Ancient divergence and recent population expansion in a leaf frog endemic to the southern Brazilian Atlantic forest

Abstract

The evolutionary history of Neotropical organisms has been often interpreted through broad-scale generalizations. The most accepted model of diversification for the Brazilian Atlantic forest (BAF) rely on putative historical stability of northern areas and massive past habitat replacement of its southern range. Here, we use the leaf frog Phyllomedusa distincta, endemic to the southern BAF, to better understand diversification patterns within this underexplored rainforest region. We used an integrative approach coupling fine-scale sampling and multilocus sequence data, with traditional and statistical phylogeographic (multilocus approximate Bayesian computation) methods to explore alternative hypotheses of diversification. We also employed species paleodistribution modeling to independently verify habitat stability upon a spatially explicit model. Our data support two divergent lineages with coherent geographic distribution that span throughout northern and southern ranges. Demographic estimates suggested the Southern lineage has experienced a recent population expansion, whereas the Northern lineage remained more stable. Hypothesis testing supports a scenario of ancient vicariance with recent population expansion. The paleodistribution model revealed habitat discontinuity during the Last Glacial Maximum (LGM) with one area of putative stability within the range of the Northern lineage. Evidence on genetic structure, demography, and paleodistribution of P. distincta support a historically heterogeneous landscape for the southern BAF, with both areas of forest stability and regions where forest occupation is probably recent. We also associate the southern end of the Cubatão shear zone with a phylogeographic break in the BAF. Taken together, our results argue for the idea of multiple mechanisms generating diversity in this biome and underscore the need of fine-scale data in revealing more detailed pictures.

Ecological niche modeling and a lack of phylogeographic structure in Vriesea incurvata suggest historically stable areas in the southern Atlantic Forest

“…Initially, ecological niche models, together with phylogeographic studies, identified favorable environments for the occurrence of different species (stable forest areas) that seem to be important drivers of biodiversity in the northern portion of AF, whereas the southern portion of the forest would have been heavily fragmented by the spread of grassland vegetation (Carnaval and Moritz, ; Carnaval et al., ; Martins et al., ; Palma‐Silva et al., ; d'Horta et al., ). However, further studies proposed that, during glaciations, the southern portion of the AF was not as severely impacted as previously suggested (Thomé et al., ; Brunes et al., ; Peres et al., ; Bünger et al., ; Cabanne et al., ; Costa et al., ). Therefore, the distinct patterns recovered for the southern and northern portions of the AF are still a subject of debate.…”

“…In the present study, we evaluated the phylogeographic patterns of V. incurvata as a contribution to telling the history of the southern AF. The northern and southern parts of the AF have been identified as two distinct bioclimatic domains (Prance, ; Carnaval et al., ), and phylogeographic studies with different species, support this proposal (Cabanne et al., ; Brunes et al., ; Leite et al., ). Contradicting the intense instability attributed to the southern portion of the AF, the results of our ENM for V. incurvata suggested that the area potentially occupied by this species remained similar in the evaluated periods, which may be related to climate stability (Fig.…”

“…Except for birds (Batalha‐Filho et al., ; Cabanne et al., ), few studies on AF organisms suggest a lack of or weak phylogeographic structure. Instead, phylogeographic breaks and, consequently, the formation of structured groups have been reported for a number of organisms, including amphibians (Brunes et al., ; Menezes et al., ), bees (Batalha‐Filho et al., ), reptiles (Pellegrino et al., ), bats (Martins et al., ), and plants (Ribeiro et al., ; Turchetto‐Zolet et al., ). The causes of such breaks have been widely debated and attributed mainly to Pleistocene climatic cycles, geomorphological dynamics, and river systems (Thomé et al., ; Ribeiro et al., ; Menezes et al., ).…”

The roles of barriers, refugia, and chromosomal clines underlying diversification in Atlantic Forest social wasps

“…However, other studied species reveal genetic responses contrary to that expected by the CM model, suggesting instead a meaningful role for geographic barriers 22 – 25 , including the newly proposed influence of sea-level changes on the biogeographic history of the AF 26 . In contrast to refugia scenarios, genetic predictions regarding barrier hypotheses include older divergence times (due to vicariant events occurring deeper in the past), interruptions of gene flow that coincide with geographic barriers, and populations showing smooth demographic oscillations 27 .…”

The complex history of genome duplication and hybridization in North American gray treefrogs

“…Among plants, hybridization between species and populations of different ploidies appears to occur regularly (Soltis and Soltis 2009; Alix et al 2017). In anurans, the complexes of Phyllomedusa tetraploidea , Odontophrynus americanus , and Bufo viridis show strong evidence that hybridization between tetraploids and diploids regularly produces triploid individuals (Stöck et al 2002, 2005, 2010; Brunes et al 2010, 2015; Grenat et al 2018), and there is some evidence that several populations of the latter complex are entirely composed of hybrid triploids that are now sexually reproducing (Stöck et al 2002, 2012). Similarly, the Australian Neobatrachus complex is composed of several autopolyploid tetraploid and diploid species who have each likely hybridized with multiple species several times since the initial polyploids were formed (Novikova et al 2020; Mable and Roberts 1997).…”