Tempo and Mode of Diversification in a Radiation of Endogean Ground Beetles
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Received: 1 April 2017 | Revised: 23 July 2017 | Accepted: 5 September 2017 DOI: 10.1111/mec.14358 ORIGINAL ARTICLE Speciation below ground: Tempo and mode of diversification in a radiation of endogean ground beetles Carmelo Andujar 1,2,3 | Sergio Perez-Gonz alez 4 | Paula Arribas1,2,3 | Juan P. Zaballos4 | Alfried P. Vogler1,2 | Ignacio Ribera5 1Department of Life Sciences, Natural History Museum, London, UK Abstract 2Department of Life Sciences, Imperial Dispersal is a critical factor determining the spatial scale of speciation, which is con- College London, Ascot, UK strained by the ecological characteristics and distribution of a species’ habitat and 3Grupo de Ecologıa y Evolucion en Islas, Instituto de Productos Naturales y the intrinsic traits of species. Endogean taxa are strongly affected by the unique Agrobiologıa (IPNA-CSIC), San Cristobal de qualities of the below-ground environment and its effect on dispersal, and contrast- la Laguna, Spain ing reports indicate either high dispersal capabilities favoured by small body size 4Departamento de Zoologıa y Antropologıa Fısica, Universidad Complutense de Madrid, and mediated by passive mechanisms, or low dispersal due to restricted movement Madrid, Spain and confinement inside the soil. We studied a species-rich endogean ground beetle 5Institut de Biologia Evolutiva (CSIC- Universitat Pompeu Fabra), Barcelona, lineage, Typhlocharina, including three genera and more than 60 species, as a model Spain for the evolutionary biology of dispersal and speciation in the deep soil. A time-cali- > Correspondence brated molecular phylogeny generated from 400 individuals was used to delimit Carmelo Andujar, Department of Life candidate species, to study the accumulation of lineages through space and time by Sciences, Natural History Museum, London, – – UK. species area age relationships and to determine the geographical structure of the Email: [email protected] diversification using the relationship between phylogenetic and geographic distances Funding information across the phylogeny. Our results indicated a small spatial scale of speciation in Natural Environment Research Council, Typhlocharina and low dispersal capacity combined with sporadic long distance, pre- Grant/Award Number: NE/M021955; European Commission, Grant/Award sumably passive dispersal events that fuelled the speciation process. Analysis of lin- Number: MSCA-IF-2015-705639; Ministerio eage growth within Typhlocharina revealed a richness plateau correlated with the de Economıa y Competitividad, Grant/Award Number: CGL2010-16944 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 Typhlo- charina may serve as a general model for the evolution of high species diversity in endogean mesofauna. KEYWORDS Anillini, density dependence, endogean, geographic speciation, long-distance dispersal (LDD), microendemism, Typhlocharina 1 | INTRODUCTION Both the frequency and the distance of dispersal events critically influence speciation, determining its geographical scale and temporal The role of dispersal in modulating gene flow is key to the speciation dynamics (Kisel & Barraclough, 2010; Lomolino, Riddle, Whittaker, & process. Dispersal determines the balance between species cohesion Brown, 2010). For organisms with a high dispersal potential, pro- and the divergence of isolated populations (Coyne & Orr, 2004; cesses of geographic differentiation are only effective at large spatial Futuyma, 1998) and promotes the establishment of new populations scales, while differentiation is quickly erased over small distances as a source for the diversification process (Nathan & Nathan, 2014). (Finlay, 2002; Wilkinson, Koumoutsaris, Mitchell, & Bey, 2012). At | Molecular Ecology. 2017;26:6053–6070. wileyonlinelibrary.com/journal/mec © 2017 John Wiley & Sons Ltd 6053 6054 | ANDUJAR ET AL. the opposite end of the spectrum, lineages with low dispersal capa- The soil environment is a complex and heterogeneous matrix of bilities may undergo geographic differentiation at a local scale, gen- minute and interconnected spaces, characterized by darkness, limited erating high levels of endemicity, geographical structure and positive temperature fluctuations and high relative humidity and CO2 levels species–area relationships even over short distances (Futuyma, 1998; (Russell & Appleyard, 1915). This matrix imposes major restrictions Kisel & Barraclough, 2010; Kisel, McInnes, Toomey, & Orme, 2011). to the movement of organisms, resulting in a reduced range for the If not constrained by geographic or ecological barriers, dispersal activity of an individual (Eisenbeis & Wichard, 