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

Abstract

Anthropogenic reintroduction can supplement natural recolonisation in reestablishing a species’ distribution and abundance. However, both reintroductions and recolonisations can give rise to population bottlenecks that reduce genetic diversity and increase inbreeding, potentially causing 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 recolonisations 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 recolonised populations without admixture possessed much lower heterozygosity, higher inbreeding, and longer runs of homozygosity, possibly caused by serial population bottlenecks and/or fewer or more genetically related founders than in the reintroduction events. Naturally recolonised 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 recolonisation 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.

A paleogenomic investigation of overharvest implications in an endemic wild reindeer subspecies

“…The current population structuring is a consequence of overharvesting and recovery occurring during a period of pronounced climate warming. Our results are congruent with earlier findings based on microsatellite data and nuclear whole genome sequencing where present-day population structuring reflects the recolonization patterns originating from the four locations that escaped extirpation (Burnett et al, 2022; Peeters et al, 2020). In addition to the sedentary behavior of the Svalbard reindeer, the effect of natural barriers for dispersal and gene flow has increased during the recovery period, as sea-ice cover decreased (Peeters et al, 2020).…”

“…All 14 C dates were calibrated with the IntCal20 calibration curve (Reimer, 2020) using the calibrate function in the package rcarbon (Crema & Bevan, 2021) in R v4.1.0 (R Core Team, 2021). The subfossil materials were combined with a previously published genomic dataset from samples collected in 2014-2018 and consisting of 90 contemporary Svalbard reindeer from a recent population genomics study (Burnett et al, 2022) PRJEB57293(Burnett et al, 2022). To put harvest-induced changes within Svalbard reindeer populations into a temporal context, we subdivided the samples into three time periods: Before (4,000-400 years before present, BP, hereafter referred to as pre-hunting ), during (400 years BP-1950 Common Era, CE, hereafter referred to as during-hunting ), and after (> 1950 CE, hereafter referred to as post-hunting ) the major harvest-induced bottleneck that occurred from the 17th to the early 20th century (Lønø 1959).…”

“…Before further analysis, sites in strong linkage disequilibrium were pruned with Plink v1.90 beta 6.24 (Chang et al, 2015) using a window size of 50 kbp, a step size of 3 kbp, and a pairwise r 2 threshold of 0.5 (- - indep-pairwise 50 3 0.5). Subsequently, regions with low mapping quality, excessive coverage as identified with CallableLoci (see above), or associated with sex chromosomes (for methods see (Burnett et al, 2022)) were removed via a custom python script. Also excluded were sites that are not variant in both the ancient ancient and modern datasets.…”

“…Six genetically distinct reindeer groups are now present on the Svalbard archipelago: four populations that expanded from their respective ‘hunting refugia’, and two populations founded by individuals from central Spitsbergen. Of the latter, one was founded along the west coast of Spitsbergen following two translocations, and another was founded by natural recolonization to south Spitsbergen, with strong genetic drift following gradual expansion (Burnett et al, 2022; Peeters et al, 2020). Svalbard reindeer disperse slowly due to their sedentary behavior and the fragmented landscape (Le Moullec et al, 2019).…”

“…The Svalbard reindeer genetic diversity is by far the lowest among the Rangifer subspecies (Kvie et al, 2016; Yannic et al, 2013). Despite this, local variation in genetic diversity is strong, with decreasing diversity from central Spitsbergen towards the peripheries of the archipelago (Peeters et al, 2020), (Burnett et al, 2022; Kvie et al, 2016). Inbreeding (i.e.…”