The limited spatial scale of dispersal in soil arthropods revealed with whole-community haplotype-level metabarcoding

Soil mesofauna communities are hyperdiverse and critical for ecosystem functioning. However, our knowledge on spatial structure and underlying processes of community assembly for soil arthropods is scarce, hampered by limited empirical data on species diversity and turnover. We implement a high-throughput-sequencing approach to generate comparative data for thousands of arthropods at three hierarchical levels: genetic, species and supra-specific lineages. A joint analysis of the spatial arrangement across these levels can reveal the predominant processes driving the variation in biological assemblages at the local scale. This multi-hierarchical approach was performed using haplotype-level-COI metabarcoding of entire communities of mites, springtails and beetles from three Iberian mountain regions. Tens of thousands of specimens were extracted from deep and superficial soil layers and produced comparative phylogeographic data for >1000 co-distributed species and nearly 3000 haplotypes. Local assemblages were highly distinctive between grasslands and forests, and within each of them showed strong spatial structures and high endemicity at the scale of a few kilometres or less. The local distance-decay patterns were self-similar for the haplotypes and higher hierarchical entities, and this fractal structure was very similar in all three regions, pointing to a significant role of dispersal limitation driving the local-scale community assembly. Our results from whole-community metabarcoding provide unprecedented insight into how dispersal limitations constrain mesofauna community structure within local spatial settings over evolutionary timescales. If generalized across wider areas, the high turnover and endemicity in the soil locally may indicate extremely high richness globally, challenging our current estimations of total arthropod-diversity on Earth.