Phylogeographic analysis and species distribution modelling of the wood frog Batrachyla leptopus (Batrachylidae) reveal interglacial diversification in south western Patagonia

PeerJ. 2020 Oct 6:8:e9980. doi: 10.7717/peerj.9980. eCollection 2020.

Abstract

Background: The evolutionary history of southern South American organisms has been strongly influenced by Pleistocene climate oscillations. Amphibians are good models to evaluate hypotheses about the influence of these climate cycles on population structure and diversification of the biota, because they are sensitive to environmental changes and have restricted dispersal capabilities. We test hypotheses regarding putative forest refugia and expansion events associated with past climatic changes in the wood frog Batrachyla leptopus distributed along ∼1,000 km of length including glaciated and non-glaciated areas in southwestern Patagonia.

Methods: Using three mitochondrial regions (D-loop, cyt b, and coI) and two nuclear loci (pomc and crybA1), we conducted multilocus phylogeographic analyses and species distribution modelling to gain insights of the evolutionary history of this species. Intraspecific genealogy was explored with maximum likelihood, Bayesian, and phylogenetic network approaches. Diversification time was assessed using molecular clock models in a Bayesian framework, and demographic scenarios were evaluated using approximate Bayesian computation (ABC) and extended Bayesian skyline plot (EBSP). Species distribution models (SDM) were reconstructed using climatic and geographic data.

Results: Population structure and genealogical analyses support the existence of four lineages distributed north to south, with moderate to high phylogenetic support (Bootstrap > 70%; BPP > 0.92). The diversification time of B. leptopus' populations began at ∼0.107 mya. The divergence between A and B lineages would have occurred by the late Pleistocene, approximately 0.068 mya, and divergence between C and D lineages was approximately 0.065 mya. The ABC simulations indicate that lineages coalesced at two different time periods, suggesting the presence of at least two glacial refugia and a postglacial colonization route that may have generated two southern lineages (p = 0.93, type I error: <0.094, type II error: 0.134). EBSP, mismatch distribution and neutrality indexes suggest sudden population expansion at ∼0.02 mya for all lineages. SDM infers fragmented distributions of B. leptopus associated with Pleistocene glaciations. Although the present populations of B. leptopus are found in zones affected by the last glacial maximum (∼0.023 mya), our analyses recover an older history of interglacial diversification (0.107-0.019 mya). In addition, we hypothesize two glacial refugia and three interglacial colonization routes, one of which gave rise to two expanding lineages in the south.

Keywords: Species distribution modelling; Amphibians; Divergence time; Glacial refugia; Patagonian glaciations; Phylogeography.

Grants and funding

This research was supported by NSF-PIRE OISE 0530267 to Jack W. Sites, Jr. and José J. Nuñez; Fondecyt 3160328 to Elkin Y. Suárez-Villota, and DID-UACH 2014-16 to José J. Nuñez. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.