Diversification of the widespread neotropical frog Physalaemus cuvieri in response to Neogene-Quaternary geological events and climate dynamics

https://doi.org/10.1016/j.ympev.2018.11.003Get rights and content

Highlights

  • Ancestral area of Physalemus cuvieri populations is southcentral Amazonia.

  • Neogene orogenic events played role in the early diversification of P. cuvieri.

  • Central South America is importance for diversification and maintenance of lineages.

  • Multiple Refugia and lineages admixture predict genetic parameters of P. cuvieri.

  • This species shows deep divergences and regional population structure.

Abstract

Here we reconstructed the demographical history and the dispersal dynamics of Physalemus cuvieri through the Neogene-Quaternary periods by coupling DNA regions with different mutation rates, ecological niche modelling, reconstruction of spatio-temporal lineage dispersal and coalescent simulations. Still, to test alternative diversification scenarios we used approximate Bayesian computation. Molecular phylogenetic analysis recovered four deep and strongly supported clades, which we interpret as population lineages. The ancestral location reconstruction placed the root in southcentral Amazonia, and the dispersal events indicate that spatial displacement was widespread early in the diversification of this species. The demographical scenario of “Multiple Refugia” with recent lineage admixture was the most likely hypothesis to predict the observed genetic parameters of P. cuvieri. Our results revealed that Neogene orogenic events might have played a prominent role in the early diversification of P. cuvieri. The species shows deep divergences with strong regional population structure, despite its widespread distribution. Final uplift of the central Brazilian Plateau and formation of the river basins in Central South America played an important role in the origin, diversification and the maintenance of P. cuvieri lineages.

Introduction

The origin and maintenance of high Neotropical biodiversity have been a controversial topic (Rull, 2008, Rull, 2011). The successive influences of Palaeogene-Neogene and Quaternary events are hypothesized to have driven the differentiation of communities from open biomes and adjacent rainforests (Rull, 2011). The increase of the latitudinal temperature gradient in South America caused by the Andean orogeny in the Palaeogene, marine transgressions during the Miocene, and the uplift of the Central Brazilian Plateau in the Miocene-Pliocene transition led to palaeogeographical reorganizations that may have directed diversification (Colli, 2005). These processes, together with the Quaternary climatic fluctuations, changed the landscape (Vuilleumier, 1971), and created complex scenarios that may have fostered both diversification and extinction events. Such complexity has been hypothesized in many phylogeographical and phylogenetic studies where Neogene and Pleistocene diversifications have been recovered (Garda and Cannatella, 2007, Maciel et al., 2010, Prado et al., 2012). In addition, climatic fluctuations remain one of the main mechanisms to promote fluctuation of population distributions through time in South American species. Species associated with rainforest biomes often show reduced population size during glacial cycles (see review by Martins, 2011). Conversely, species associated with open formations have varying responses and maintained (e.g. Werneck et al., 2012), expanded (e.g. Collevatti et al., 2012b), or decreased (e.g. Collevatti et al., 2015b) their geographical ranges during glacial cycles.

The shared influence of both the geological events of the Neogene and the climatic cycles of the Quaternary were suggested to have influenced the diversification of the herpetofauna widely distributed in the South American open formations (Prado et al., 2012, Werneck et al., 2012, Santos et al., 2014, Guarnizo et al., 2016). Overall, the studies recover deeper diversification events occurring mainly in the Neogene guided by the landscape compartmentalization that promoted vicariance events. Additional diversification at the population level and changes in the distribution and demography of populations would have been promoted by the Quaternary’s climatic fluctuations (Prado et al., 2012, Werneck et al., 2012, Santos et al., 2014, Guarnizo et al., 2016). Moreover, two spatial patterns of diversification have been recovered in phylogeographical studies of Neotropical herpetofauna. One follows diversification of lineages in a northwest to southeast direction (Prado et al., 2012, Guarnizo et al., 2016), and another follows a southwest-northeast direction (Werneck et al., 2012). The former pattern would be related to species endemic to the Cerrado biome, and the latter would be associated with species distributed throughout the whole South American diagonal of open formations (Guarnizo et al., 2016).

