Whole-Genome Evaluation of Genetic Rescue: The Case of a Curiously Isolated and Endangered Butterfly

Abstract

Genetic rescue, or the translocation of individuals among populations to augment gene flow, can help ameliorate inbreeding depression and loss of adaptive potential in small and isolated populations. Genetic rescue is currently under consideration for an endangered butterfly in Canada, the Half-moon Hairstreak (Satyrium semiluna). A small, unique population persists in Waterton Lakes National Park, Alberta, isolated from other populations by more than 400 km. However, whether genetic rescue would actually be helpful has not been evaluated. Here, we generate the first chromosome-level genome assembly and whole-genome resequence data for the species. We find that the Alberta population maintains extremely low genetic diversity and is genetically very divergent from the nearest populations in British Columbia and Montana. Runs of homozygosity suggest this is due to a long history of inbreeding, and coalescent analyses show that the population has been small and isolated, yet stable, for up to 40k years. When a population like this maintains its viability despite inbreeding and low genetic diversity, it has likely undergone purging of deleterious recessive alleles and could be threatened by the reintroduction of such alleles via genetic rescue. Ecological niche modelling indicates that the Alberta population also exhibits environmental associations that are atypical of the species. Together, these evolutionary and ecological divergences suggest that population crosses may result in outbreeding depression. We therefore infer that genetic rescue has a relatively unique potential to be harmful rather than helpful for this population at present. However, because of its reduced adaptive potential, the Alberta population may still benefit from future genetic rescue as climate and habitat conditions change. Proactive experimental population crosses should therefore be completed to assess reproductive compatibility and progeny fitness.