Dispersal limitation as a driver of the assemblage and diversification of insular soil mesofauna
Dispersal is a key process shaping island biotas, being fundamental for colonization and consequential within islands for the geographic structuring of genetic variation within species, speciation, and intra-island diversification (Gillespie et al., 2012; Salces-Castellano et al., 2020; Warren et al., 2014). Integrating across the distances and frequencies over which active and passive dispersal processes contribute to species cohesion and speciation (Fig. 1) provides a predictive framework for evolutionary trajectories at the level of individual lineages (Gillespie et al., 2012). Competing models can be proposed for the likely shape of the dispersal kernel for the typically tiny and flightless component of mesofaunal soil species, with differing implications for their spatial patterns of diversity (Fig. 1) (Andújar et al., 2017). The first is a model of limited active but high passive dispersal potential, mediated by the small size of soil mesoarthropods, according to the ”everything is everywhere hypothesis” (Fenchel & Finlay, 2004; Finlay, 2002) which predicts large spatial distances for species cohesion. The second model is one of limited active and passive dispersal potential, and thus predicts a limited spatial scale for speciation (Andújar et al., 2017; Arribas, Andújar, Salces-Castellano, et al., 2021).
Analyses of mesofauna from continental soils have led to contrasting inferences for how dispersal shapes their community assembly and diversification. Strong dispersal constraints have rarely been recognised for soil mesofauna, and long-distance dispersal has been considered to characterise soil mesofauna, largely mediated by passive dispersal by air, water or in marine plankton (Decaëns, 2010; Thakur et al., 2019; Wardle, 2002). In contrast, molecular studies of soil mesofaunal lineages and communities frequently reveal dispersal limitation, associated with both diversification and community turnover across limited spatial scales (Andújar et al., 2017; Arribas et al., 2021; Francesco Cicconardi, Fanciulli, & Emerson, 2013; Collins et al., 2019). The BIOTA inventory for the island of Tenerife reveals that 236 of 297 recorded species of Acari (79%) , 62 of 88 Collembola (70%), and 699 of 1360 Coleoptera (51%), are considered to be non-endemic, having populations outside of the Canary Islands. These data are more consistent with a model of high dispersal potential for soil mesofauna. However, our metabarcode data provide greater support for a model where dispersal is limited, where island populations are evolutionarily independent entities, within which futher diversification can occur.
Following island colonisation and establishment, dispersal limitation may favour subsequent intra-island genetic differentiation, the extent of which will be mediated by species traits (e.g. niche, species-specific dispersal ability), and the selective landscape (e.g. spatial variation in biotic and abiotic conditions). Under this model, spatially structured lineages and communities are expected to emerge, and there are clear signatures for this within our data. Within each of the studied habitats, for haplotype, species, and supraespecific levels of variation, community similarity is a function of geographic distance (Fig. 2C and 3). This self-similarity of distance decay at haplotype and species level (Fig. 3B) is consistent with a role for dispersal limitation driving community assembly (Baselga et al., 2015; Gómez-Rodríguez & Baselga, 2018). The influence of dispersal constraints within the soil matrix appears to act at short spatial distances, and the evident high turnover with physical distance suggests that our sampled communities within each habitat are not from a single panmictic metacommunity. At the lineage level, our results reveal multiple signals of dispersal limitation constraining diversification. Many of the soil mesofaunal OTUs recovered from our wocDNA metabarcode data are not recorded (at least molecularly) outside the island (Fig. 4; Table S7), have restricted distributions within the island, and present spatially structured genetic variation (Fig. 6). Additionally, among the 533 15% lineages recovered, 122 comprises two or more OTUs. If we assume each 15% lineage represents a single colonization event into Tenerife, 49.2% of all OTUs may be derived from intra-island divergence events. Thirty-nine OTUs show a significant correlation between genetic and spatial distances, 34 of these comprising two or more OTUs, further supporting in situ spatial structuring and diversification within lineages (Fig. 4 and 6).