ABSTRACT
Chromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations until one arrangement becomes fixed. Many questions remain about how inversion polymorphisms arise, how they are maintained over the long term, and ultimately, whether and how they contribute to speciation. The long-snouted seahorse (Hippocampus guttulatus) is genetically subdivided into geographic lineages and marine-lagoon ecotypes, with shared structural variation underlying lineage and ecotype divergence. Here, we aim to characterize structural variants and to reconstruct their history and suspected role in ecotype formation. We generated a near chromosome-level genome assembly and described genome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequences from Atlantic, Mediterranean, and Black Sea populations. By also analysing linked-read sequencing data, we found evidence for two chromosomal inversions that were several megabases in length and showed contrasting allele frequency patterns between lineages and ecotypes across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one likely being maintained by divergent selection and the other by pseudo-overdominance. A possible selective coupling between the two inversions was further supported by the absence of specific haplotype combinations and a putative functional interaction between the two inversions in reproduction. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels for the two inversions, with a likely impact on their dynamics and contribution to divergence and speciation.
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 ( s l o p e = - 0.089 per additional year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset ( s l o p e = - 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.
