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 (N e ). In real populations, multiple factors that modulate the variance in reproductive success among individuals cause N e 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 N e /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 N e /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 N e /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.

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.…”

Population genomics reveals the underlying structure of the small pelagic European sardine and suggests low connectivity within Macaronesia

“…A total of 15 samples from three were collected during oceanographic surveys and the remaining 73 specimens, from ten distinct geographic locations, were sampled at local markets (Table S1). Sequence data for the samples from Bay of Biscay, Gulf of Cadiz, Mar Menor and the Gulf of Lion (n=20) were obtained from Barry et al (2022), adding further sampling locations to our dataset.…”

“…each position of the genome is covered by 3 reads) and seven to 20 X sequencing depth (details in Additional file 1: Table S1). Raw data for 20 sardine individuals from (Barry et al, 2022) was further processed using the same procedure as described in the next section (sequencing depth between 15 and 22 X). Table S1 indicates the assignment of samples to the different subsets considered for further analysis.…”

“…In this study, we produced an European sardine genomic data set consisting of whole genome nuclear data and complete mitochondrial genomes for 88 individuals that were analyzed together with data from 20 sardine individuals from a previous study (Barry et al, 2022), in a total of 108 samples from a total of 16 locations across 5000 km of the species distribution range. This enabled investigating previously suggested barriers to gene flow, mapping the major genetic clusters that characterize S. pilchardus in a large part of its distribution, the comparison between markers with different modes of inheritance but also to get a first insight into the genomics barriers contributing to the observed population structure.…”

Sweepstakes reproductive success via pervasive and recurrent selective sweeps

“… Árnason, 2004 ; Árnason and Halldórsdóttir, 2015 ; Niwa et al, 2016 ). Empirical evidence for variance in reproductive success due to life-table characteristics has been found using genome-wide polymorphism data in marine fishes ( Barry et al, 2021 ). Reproductive skew needs to be studied using gene genealogies on a genome-wide scale.…”