatellites from ten locations around the greater Caribbean. The overall F _ST of 0.0016 (P = 0.005) suggested low yet significant levels of structuring among sites. An isolation by geographic distance model did not explain spatial patterns of genetic differentiation in P. argus (P = 0.19; Mantel r = 0.18), whereas a biophysical connectivity model provided a significant explanation of population differentiation (P = 0.04; Mantel r = 0.47). Thus, even for a widely dispersing species, dispersal occurs over a continuum where basin-wide larval retention creates genetic structure. Our study provides a framework for future explorations of wide-scale larval dispersal and marine connectivity by integrating empirical genetic research and probabilistic modeling.

     

The genetic population structure and temporal genetic stability of gilthead sea bream Sparus aurata populations in the Aegean and Ionian Seas,using microsatellite DNA markers

We examined 662 gilthead sea bream Sparus aurata from wild samples of the species in the Aegean and Ionian Seas, using 20 EST-linked microsatellite markers, in three multiplex panels, as well as seven anonymous loci. Most of the markers were revealed to be highly polymorphic. We found low genetic differentiation between the sampling stations/areas with total F_ST 0.002 (P < 0.05). Based on comparison of five temporal samples, our results indicate genetic data consistency over time for all tested samples, pointing to stable populations, despite reported repeated escape events. Our results confirm the genetic population structure previously observed in these specific areas, using by far more markers than in previous studies in both coding and non-coding DNA loci. The limited genetic structure and the temporal genetic stability indicate neither major genetic differentiation of local populations by geographic isolation nor influence from anthropogenic factors. These results provide a baseline for future reference in any management programme of both wild and farmed population of S. aurata as well as of other aquaculture species with a potential introgression among farmed and wild populations.     

The impact of maternal experience on post-weaning survival in an endangered arctic fox population

Behavioural differences in parental care can influence offspring survival through variation in e.g. antipredator behaviour and ability to provide food. In a broad range of species, offspring survival has been found to be higher for experienced females compared to inexperienced first-time breeders. The increase in offspring survival for experienced females has mainly been explained by improved experience in providing food. In this paper, we have studied post-weaning juvenile survival in relation to maternal experience in an endangered population of arctic foxes (Vulpes lagopus) in Fennoscandia. For cubs raised by inexperienced and experienced females, the survival rate was 0.42 (CI 95% ± 0.31) and 0.87 (CI 95% ± 0.08), respectively. There was no difference in body condition between the cubs and no observations of starvation. We suggest that the difference in survival was due to lack of experience to one of the most common predators, the golden eagle (Aquila chrysaetos). Golden eagles were mainly observed on dens with litters where the females were inexperienced first-time breeders. From a conservation perspective, it is therefore important to increase adult survival through actions to enlarge the proportion of experienced breeders.     

Age-dependent genetic structure of arctic foxes in Svalbard

Arctic foxes are highly mobile arctic predators with a very weak population genetic structure over large parts of their range. Less is, however, known about the more local genetic structure within regions. Here, we analyze genotypes at 12 microsatellite loci for 561 arctic foxes trapped in the high-arctic archipelago Svalbard and investigate the genetic structure in three different age classes. Significant linkage disequilibrium, deficit of heterozygotes, genetic differentiation, and a decrease in relatedness with distance among animals trapped in their first winter suggested that some litter mates remain in proximity of each other during the first winter. This pattern was stronger for females than for males, indicating male-biased juvenile dispersal, and weaker for older animals. There was no genetic differentiation among adult foxes harvested in different hunting areas. The foxes from the protected area around Hornsund were however more differentiated than expected based on geographic distance alone, suggesting a possible disrupting effect of harvest on the spatial genetic structure in the rest of Svalbard. Our results also indicated a possible kin structure among adult females, suggesting natal philopatry, but further investigations will be needed to reach firm conclusions concerning kin structure in arctic foxes.     

Fire and ice: genetic structure of the Uinta ground squirrel (Spermophilus armatus) across the Yellowstone hotspot

The range of the Uinta ground squirrel, Spermophilus armatus , is centred over one of the most tectonically active regions today, the Yellowstone hotspot. We document the role of Quaternary tectonic and climatic history on the genetic structure of this species by screening museum and extant individuals throughout its range. Phylogeographic, divergence time, and demographic analyses of partial mitochondrial cytochrome b and control region DNA sequences yield insight into the cadence of evolution across three spatiotemporal scales: (i) a relatively deep intraspecific divergence of S. armatus into three lineages coincident with the last major volcanic eruption in the region and maintained by the Snake River Plain; (ii) demographic expansion in two lineages corresponding to the time of last deglaciation of the region; and (iii) a recent (< 50 years) local extinction of the third lineage coincident with climatic change and conversion of habitat for agricultural purposes in eastern Idaho. Beyond these inferences, our study highlights the unique value of museum material to phylogeography, and shows that small mammal recolonization of previously glaciated montane 'islands' differs from northward postglacial expansion observed in areas previously covered by continental ice sheets. Montane 'islands' may harbour high genetic diversity because of admixture and recurrent expansion/extinction.     

