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 demographic history and 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 a strong negative association between genetic diversity and
extinction when considering only heterozygosity in models. However, this
association disappeared when accounting for ecological covariates,
suggesting a confounding between demography and genetics and a more
complex role for heterozygosity on extinction risk. Modelling interactions
between heterozygosity and demographic variables revealed that
associations between extinction and heterozygosity were context-dependent.
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 small
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.
These results highlight that inferences about the importance of genetic
diversity for population viability should not rely on genomic data alone
but requires investments in obtaining demographic and environmental data
from natural populations.