Introduction
Oceanic islands have been the all-time favourite natural laboratory to
test predictions about evolution of biota through time (Warren et al.
2015; Whittaker et al. 2017). The theory of island biogeography, a
conceptual model to predict species richness on islands, is at the core
of many of those advances (Warren et al. 2015). In its original
formulation, the theory assumes that the number of species in a given
island represents an equilibrium between immigration and extinction
rates, both dependent on the island surface and the distance from the
nearest continent acting as species pool (MacArthur & Wilson 1967).
The inclusion of geological and climatic processes added more nuance to
these assumptions. Oceanic islands change in size, configuration, and
isolation through time with comparable geodynamic cycles, in which a
sequence of islands is produced as the plate moves over a volcanic
hotspot. Each island subsequently erodes and eventually subsides as it
is carried away from the hotspot. By incorporating such geodynamic
information, the general dynamic model of oceanic island biogeography
(Whittaker et al. 2008) has successfully predicted an increase of the
number of species in a given island during the emergence and building
phases, driven by immigration and in situ speciation. The model
predicts subsequent decay of the number of species, as erosion and
gravitational collapses reduce the extension and habitat heterogeneity.
At the point of the highest geological heterogeneity within each cycle,
the total number of species in an island achieves its maximum relative
to the carrying capacity. Accordingly, islands with higher altitudes and
larger surface will sustain more species as they offer more
opportunities for local adaptation and diversification.
This island dynamic model has successfully predicted the number of
species at a large set of oceanic archipelagos based on the roles of
immigration, speciation, and extinction (Warren et al. 2015).
Nevertheless, the model does not explicitly inform on how species
interactions interplay with the processes driving diversity within each
island at the community level (Rosindell et al. 2017). It has been
proposed that immigration-speciation dynamics mostly drive diversity in
young islands where low competition and empty niche space provide
increased ecological opportunities. However, as the island approaches
the carrying capacity, species interactions within established
communities might gain importance, with niche segregation and ecological
speciation playing an important role in optimising ecological networks
to better exploit the available niche space (Gillespie et al. 2020).
Ultimately, as the island approaches senescence and gets eroded under
the sea, diversity is driven—more or less randomly—by extinction.
The specific role of species interactions has been difficult to
quantify, particularly in archipelagos formed by several islands, in
which dispersal favours colonisation across them even allowing for the
presence of metacommunities (Lawson et al. 2019). These problems can be
alleviated by focusing on a subset of habitats that, due to their
particular ecological conditions, filter their potential colonisers to
lineages evolving in situ , because the habitats impose strong
constraints that limit the likelihood of arrival and survival of
immigrants from other islands (Patiño et al. 2017). Yet, most habitats
potentially fulfilling these requisites, such as mountain summits or
lakes (Itescu et al. 2019), are not present through the entire island’s
life cycle since they depend on the island’s geological state. Because
of this dependency of most habitats to geological history of an island,
it is unlikely to find a whole habitat-specific animal community
throughout the whole history of an island, if not considering that
oceanic volcanic islands host an impressive diversity of subterranean
habitats. Subterranean habitats impose strong constraints against the
arrival and survival of immigrants from other islands, favour in
situ speciation, and can be found across all the geological history of
the island.
Subterranean adapted fauna importantly contributes to the pool of
endemic species in many archipelagos (Naranjo et al. 2020). Lava tubes
are the most iconic example amongst their caves (Sauro et al. 2020).
However, caves are just a small, human-accessible fraction of the
subterranean habitats available to potential colonisers. Due to their
small body size, most subterranean animals dwell in the labyrinthic
network of pores and small fissures forming within volcanic rocks and
clasts—a habitat termed Milieu Souterrain Superficiel (MSS;
Oromí et al. 1986; Mammola et al. 2016). Collecting ecological data in
these environments is notoriously challenging (Mammola et al. 2021a).
However, once the exploration and sampling impediments are overcome, our
efforts are compensated by the set of unique properties that make
subterranean habitats ideal laboratories for eco-evolutionary research
(Mammola & Martinez 2021)—including their discrete nature largely
preventing long-range migration (Mammola,2019) and the presence of
relatively simple communities showing high trait convergence (Gibert &
Deharveng 2002; Trontelj et al. 2012; Mammola et al. 2022). Given that
subterranean habitats in oceanic islands are de facto “islands
within islands” (Esposito et al. 2015), they should represent the
perfect model system to explore broad questions within the realm of
island biogeography (Culver 1970, 1971; Fattorini et al. 2016; Balog et
al. 2020).
The aim of this paper is to investigate how the interaction between
ecological and evolutionary processes shape the diversity patterns in
oceanic archipelagos. Our goal was to derive the expectation in species
diversity predicted from the island biogeographic theory from the
relative contribution of speciation, community-level interactions, and
extinction at different stages of their ontogenetic cycle. We
accomplished our objective in four steps, each of them associated with a
specific hypothesis. (1) Firstly, we described the trait space of all
the subterranean species in each island. We expected it to converge due
to the ecological filtering exerted by the colonisation of subterranean
habitats, yet exhibiting a certain degree of variation according to each
island’s ontogenetic state. (2) Secondly, we explored how this overall
convergence in the trait space might be explained by the different
contributions of each species to their overall trait space of islands
with different ages. We expected that species contribute progressively
less as an island approaches its maximum geological complexity,
reflecting increasing niche occupancy and a progressive reduction of
ecological opportunity. The contribution of individual species might
increase as an island approaches its senescence and extinction reduces
its species richness. (3) Third, we hypothesised that the reduction in
species contribution is a consequence of an optimised use of the
available niche space driven by species interactions. Under this
assumption, we expect that functionally similar species will experience
a stronger ecological and geographical isolation in mature islands;
whereas the distribution of species and their niche occupancy will be
more random in senescent or young islands (4) Finally, we proposed that
species interactions might select a non-random combination of traits in
each island, leading to trait spaces with smaller volume and higher
degree of order in mature islands than those expected by chance from a
sample of the archipelago’s species pool. By confirming these
hypotheses, we could provide a mechanistic description of the drivers of
diversity in oceanic islands (Wilson 1969; Losos et al. 2010) by
establishing causal relationships between species functional properties
and island diversity metrics accounting for each island’s age.