Haplotype-level metabarcoding to study the relationship between species occurrence and population genetic structure at the catchment scale in aquatic insects

A longstanding question in ecology and evolutionary biology is which evolutionary mechanisms explain why some species occur frequently while others do not. Previous studies have investigated this phenomenon through computer simulations, empirical studies, and ecological experiments involving a limited number of species. However, community-wide investigations addressing species diversity and underlying genetic diversity in natural settings remain underexplored. To address such species-genetic diversity correlations (SGDC), we employed haplotype-level bulk DNA metabarcoding to infer haplotypes from many aquatic insect species with varying occurrence across 59 sites in the catchment. To examine the relationship between species occurrence and population genetic structure, we assessed the correlations between environmental parameters, female wing length, a proxy for dispersal ability, and haplotype data. We identified 889 haplotypes belonging to 198 taxonomically identified operational taxonomic units (OTUs). While species with higher occurrence in the catchment had greater total genetic diversity across the landscape (ɣ-genetic diversity) and were likely exposed to a wider range of environmental conditions, we found no correlation between species occurrence and genetic differentiation (β-genetic diversity). Furthermore, we observed no significant correlation between local intraspecific genetic diversity and local species diversity (α-SGDC) across all examined OTUs, and only one OTU ( Rhyacophila sp.) showed a correlation between genetic differentiation and community divergence (β-SGDC). These results may be explained by the contrasting factors influencing both levels of biodiversity. Notably, gene flow likely offsets genetic differentiation in the metapopulation, while species sorting appears to influence divergence in the metacommunity. Our findings suggest an alternative approach to studying the relationship between species occurrence, population genetic structure, and SGDC from a community-level perspective. They also have important implications for addressing biodiversity loss driven by rapid environmental changes resulting from human activities and climate change.