Genomic legacy of migration in endangered caribou.

Wide-ranging animals, including migratory species, are significantly threatened by the effects of habitat fragmentation and habitat loss. In the case of terrestrial mammals, this results in nearly a quarter of species being at risk of extinction. Caribou are one such example of a wide-ranging, migratory, terrestrial, and endangered mammal. In populations of caribou, the proportion of individuals considered as "migrants" can vary dramatically. There is therefore a possibility that, under the condition that migratory behavior is genetically determined, those individuals or populations that are migratory will be further impacted by humans, and this impact could result in the permanent loss of the migratory trait in some populations. However, genetic determination of migration has not previously been studied in an endangered terrestrial mammal. We examined migratory behavior of 139 GPS-collared endangered caribou in western North America and carried out genomic scans for the same individuals. Here we determine a genetic subdivision of caribou into a Northern and a Southern genetic cluster. We also detect >50 SNPs associated with migratory behavior, which are in genes with hypothesized roles in determining migration in other organisms. Furthermore, we determine that propensity to migrate depends upon the proportion of ancestry in individual caribou, and thus on the evolutionary history of its migratory and sedentary subspecies. If, as we report, migratory behavior is influenced by genes, caribou could be further impacted by the loss of the migratory trait in some isolated populations already at low numbers. Our results indicating an ancestral genetic component also suggest that the migratory trait and their associated genetic mutations could not be easily re-established when lost in a population.

Selection of both habitat and genes in specialized and endangered caribou.

Genetic mechanisms determining habitat selection and specialization of individuals within species have been hypothesized, but not tested at the appropriate individual level in nature. In this work, we analyzed habitat selection for 139 GPS-collared caribou belonging to three declining ecotypes sampled throughout Northwestern Canada. We used Resource Selection Functions (RSFs) comparing resources at used and available locations. We found that the three caribou ecotypes differed in their use of habitat suggesting specialization. On expected grounds, we also found differences in habitat selection between summer and winter, but also, originally, among the individuals within an ecotype. We next obtained Single Nucleotide Polymorphisms (SNPs) for the same caribou individuals, we detected those associated to habitat selection, and then identified genes linked to these SNPs. These genes had functions related in other organisms to habitat and dietary specializations, and climatic adaptations. We therefore suggest that individual variation in habitat selection was based on genotypic variation in the SNPs of individual caribou, indicating that genetic forces underlie habitat and diet selection in the species. We also suggest that the associations between habitat and genes that we detected may lead to lack of resilience in the species, thus contributing to caribou endangerment. Our work emphasizes that similar mechanisms may exist for other specialized, endangered species. This article is protected by copyright. All rights reserved.

Genomics, environment and balancing selection in behaviourally bimodal populations: The caribou case.

Selection forces that favour different phenotypes in different environments can change frequencies of genes between populations along environmental clines. Clines are also compatible with balancing forces, such as negative frequency-dependent selection (NFDS), which maintains phenotypic polymorphisms within populations. For example, NFDS is hypothesized to maintain partial migration, a dimorphic behavioural trait prominent in species where only a fraction of the population seasonally migrates. Overall, NFDS is believed to be a common phenomenon in nature, yet a scarcity of studies were published linking naturally occurring allelic variation with bimodal or multimodal phenotypes and balancing selection. We applied a Pool-seq approach and detected selection on alleles associated with environmental variables along a North-South gradient in western North American caribou, a species displaying partially migratory behaviour. On 51 loci, we found a signature of balancing selection, which could be related to NFDS and ultimately the maintenance of the phenotypic polymorphisms known within these populations. Yet, remarkably, we detected directional selection on a locus when our sample was divided into two behaviourally distinctive groups regardless of geographic provenance (a subset of GPS-collared migratory or sedentary individuals), indicating that, within populations, phenotypically homogeneous groups were genetically distinctive. Loci under selection were linked to functional genes involved in oxidative stress response, body development and taste perception. Overall, results indicated genetic differentiation along an environmental gradient of caribou populations, which we found characterized by genes potentially undergoing balancing selection. We suggest that the underlining balancing force, NFDS, plays a strong role within populations harbouring multiple haplotypes and phenotypes, as it is the norm in animals, plants and humans too.

Genome-wide set of SNPs reveals evidence for two glacial refugia and admixture from postglacial recolonization in an alpine ungulate.

