Age-specific survivorship and fecundity shape genetic diversity in marine fishes.

Abstract

Genetic diversity varies among species due to a range of eco‐evolutionary processes that are not fully understood. The neutral theory predicts that the amount of variation in the genome sequence between different individuals of the same species should increase with its effective population size (Ne). In real populations, multiple factors that modulate the variance in reproductive success among individuals cause Ne to differ from the total number of individuals (N). Among these, age‐specific mortality and fecundity rates are known to have a direct impact on the Ne/N ratio. However, the extent to which vital rates account for differences in genetic diversity among species remains unknown. Here, we addressed this question by comparing genome‐wide genetic diversity across 16 marine fish species with similar geographic distributions but contrasted lifespan and age‐specific survivorship and fecundity curves. We sequenced the whole genome of 300 individuals to high coverage and assessed their genome‐wide heterozygosity with a reference‐free approach. Genetic diversity varied from 0.2% to 1.4% among species, and showed a negative correlation with adult lifespan, with a large negative effect (slope=−0.089 per additional year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset (slope=−0.129 per additional year of lifespan). Using published vital rates for each species, we showed that the Ne/N ratio resulting simply from life tables parameters can predict the observed differences in genetic diversity among species. Using simulations, we further found that the extent of reduction in Ne/N with increasing adult lifespan is particularly strong under Type III survivorship curves (high juvenile and low adult mortality) and increasing fecundity with age, a typical characteristic of marine fishes. Our study highlights the importance of vital rates as key determinants of species genetic diversity levels in nature.