A palaeogenomic investigation of overharvest implications in an endemic wild reindeer subspecies.

Overharvest can severely reduce the abundance and distribution of a species and thereby impact its genetic diversity and threaten its future viability. Overharvest remains an ongoing issue for Arctic mammals, which due to climate change now also confront one of the fastest changing environments on Earth. The high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus), endemic to Svalbard, experienced a harvest-induced demographic bottleneck that occurred during the 17-20th centuries. Here, we investigate changes in genetic diversity, population structure, and gene-specific differentiation during and after this overharvesting event. Using whole-genome shotgun sequencing, we generated the first ancient and historical nuclear (n = 11) and mitochondrial (n = 18) genomes from Svalbard reindeer (up to 4000 BP) and integrated these data with a large collection of modern genome sequences (n = 90) to infer temporal changes. We show that hunting resulted in major genetic changes and restructuring in reindeer populations. Near-extirpation followed by pronounced genetic drift has altered the allele frequencies of important genes contributing to diverse biological functions. Median heterozygosity was reduced by 26%, while the mitochondrial genetic diversity was reduced only to a limited extent, likely due to already low pre-harvest diversity and a complex post-harvest recolonization process. Such genomic erosion and genetic isolation of populations due to past anthropogenic disturbance will likely play a major role in metapopulation dynamics (i.e., extirpation, recolonization) under further climate change. Our results from a high-arctic case study therefore emphasize the need to understand the long-term interplay of past, current, and future stressors in wildlife conservation.

Sea ice loss increases genetic isolation in a high Arctic ungulate metapopulation.

Sea ice loss may have dramatic consequences for population connectivity, extinction-colonization dynamics, and even the persistence of Arctic species subject to climate change. This is of particular concern in face of additional anthropogenic stressors, such as overexploitation. In this study, we assess the population-genetic implications of diminishing sea ice cover in the endemic, high Arctic Svalbard reindeer (Rangifer tarandus platyrhynchus) by analyzing the interactive effects of landscape barriers and reintroductions (following harvest-induced extirpations) on their metapopulation genetic structure. We genotyped 411 wild reindeer from 25 sampling sites throughout the entire subspecies' range at 19 microsatellite loci. Bayesian clustering analysis showed a genetic structure composed of eight populations, of which two were admixed. Overall population genetic differentiation was high (mean FST  = 0.21). Genetic diversity was low (allelic richness [AR] = 2.07-2.58; observed heterozygosity = 0.23-0.43) and declined toward the outer distribution range, where populations showed significant levels of inbreeding. Coalescent estimates of effective population sizes and migration rates revealed strong evolutionary source-sink dynamics with the central population as the main source. The population genetic structure was best explained by a landscape genetics model combining strong isolation by glaciers and open water, and high connectivity by dispersal across winter sea ice. However, the observed patterns of natural isolation were strongly modified by the signature of past harvest-induced extirpations, subsequent reintroductions, and recent lack of sea ice. These results suggest that past and current anthropogenic drivers of metapopulation dynamics may have interactive effects on large-scale ecological and evolutionary processes. Continued loss of sea ice as a dispersal corridor within and between island systems is expected to increase the genetic isolation of populations, and thus threaten the evolutionary potential and persistence of Arctic wildlife.

Spatial heterogeneity in climate change effects decouples the long-term dynamics of wild reindeer populations in the high Arctic.

The 'Moran effect' predicts that dynamics of populations of a species are synchronized over similar distances as their environmental drivers. Strong population synchrony reduces species viability, but spatial heterogeneity in density dependence, the environment, or its ecological responses may decouple dynamics in space, preventing extinctions. How such heterogeneity buffers impacts of global change on large-scale population dynamics is not well studied. Here, we show that spatially autocorrelated fluctuations in annual winter weather synchronize wild reindeer dynamics across high-Arctic Svalbard, while, paradoxically, spatial variation in winter climate trends contribute to diverging local population trajectories. Warmer summers have improved the carrying capacity and apparently led to increased total reindeer abundance. However, fluctuations in population size seem mainly driven by negative effects of stochastic winter rain-on-snow (ROS) events causing icing, with strongest effects at high densities. Count data for 10 reindeer populations 8-324 km apart suggested that density-dependent ROS effects contributed to synchrony in population dynamics, mainly through spatially autocorrelated mortality. By comparing one coastal and one 'continental' reindeer population over four decades, we show that locally contrasting abundance trends can arise from spatial differences in climate change and responses to weather. The coastal population experienced a larger increase in ROS, and a stronger density-dependent ROS effect on population growth rates, than the continental population. In contrast, the latter experienced stronger summer warming and showed the strongest positive response to summer temperatures. Accordingly, contrasting net effects of a recent climate regime shift-with increased ROS and harsher winters, yet higher summer temperatures and improved carrying capacity-led to negative and positive abundance trends in the coastal and continental population respectively. Thus, synchronized population fluctuations by climatic drivers can be buffered by spatial heterogeneity in the same drivers, as well as in the ecological responses, averaging out climate change effects at larger spatial scales.

