Populations that are small and isolated face an elevated risk of extinction, partly due to genetic factors. These genetic factors include reduced fitness due to inbreeding depression and the accumulation of deleterious mutations, and reduced potential for adaptation due to the loss of genetic diversity over time. Though experiments in the lab have repeatedly demonstrated that small and isolated populations are doomed to mutation accumulation and, ultimately, extinction, it remains unclear whether this process poses a significant risk to populations in the wild. In the 1990s, several studies revealed that island foxes (Urocyon littoralis) on California’s Channel Islands harbor exceptionally low levels of genetic diversity, indicating a long history of small population size and isolation on the islands. In one particular population on San Nicolas Island, the foxes were genetically indistinguishable from one another. This level of genetic monomorphism has not been observed in any other wild population, and begs the question of how island foxes have persisted for thousands of years without showing obvious physical symptoms of genetic deterioration. Through collaboration with other geneticists and experts on skeletal morphology, I investigated this apparent paradox. In two publications [1, 2], we describe the results and implications of whole genome sequence analyses, morphological examinations, and simulations of island fox evolution to understand the unique history of island foxes and how their story reveals the conditions in which small populations in isolation may thrive for thousands of generations.
Robinson, J.A., Ortega Del-Vecchyo, D., Fan, Z., Kim, B.Y., vonHoldt, B.M., Marsden, C.D., Lohmueller, K.E., and Wayne, R.K., 2016. Genomic flatlining in the endangered island fox. Current Biology 26, 1183–1189. doi:10.1016/j.cub.2016.02.062
Robinson, J.A., Brown, C., Kim, B.Y., Lohmueller, K.E., and Wayne, R.K., 2018. Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in island foxes. Current Biology 28, 3487–3494. doi:10.1016/j.cub.2018.08.066
For more than 50 years, biologists have been studying a population of gray wolves (Canis lupus) and moose (Alces alces) on Isle Royale in Lake Superior in the longest-running continuous study of the interactions between predators and prey. Over that time, biologists have witnessed the rise of the wolf population to a peak of fifty individuals, and the subsequent decline to just two individuals as the population deteriorated due to severe inbreeding. The population was established naturally when two to three wolves crossed over from the mainland during a winter cold enough that an ice bridge formed, connecting the mainland to Isle Royale. Since then, there have been limited observations of wolves moving into or out of Isle Royale. Examination of skeletal remains revealed an increasing prevalence of skeletal defects in Isle Royale wolves over time, coincident with increasing levels of inbreeding. In recent years, every wolf born on Isle Royale has possessed at least one skeletal deformity, and reproduction in the population has ceased. I collaborated with Isle Royale wolf biologists and an expert on wolf skeletal morphology to examine the genomic consequences of severe inbreeding depression in Isle Royale wolves. Our study sheds light on the effects of inbreeding in contrast to long-term small population size, and suggests that the number of wolves on Isle Royale is too small to sustain a viable population in the long run, as severe inbreeding will be inevitable without sustained connectivity with the mainland. These results have immediate implications for the reintroduction of wolves to Isle Royale, and also provides lessons for the management of other extremely small and isolated populations of conservation concern.
Baboons (genus Papio) are social Old World primates that have been extensively studied in the wild and in captivity by primatologists, ecologists, evolutionary biologists, and biomedical researchers. Unlike many other primates, baboons spend much of their time on the ground in savannas and open woodlands, allowing researchers to observe and follow them more easily. This research has provided a wealth of information about the behavior and biology of baboons under natural conditions. In captivity, baboons are an important model for biomedical research because they share many similarities with humans relative to other model organisms, such as mice or fruit flies. I am studying whole genome sequences from a large pedigreed colony of olive and yellow baboons (P. anubis and P. cynocephalus) at the Southwest National Primate Research Center (snprc.org) to conduct a deep investigation of deleterious mutations. Linking deleterious mutations to aberrant traits in wild populations is extremely challenging, therefore direct investigation and quantification of the genome-wide burden of deleterious variation can only be done in a well-studied population in a controlled environment. This work is sorely needed for the effective prediction and management of genetic health in many contexts, from conservation to healthcare.