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

Abstract

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.

Sea or summit? Wild reindeer spatial responses to changing high‐arctic winters

“…Although our "snapshot-in-time" data call for cautious interpretation, this study adds novel and nuanced insights into how a variety of behavioral strategies may potentially buffer negative effects of a changing winter climate in isolated arctic ungulate populations. The increasing isolation of some coastal reindeer populations, inhabiting islands and peninsulas separated by landscape barriers and a lack of sea ice (Poole et al 2010, Jenkins et al 2018, Peeters et al 2020, makes them particularly vulnerable to changes in snowpack conditions and forage accessibility.…”

“…For instance, Jenkins et al (2016) found a negative temporal trend in landscape connectivity for island-dwelling caribou populations in the Canadian Arctic Archipelago, predicting a further decrease due to future loss of sea ice (see also Mallory and Boyce 2018). In both Svalbard reindeer and arctic island-dwelling caribou (R. t. groenlandicus, R. t. peary), there are strong links between sea-ice dynamics and the level of genetic isolation among populations (Jenkins et al 2018, Peeters et al 2020. This highlights the importance of behavioral plasticity at small spatial scales for population viability in arctic island ungulates.…”

“…However, arctic terrestrial wildlife's ability to respond to environmental change is increasingly limited by habitat fragmentation, either directly or indirectly caused by human activity (Mallory and Boyce 2018). The rapid loss of arctic sea ice (Onarheim et al 2014), an important corridor for seasonal migrations (Miller 2002, Hansen et al 2010b, Poole et al 2010, Mathieu et al 2013) and dispersal (Post et al 2013, Jenkins et al 2016, Peeters et al 2020 in some reindeer and caribou populations, increases the level of spatial isolation. For instance, Jenkins et al (2016) found a negative temporal trend in landscape connectivity for island-dwelling caribou populations in the Canadian Arctic Archipelago, predicting a further decrease due to future loss of sea ice (see also Mallory and Boyce 2018).…”

Environmental effects on spatial population dynamics and synchrony: lessons from northern ecosystems

“…The few remaining and critically small populations gradually recolonised the former distribution range, partly mediated by reintroductions (Le Moullec et al 2019b). Landscape genetics analyses further indicated that the spatial population structure was determined by restricted dispersal across steep mountains, glaciers, fjords and open sea between islands (Peeters et al 2020). Furthermore, the seasonal occurrence of sea ice facilitated dispersal and was a key driver of gene flow and source−sink dynamics among populations.…”

“…The lack of sea ice as a dispersal corridor will likely decrease recolonisation probabilities and increase the risk of inbreeding and loss of genetic diversity, particularly in small and isolated populations (Saccheri et al 1998). Peeters et al (2020) demonstrated how population genetic structure and connectivity can be influenced by interactions of past (overexploitation) and ongoing (climate change) anthropogenic drivers. Climate change and harvesting can thus strongly influence the evolutionary potential and persistence of species through effects on population connectivity and spatial genetic struc-ture.…”