Isolation by environment and recurrent gene flow shaped the evolutionary history of a continentally distributed Neotropical treefrog

Abstract

Aim Phylogeographic studies show how historical and current changes in landscapes shape the geographic distribution of genetic diversity in species of animals and plants. In particular, for the species of the Diagonal of Open Formations (DOF), the compartmentalization of the Central Brazilian Plateau (CBP) during the Tertiary and climatic oscillations during the Quaternary have often been invoked to explain the origin and current patterns of biodiversity. We investigated how landscape changes and climatic oscillations shaped the distribution and diversification history of a widespread South American treefrog. Location South American Diagonal of Open Formations (DOF) including Caatinga, Cerrado, and Chaco biomes. Taxon Treefrog Boana raniceps. Methods We used a multi‐locus dataset from 288 individual frogs collected at 115 localities throughout most of the species’ distribution. We used population assignment analysis, species distribution models, historical demography models, approximate Bayesian computation and landscape genetic analyses to test alternative hypotheses of diversification. Results We found two genetic lineages that diverged during the mid‐Pleistocene with continued gene flow. Approximate Bayesian computation supported a scenario of isolation with migration until the Last Glacial Maximum, followed by more recent population expansion in north‐eastern Brazil and stability at the southwest in South America. Isolation by environment was the best predictor of genetic distance between populations, which is in accordance with their different environmental niches. As Boana raniceps is a lowland species, steep slopes in the CBP likely restrained gene flow enough to sustain population divergence. We found evidence for major range contraction during the Last Glacial Maximum, raising the possibility of synergic action of climate change and the CBP compartmentalization in regulating migration. Main conclusions Our findings highlight how landscape and climatic changes can shape the diversification of DOF biota. Past climatic fluctuations and environmental resistance due to topography acted in concert, forming a semipermeable barrier to gene flow, promoting intraspecific differentiation in a continentally distributed species.

Systematics and biogeography of theBoana albopunctataspecies group (Anura, Hylidae), with the description of two new species from Amazonia

“…Within this clade, B. heilprini is the most distinct since it is confined to Hispaniola and is phylogenetically distant from a clade formed by all the other species of the group (Duellman, Marion, & Hedges, 2016). We can also distinguish B. raniceps and the B. albopunctata clade (B. lanciformis, B. albopunctata, B. multifasciata, B. paranaiba, B. caiapo, B. leucocheila), which occur widely in the open habitats of the Cerrado and Amazonia (Camurugi et al, 2021), from the Amazonian clade. According to Caminer and Ron (2014) Within this Amazonian clade, Funk, Caminer, and Ron (2012) identified no less than seven putative unnamed species based on mitochondrial divergence and acoustic data.…”

Speciation with gene flow between two Neotropical sympatric species (Pitcairnia spp.: Bromeliaceae)

“…Studies that suggest speciation with gene flow have been demonstrated for organisms of Neotropical region, including animals (e.g., Heliconius butterflies: Martin et al, 2013 ; Cnemidophourus lizards: Oliveira et al, 2015 ; Amphilophus cichlid fishes: Kautt et al, 2016 , 2020 ; and treefrog Boana raniceps : Camurugi et al, 2021 ) and plants (e.g., magic flowers Achimenes : Roberts & Roalson, 2018 ; and Plathymenia reticulata : Muniz et al, 2022 ). In fact, interspecific gene flow can contribute to the pool of standing genetic variation and thus to diversification of species (Brawand et al, 2015 ; Seehausen, 2004 ) and showed to have an important role in diversification and adaptive radiation of bromeliads (Lexer et al, 2016 ; Loiseau et al, 2021 ; Palma‐Silva, Ferro, et al, 2016 ; Palma‐Silva, Leal, et al, 2016 ).…”

“…Currently, there are several lines of evidence for speciation with gene flow in plants (e.g., Muniz et al, 2022;Papadopulos et al, 2011Papadopulos et al, , 2019Roberts & Roalson, 2018) as well as in animals (e.g., Camurugi et al, 2021;Kautt et al, 2016Kautt et al, , 2020Martin et al, 2013;Niemiller et al, 2008;Oliveira et al, 2015;Roux et al, 2016). One prediction of this model is that the level of divergence should be heterogeneous across the genome, given that alleles at some loci are likely to be shared between incipient species, while selection maintains divergence at other loci (Feder et al, 2012;Nosil et al, 2009;Riesch et al, 2017;Seehausen et al, 2014;Turner et al, 2005;Wu, 2001).…”

Drivers of neutral and adaptive differentiation in pike (Esox lucius) populations from contrasting environments

“…However, studies investigating the relative importance of different modes of isolation are scarce and show contrasting results. Some studies suggest that resistance is the most important mechanism affecting neutral genetic variation (Camurugi et al, 2021; Oliveira et al, 2019; Xuereb et al, 2018). Other studies point to a main effect of the environment (Jiang et al, 2019; Quéméré et al, 2016; Rödin‐Mörch et al, 2019), and yet others indicate that distance is the main determinant of genetic structure (Ferreira et al, 2020; Vidal et al, 2019).…”