Comparative tests of the species‐genetic diversity correlation at neutral and nonneutral loci in four species of stream insect

Abstract

A fundamental question linking population genetics and community ecology is how adaptive processes (e.g., natural selection) and neutral processes (e.g., drift-migration equilibrium) underpin the species-genetic diversity correlation (SGDC). Here, we combine genome scans and outlier loci detection with community analysis to separately test for neutral and nonneutral SGDCs in four species of stream insect. We sampled 60 localities in Japan and examined the relationships among population AFLP band richness (Br), taxon richness of the total community (S) and of the trophic guild (S ), and 15 habitat parameters that could potentially drive adaptation and influence richness. Neutral Br was positively correlated with S only in the dominant species of these communities, suggesting Br may be constrained when intraspecific competition is pronounced. Nonneutral Br was correlated with S in a species restricted to high elevations where habitat heterogeneity was highest. Community distance and genetic distance (β-SGDC) was correlated in two of the four species at both neutral and nonneutral loci. Distance-based redundancy analysis found geographic isolation and elevation to drive divergence of both communities and populations. This suggests that both neutral and adaptive divergence occurred through the shared influences of geographic isolation and local adaptation at the two levels of diversity.

Partitioning genetic and species diversity refines our understanding of species–genetic diversity relationships

“…Our work extends and refines previous studies that suggested investigating neutral and adaptive genetic diversity simultaneously to reveal neutral signatures in species–genetic diversity relationships (Bertin et al., ; Watanabe & Monaghan, ) and shows that this framework can be successfully applied in single‐species studies when large genomic datasets are available. The efficiency of such approach, however, depends on how much the adaptive and neutral genetic diversity deviate from each other, and may thus be better suited for studies focusing on fragmented ecosystems occurring over environmental gradient, as was the case here.…”

“…Recent studies have stressed the usefulness of partitioning neutral and adaptive genetic diversity (Bertin et al., ; Watanabe & Monaghan, ) and of simultaneously analyzing various species diversity components (Lamy et al., ) to investigate species–genetic diversity relationships. Our results show that combining these two approaches can help to unravel the origin of covariation between these two levels of diversity.…”

“…SGDC studies have traditionally focused on neutral genetic diversity, although adaptive diversity has been occasionally considered (Bertin et al., ; Kahilainen, Puurtinen, & Kotiaho, ; Vellend et al., ; Watanabe & Monaghan, ). While neutral processes affect the whole genome uniformly, selection acts on specific regions, which bear the footprint of selection (Holderegger, Kamm, & Gugerli, ).…”

“…In SGDC studies, this approach can provide a clarified portrayal of similarity in the role of neutral processes on species and genetic diversity, and can thus help determine whether neutral processes are participating in the production of species–genetic diversity correlations. Two recent studies have applied this approach (Bertin et al., ; Watanabe & Monaghan, ). Bertin et al.…”

“…However, because both Bertin et al. () and Watanabe and Monaghan () used AFLP markers, only a few loci putatively under selection were identified (an average of eight across all species’ datasets). Because genetic diversity estimates are sensitive to the number of genetic markers (Dutoit, Burri, Nater, Mugal, & Ellegren, ), such a low number of outlier loci is insufficient to calculate robust genetic diversity estimates of non‐neutral diversity.…”