Accounting for cryptic population substructure enhances detection of inbreeding depression with genomic inbreeding coefficients: an example from a critically endangered marsupial

Abstract

Characterizing inbreeding depression in wildlife populations can be critical to their conservation. Coefficients of individual inbreeding can be estimated from genome‐wide marker data. The degree to which sensitivity of inbreeding coefficients to population genetic substructure alters estimates of inbreeding depression in wild populations is not well understood. Using generalized linear models, we tested the power of two frequently used inbreeding coefficients that are calculated from genome‐wide SNP markers, FH and F^III, to predict four fitness traits estimated over two decades in an isolated population of the critically endangered Leadbeater's possum. FH estimates inbreeding as excess observed homozygotes relative to equilibrium expectations, whereas F^III quantifies allelic similarity between the gametes that formed an individual, and upweights rare homozygotes. We estimated FH and F^III from 1,575 genome‐wide SNP loci in individuals with fitness trait data (N = 179–237 per trait), and computed revised coefficients, FHby group and F^IIIby group, adjusted for population genetic substructure by calculating them separately within two different genetic groups of individuals identified in the population. Using FH or F^III in the models, inbreeding depression was detected for survival to sexual maturity, longevity and whether individuals bred during their lifetime. F^IIIby group (but not FHby group) additionally revealed significant inbreeding depression for lifetime reproductive output (total offspring assigned to each individual). Estimates of numbers of lethal equivalents indicated substantial inbreeding load, but differing between inbreeding estimators. Inbreeding depression, declining population size, and low and declining genetic diversity suggest that genetic rescue may assist in preventing extinction of this unique Leadbeater's possum population.

The vegetation structure and condition of contracting lowland habitat for Leadbeater's possum (Gymnobelideus leadbeateri)

“…Urgent interventions are also required to address the small population size and loss of genetic diversity. Evidence of inbreeding depression in this population has recently been documented (Zilko et al 2020). A genetic rescue strategy is currently being implemented, whereby mixed pairs of lowland and highland individuals will be established in captivity and subsequently translocated to the wild in order to achieve outbreeding.…”

Detection of Breinlia sp. (Nematoda) in the Leadbeater's possum (Gymnobelideus leadbeateri)

“…Conservation measures for this species include habitat protection, revegetation, nest box provision and translocation, in order to maintain breeding habitat and facilitate population genetic diversity and growth ( Harley, 2016 ). The lowland possum population has declined to ≤40 individuals; a genetic rescue programme is presently underway that involves the formation of mixed lowland-highland pairs in captivity to alleviate inbreeding in the lowland population ( Zilko et al, 2020 ).…”

Applying Population Viability Analysis to Inform Genetic Rescue That Preserves Locally Unique Genetic Variation in a Critically Endangered Mammal

“…The geographic isolation of the Yellingbo population makes contemporary gene flow with other populations highly unlikely [36]. This population had greatly reduced genetic diversity compared to all conspecific populations and exhibited substantial inbreeding depression for survival to sexual maturity, longevity, probability of breeding during lifetime, and lifetime reproductive output [37]. Inbreeding depression likely contributed to the decline from~120 individuals in 1997 to 35 individuals in 2017.…”

“…Inbreeding depression likely contributed to the decline from~120 individuals in 1997 to 35 individuals in 2017. Heterozygosity concurrently declined by 12%, putatively limiting the capacity of the population to adapt to environmental change and prevent the expression of deleterious variation [37]. Furthermore, suitable habitat for Leadbeater's possum has declined in extent and quality, mainly because of habitat succession and altered hydrology [32].…”

“…Furthermore, suitable habitat for Leadbeater's possum has declined in extent and quality, mainly because of habitat succession and altered hydrology [32]. Based on monotonic decline in population size, presence of inbreeding depression, and deteriorating habitat condition, the extinction of the Yellingbo population is highly likely without intervention [37,38]. Translocation of lowland Yellingbo individuals to high-quality habitat beyond Yellingbo and outcrossing with genetically diverse highland animals is planned to prevent the extinction of this population.…”