Deciphering the drivers of negative species–genetic diversity correlation in Alpine amphibians

Abstract

The evolutionary and ecological importance of neutral and adaptive genetic diversity is widely recognized. Nevertheless, genetic diversity is rarely assessed for conservation planning, which often implicitly assumes a positive correlation between species and genetic diversity. Multiple drivers can cause the co‐variation between the genetic diversity of one species and the richness of the whole communities, and explicit tests are needed to identify the processes that can determine species–genetic diversity correlations (SGDCs). Here, we tested whether intrapopulation genetic diversity (at neutral loci) and species richness co‐vary in the amphibian communities of a southern Alpine region (Trentino, Italy), using the common frog (Rana temporaria) as focal species for the study of genetic diversity. We also analysed ecological similarity, niche overlap and interspecific interactions between the species, to unravel the processes determining SGDC. The neutral genetic diversity of common frogs was negatively related to species richness. The negative SGDC was probably due to an opposite influence of environmental gradients on the two levels of biodiversity, since the focal species and the other amphibians differ in ecological preferences, particularly in terms of thermal optimum. Conversely, we did not find evidence for a role of interspecific interactions in the negative SGDC. Our findings stress that species richness cannot be used as a universal proxy for genetic diversity, and only combining SGDC with analyses on the determinants of biodiversity can allow to identify the processes determining the relationships between genetic and species diversity.

Latitudinal biodiversity gradients at three levels: Linking species richness, population richness and genetic diversity

“…Our results contribute to the idea that disentangling intraspecific diversity patterns can be much more complicated than species richness as many factors require simultaneous consideration (see Blanchet et al, 2017;Marchesini et al, 2018;Martinez et al, 2018;Medina et al, 2018;Millette et al, 2019;Paz-Vinas et al, 2018;Willoughby et al, 2017). The limited scope in the scale of genetic diversity, and perhaps the minimum and maximum degree of genetic diversity required for viable populations (e.g.…”

“…Large quantities of data on intraspecific diversity have recently become available for broad-scale analyses due to technological advances and the accumulation of smaller-scale empirical works (DeWoody & Avise, 2000;Hughes, Daily, & Ehrlich, 1997;Lawrence et al, 2019;Martinez, Willoughby, & Christie, 2018;Medina, Cooke, & Ord, 2018;Miraldo et al, 2016;Willoughby et al, 2015). When collated, such data allow for the extension of species-centric latitudinal concepts towards understanding how broad-scale intraspecific diversity patterns may better inform, for example, the speciation process (Adams & Hadly, 2013;Schluter & Pennell, 2017;Smith, Seeholzer, Harvey, Cuervo, & Brumfield, 2017) and biodiversity conservation by revealing hot/cold spots of intraspecific diversity (Marchesini, Vernesi, Battisti, & Ficetola, 2018;Paz-Vinas et al, 2018). Herein, we focus our discussion specifically on broad-scale patterns of two metrics of intraspecific diversity: population richness within species and genetic diversity, and how these metrics relate to species richness gradients.…”

“…Furthermore, the joint investigation of the distribution of species richness, population richness and genetic diversity may allow more accurate inferences about ecological history, including glacial refugia, recolonization, and founder effects (Bernatchez & Wilson, 1998;Blanchet, Prunier, & De Kort, 2017;Fedorov & Stenseth, 2002;Galbreath & Cook, 2004;Marske et al, 2013;Tamkee, Parkinson, & Taylor, 2010). Some research has bridged how aspects of genetic diversity may relate to and have consequences for communities and species richness (Antonovics, 1976(Antonovics, , 2003Hughes, Inouye, Johnson, Underwood, & Vellend, 2008;Lamy, Laroche, David, Massol, & Jarne, 2017;Laroche, Jarne, Lamy, David, & Massol, 2014;Marchesini et al, 2018;Marske et al, 2013;Pfeiffer et al, 2018;Vellend, 2005Vellend, , 2010Vellend & Geber, 2005;Vellend et al, 2014). Still lacking, however, is a strong conceptual foundation linking species richness, population richness and genetic diversity within the framework of the latitudinal gradient.…”

“…Dynamics between and within populations are the stepping stone linking genetic diversity with species richness (Fine, 2015;Marchesini et al, 2018;Marske et al, 2013;Paz-Vinas et al, 2018;Singhal et al, 2018). Increasing genetic differentiation leads to population divergence and eventually speciation due to isolation and/or selection (Schluter, 2016;Schluter & Pennell, 2017;Taylor, 1999;Wiens, 2004).…”

Integrating Multiple Lines of Evidence to Explore Intraspecific Variability in a Rare Endemic Alpine Plant and Implications for Its Conservation

“…Secondly, it is a matter of fact that for the flora of the Alps and other large mountain ranges, species richness only partly correlates to genetic diversity. In a milestone contribution to this subject, [ 8 ] demonstrated that while the highest species richness is found in the South-Western Alps, the greatest genetic diversity within and among species is located in the central and eastern part of the Alpine chain [ 9 , 10 , 11 , 12 ]. Environmental characteristics can influence taxonomic and genetic diversity in different ways, resulting in a negative correlation between these two features [ 13 ].…”