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?