Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders

Abstract

1. Ecological specialization is an important mechanism enhancing species coexistence within a given community. Yet, unravelling the effect of multiple selective evolutionary and ecological factors leading the process of specialization remains a key challenge in ecology. Subterranean habitats provide highly replicated experimental arenas in which to disentangle the relative contribution of evolutionary history (convergent evolution vs. character displacement) and ecological setting (environmental filtering vs. competitive exclusion) in driving community assembly.2. We tested alternative hypotheses about the emergence of ecological specialization using the radiation of a lineage of sheet-weaver cave-dwelling spiders as model system. We observed that at the local scale, a differential specialization to cave microhabitats generally parallels moderate levels of morphological similarity and close phylogenetic relatedness among species. Conversely, geographic distance contributed little in explaining microhabitat occupation, possibly mirroring a limited role of competitive exclusion. Yet, compared to non-coexisting species, co-occurring species adapted to different microhabitats showed lower morphological niche overlap (i.e. higher dissimilarity) and deeper genetic distance.3. The framework here developed suggests that in the subterranean domain, habitat specialization is primarily driven by environmental filtering, secondarily by convergent evolution, and only marginally by character displacement or competitive exclusion. This pattern results in the establishment of replicated communities across geographical space, composed by ecologically equivalent species. Such process of community assembly well explains the numerous adaptive radiations observed in subterranean habitats, an eco-evolutionary pattern well documented in oceanic islands or mountain summit communities. K E Y W O R D S biotic interactions, cave, functional traits, n-dimensional hypervolume, niche space, phenotypic variability, subterranean biology, Western Italian Alps | 1065 Functional Ecology MAMMOLA et AL. S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Mammola S, Arnedo MA, Fišer C, Cardoso P, Dejanaz AJ, Isaia M. Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders.

Exploring ecological specialization in pipefish using genomic, morphometric and ecological evidence

“…Ecological specialization, the spatial and temporal differentiation of species in the use of habitat and resources (Devictor et al., 2010), is a pivotal eco‐evolutionary paradigm to explain phylogeographical patterns, community assembly rules and the majority of adaptive radiations (Gillespie et al., 2020; Mammola et al., 2020; Todd Streelman & Danley, 2003; Wilson et al., 2020). Although marine fishes often show complex adaptations in spatially heterogeneous environments (e.g.…”

Fundamental research questions in subterranean biology

“…within subterranean habitats). This is largely driven by a paucity of functional ecology studies, the weakness of trait‐based approaches (Cardoso, 2012; Fernandes et al ., 2016; Fišer et al ., 2019; Mammola et al ., 2020), and the lack of robust systematic sampling techniques for most taxonomic groups (Wynne et al ., 2019). Bridging these gaps will significantly influence how we address and prioritize future research on the conservation and ecosystem services of subterranean habitats (e.g.…”

“…Second, subterranean communities generally exhibit lower diversity and abundance of organisms than surface ones and are characterized by a bottom‐truncated functional diversity (Gibert & Deharveng, 2002), allowing us to disentangle the effect of abiotic conditions and biotic interactions in filtering species possessing specific traits within the community (Cardoso, 2012). Third, caves have some conspicuous environmental gradients from the surface towards the subsurface (Howarth, 1982; Tobin, Hutchins, & Schwartz, 2013; Mammola et al ., 2019 d ), offering a mosaic structure of subterranean microhabitats defined by distinct habitat‐filtering properties (Trontelj, Blejec, & Fišer, 2012; Mammola et al ., 2020).…”

“…As sequencing becomes increasingly applied to subterranean taxa, environmental DNA sampling and monitoring may be also used to detect these species in areas difficult to access (Gorički et al ., 2017; Niemiller et al ., 2018), thus resulting in more accurate maps of their distributions. To our knowledge, patterns of phylogenetic and functional diversity at continental to global scales have not been documented for any subterranean taxon (Q26), despite the growing knowledge of phylogenetic relationships and species traits (Morvan et al ., 2013; Fernandes, Batalha, & Bichuette, 2016; Fišer et al ., 2019; Mammola et al ., 2020). Documenting these patterns will further underscore the relative importance of dispersal, extinction, and different speciation modes in shaping geographic variation of species richness.…”

A trade‐off between latitude and elevation contributes to explain range segregation of broadly distributed cave‐dwelling spiders

“…General theory predicts that segregation along spatial gradients should be particularly visible in highly dispersive species, such as birds (Auer & King, 2014; Burner et al., 2020; Graham et al., 2009), insofar as the effect of antagonistic interactions require the species to be in contact (that is, some sort of spatial proximity). Conversely, the effect of competition is often found to be of limited importance in driving the distribution of poorly dispersive species, such as subterranean ones (Mammola et al., 2020; Zakšek et al., 2019). Lacking effective dispersal, range size of subterranean organisms is often best predicted by historical factors (Zagmajster et al., 2014) and availability of habitats (Christman & Culver, 2001; Culver et al., 2006).…”