Genomics-informed captive breeding can reduce inbreeding depression and the genetic load in zoo populations

Abstract

Zoo populations of threatened species are a valuable resource for the restoration of wild populations. However, their small effective population size poses a risk to long-term viability, especially in species with high genetic load. Recent bioinformatic developments can identify harmful genetic variants in genome data. Here, we advance this approach, analysing the genetic load in the threatened pink pigeon (Nesoenas mayeri). We lift-over the mutation-impact scores that had been calculated for the chicken (Gallus gallus) to estimate the genetic load in six pink pigeons. Additionally, we perform in-silico crossings to predict the genetic load and realised load of potential offspring. We thus identify the optimal mate pairs that are theoretically expected to reproduce offspring with the least inbreeding depression. We use computer simulations to show how genomics-informed conservation can reduce the genetic load and maintain genome-wide diversity, arguing this will become instrumental in maintaining the long-term viability of zoo populations.

Genetic load and viability of a future restored northern white rhino population

“…One notable difference between our study and others is that our realized load estimates for the NWR and SWR genomes are many times higher than other studies because we included all putatively deleterious variants across the entire genome rather than restricting the analysis to the exome (e.g., Henn et al., 2016) or to ultraconserved regions (Speak et al., 2023). Estimating realized load from only the exome produces values comparable to those seen in studies of the exome or ultraconserved elements (mean realized load = 0.75 for NWR and 0.87 for SWR).…”

“…Simulations have even been proposed as a potential source of data for training models to predict IUCN extinction risk categories and recovery potential of species (van Oosterhout et al., 2022a, 2022b). Here, we used forward‐simulated populations from empirically derived genetic variation (Speak et al., 2023), a novel approach that is especially relevant when the founders of a future restored population are known.…”

“…For these reasons, estimates of the fitness effects of genetic variants are imprecise, and management decisions based solely on presumably functional genetic variation of individuals can be misleading (Kardos et al., 2021; Ralls et al., 2020). As genomic data representing diverse taxa continue to grow, and especially when coupled with databases linking survival and lifetime reproduction (Grueber & Sunnucks, 2022), so too will our power to link genotype to genomic health, fitness, and population viability and eventually use genomics‐informed strategies to manage realized load (Speak et al., 2023). These insights will be key for applying conservation strategies, including rapidly advancing in vitro conservation technologies, with greater precision.…”

Unravelling the mystery of endemic versus translocated populations of the endangered Australian lungfish (Neoceratodus forsteri)

“…In addition, the risk of introducing deleterious alleles when individuals from a large and genetically variable population are used to rescue a small one has been recently suggested and should be considered (Kyriazis et al., 2021). Restocking may boost adaptive genetic variability and provide some insurance against unpredictable future conditions, but preliminary analyses on local adaptation patterns can reduce the risk of outbreeding depressions, and genomic typing of introduced animals is a promising approach to exclude individuals with large inbreeding coefficients and large genetic load (Speak et al., 2023; van Oosterhout, 2020). In the case of N. forsteri these complex genetic considerations will not come easily, given their low genetic diversity and mixed genetic provenance of the Brisbane and North Pine River populations.…”

Can genetic rescue help save Arabia's last big cat?

“…These simulations highlighted the critical effect of the genetic load on the long-term viability of the leopard, which illustrates the importance of estimating and accounting for genetic load in genetic rescue. A conservation management program would therefore greatly benefit from estimating the genetic load and incorporating these data into computer simulations to assess different genetic rescue scenarios (Bertorelle et al, 2022;Speak et al, 2023;Van Oosterhout, 2020).…”