Cryptic Genetic Diversity Is Paramount in Small-Bodied Amphibians of the Genus Euparkerella (Anura: Craugastoridae) Endemic to the Brazilian Atlantic Forest

Luciana A Fusinatto,João Alexandrino,Fernando Sequeira,Célio F B Haddad,Carlos F D Rocha,Tuliana O Brunes,Diego Fontaneto

doi:10.1371/journal.pone.0079504

Abstract

Morphological similarity associated to restricted distributions and low dispersal abilities make the direct developing “Terrarana” frogs of the genus Euparkerella a good model for examining diversification processes. We here infer phylogenetic relationships within the genus Euparkerella, using DNA sequence data from one mitochondrial and four nuclear genes coupled with traditional Bayesian phylogenetic reconstruction approaches and more recent coalescent methods of species tree inference. We also used Bayesian clustering analysis and a recent Bayesian coalescent-based approach specifically to infer species delimitation. The analysis of 39 individuals from the four known Euparkerella species uncovered high levels of genetic diversity, especially within the two previously morphologically-defined E. cochranae and E. brasiliensis. Within these species, the gene trees at five independent loci and trees from combined data (concatenated dataset and the species tree) uncovered six deeply diverged and geographically coherent evolutionary units, which may have diverged between the Miocene and the Pleistocene. These six units were also uncovered in the Bayesian clustering analysis, and supported by the Bayesian coalescent-based species delimitation (BPP), and Genealogical Sorting Index (GSI), providing thus strong evidence for underestimation of the current levels of diversity within Euparkerella. The cryptic diversity now uncovered opens new opportunities to examine the origins and maintenance of microendemism in the context of spatial heterogeneity and/or human induced fragmentation of the highly threatened Brazilian Atlantic forest hotspot.

Highlights

The Neotropics harbor one of the highest levels of biodiversity on earth [1], but only a fraction of this biodiversity has been described [2]
Species discovery has often been accompanied by challenging systematics and problematic taxonomies for several groups of amphibians
For the mtDNA gene (CO-I), we obtained an alignment of 543 base pair sequences, corresponding to 14 unique haplotypes and 194 segregating sites (Table 1)

Summary

Introduction

The Neotropics harbor one of the highest levels of biodiversity on earth [1], but only a fraction of this biodiversity has been described [2]. Amphibians are among the vertebrates in which species discovery has increased considerably in the last decades [3,4,5,6,7]. The search for new species in poorly known regions, the use of molecular data and of integrative approaches (combining natural history with genetic, morphological, and ecological data) all have contributed to increasing knowledge on amphibian biodiversity [8,9,10,11,12]. The case of the Neotropical direct developing anurans of the taxon Terrarana is paradigmatic of this taxonomic complexity [5].

Methods

Results

Conclusion