Past glaciation events have played a major role in shaping the genetic diversity and distribution of wild sheep in North America. The advancement of glaciers can isolate populations in ice-free refugia, where they can survive until the recession of ice sheets. The major Beringian refugium is thought to have held thinhorn sheep (Ovis dalli) populations during times of glacial advance. While isolation in the major refugium can account for much of the genetic and morphological diversity seen in extant thinhorn sheep populations, mounting evidence suggests the persistence of populations in smaller minor refugia. We investigated the refugial origins of thinhorn sheep using ~10 000 SNPs obtained via a cross-species application of the domestic sheep ovine HD BeadChip to genotype 52 thinhorn sheep and five bighorn sheep (O. canadensis) samples. Phylogenetic inference revealed a distinct lineage of thinhorn sheep inhabiting British Columbia, which is consistent with the survival of a group of thinhorn sheep in a minor refugium separate from the Beringian refugium. Isolation in separate glacial refugia probably mediated the evolution of the two thinhorn sheep subspecies, the white Dall's sheep (O. d. dalli), which persisted in Beringia, and the dark Stone's sheep (O. d. stonei), which utilized the minor refugium. We also found the first genetic evidence for admixture between sheep from different glacial refugia in south-central Yukon as a consequence of post glacial expansion and recolonization. These results show that glaciation events can have a major role in the evolution of species inhabiting previously glaciated habitats and the need to look beyond established refugia when examining the evolutionary history of such species.

Seasonal movements in caribou ecotypes of Western Canada.

BACKGROUND: Several migratory ungulates, including caribou, are dramatically declining. Caribou of the Barren-ground ecotype, which forms its own subspecies, are known to be mainly migratory. By contrast, within the Woodland subspecies, animals of the Boreal ecotype are known to be mainly sedentary, while those within the Northern and Central Mountain ecotypes to be partially migratory, with only some individuals migrating. Promotion of conservation actions (e.g., habitat protection) that are specific to both residents and migrants, as well as to the areas they frequent seasonally (which may be separate for migrants), requires distinguishing migration from other movement behaviours, which might be a challenge. METHODS: We aimed at assessing seasonal movement behaviours, including migratory, resident, dispersing, and nomadic, for caribou belonging to the Barren-ground and Woodland subspecies and ecotypes. We examined seasonal displacement, both planar and altitudinal, and seasonal ranges overlap for 366 individuals that were GPS-collared in Northern and Western Canada. Lastly, we assessed the ability of caribou individuals to switch between migratory and non-migratory movement behaviours between years. RESULTS: We detected migratory behaviour within each of the studied subspecies and ecotypes. However, seasonal ranges overlap (an index of sedentary behaviour) varied, with proportions of clear migrants (0 overlap) of 40.94% for Barren-ground caribou and 23.34% for Woodland caribou, and of 32.95%, 54.87%, and 8.86% for its Northern Mountain, Central Mountain, and Boreal ecotype, respectively. Plastic switches of individuals were also detected between migratory, resident, dispersing, and nomadic seasonal movements performed across years. CONCLUSIONS: Our unexpected findings of marked seasonal movement plasticity in caribou indicate that this phenomenon should be better studied to understand the resilience of this endangered species to habitat and climatic changes. Our results that a substantial proportion of individuals engaged in seasonal migration in all studied ecotypes indicate that caribou conservation plans should account for critical habitat in both summer and winter ranges. Accordingly, conservation strategies are being devised for the Woodland subspecies and its ecotypes, which were found to be at least partially migratory in this study. Our findings that migration is detectable with both planar and altitudinal analyses of seasonal displacement provide a tool to better define seasonal ranges, also in mountainous and hilly environments, and protect habitat there.

Invasive Adenocarcinoma of the Head of a Boreal Woodland Caribou (Rangifer tarandus caribou), Alberta, Canada.

An emaciated, 14-yr-old female boreal woodland caribou (Rangifer tarandus caribou) was found dead with an ulcerated wound on the left side of the head. Radiographs documented osteolysis of portions of the mandible and cranium. Histopathology revealed an invasive adenocarcinoma infiltrating the soft tissues and bones of the head.

Seasonal effects of Pacific-based climate on recruitment in a predator-limited large herbivore.

