Purging of Highly Deleterious Mutations Through an Extreme Bottleneck

Transitions to captivity often produce population bottlenecks. On the one hand, bottlenecks increase inbreeding and decrease effective population size, thus increasing extinction risk. On the other hand, elevated homozygosity associated with inbreeding may purge deleterious mutations. Previous empirical studies of purging in captive breeding programs have focused on phenotypic measurements. We test natural selection's ability to purge deleterious mutations following an extreme population bottleneck by analyzing patterns of genetic diversity in wild and captive-bred individuals of the Lord Howe Island stick insect, Dryococelus australis. Dryococelus australis has been bred in captivity for two decades, having passed through an extreme bottleneck-only two mating pairs with few new additions since then. The magnitude of the bottleneck together with high female fecundity but low offspring recruitment set up nearly ideal conditions for the purging of deleterious mutations. As expected, captive-bred individuals had a greater number of long runs of homozygosity compared with wild individuals, implying strong inbreeding in captivity which would facilitate purging in homozygous regions. Stop-codon mutations were preferentially depleted in captivity compared with other mutations in coding and noncoding regions. The more deleterious a mutation was predicted to be, the more likely it was found outside of runs of homozygosity, implying that inbreeding facilitates the expression and thus removal of deleterious mutations, even after such an extreme bottleneck and under the benign conditions of captivity. These data implicate inbreeding and recessive deleterious mutation load in fitness variation among captive and wild D. australis.