The synergy of several approaches and a range of spatial and temporal scales are required to explain the complexity of present-day genetic patterns (Rull, 2011). An approach using multiple lines of evidence for phylogeographical inference, coupling multiple markers spanning a wide range of mutation rates, ecological niche modelling (ENM hereafter), coalescent analyses, and reconstruction of spatio-temporal lineage dispersal processes (Lemey et al., 2009, Lemey et al., 2010, Collevatti et al., 2015a, Collevatti et al., 2015b) may give clues to the forces driving demographical and spatial patterns through the Neogene and the Quaternary. In this context, species with widespread distributions are ideal models to investigate subcontinental diversification processes in these boundaries (Werneck et al., 2012). This is the case of the Neotropical frog Physalaemus cuvieri Fitzinger, 1826, which is widely distributed in the South American open formations. This species is considered a cryptic species complex, but no taxonomic revision has yet been conducted (Lourenço et al., 2015).

We use an extensive sampling of P. cuvieri and DNA regions with different mutation rates to reconstruct the demographical history and the dispersal dynamics of the species through the Neogene-Quaternary periods. With the climatic oscillations in the Late Pliocene and the consequent cycles of retraction and expansion of the open areas (Pennington et al., 2000, Freitas and Suchard, 2001, Werneck, 2011, Collevatti et al., 2012a), we expect a high population genetic differentiation due to the structuring of distinct sectors of newly colonized areas with low genetic diversity and to the high frequency of surfing alleles, ones that become widespread because of demographic expansion of a population from their point of origin. In opposition, populations in stable areas may have higher genetic diversity (Excoffier et al., 2009). Therefore, we analysed the relationships of genetic diversity with climatic stability through time and with distance from the edge of the historical refugium predicted by ENM. We also used coalescent simulations and approximate Bayesian computation (ABC hereafter) to test alternative diversification scenarios derived from previous biogeographical hypotheses (Ab’Saber, 2000) and population demographical dynamics inferred by ENMs.

Section snippets

Data collection

We sampled 75 localities (595 individuals) throughout the geographical distribution of P. cuvieri in Brazil (Fig. 1a) (see Appendix A, Table A.1 in Supporting Information). We sequenced the mitochondrial regions, 12S, 16S, and cytochrome b (cytb) and the exon 1 of the nuclear gene rhodopsin (rhod). Details of primers, amplifications conditions, alignment, recombination tests, treatment of heterozygous individuals, and the best-fit model of sequence evolution are given in Appendix A.

Genetic diversity and population structure

To

Genetic diversity and population structure

The combined dataset alignment consisted of a fragment of 1215 base pairs (973 bp for mtDNA and 242 bp for nuDNA). Most localities presented low nucleotide diversity and high haplotype diversity for mtDNA. We recovered 235 haplotypes for mtDNA and 19 haplotypes for nuDNA (Table 1, Fig. 1b). Please see also the whole molecular phylogenetic tree in Fig. A.2. Among the 235 mitochondrial haplotypes, 61 represent unique haplotypes, restricted to single localities. Fifteen localities had only unique

Phylogeographical patterns

We recovered a deep phylogenetic structure between lineages of P. cuvieri, mirroring a recent phylogenetic study for the genus (Lourenço et al., 2015) that recognized three distinct lineages within P. cuvieri, which are geographically concordant with the population lineages that we identified. Our results suggest that the final uplift of the central Brazilian Plateau in the Miocene-Pliocene transition, which increased landscape heterogeneity in Cerrado, had an important role in the early

Conclusions

Our results revealed a complex history of diversification of P. cuvieri, with Neogene orogenic events playing a prominent role in the early diversification. Physalaemus cuvieri shows deep divergences with strong regional population structure, despite its widespread distribution. Our finding highlights the presence of cryptic lineages under the name of P. cuvieri. This reinforces the need for further analysis with both multi locus molecular approaches (Knowles and Carstens, 2007, Weisrock et

Acknowledgments

We thank Thiago F. Rangel for providing access to Bioensembles and the WCRP Working Group on Coupled Modelling for making available their model outputs. We also acknowledge Philippe Lemey for advice on the use of random walk analyses and Spread software, Liliana Ballesteros for assistance in ArcGis, and Levi Carina Terribile for support on ecological niche modelling. We are grateful to many people who kindly collected and donated specimens and sample tissues. This work was supported by CNPq

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