Abstract
The Atlantic Forest (AF) domain is one of the Earth’s biodiversity hotspots, known for its high levels of species diversity and endemism. Factors related to palaeoenvironmental dynamics, such as the establishment of vegetational refugia and river basins, have different impacts on biological communities and biodiversity patterns in this domain. Here, we sample genome-wide RADseq data from a widespread treefrog (Dendropsophus elegans), inhabiting natural and human-impacted ecosystems at the Brazilian AF to test the impact of riverine boundaries and climatic refugia on population structure and diversification. We estimate divergence times and migration rate across identified genetic breaks related to the rivers Doce, Paraíba do Sul, Ribeira de Iguape, and Paraguaçu, known to represent barriers to gene flow for other AF endemic species, and test the role of climatic refugia. Finally, we investigate the impact of spatio-temporal population history on morphological variation in this species. We recovered a phylogeographic history supporting three distinct clades separated into two geographically structured populations, corresponding to the north and south of AF. In addition, we identified an admixture zone between north and south populations in the latitude close to the Doce River. Our findings support a pattern of isolation-by-distance and the existence of a secondary contact zone between populations, which might have been promoted by gene flow during population expansion. Further, we found support for models considering migration parameters for all the tested rivers with different population divergence times. Based on the species history and the AF palaeoenvironmental dynamics, we corroborate the role of forest refugia impacting population structure for this species through recent range expansion after the Last Glacial Maximum (LGM). The Doce and Paraíba do Sul Rivers coincide with the main genetic breaks, suggesting they might also have played a role in the diversification processes. Finally, despite finding subtle correlations for phenotypic data among different populations, variation is not strongly detectable and does not seem associated with speciation-level processes that could warrant taxonomic changes. Such results can be explained by phenotypic plasticity of the evaluated traits and by recent divergence times, where there has been insufficient time and weak selective pressures to accumulate enough phenotypic differences.
Highlights
Spatial patterns of biodiversity are arranged according to species’ evolutionary history, such as its responses to environmental variation
At the intraspecific-level relationships, D. elegans is represented by three main geographically distinct clades (Figure 2): the north clade (61% bootstrap) that is distributed northern of Doce River, at Minas Gerais state to the Alagoas state; the south clade (100% bootstrap), with the northern limit of the distribution corresponding to the Paraíba do Sul River extending southern into Paraná state; and the central clade (87% bootstrap), with a narrow distribution between the Doce River to the north of the Paraíba do Sul River, including Espírito Santo and Minas Gerais states (Figure 1)
Genomic breaks coincided with the main AF rivers (Ribeira de Iguape, Paraíba do Sul, Doce, and Paraguaçu), suggesting their strong role in the species diversification process even though allowing gene flow in certain periods
Summary
Spatial patterns of biodiversity are arranged according to species’ evolutionary history, such as its responses to environmental variation. Current patterns of spatial genetic structure and gene flow among populations have been affected by past climatic fluctuations and the establishment of biogeographic boundaries, all modulated by species’ ecology (Antonelli et al, 2018; Pirani et al, 2019; Sheu et al, 2020). In the Neotropics, climatic oscillations during the Quaternary have impacted species distribution and genetic patterns – a major process accounting for several species’ current distributions (Carnaval et al, 2009; Cheng et al, 2013; Rull and Carnaval, 2020). It is long proposed that, during interglacial periods, the extension of Neotropical forested areas has been larger relative to open ecosystems (Vanzolini and Willians, 1970; Leite and Rogers, 2013). During the Pleistocene glacial periods, biota experienced increased aridification and concentrations of CO2, which likely resulted in retraction of forests and expansion of open areas (e.g., Antonelli et al, 2010). Populations of plants and animals associated with forested habitats that were unable to disperse across open areas could have been isolated for thousands of years, accumulating genetic differences that could potentially result in allopatric speciation (e.g., Resende et al, 2010; Damasceno et al, 2021)
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