Genetic purging in captive endangered ungulates with extremely low effective population sizes

Abstract

Inbreeding threatens the survival of small populations by producing inbreeding depression, but also exposes recessive deleterious effects in homozygosis allowing for genetic purging. Using inbreeding-purging theory, we analyze early survival in four pedigreed captive breeding programs of endangered ungulates where population growth was prioritized so that most adult females were allowed to contribute offspring according to their fitness. We find evidence that purging can substantially reduce inbreeding depression in Gazella cuvieri (with effective population size Ne = 14) and Nanger dama (Ne = 11). No purging is detected in Ammotragus lervia (Ne = 4), in agreement with the notion that drift overcomes purging under fast inbreeding, nor in G. dorcas (Ne = 39) where, due to the larger population size, purging is slower and detection is expected to require more generations. Thus, although smaller populations are always expected to show smaller fitness (as well as less adaptive potential) than larger ones due to higher homozygosis and deleterious fixation, our results show that a substantial fraction of their inbreeding load and inbreeding depression can be purged when breeding contributions are governed by natural selection. Since management strategies intended to maximize the ratio from the effective to the actual population size tend to reduce purging, the search for a compromise between these strategies and purging could be beneficial in the long term. This could be achieved either by allowing some level of random mating and some role of natural selection in determining breeding contributions, or by undertaking reintroductions into the wild at the earliest opportunity.

Prediction of fitness under different breeding designs in conservation programs

“…Our pedigrees, encompassing t = N generations, were long enough to detect purging while inducing a relatively small underestimate of δ. This agrees with similar purging estimates obtained in ungulate species, where purging was detected in pedigrees with about t = 9 generations with overall effective population sizes N e slightly over 10, while detection of purging failed when the number of generations (t = 7) was well below the effective size (N e = 39) (López-Cortegano, Moreno & García-Dorado, 2021). Furthermore, an effective size below 10 can also be too small to allow for purging efficient enough to be detected.…”

“…If this was maintained under similar conditions and similar population size over a period of time much longer than the generations evaluated, the population may have reached a mutation-selection-drift equilibrium, where δ is constant and the fitness decline can be the result of the fixation of deleterious alleles and not inbreeding depression. Finally, as noted above, López-Cortegano et al (2021) recently estimated large and significant d values in two captive gazelle populations that were maintained for about eight generations with N e > 10, and it is worthwhile to note that, in this latter case, management was intended to minimize coancestry between mating individuals but the contribution of offspring per female was not under control. Therefore, the available evidence suggests that purging can substantially reduce the fitness inbreeding depression in not too small populations (say, N e > 10) as far as the managing protocols allow for natural selection, as shown in our simulation study.…”

“…Finally, as noted above, López‐Cortegano et al . (2021) recently estimated large and significant d values in two captive gazelle populations that were maintained for about eight generations with N e > 10, and it is worthwhile to note that, in this latter case, management was intended to minimize coancestry between mating individuals but the contribution of offspring per female was not under control. Therefore, the available evidence suggests that purging can substantially reduce the fitness inbreeding depression in not too small populations (say, N e > 10) as far as the managing protocols allow for natural selection, as shown in our simulation study.…”

Insights from the rescue and breeding management of Cuvier’s gazelle (Gazella cuvieri) through whole‐genome sequencing

“…Then, we filtered the resulting BAM files to keep only mapped reads and primary alignments. Next, GATK HaplotypeCaller (version 4.1.4.0) (DePristo et al, 2011 ; McKenna et al, 2010 ) was used to call genotypes in each sample independently and GenotypeGVCFs was used for joint genotyping. Furthermore, we filtered the resulting vcf file using GATK SelectVariants ‐‐select‐type‐to‐include (version 4.1.4.0) to keep only variable single nucleotide positions.…”

“…We calculated the number of heterozygous positions in the callable region for each scaffold to retrieve the genome‐wide heterozygosity of each gazelle. Because the samples have an average coverage of ~7×, we used ANGSD (Korneliussen et al, 2014 ) to estimate genome‐wide heterozygosity from genotype likelihoods and compared it to the estimates from the genotype calling using GATK (DePristo et al, 2011 ; McKenna et al, 2010 ). We estimated genome‐wide heterozygosity following filtering for callability (‐sites), using allele frequencies (‐doSaf 1), taking genotype likelihoods into account with the SAMtools algorithm (‐GL 1) and specifying several filters: discard bad reads (‐remove_bads1), use reads where the mate can be mapped (‐only_proper_pairs 1), adjust quality for reads with multiple mismatches to the reference (‐C 50), adjust quality scores around insertion/deletions (‐baq 1), minimum mapping and base qualities of 30 (‐minMapQ 30, ‐minQ 30) include sites with a maximum read length of 30 (‐setMaxDepth 30).…”