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).