Niches within a niche: ecological differentiation of subterranean amphipods across Europe's interstitial waters

Abstract

Species that successfully colonized subterranean environments are subject to two opposing selection processes. Stringent abiotic factors select for convergent adaptations, such as loss of eyes and pigments, while interspecific competition drives between‐species divergence. Subterranean species can resolve opposing selection by adaptation to physically different microhabitats. Yet, species frequently co‐occur in physically homogeneous subterranean habitats, like interstitial. These co‐occurrences in such a narrow ecological context can be explained either by equalizing mechanisms, in which neither of the co‐occurring species has a competitive advantage, or by more complex niche models that include species’ differentiation along a trophic niche axis. We tested these hypotheses using the amphipod genus Niphargus. We analysed Europe‐wide co‐occurrence records of Niphargus species from interstitial habitats, split into six independent large‐scale regions. Firstly, we addressed whether species’ pairwise co‐occurrences are random using a probabilistic model. Secondly, we tested whether species cluster into distinct functional–morphological groups and whether ecologically or phylogenetically distinct species are more likely to co‐occur. We found that 68% of species co‐occurrences were not different from random expectation, indicating that most species had access to most sites within each region. The remaining 32% co‐occurred either significantly more or less often than expected by chance. Cluster analysis of functional morphological characters showed that interstitial species belong to two feeding types, micro‐ and macrofeeders, likely representing two peaks of the interstitial adaptive landscape, and hinting that niche divergence, as a mechanism allowing coexistence, is favoured. Finally, we found that the number of co‐occurrences increases with increasing differentiation of functional morphology, but not phylogenetic differences. We conclude that ecological differentiation may be important in shaping such interstitial communities.

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

“…In fact, in the only known case of two sister species of Troglohyphantes coexisting at the local scale, the species’ morphology diverged substantially to enhance the occupation of distinct microhabitats (cave vs. MSS; Mammola, Arnedo, et al, ). This result is also partially congruent to similar analysis of interstitial amphipods, where the frequency of co‐occurrence records showed a positive relationship with degree of their ecological differentiation, but was not affected by phylogenetic relatedness (Fišer et al, ).…”

“…This hypothesis received only little support (Derkarabetian et al, ), but can be rejected in this study since the crown age of the clade of species living in cave entrances [(( T. lucifer + T. lucifuga ) + T. pluto ); mean age estimation (confidence interval) = 7.5 (16–3) My] is not younger than the clade of the most specialized eyeless species from deep caves [((( T. bolognai + T. bolognai ) + T. konradi ) + T. pedemontanus ); 6 (12–2.5) My] (Figure ). By contrast, several studies on subterranean beetles (Martins & Ferreira, ; Vergnon et al, ), amphipods from caves (Delić et al, ; Fišer et al, ; Trontelj et al, ; Zakšek, Delić, Fišer, Jalžić, & Trontelj, ), interstitial habitats (Fišer, Delić, Luštrik, Zagmajster, & Altermatt, ) or deep wells (Hutchins, Schwartz, & Nowlin, ), but also spiders (Arnedo, Oromí, Múrria, Macías‐Hernández, & Ribera, ; Mammola, Arnedo, et al, ; Mammola et al, ), suggested that variation in functional traits corresponds to ecological diversification of subterranean species. These studies strongly concur with the results presented here and support the hypothesis that rather than evolutionary dead ends, subterranean organisms continue evolving and actively specializing into new microhabitats (Cieslak, Fresneda, & Ribera, ; Copilaş‐Ciocianu, Fišer, Borza, & Petrusek, ; Stern et al, ).…”

“…The role of phylogeny in ecological specialization of subterranean species, on the other hand, has been incompletely explored. Few studies have used phylogenies to show the convergent origin of functional traits (Fišer et al, ; Trontelj et al, ), but none have explored the role of historical contingency in subterranean community assembly. Results of our study imply that common phylogenetic origin explains ecological diversity of subterranean species as importantly as convergent evolution.…”

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.…”

“…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.…”