Ancient reindeer mitogenomes reveal island-hopping colonisation of the Arctic archipelagos.

Climate warming at the end of the last glacial period had profound effects on the distribution of cold-adapted species. As their range shifted towards northern latitudes, they were able to colonise previously glaciated areas, including remote Arctic islands. However, there is still uncertainty about the routes and timing of colonisation. At the end of the last ice age, reindeer/caribou (Rangifer tarandus) expanded to the Holarctic region and colonised the archipelagos of Svalbard and Franz Josef Land. Earlier studies have proposed two possible colonisation routes, either from the Eurasian mainland or from Canada via Greenland. Here, we used 174 ancient, historical and modern mitogenomes to reconstruct the phylogeny of reindeer across its whole range and to infer the colonisation route of the Arctic islands. Our data shows a close affinity among Svalbard, Franz Josef Land and Novaya Zemlya reindeer. We also found tentative evidence for positive selection in the mitochondrial gene ND4, which is possibly associated with increased heat production. Our results thus support a colonisation of the Eurasian Arctic archipelagos from the Eurasian mainland and provide some insights into the evolutionary history and adaptation of the species to its High Arctic habitat.

Contrasting genomic consequences of anthropogenic reintroduction and natural recolonization in high-arctic wild reindeer.

Anthropogenic reintroduction can supplement natural recolonization in reestablishing a species' distribution and abundance. However, both reintroductions and recolonizations can give rise to founder effects that reduce genetic diversity and increase inbreeding, potentially causing the accumulation of genetic load and reduced fitness. Most current populations of the endemic high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus) originate from recent reintroductions or recolonizations following regional extirpations due to past overharvesting. We investigated and compared the genomic consequences of these two paths to reestablishment using whole-genome shotgun sequencing of 100 Svalbard reindeer across their range. We found little admixture between reintroduced and natural populations. Two reintroduced populations, each founded by 12 individuals around four decades (i.e. 8 reindeer generations) ago, formed two distinct genetic clusters. Compared to the source population, these populations showed only small decreases in genome-wide heterozygosity and increases in inbreeding and lengths of runs of homozygosity. In contrast, the two naturally recolonized populations without admixture possessed much lower heterozygosity, higher inbreeding and longer runs of homozygosity, possibly caused by serial population founder effects and/or fewer or more genetically related founders than in the reintroduction events. Naturally recolonized populations can thus be more vulnerable to the accumulation of genetic load than reintroduced populations. This suggests that in some organisms even small-scale reintroduction programs based on genetically diverse source populations can be more effective than natural recolonization in establishing genetically diverse populations. These findings warrant particular attention in the conservation and management of populations and species threatened by habitat fragmentation and loss.

Adaptation to the High-Arctic island environment despite long-term reduced genetic variation in Svalbard reindeer.

Typically much smaller in number than their mainland counterparts, island populations are ideal systems to investigate genetic threats to small populations. The Svalbard reindeer (Rangifer tarandus platyrhynchus) is an endemic subspecies that colonized the Svalbard archipelago ca. 6,000-8,000 years ago and now shows numerous physiological and morphological adaptations to its arctic habitat. Here, we report a de-novo chromosome-level assembly for Svalbard reindeer and analyze 133 reindeer genomes spanning Svalbard and most of the species' Holarctic range, to examine the genomic consequences of long-term isolation and small population size in this insular subspecies. Empirical data, demographic reconstructions, and forward simulations show that long-term isolation and high inbreeding levels may have facilitated the reduction of highly deleterious-and to a lesser extent, moderately deleterious-variation. Our study indicates that long-term reduced genetic diversity did not preclude local adaptation to the High Arctic, suggesting that even severely bottlenecked populations can retain evolutionary potential.