Signature of the Paleo-Course Changes in the São Francisco River as Source of Genetic Structure in Neotropical Pithecopus nordestinus (Phyllomedusinae, Anura) Treefrog.

Daniel Pacheco Bruschi,Elen Arroyo Peres,Shirlei Maria Recco-Pimentel,Luciana Bolsoni Lourenço,Thadeu Sobral-Souza,Luiz Filipe De Macedo Bartoleti

doi:10.3389/fgene.2019.00728

Abstract

Historical processes that have interrupted gene flow between distinct evolutionary lineages have played a fundamental role in the evolution of the enormous diversity of species found in the Neotropical region. Numerous studies have discussed the role of geographic barriers and Pleistocene forest refugia in the diversification of the region’s biodiversity. In the present study, we investigated the relative contribution of these different factors to the evolutionary history of Pithecopus nordestinus, a Neotropical tree frog, which is amply distributed in the Brazilian Atlantic Forest and adjacent areas of the Caatinga biome. We used an extensive sample and multilocus DNA sequences to provide an overview of the intraspecific genetic diversity of P. nordestinus, characterize historical diversification patterns, and identify possible phylogenetic splits. We tested different scenarios of diversification based on Pleistocene Refugia and river barrier models using approximate Bayesian computation (ABC) and ecological niche modeling (ENM). The phylogenetic approach indicate the occurrence of processes of phylogeographic divergence in both time and space, related to historical shifts in the course of the São Francisco River during Plio-Pleistocene period, resulting in two principal, highly divergent clades. The ABC model provided strong statistical support for this scenario, confirming the hypothesis that the São Francisco River acted as an effective geographical barrier during vicariant events in the evolutionary history of P. nordestinus. We believe that the climatic changes that occurred during the Pleistocene also played a secondary role in the genetic signatures identified, reinforcing the divergence of populations isolated by physical barriers. These findings reinforce the conclusion that the two models of diversification (geographic barriers and refugia) are not mutually exclusive in the Neotropical domain but may interact extensively during the diversification of species on a regional scale.

Highlights

Models of speciation are widely invoked to explain the origin and diversification of lineages and species complexes in the Brazilian Atlantic Forest, a global hotspot
We modeled the species potential distribution area in the present and in the past, and based on the historical species distribution and the main lineages recovered in our analyses, we designed and evaluated two biogeographic scenarios using coalescent simulations, as follows: i) São Francisco River (SFR) as a barrier to gene flow between ancient interbreeding populations currently located in opposite margins and ii) ancient lineages diversified during Pleistocene climate shifts that created refugia, bisected populations
The mitochondrial gene (16S and ND2, Figures 4A, B, respectively) showed similar topologies and recovered the three major geographically structured P. nordestinus clades: the first includes specimens distributed on the north of SFR (Rio Grande do Norte, Ceará, Paraíba, Pernambuco, and Alagoas states, hereafter referred to Northern group); the second is composed by few haplotypes from western Bahia (Catieté and Aurelino Leal populations, hereafter referred to Western group); and a third clade genetically more distant from the other two that includes individuals collected in Sergipe and remaining localities in Bahia states, all distributed in South of the SFR

Summary

Introduction

Models of speciation are widely invoked to explain the origin and diversification of lineages and species complexes in the Brazilian Atlantic Forest, a global hotspot. The phylogeographic patterns can be explained by the Riverine Barrier hypothesis, initially proposed by Wallace (1852), which establishes that rivers are effective barriers to gene flow between populations on opposite margins, resulting in their isolation and genetic differentiation along time (Amaral et al, 2013; Cazé et al, 2016) According to this hypothesis’ predictions, lower levels of genetic differentiation would be expected among populations from the same margin, species from opposite river margins would be typically sister taxa, and the timing of divergence events would coincide with the geological changes in the landscape (Moritz et al, 2000)

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Discussion

Conclusion