Speciation below ground: Tempo and mode of diversification in a radiation of endogean ground beetles

Abstract

Dispersal is a critical factor determining the spatial scale of speciation, which is constrained by the ecological characteristics and distribution of a species' habitat and the intrinsic traits of species. Endogean taxa are strongly affected by the unique qualities of the below-ground environment and its effect on dispersal, and contrasting reports indicate either high dispersal capabilities favoured by small body size and mediated by passive mechanisms, or low dispersal due to restricted movement and confinement inside the soil. We studied a species-rich endogean ground beetle lineage, Typhlocharina, including three genera and more than 60 species, as a model for the evolutionary biology of dispersal and speciation in the deep soil. A time-calibrated molecular phylogeny generated from >400 individuals was used to delimit candidate species, to study the accumulation of lineages through space and time by species-area-age relationships and to determine the geographical structure of the diversification using the relationship between phylogenetic and geographic distances across the phylogeny. Our results indicated a small spatial scale of speciation in Typhlocharina and low dispersal capacity combined with sporadic long distance, presumably passive dispersal events that fuelled the speciation process. Analysis of lineage growth within Typhlocharina revealed a richness plateau correlated with the range of distribution of lineages, suggesting a long-term species richness equilibrium mediated by density dependence through limits of habitat availability. The interplay of area- and age-dependent processes ruling the lineage diversification in Typhlocharina may serve as a general model for the evolution of high species diversity in endogean mesofauna.

The limited spatial scale of dispersal in soil arthropods revealed with whole-community haplotype-level metabarcoding

“…This scale and dynamics of community assembly contrasts with patterns and processes reported for the microbial eukaryote diversity of the soil (Bahram et al, 2016) and aligns with recent empirical evidences suggesting that at the local scale dispersal rates may be much lower for soil mesofauna than for microfauna (Zinger et al, 2019). In the context of the overall arthropod diversity (for which soil mesofauna comprises the majority of the smallest fraction), our results are not supporting the macroecological prediction for a reduce impact of dispersal limitation in the assemblage for small-bodied components compared with their bigger counterparts (de Bie et al, 2012; Ricklefs, 2004) and highlight the uniqueness of ecological and evolutionary processes driving the biodiversity of these edaphic arthropods (Andújar, Arribas, & Vogler, 2017; Andújar, Pérez-González, et al, 2017).…”

“…The small spatial scale of turnover and endemicity is consistent with population genetic studies in soil mesofauna showing deep genetic breaks even over relative short geographic distances (Andújar, Pérez-González, et al, 2017; Cicconardi et al, 2013). In contrast, our results are not concordant with the extended view of long-distance dispersal as prevalent process for soil mesofauna, as might be expected from evidences of passive dispersal by air, water or in marine plankton (Decaëns, 2010; Thakur et al, 2019; Wardle, 2002).…”

“…In fact, a high prevalence of aerial, aquatic and marine rafting has been demonstrated for various mesofaunal lineages (Coulson, Hodkinson, Webb, & Harrison, 2002; Nkem et al, 2006; Schuppenhauer, Lehmitz, & Xylander, 2019), and studies have shown mesofaunal assemblages with no apparent dispersal limitation across continental-scale areas (Baird, Leihy, Scheepers, & Chown, 2019), especially for the smallest-bodied soil arthropods (Gan, Zak, & Hunter, 2019). On the other hand, molecular studies have revealed high differentiation and ancient microendemicity even in morphologically indistinguishable clades, indicating long-term constraints to dispersal (Andújar, Pérez-González, et al, 2017; Cicconardi, Fanciulli, & Emerson, 2013). These empirical data limited to particular mesofauna lineages and their contrasting findings highlight the difficulty of establishing the role of dispersal constraints in community assembly.…”

A review of the genus Pelodiaetus Jeannel (Coleoptera, Carabidae, Anillini) of New Zealand, with re-description of the genus, description of a new species, and notes on the evolutionary history

“…However, in the fourth case, on the contrary, a small Zeanillus lives with a large Pelodiaetodes. Generally, miniaturization is one of the ways of speciation in the Anillini allowing species to occur syntopically and to exploit resources more effectively (Sokolov 2013, Andújar et al 2017. Often these species are closely related and probably formed as a result of sympatric speciation, as was demonstrated for North American Anillinus lescheni Sokolov and Carlton and A. stephani Sokolov and Carlton (Sokolov et al 2004), for some European Typhlocharis Dieck (Pérez-Gonzáles and Zaballos 2013), and for Mexican Zapotecanillus oaxacanus Sokolov and Z. nanus Sokolov (Sokolov 2013).…”

Coming to Common Ground: The Challenges of Applying Ecological Theory Developed Aboveground to Rhizosphere Interactions

“…Such specific characteristics belowground dictates dynamics of organism movement and sensory perception specific to the soil medium. For instance, arthropods adapted to live in deep soil layers show reduced body size, or loss of sight and flight capacity (Andújar et al, 2017). To summarize, fundamental differences between the above-and belowground realms suggest that patterns of interactions above-and belowground are, at least partially, governed by different mechanisms.…”