Demography and environment modulate the effects of genetic diversity on extinction risk in a butterfly metapopulation

Linking genetic diversity to extinction is a common goal in genomic studies. Recently, a debate has arisen regarding the importance of genetic variation in conservation as some studies have failed to find associations between genome-wide genetic diversity and extinction risk. However, only rarely are genetic diversity and fitness measured together in the wild, and typically variation in demographic history or environment are ignored. It is therefore difficult to infer whether a lack of an association is real or obscured by confounding factors. To address these shortcomings, we analysed genetic data from 7,501 individuals with extinction data from 279 meadows and mortality of 1,742 larval nests in a butterfly metapopulation. We found strong negative associations between genetic diversity and extinction when heterozygosity was included alone in models. However, this association was no longer present when ecological covariates were included. Interactions between heterozygosity and demographic variables revealed that associations are context-dependent or only detectable when confounding factors are controlled. For example, extinction declined with increasing heterozygosity in large but not currently small populations, although negative associations between heterozygosity, extinction, and mortality were detected in populations with a recent history of decline. We conclude that low genetic diversity is an important predictor of extinction, predicting >25% increase in extinction beyond ecological factors in certain contexts. This highlights that inferences about the importance of genetic diversity should not rely on genomic data alone but requires investments in obtaining demographic and environmental data from natural populations to jointly assess their impact on population extinction risk.