Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction

Abstract

The observation that small isolated populations often suffer reduced fitness from inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we performed whole-genome sequencing and morphological analysis of an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through population genetic simulations and comparison with wolf genomes from a variety of demographic histories, we find evidence that severe inbreeding depression in this population is due to increased homozygosity of strongly deleterious recessive mutations. Our results have particular relevance in light of the recent translocation of wolves from the mainland to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon

“…California), and those at the extreme of the expansion front (Alaska), displayed deleterious mutations at higher derived allele frequencies, and more frequently in homozygous state, in line with the nearly neutral theory. Similar findings have been observed in domesticated species [86] and recently in Isle Royale wolves [26] where decreased population sizes and inbreeding increased the frequency of deleterious recessive mutations. Overall, these results are consistent with recent empirical findings in which small populations or populations at the expansion front carry more homozygous derived deleterious mutations [26,27,86].…”

“…On the one hand, processes such as strong and repeated bottlenecks [24,32], including domestication [86,88], large expansions [89,90] [86] and recently in Isle Royale wolves [26] where decreased population sizes and inbreeding increased the frequency of deleterious recessive mutations. Overall, these results are consistent with recent empirical findings in which small populations or populations at the expansion front carry more homozygous derived deleterious mutations [26,27,86]. These deleterious mutations in homozygous state are expected to be purged by purifying selection [23,92].…”

“…Combining population genomics data with demographic modelling represents a powerful strategy to test alternative hypotheses about historical drivers of existing genomic diversity. Previous studies employing a similar approach have focussed mostly on species with a narrow geographic range, such as small islands [26,27], which are on the verge of extinction [28][29][30][31] are strongly bottlenecked [32], sheddig light on the evolutionary consequences of small population size. Few studies, however, have investigated how historical processes have shaped the geographical patterns in the distribution of genomic diversity in more broadly distributed species, e.g., at the scale of a whole continent.…”

Testing for hybridisation of the Critically Endangered Iguana delicatissima on Anguilla to inform conservation efforts

“…In addition, before any translocations are undertaken under the auspices of 'genetic rescue' (Bell et al 2019) it is necessary to assess the genomic heterozygosity of the donor population and to examine the history of population (i.e. have historic bottlenecks been recorded) (Robinson et al 2019). The prevalence and the risk of disease should also be thoroughly assessed (Hellebuyck et al 2017).…”

Putting the genes into community genetics

“…Focusing on individual genotype variation rather than genetic diversity also facilitates interpretation of non‐intuitive outcomes in other studies in which an increase in genetic diversity had neutral or negative ecological consequences. For example, genetic mixing of mainland wolves and Isle Royale wolves increased genetic variation, but led to an increased frequency of deleterious traits at the individual genotype level, which in turn led to population collapse (Robinson et al, ). Loss of a wolf population has ecological consequences, affecting the distribution of prey carcasses on a landscape, which in turn affects microbial composition, Microbial abundance and soil nutrients (Bump, Peterson, & Vucetich, ).…”