1987). Arthropods is a stochastic process affecting individuals, which follow a trajectory adapted to live in deep soil layers (euedaphics sensu Eisenbeis & of limited movement from their site of birth (Harte, McCarthy, Tay- Wichard, 1987; endogeans sensu Giachino & Vailati, 2010) show a lor, Kinzig, & Fischer, 1999), and over time give rise to predictable general trend to body size reduction, depigmentation, shortening of macroecological patterns of decreasing similarity at greater distances extremities and loss of eyes and flight capacity (Eisenbeis & Wichard, (Baselga et al., 2013; Diniz-Filho & Bini, 2011). Such idealized homo- 1987; Gisin, 1943). Therefore, adaptations of deep soil mesofauna geneous landscapes do not exist, and the separation of habitat converge on a general decrease in dispersal potential by active patches imposes barriers to the free movement of organisms and movement, but at the same time some of these adaptations, such as modulates the divergence of populations. In addition, dispersal size reduction or the adaptation to survive underwater during flood capacity of species is constrained by the properties of the species’ events, enhance the likelihood of passive dispersal over short and habitat, given the differences in habitat availability and stability at long distances. The interplay of these active and passive dispersal ecological and geological timescales (the habitat-templet concept; events determines the probability function of dispersal (dispersal ker- Southwood, 1977; Korfiatis & Stamou, 1999). Thus, the factors shap- nel) for a species (Nathan et al., 2008) and overall will determine the ing evolutionary diversification may be similar across lineages associ- scale and dynamics of differentiation in soil lineages. ated with particular habitat types. For example, lineages of aquatic Understanding the processes that drive the distribution of soil insects differ in their dynamics of diversification due to the differ- organisms over spatial and temporal scales is essential to estimate ence in geological stability of standing or flowing water bodies (Rib- the magnitude and evolution of soil biodiversity (Ettema & Wardle, era, 2008). Furthermore, the species diversity in an area may be 2002). However, we currently lack relevant information on specia- constrained by competitive interactions that limit the number of spe- tion patterns and geographical distributions of soil lineages (Decaens,€ cies able to coexist. This may affect the dynamics of lineage growth 2010). Different studies have found high levels of cryptic diversity by reducing the rate of net diversification towards the recent, after and microendemicity in several lineages of soil arthropods (e.g., an initial diversification pulse (Alroy, 1996; Foote, 1997; Kisel et al., Andujar et al., 2015; Bennett, Hogg, Adams, & Hebert, 2016; Casale, 2011; Rabosky, 2009; Sepkoski, Bambach, Raup, & Valentine, 1981). 2009; Cicconardi, Fanciulli, & Emerson, 2013; Cicconardi, Nardi, Thus, the interaction of both dispersal constraints and habitat Emerson, Frati, & Fanciulli, 2010), pointing to a very small spatial parameters will shape the spatial and temporal dynamics of specia- scale of diversification in soil mesofauna. In contrast, other studies tion and biodiversity patterns. have proposed a high dispersal capacity mainly promoted by passive FIGURE 1 (a) Relationship between clade age and species richness with density-dependent diversification due to geographical, ecological or other factors imposing a maximum species richness or “carrying capacity” of the clade. (a1) Individual clades (marked with different symbols) may vary in age, with square and open circle being the youngest clades. Independently of the age, when evolutionary time is enough, clades reach the equilibrium species richness which depends on its “carrying capacity” and not on clade age. The graph shows an initial richness accumulation phase where clades may vary in diversification rate with the slope of the log-diversity curve proportional to the net rate of diversification (modified from Rabosky, 2009). In this phase, there is a positive relationship between clade age and species richness (a2). As ecological niches or geographical space is filled, clades reach the richness equilibrium phase where there is no relationship between clade age and species richness and the net diversification rate will be 0 (a3). In those cases where the diversity is limited by geographical space and speciation is mainly allopatric, we additionally will expect a richness–area relationship at both accumulation and equilibrium phases and a positive area–age relationship during the accumulation phase and no correlation at the equilibrium phase. Note that if diversification