Genomes of Galápagos Mockingbirds Reveal the Impact of Island Size and Past Demography on Inbreeding and Genetic Load in Contemporary Populations

Abstract

Restricted range size brings about noteworthy genetic consequences that may affect the viability of a population and eventually its extinction. Particularly, the question if an increase in inbreeding can avert the accumulation of genetic load via purging is hotly debated in the conservation genetic field. Insular populations with limited range sizes represent an ideal setup for relating range size to these genetic factors. Leveraging a set of eight differently sized populations of Galápagos mockingbirds (Mimus), we investigated how island size shaped effective population size (N_e), inbreeding and genetic load. We assembled a genome of M. melanotis and genotyped three individuals per population by whole-genome resequencing. Demographic inference showed that the N_e of most populations remained high after the colonisation of the archipelago 1–2 Mya. N_e decline in M. parvulus happened only 10–20 Kya, whereas the critically endangered M. trifasciatus showed a longer history of reduced N_e. Despite these historical fluctuations, the current island size determines N_e in a linear fashion. In contrast, significant inbreeding coefficients, derived from runs of homozygosity, were identified only in the four smallest populations. The index of additive genetic load suggested purging in M. parvulus, where the smallest populations showed the lowest load. By contrast, M. trifasciatus carried the highest genetic load, possibly due to a recent rapid bottleneck. Overall, our study demonstrates a complex effect of demography on inbreeding and genetic load, providing implications in conservation genetics in general and in a conservation project of M. trifasciatus in particular.