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

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.

At each site its diversity: DNA barcoding reveals remarkable earthworm diversity in neotropical rainforests of French Guiana

“…French Guiana in particular is characterized by a high coverage of primary forest and a large water network including 840 rivers stretching over a total distance of 112,000 km ("L'office de l'Eau de Guyane," n.d.). These rivers are often large enough to easily become geographic barriers to earthworm dispersion, leading to the formation of isolated populations and increasing the likelihood of local radiation events as it has been also shown for other taxa (Boubli et al, 2015;Bruschi et al, 2019;Siqueira et al, 2013). This could therefore explain the different species pools that we observed in each study location, and the importance of the spatial turnover component of regional beta diversity.…”

Genomic data from the Brazilian sibilator frog reveal contrasting pleistocene dynamics and regionalism in two South American dry biomes

“…Regardless, pervasive gene flow rejects any vicariance-based hypotheses (Table 1). Broad temporal concordance among some species of lizards (Werneck et al, 2015) and treefrogs (Bruschi et al, 2019) suggests that a single event promoted divergence in this region. However, genetic breaks are absent in other taxa, including lizards (Fonseca et al, 2018;Recoder et al, 2014) and frogs Oliveira, Martinez, et al, 2018;Thomé et al, 2016).…”

Coalescent simulations indicate that the São Francisco River is a biogeographic barrier for six vertebrates in a seasonally dry South American forest

“…Because SML usually performs better than ABC in model-based analysis (Gehara et al, 2020), hereafter we will base our discussion on parameter estimates from that method. The Caatinga potentially passed through several droughts associated with Pleistocene glaciation cycles, possibly decreasing the river's water level and its corresponding strength as a barrier (Barreto, 1996;Nascimento et al, 2013;Bruschi et al, 2019). This may explain the apparent asynchrony in divergence times; among the six species, we recovered divergence times of < 450 kya (D. muelleri, Ph.…”

“…Certain squamates (Machado et al, 2014;Fonseca et al, 2018), frogs (Oliveira et al, 2018a;Thomé et al, 2021a), birds (Corbett et al, 2020), insects (Andrade-Souza et al, 2017), and plants (Balbino et al, 2018) exhibit no genetic break totally concordant with the SFR. On the other hand, concordant genetic breaks indicate that the river clearly structures other lizards (Passoni et al, 2008;Siedchlag et al, 2010;Werneck et al, 2012;Almeida et al, 2020), frogs (Bruschi et al, 2019), mammals (Nascimento et al, 2011;Faria et al, 2013;Fegies et al, 2021), fishes (Costa et al, 2018), and plants (Menezes et al, 2016). Meanwhile, the SFR acts merely as a soft barrier for certain species, contributing to fine interpopulation structure while allowing gene flow across its margins (Werneck et al, 2015;Miranda et al, 2016;Oliveira et al, 2018b;Lanna et al, 2020;Thomé et al, 2021b).…”

“…Thus, even low migration, which is expected in the case of a soft barrier, can prevent allele fixation, producing a "fuzzy" genetic break with coalescent trees discordant with any historical split. It is imperative to model the effects of these factors when testing a geographic barrier, but only a few studies to date have tested the SFRH with a model-based approach (Oliveira et al, 2015;Miranda et al, 2016;Bruschi et al, 2019;Lanna et al, 2020;Thomé et al, 2021b).…”