Nucleotide diversity is a poor predictor of short-term adaptive potential

Abstract

Significance statementThe current paradigm in conservation genetics suggests that species with the lowest molecular genetic diversity have the lowest capacity to adapt. Despite previous concern that traditional measures of molecular genetic variation are not useful predictors of adaptive potential, the conflation of genetic diversity and adaptive potential remains prevalent in both scientific literature and global policy. By combining new theory with a large dataset of genetic variation across hundreds of species, we show that molecular sequence variation is weakly related to the level of heritable variation in traits across species. This demonstrates that genetic diversity does not reliably predict adaptive potential, and highlights the urgent need to move beyond simple measures when assessing the evolutionary resilience of populations. A capacity to adapt is essential for a population to avoid extinction in a changing world and is recognised as a global conservation priority. Adaptation requires additive (heritable) genetic variation for traits that influence survival and fecundity, but measuring this variation is difficult, particularly in species of conservation concern. Instead, molecular genetic diversity is often used to infer adaptive potential. However, previous research has cast doubt on the suitability of traditional molecular markers (allozymes and microsatellites) for this purpose given their weak relationship with heritability - a common measure of additive genetic variance. Recent advances in sequencing technology have since shifted focus towards nucleotide diversity and variation in functional regions, but their practicality for predicting adaptive potential remains debated and untested. Furthermore, heritability itself is a poor proxy for adaptive potential because it depends on environmental variance. We collated 2,113 published estimates of evolvability - a measure of additive genetic variance that avoids environmental confounding - across 193 eukaryotic species, and evaluated how well evolvability is predicted by molecular diversity. We find that microsatellite and nucleotide diversity are not significantly correlated to each other, and neither predict evolvability (nucleotide diversity explains 0.7% of interspecific differences in evolvability and doubling nucleotide diversity only corresponds to a 9.2% increase in evolvability). With new theoretical work, we show that such weak associations are expected. Together, our results suggest that simple molecular measures of genetic variation are insufficient for predicting adaptive potential and continued reliance on these metrics risks misinforming conservation management.