The goals of captive breeding programs are often to prevent extinction and/or extirpation while maintaining genetic diversity and fitness until reintroductions or supplementation of wild populations can occur. However, due to genetic changes that occur in captive populations, approximately one-third of such conservation programs fail to successfully establish new populations or contribute genes to existing populations.
Genetic impacts of captive breeding
In conjunction with Bob Lacy of the Brookfield Zoo in Chicago and under the direction of Andrew DeWoody, I characterized the genetic impacts of captive breeding. We utilized six populations of white-footed mice (Peromyscus leucopus) for 20 generations using two replicates of three protocols: minimizing mean kinship (MMK), random mating (RAN), or selection for docility (DOC). We evaluated the genetic changes in captive populations using neutral microsatellite loci that should reflect evolution due to drift and inbreeding. We found that MMK resulted in the slowest rate of loss of genetic diversity whereas the RAN and DOC protocols resulted in a more rapid loss of genetic diversity (with more variance across replicate populations). After 20 generations, the MK populations retained ~60% of the allelic diversity found in the source population compared to 48% and 45% in the RAN and DOC protocols, respectively. By comparing simulated populations to empirical data, we found conflicting evidence for adaptation to captivity via genetic hitchhiking of neutral microsatellites to nearby genes under selection. Our results suggest that MMK reduces the loss of alleles due to drift and inbreeding.
In additional work, co-authors and I used nearly 5500 single nucleotide polymorphisms (SNPs) to measure the impact of breeding regimes on genomic diversity. Using the same populations of captive mice but at more generations, we found that the MMK protocol most effectively retained genomic diversity and reduced the effects of selection. Additionally, genomic diversity was significantly related to fitness, as assessed with pedigrees and SNPs supported with genomic sequence data. Because captive-born individuals are often less fit in wild settings compared to wild-born individuals, captive-estimated fitness correlations likely underestimate the effects in wild populations. Therefore, this work suggests that minimizing inbreeding and selection in captive populations is critical to increasing the probability of releasing fit individuals into the wild. As such, MMK should be the gold standard breeding protocol for threatened and endangered species reared in captivity.
Effects of inbreeding, drift, and selection in captive populations. Mean multilocus heterozygosity (MLH) for six captive populations and the wild source population. Replicate populations are shown by solid (replicate 1) and dashed (replicate 2) lines. Estimates are shown for all genotyped SNPs (A), neutral SNPs (B) and nonneutral SNPs (C) as determined via simulations. Error bars represent SE calculated across individual estimates.