Evidence of introgression in endemic frogs from thecampo rupestrecontradicts the reduced hybridization hypothesis

Abstract

The campo rupestre ecosystem is considered an old, climatically buffered, infertile landscape. As a consequence, long-term isolation is thought to have played an important role in the diversification of its biota. Here, we tested for hybridization between two endemic leaf frogs from the campo rupestre. We used sequence markers and coalescent models to verify haplotype sharing between the species, to test the existence and direction of gene flow, and to reconstruct the spatiotemporal dynamics of gene flow. Additionally, ecological niche modelling (ENM) was used to assess for potential co-occurrence by overlapping the climatic niche of these species since the middle Pleistocene. We found haplotype sharing and/or lack of differentiation in four nuclear fragments, one of them associated with introgression. The coalescent models support introgressive hybridization unidirectionally from Pithecopus megacephalus to P. ayeaye, occurring ~300 kya. ENM corroborates this scenario, revealing areas of potential environmental niche overlap for the species at about 787 kya. These results contradict the expectation of reduced hybridization, while ENM suggests climatic fluctuation rather than stability for the two species. The reduced hybridization hypothesis needs to be further investigated because our results suggest that it may have unrealistic premises at least for animals.

Colonization rather than fragmentation explains the geographical distribution and diversification of treefrogs endemic to Brazilian shield sky islands

“…This process also explains the contemporary geographical distribution of the genetic diversity in Vellozia auriculata bushes (Fiorini et al, 2019) and in the Alvarenga's treefrog (de Oliveira et al, 2021). Introgressive hybridization has also been reported for two Pithecopus monkey‐frogs (Magalhães et al, 2021). da Silva et al (2018), in turn, demonstrated that many species endemic to Brazilian highlands are shared between Quadrilátero Ferrífero in ER and Mantiqueira mountains (located south of the ER).…”

“…Changes in effective population size associated with Pleistocene climate regimes in the SE have also been reported for the Alvarenga's treefrog (de Oliveira et al, 2021) and for the cactus P. aurisetus (Bonatelli et al, 2014; Perez et al, 2016). This indicates that, even for some plants, the OCBIL premise of climatic buffering for the campo rupestre may be unrealistic (Magalhães et al, 2021).…”

“…However, there are still several shortfalls in the ecology and evolution of animals (Miola et al, 2021), even with the recent improvement in studies of anurofauna (e.g. de Oliveira et al, 2021; Magalhães et al, 2021). Our study adds one more piece to understanding the patterns and processes responsible for generating the ER's diversity and endemism.…”

“…For anurans, the ER houses more than 160 species, of which 30% are endemic (Leite, 2012) and often associated with campo rupestre (Leite, 2012; Leite et al, 2008). Only seven studies have examined the evolutionary history of these endemics at the phylogeographical level (Carvalho et al, 2021; de Oliveira et al, 2021; Magalhães et al, 2021; Nascimento et al, 2018; Ramos et al, 2018; Thomé et al, 2016; Thomé & Carstens, 2016).…”

“…Recent research has shown that the Pleistocene climate dynamics' influence on the ER biota diversification may be more widespread than expected by the OCBIL theory (de Oliveira et al, 2021;Magalhães et al, 2021;Vasconcelos et al, 2020). Given that (i) species delimitation based solely on one genetic marker can be misleading (Camargo & Sites, 2013;Knowles & Carstens, 2007), (ii) mtDNA-based molecular dating tends to overestimate divergence times in phylogeny reconstruction (McCormack et al, 2011;Smith et al, 2013), and (iii)…”