1. Climate is an important factor influencing the population dynamics of large herbivores operating directly on individuals or through its effect on forage characteristics. However, the seasonal effect of climate may differ between forage- and predator-limited populations because of a climatic influence on predation rates. The influence of climate on predator-limited large herbivores is less well known than on forage-limited populations. Further, the effect of Pacific-based climate on large herbivore populations has been rarely assessed. 2. We investigated the effect of the Pacific Decadal Oscillation (PDO), across different seasons, on recruitment in 10 populations (herds) of mountain-dwelling caribou Rangifer tarandus caribou L. in the Yukon Territory, Canada. These low-density populations occur in highly seasonal environments and are considered predator-limited with high neonatal calf mortality. Hence, in most years females do not spend resources through lactational support during the summer and resource intake is devoted to self-maintenance. We predicted that climate affecting environmental conditions at calving would have a strong effect on recruitment via its influence on predation rates. We also predicted that climatic conditions prior to conception could have an effect on recruitment through its influence on female fecundity. We modelled recruitment (n = 165) by seasonal PDO values using generalized linear mixed-effects models with herd-varying coefficients. 3. We found that recruitment variability was best explained by variation in winter climate (beta = 0.110, SE = 0.007) prior to birth (in utero) and May climate (beta = 0.013, SE = 0.006) at calving. There was little support for a pre-conception climate effect influencing female body condition and hence fecundity. These results confirm that recruitment in these populations is limited by predation and that forage-limitation is not a significant factor in their population dynamics. There was considerable variability in herd-specific relationships between the PDO and recruitment. Incorporating herd-specific characteristics, such as variable predator densities or terrain characteristics within a herd range, may shed greater light on the complex relationship between climate and ungulate population dynamics.

An assessment of sampling designs using SCR analyses to estimate abundance of boreal caribou.

Accurately estimating abundance is a critical component of monitoring and recovery of rare and elusive species. Spatial capture-recapture (SCR) models are an increasingly popular method for robust estimation of ecological parameters. We provide an analytical framework to assess results from empirical studies to inform SCR sampling design, using both simulated and empirical data from noninvasive genetic sampling of seven boreal caribou populations (Rangifer tarandus caribou), which varied in range size and estimated population density. We use simulated population data with varying levels of clustered distributions to quantify the impact of nonindependence of detections on density estimates, and empirical datasets to explore the influence of varied sampling intensity on the relative bias and precision of density estimates. Simulations revealed that clustered distributions of detections did not significantly impact relative bias or precision of density estimates. The genotyping success rate of our empirical dataset (n = 7,210 samples) was 95.1%, and 1,755 unique individuals were identified. Analysis of the empirical data indicated that reduced sampling intensity had a greater impact on density estimates in smaller ranges. The number of captures and spatial recaptures was strongly correlated with precision, but not absolute relative bias. The best sampling designs did not differ with estimated population density but differed between large and small ranges. We provide an efficient framework implemented in R to estimate the detection parameters required when designing SCR studies. The framework can be used when designing a monitoring program to minimize effort and cost while maximizing effectiveness, which is critical for informing wildlife management and conservation.

The geography of conflict between elk and agricultural values in the Cypress Hills, Canada.

Complex ecological issues like depredation and its management are determined by multiple factors acting at more than one scale and are interlinked with complex human social and economic behaviour. Depredation by wild herbivores can be a major obstacle to agricultural community support for wildlife conservation. For three decades, crop and fence damage, competition with livestock for native rangeland and tame pasture, and depredation of stored feed by elk (Cervus elaphus canadensis) have been the cause of conflict with agricultural producers in the Cypress Hills, Alberta and Saskatchewan. Tolerance of elk presence on private lands is low because few benefits accrue to private landowners; rather they largely perceive elk as a public resource produced at their expense. Government management actions have focused on abatement inputs (e.g., population reduction; fencing) and compensation, but incentives to alter land use patterns (crop choice and location) in response to damages have not been considered. Nor has there been information on spatial structure of the elk population that would allow targeted management actions instead of attempting to manage the entire population. In this study we analysed the spatial structure of the Cypress Hills elk population, the distribution of the elk harvest in relation to agricultural conflicts, developed models of the spatial patterns of conflict fields, and evaluated compensation patterns for damage by wild herbivores. We propose modifications to current abatement and compensation programs and discuss alternative approaches involving changes to agricultural land use patterns that may reduce the intensity of conflicts with elk, and increase the acceptance capacity of landowners.