Resolving the evolutionary history of bighorn sheep to inform future management: an answer to the California bighorn lineage question

Abstract

Although translocations can be effective for augmenting and restoring wild populations, they can disrupt native patterns of genetic structure, diversity, and local adaptation, thereby hampering conservation efforts. Managers must weigh potential costs and benefits of choosing well-differentiated donor individuals that could confer a boost to genetic diversity while avoiding outbreeding depression or ecological mismatch. This decision is more daunting when taxonomy is unclear or debated. For example, bighorn sheep (Ovis canadensis) populations in the United States that have been managed as the "California" lineage (part of the formerly recognized subspecies O. c. californiana) originate from serial translocations sourced from populations in British Columbia, resulting in reduced genetic diversity and elevated risk of inbreeding. After research on skull shape and RFLP analysis of mtDNA failed to find support for that subspecies, some jurisdictions treated the California lineage as part of the Rocky Mountain subspecies (O. c. canadensis) and mixed individuals in subsequent translocations, in part to increase genetic diversity of bottlenecked populations. Yet detailed genetic data addressing validity of those putative lineages were lacking. We reconstructed the genetic history of bighorn sheep by sampling the major putative subspecies or lineages, focusing on native (remnant) genetic variation, and generating high-throughput DNA sequencing data ([~]15,000-25,000 SNPs). Complementary phylogenetic and population genetic analyses supported the distinctiveness of four bighorn lineages at levels corresponding to subspecies. Our results confirm the genetic identity of the no longer putative California bighorn lineage, answering a question that puzzled geneticists and managers for decades. Moving forward, we recommend that managers 1) maintain the natural variation held in native populations by protecting them from intentional translocations or unintentional mixing with nearby populations; 2) prioritize withinlineage translocations for population augmentation or repatriation to previously occupied regions; and 3) cautiously consider any translocations that would lead to mixing of distinct evolutionary lineages.