Gene flow on ice: the role of sea ice and whaling in shaping Holarctic genetic diversity and population differentiation in bowhead whales (Balaena mysticetus)

Sea ice is believed to be a major factor shaping gene flow for polar marine organisms, but it remains unclear to what extent it represents a true barrier to dispersal for arctic cetaceans. Bowhead whales are highly adapted to polar sea ice and were targeted by commercial whalers throughout Arctic and subarctic seas for at least four centuries, resulting in severe reductions in most areas. Both changing ice conditions and reductions due to whaling may have affected geographic distribution and genetic diversity throughout their range, but little is known about range‐wide genetic structure or whether it differed in the past. This study represents the first examination of genetic diversity and differentiation across all five putative stocks, including Baffin Bay‐Davis Strait, Hudson Bay‐Foxe Basin, Bering‐Beaufort‐Chukchi, Okhotsk, and Spitsbergen. We also utilized ancient specimens from Prince Regent Inlet (PRI) in the Canadian Arctic and compared them with modern stocks. Results from analysis of molecular variance and demographic simulations are consistent with recent and high gene flow between Atlantic and Pacific stocks in the recent past. Significant genetic differences between ancient and modern populations suggest PRI harbored unique maternal lineages in the past that have been recently lost, possibly due to loss of habitat during the Little Ice Age and/or whaling. Unexpectedly, samples from this location show a closer genetic relationship with modern Pacific stocks than Atlantic, supporting high gene flow between the central Canadian Arctic and Beaufort Sea over the past millennium despite extremely heavy ice cover over much of this period.     

Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge

Biogeographic barriers, some transitory in duration, are likely to have been important contributing factors to modern marine biodiversity in the Indo-Pacific region. One such barrier was the Torres Strait land bridge between continental Australia and New Guinea that persisted through much of the late Pleistocene and separated Indian and Pacific Ocean taxa. Here, we examine the patterns of mitochondrial DNA diversity for marine animals with present-day distributions spanning the Torres Strait. Specifically, we investigate whether there are concordant signatures across species, consistent with either vicariance or recent colonization from either ocean basin. We survey four species of reef fishes (Apogon doederleini, Pomacentrus coelestis, Dascyllus trimaculatus, and Acanthurus triostegus) for mtDNA cytochrome oxidase 1 and control region variation and contrast these results to previous mtDNA studies in diverse marine animals with similar distributions. We find substantial genetic partitioning (estimated from F-statistics and coalescent approaches) between Indian and Pacific Ocean populations for many species, consistent with regional persistence through the late Pleistocene in both ocean basins. The species-specific estimates of genetic divergence, however, vary greatly and for reef fishes we estimate substantially different divergence times among species. It is likely that Indian and Pacific Ocean populations have been isolated for multiple glacial cycles for some species, whereas for other species genetic connections have been more recent. Regional estimates of genetic diversity and directionality of gene flow also vary among species. Thus, there is no apparent consistency among historical patterns across the Torres Strait for these co-distributed marine animals.     

Arctic fox Vulpes lagopus population structure: circumpolar patterns and processes

Movement is a prominent process shaping genetic population structure. In many northern mammal species, population structure is formed by geographic distance, geographical barriers and various ecological factors that influence movement over the landscape. The Arctic fox Vulpes lagopus is a highly mobile, opportunistic carnivore of the Arctic that occurs in two main ecotypes with different ecological adaptations. We assembled microsatellite data in 7 loci for 1834 Arctic foxes sampled across their entire distribution to describe the circumpolar population structure and test the impact of (1) geographic distance, (2) geographical barriers and (3) ecotype designation on the population structure. Both Structure and Geneland demonstrated distinctiveness of Iceland and Scandinavia whereas low differentiation was observed between North America–northern Greenland, Svalbard and Siberia. Genetic differentiation was significantly correlated to presence of sea ice on a global scale, but not to geographical distance or ecotype designation. However, among areas connected by sea ice, we recorded a pattern of isolation by distance. The maximum likelihood approach in Migrate suggested that connectivity across North America–northern Greenland and Svalbard was particularly high. Our results demonstrate the importance of sea ice for maintaining connectivity between Arctic fox populations and we therefore predict that climate change will increase genetic divergence among populations in the future.     

Historical and ecological determinants of genetic structure in arctic canids

Wolves (Canis lupus) and arctic foxes (Alopex lagopus) are the only canid species found throughout the mainland tundra and arctic islands of North America. Contrasting evolutionary histories, and the contemporary ecology of each species, have combined to produce their divergent population genetic characteristics. Arctic foxes are more variable than wolves, and both island and mainland fox populations possess similarly high microsatellite variation. These differences result from larger effective population sizes in arctic foxes, and the fact that, unlike wolves, foxes were not isolated in discrete refugia during the Pleistocene. Despite the large physical distances and distinct ecotypes represented, a single, panmictic population of arctic foxes was found which spans the Svalbard Archipelago and the North American range of the species. This pattern likely reflects both the absence of historical population bottlenecks and current, high levels of gene flow following frequent long-distance foraging movements. In contrast, genetic structure in wolves correlates strongly to transitions in habitat type, and is probably determined by natal habitat-biased dispersal. Nonrandom dispersal may be cued by relative levels of vegetation cover between tundra and forest habitats, but especially by wolf prey specialization on ungulate species of familiar type and behaviour (sedentary or migratory). Results presented here suggest that, through its influence on sea ice, vegetation, prey dynamics and distribution, continued arctic climate change may have effects as dramatic as those of the Pleistocene on the genetic structure of arctic canid species.