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.