Introduction
Colonisation and speciation, together with extinction, are key processes contributing to island diversity and core processes within models of island biogeography (e.g. MacArthur & Wilson, 1963, 1967; Hubbell, 2001; Rosindell et al. , 2011). Most of our understanding of island diversity, and the mechanisms of diversification and community assembly on islands, comes from the study of aboveground systems (e.g., Gillespie & Roderick, 2002; Warren et al. , 2014; Patiño et al. , 2017), while the patterns and processes of importance for underground biotas remain poorly understood (FAO report, 2020). This lack of knowledge presents a major limitation to understanding island biodiversity and dynamics, as patterns and processes are not necessarily coupled between aboveground and belowground components of ecosystems (Bardgett & van der Putten, 2014; Shade et al., 2018)
Soil biodiversity, in particular soil mesofauna (i.e. small-bodied invertebrates measuring between 0.1 and 2 mm), is globally poorly understood (Cameron et al., 2018; Decaëns, 2010; White et al., 2020). Knowledge regarding fundamental biological and ecological traits of soil mesofauna is absent for most species. For example, dispersal dynamics within soil fauna remains an open and central question in soil biodiversity research (Ettema & Wardle, 2002; Thakur et al., 2019). Within insular settings, soil faunal diversity is expected to be strongly influenced by variation among species for dispersal capacity and niche breadth, as these traits underpin both island colonization and within island processes of population structure and speciation (Emerson & Gillespie, 2008; Gillespie et al., 2012; Kisel & Barraclough, 2010; Warren et al., 2014). Thus, insular systems provide an important focus for the development of a broader understanding of how dispersal and niche traits shape soil mesofaunal biodiversity.
Arthropod mesofaunal lineages typically exhibit various adaptations to soil environments, including the reduction of wings, eyes, and legs, and are thus likely to be limited in their propensity for active dispersal (Decaëns, 2010; Wardle, 2002). When extrapolated over extended periods of evolutionary time, such dispersal limitation is consistent with the high turnover across limited spatial scales and high local endemicity that has been reported for soil mesofaunal lineages (e.g., Andújar et al., 2017; Arribas, Andújar, Salces-Castellano, Emerson, & Vogler, 2021; Cicconardi, Nardi, Emerson, Frati, & Fanciulli, 2010; Collins, Hogg, Convey, Barnes, & McDonald, 2019; Morek, Surmacz, López-López, & Michalczyk, 2021). However, it has also been argued that their small body size and often high local abundances may increase the probability of passive dispersal and long-distance movement (Ettema & Wardle, 2002; Thakur et al., 2019), supporting the ”Everything is everywhere but environment selects” hypothesis for soil mesofauna (Fenchel & Finlay, 2004; Finlay, 2002). In the context of oceanic islands, if passive dispersal is sufficiently high, island colonisation by soil fauna lineages should be a recurrent process maintaining species cohesion between islands and source regions, and panmictic populations at intra-island scales (Fig. 1A). In contrast, if passive dispersal is strongly constrained for soil fauna, it is reasonable to assume that colonization will occur primarily through sporadic events of long-distance dispersal (i.e. LDD events, Nathan, 2005), and that geographic speciation, even within islands, will play a more important role in community assembly (Fig. 1A).
While island colonisation will depend on dispersal capacity, successful establishment is also reliant upon species-specific traits related to climatic niche breadth. In general, islands have been proposed to favour generalist species, either by colonization filters that select for species with wide niche breadth (ecological tolerance) (Gaston, 2003; Reaka, 1980) or through lower levels of competition favouring ecological release following colonisation (Olesen, Eskildsen, & Venkatasamy, 2002). It has also been demonstrated that climatic gradients within islands can be characterised by very differentiated invertebrate communities, comprising species with strong habitat specificity (Lim et al., 2021). Ecological speciation involving climatic-niche shifts has been described as an essential process generating diversity within oceanic island biotas (Gillespie, Roderick, & Howarth, 2001). However, recent studies focused on arthropod assemblages have highlighted an important role for climatic niche conservatism as a driver of community assembly and diversification within islands (Lim et al., 2021; Salces-Castellano et al., 2020).
Habitat specialisation and climatic niche conservatism across soil fauna lineages has been poorly explored. However, previous studies on the community assembly of soil mesofauna have shown strong evidence for specialisation to open versus forested vegetation types (Arribas, Andújar, Salces-Castellano, et al., 2021; Caruso, Taormina, & Migliorini, 2012), with further evidence for specialisation among different forest types (Noguerales et al., 2021). Oceanic islands that have remained geographically isolated over evolutionary timescales and present variation in habitat types provide near-ideal conditions to explore further the relative contribution of generalist and specialist species composing soil island biotas and the role of habitat-shifts in the process of diversification within insular settings.
Here we take advantage of a relatively young and dynamic oceanic island to advance our understanding of eco-evolutionary processes driving community assembly within soil mesofauna. We achieve this by appling whole organism community DNA (wocDNA) metabarcoding to soil mesofaunal communities sampled across the four dominant habitats within the island of Tenerife. Tenerife is one of the seven principal Canary Islands, an archipelago within the subtropical region of the North Atlantic Ocean. The oldest massif of Tenerife emerged approximately 9 Ma, but most of its 2,034 km2 landscape dates back to less than 3 Ma, with extensive volcanic activity in the last 2 Ma (Ancochea, Maria, Ibarrola, Cendrero, & Coello, 1990; Carracedo et al., 2004). Maximum altitude exceeds 3,000 m, giving rise to an altitudinal-zonal distribution of main habitat types, strongly mediated by trade winds.
We use spatially explicit and reliable (Andújar et al., 2021) haplotype-level DNA sequence data for the mtDNA COI gene to conduct community ecological and metaphylogeographic (Turon, Antich, Palacín, Præbel, & Wangensteen, 2019) analyses at multiple levels of genetic similarity, from the level of haplotypes, through to species and supraspecific groupings. We estimate local, habitat-level, and island-level richness, together with measures of local endemicity and the structuring of community variation across habitats and geographic distance. We use these data for a joint evaluation of the patterns and processes driving the diversity and structure of soil mesofauna from the level of the community down to individual lineages, and address the following four questions. Is dispersal limitation of soil mesofauna sufficient to drive geographic structuring of communities and lineage diversification? How do habitat specificity and habitat shift contribute to community assembly? What is the relative importance of spatialvs environmental processes as drivers of community structure and lineage diversification? How do wocDNA diversity estimates compare with more traditional assessments, and how do they compare to similar estimates from comparable continental soils?