Multiple Quaternary Refugia in the Eastern Guiana Shield Revealed by Comparative Phylogeography of 12 Frog Species

Abstract

The Guiana Shield (GS) is one of the most pristine regions of Amazonia and biologically one of the richest areas on Earth. How and when this massive diversity arose remains the subject of considerable debate. The prevailing hypothesis of Quaternary glacial refugia suggests that a part of the eastern GS, among other areas in Amazonia, served as stable forested refugia during periods of aridity. However, the recently proposed disturbance-vicariance hypothesis proposes that fluctuations in temperature on orbital timescales, with some associated aridity, have driven Neotropical diversification. The expectations of the temporal and spatial organization of biodiversity differ between these two hypotheses. Here, we compare the genetic structure of 12 leaf-litter inhabiting frog species from the GS lowlands using a combination of mitochondrial and nuclear sequences in an integrative analytical approach that includes phylogenetic reconstructions, molecular dating, and Geographic Information System methods. This comparative and integrated approach overcomes the well-known limitations of phylogeographic inference based on single species and single loci. All of the focal species exhibit distinct phylogeographic patterns highlighting taxon-specific historical distributions, ecological tolerances to climatic disturbance, and dispersal abilities. Nevertheless, all but one species exhibit a history of fragmentation/isolation within the eastern GS during the Quaternary with spatial and temporal concordance among species. The signature of isolation in northern French Guiana (FG) during the early Pleistocene is particularly clear. Approximate Bayesian Computation supports the synchrony of the divergence between northern FG and other GS lineages. Substructure observed throughout the GS suggests further Quaternary fragmentation and a role for rivers. Our findings support fragmentation of moist tropical forest in the eastern GS during this period when the refuge hypothesis would have the region serving as a contiguous wet-forest refuge.

Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses

“…Commonly applied tests include the evaluation of spatially concordant phylogeographic breaks (10,11), temporally synchronous population divergence (12,13), or concerted demographic expansion/contraction (14,15) among members of an ecological community. Methodological advances of the last decade, especially coalescent-based tools for hypothesis testing and parameter estimation (16,17) that include statistical assessment of concordance across taxa, such as the widely used hierarchical approximate Bayesian computation (hABC) This article is a PNAS Direct Submission.…”

“…Morphological or life-history traits directly related to dispersal potential, such as body size, wing development, reproductive mode, or larval type (13,38,39,43), have been commonly used to interpret contrasting responses to biogeographic barriers. In some cases, habitat (or microhabitat) preference has also been associated with differences in spatial genetic structure, especially when (micro)habitats differ in their long-term stability (23,38,44) or their responses to environmental change (26,45).…”

Out of the deep: Cryptic speciation in a Neotropical gecko (Squamata, Phyllodactylidae) revealed by species delimitation methods

“…Traditional hypotheses for the origins of the high Neotropical biodiversity include vegetation refugia created by Pleistocene climatic fluctuations (Vanzolini, 1968;Williams and Vanzolini, 1966), a scenario suggested to account for the diversification of forest animals (Fouquet et al, 2012;Haffer, 1969; Moraes-Barros Table 2 Different 'species trees' used in the Bayesian species delimitation analysis (BPP), based on the groups defined by the GMYC analysis. The lowest and highest posterior probability of the model for different BPP runs is shown.…”

The complete mitochondrial genome of Anomaloglossus baeobatrachus (Amphibia: Anura: Aromobatidae)

“…It is currently known to occur in French Guiana, Suriname and the State of Amapa (Fouquet et al 2012), and the State of Para (Avila-Pires et al 2010). The taxonomy of the genus Anomaloglossus is not well resolved, as several mitochondrial lineages currently associated with nominal species might in fact represent undescribed species (Fouquet et al 2007(Fouquet et al , 2012Kok et al 2012). This is the case of A. baeobatrachus for which four distinct mitochondrial lineages have been identified (Fouquet et al 2012).…”

“…The taxonomy of the genus Anomaloglossus is not well resolved, as several mitochondrial lineages currently associated with nominal species might in fact represent undescribed species (Fouquet et al 2007(Fouquet et al , 2012Kok et al 2012). This is the case of A. baeobatrachus for which four distinct mitochondrial lineages have been identified (Fouquet et al 2012). Molecular data can significantly contribute in resolving the systematics and species boundaries within this genus but available genomic data are still scarce.…”