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. Individual genome-wide heterozygosity varied from 0.2 to 1.4%, and adult lifespan was by far the most significant predictor of genetic diversity, with a large negative effect (slope = −0.089 per additionnal year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset (slope = −0.129 per additionnal year of lifespan). Using published vital rates for each species, we showed that the ratio only generated by life tables predict the observed differences in genetic diversity among species. 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, which is typical of marine fish. Our study highlights the importance of vital rates in the evolution of genetic diversity within species in nature.Author SummaryUnderstanding 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 to 1.4% in the European pilchard. 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 a species’ genetic diversity and explains why this effect varies widely across taxonomic groups.

Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species

“…Instead, we find that population connectivity in all three species is restricted and that gaps in suitable habitat may impose barriers to effective dispersal in coastal species in general. The present study thus corroborates recent findings emphasizing that life‐history influences genetic patterns of marine coastal fish species (Barry et al, 2021) and illustrates the power of a comparative multispecies approach.…”

Migratory behaviour is positively associated with genetic diversity in butterflies

“…Overall, our results suggest that the particular characteristics of migratory behaviour in Lepidoptera are strongly influential in determining high levels of species' genetic diversity. Beyond the potential consequences of movement behaviour, other traits such as fecundity and behavioural adaptations such as insertion of sperm plugs are likely to influence levels of genetic diversity, as has been found in other animal groups (Romiguier et al, 2014; Chen et al, 2017; Barry et al, 2022). However, correlates of genetic diversity seem to be strongly dependent on the phylogenetic scale of sampling (Mackintosh et al, 2019), and to what extent our results may apply to other taxonomic groups requires further exploration.…”

Effects of insularity on genetic diversity within and among natural populations

“…Given only a few common conditions, such as “long” life histories, severe disturbances that will ultimately result in declines in GD might have no obvious immediate effect on some groups of animals, but severely impact others. For example, adult lifespan appeared to be the best predictor of GD based on the whole genome analysis of 16 European marine fish species, but downstream simulations demonstrated that this relationship did not hold for birds and mammals (Barry et al, 2022). This lag seems analogous to the concept of “extinction debt” (Tilman et al, 1994), where changing environmental conditions will ultimately result in the extinction of species, and yet they persist on sampling timescales, even if they are in a terminal decline.…”