High genetic load without purging in caribou, a diverse species at risk.

High intra-specific genetic diversity is associated with adaptive potential, which is key for resilience to global change. However, high variation may also support deleterious alleles through genetic load, thereby increasing the risk of inbreeding depression if population sizes decrease. Purging of deleterious variation has been demonstrated in some threatened species. However, less is known about the costs of declines and inbreeding in species with large population sizes and high genetic diversity even though this encompasses many species globally that are expected to undergo population declines. Caribou is a species of ecological and cultural significance in North America with a wide distribution supporting extensive phenotypic variation but with some populations undergoing significant declines resulting in their at-risk status in Canada. We assessed intra-specific genetic variation, adaptive divergence, inbreeding, and genetic load across populations with different demographic histories using an annotated chromosome-scale reference genome and 66 whole-genome sequences. We found high genetic diversity and nine phylogenomic lineages across the continent with adaptive diversification of genes, but also high genetic load among lineages. We found highly divergent levels of inbreeding across individuals, including the loss of alleles by drift but not increased purging in inbred individuals, which had more homozygous deleterious alleles. We also found comparable frequencies of homozygous deleterious alleles between lineages regardless of nucleotide diversity. Thus, further inbreeding may need to be mitigated through conservation efforts. Our results highlight the "double-edged sword" of genetic diversity that may be representative of other species atrisk affected by anthropogenic activities.

Genomics of founders for conservation breeding: the Jasper caribou case.

Conservation breeding programs are increasingly used as recovery actions for wild animals; bringing founders into captivity to rear captive populations for future reintroduction into the wild. The International Union for the Conservation of Nature recommends that founders should come from genetically close populations and should have sufficient genetic diversity to avoid mating among relatives. Genomic data are highly informative for evaluating founders due to their high resolution and ability to capture adaptive divergence, yet, their application in that context remains limited. Woodland caribou are federally listed as a Species at Risk in Canada, with several populations facing extirpation, such as those in the Rocky Mountains of Alberta and British Columbia (BC). To prevent local extirpation, Jasper National Park (JNP) is proposing a conservation breeding program. We examined single nucleotide polymorphisms for 144 caribou from 11 populations encompassing a 200,0002 km area surrounding JNP to provide information useful for identifying appropriate founders for this program. We found that this area likely hosts a caribou metapopulation historically characterized by high levels of gene flow, which indicates that multiple sources of founders would be appropriate for initiating a breeding program. However, population structure and adaptive divergence analyses indicate that JNP caribou are closest to populations in the BC Columbia range, which also have suitable genetic diversity for conservation breeding. We suggest that collaboration among jurisdictions would be beneficial to implement the program to promote recovery of JNP caribou and possibly other caribou populations in the surrounding area, which is strategically at the periphery of the distribution of this endangered species. Supplementary Information: The online version contains supplementary material available at 10.1007/s10592-023-01540-3.

Population dynamics of caribou shaped by glacial cycles before the last glacial maximum.

Pleistocene glacial cycles influenced the diversification of high-latitude wildlife species through recurrent periods of range contraction, isolation, divergence, and expansion from refugia and subsequent admixture of refugial populations. We investigate population size changes and the introgressive history of caribou (Rangifer tarandus) in western Canada using 33 whole genome sequences coupled with larger-scale mitochondrial data. We found that a major population expansion of caribou occurred starting around 110,000 years ago (kya), the start of the last glacial period. Additionally, we found effective population sizes of some caribou reaching ~700,000 to 1,000,000 individuals, one of the highest recorded historical effective population sizes for any mammal species thus far. Mitochondrial analyses dated introgression events prior to the LGM dating to 20-30 kya and even more ancient at 60 kya, coinciding with colder periods with extensive ice coverage, further demonstrating the importance of glacial cycles and events prior to the LGM in shaping demographic history. Reconstructing the origins and differential introgressive history has implications for predictions on species responses under climate change. Our results have implications for other whole genome analyses using pairwise sequentially Markovian coalescent (PSMC) analyses, as well as highlighting the need to investigate pre-LGM demographic patterns to fully reconstruct the origin of species diversity, especially for high-latitude species.

