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 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 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 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. Author Summary Understanding how and why genetic diversity varies across species has important implications for evolutionary and conservation biology. Although genomics has vastly improved our ability to document intraspecific DNA sequence variation at the genome level, the range and determinants of genetic diversity remain partially understood. At a broad taxonomic scale in eukaryotes, the main determinants of diversity are reproductive strategies distributed along a trade-off between the quantity and the size of offspring, which likely affect the long-term effective population size. Long-lived species also tend to show lower genetic diversity, a result which has however not been reported by comparative studies of genetic diversity at lower taxonomic scales. Here, we compared genetic diversity across 16 European marine fish species showing marked differences in longevity. Adult lifespan was the best predictor of genetic diversity, with genome-wide average heterozygosity ranging from 0.2% in the black anglerfish (L. budegassa) to 1.4% in the European pilchard (S. pilchardus). Using life tables summarizing age-specific mortality and fecundity rates for each species, we showed that the variance in lifetime reproductive success resulting from age structure, iteroparity and overlapping generations can predict the range of observed differences in genetic diversity among marine fish species. We then used computer simulations to explore how combinations of vital rates characterizing different life histories affect the relationship between adult lifespan and genetic diversity. We found that marine fishes that display high juvenile but low adult mortality, and increasing fecundity with age, are typically expected to show reduced genetic diversity with increased adult lifespan. However, the impact of adult lifespan vanished using bird and mammal-like vital rates. Our study shows that variance in lifetime reproductive success can have a major impact on species genetic diversity and explains why this effect varies widely across taxonomic groups.