National contributions to global ecosystem values.

Current conservation templates prioritize biogeographic regions with high intensity ecosystem values, such as exceptional species richness or threat. Intensity-based targets are an important consideration in global efforts, but they do not capture all available opportunities to conserve ecosystem values, including those that accrue in low intensity over large areas. We assess six globally-significant ecosystem values-intact wilderness, freshwater availability, productive marine environments, breeding habitat for migratory wildlife, soil carbon storage, and latitudinal potential for range shift in the face of climate change-to highlight opportunities for high-impact broadly-distributed contributions to global conservation. Nations can serve as a cohesive block of policy that can profoundly influence conservation outcomes. Contributions to global ecosystem values that exceed what is predicted by a nation's area alone, can give rise to countries with the capacity to act as 'conservation superpowers', such as Canada and Russia. For these conservation superpowers, a relatively small number of national policies can have environmental repercussions for the rest of the world.

The eastern migratory caribou: the role of genetic introgression in ecotype evolution.

Understanding the evolutionary history of contemporary animal groups is essential for conservation and management of endangered species like caribou (Rangifer tarandus). In central Canada, the ranges of two caribou subspecies (barren-ground/woodland caribou) and two woodland caribou ecotypes (boreal/eastern migratory) overlap. Our objectives were to reconstruct the evolutionary history of the eastern migratory ecotype and to assess the potential role of introgression in ecotype evolution. STRUCTURE analyses identified five higher order groups (i.e. three boreal caribou populations, eastern migratory ecotype and barren-ground). The evolutionary history of the eastern migratory ecotype was best explained by an early genetic introgression from barren-ground into a woodland caribou lineage during the Late Pleistocene and subsequent divergence of the eastern migratory ecotype during the Holocene. These results are consistent with the retreat of the Laurentide ice sheet and the colonization of the Hudson Bay coastal areas subsequent to the establishment of forest tundra vegetation approximately 7000 years ago. This historical reconstruction of the eastern migratory ecotype further supports its current classification as a conservation unit, specifically a Designatable Unit, under Canada's Species at Risk Act. These findings have implications for other sub-specific contact zones for caribou and other North American species in conservation unit delineation.

Experimentally derived δ¹³C and δ¹5N discrimination factors for gray wolves and the impact of prior information in Bayesian mixing models.

Stable isotope analysis of diet has become a common tool in conservation research. However, the multiple sources of uncertainty inherent in this analysis framework involve consequences that have not been thoroughly addressed. Uncertainty arises from the choice of trophic discrimination factors, and for Bayesian stable isotope mixing models (SIMMs), the specification of prior information; the combined effect of these aspects has not been explicitly tested. We used a captive feeding study of gray wolves (Canis lupus) to determine the first experimentally-derived trophic discrimination factors of C and N for this large carnivore of broad conservation interest. Using the estimated diet in our controlled system and data from a published study on wild wolves and their prey in Montana, USA, we then investigated the simultaneous effect of discrimination factors and prior information on diet reconstruction with Bayesian SIMMs. Discrimination factors for gray wolves and their prey were 1.97‰ for δ13C and 3.04‰ for δ15N. Specifying wolf discrimination factors, as opposed to the commonly used red fox (Vulpes vulpes) factors, made little practical difference to estimates of wolf diet, but prior information had a strong effect on bias, precision, and accuracy of posterior estimates. Without specifying prior information in our Bayesian SIMM, it was not possible to produce SIMM posteriors statistically similar to the estimated diet in our controlled study or the diet of wild wolves. Our study demonstrates the critical effect of prior information on estimates of animal diets using Bayesian SIMMs, and suggests species-specific trophic discrimination factors are of secondary importance. When using stable isotope analysis to inform conservation decisions researchers should understand the limits of their data. It may be difficult to obtain useful information from SIMMs if informative priors are omitted and species-specific discrimination factors are unavailable.