Genomic data support reticulate evolution in whiptail lizards from the Brazilian Caatinga.

Abstract

Species relationships and speciation have traditionally been represented by phylogenetic trees, but not all evolutionary histories fit into bifurcating divergence models. Introgressive hybridization challenges this assumption by sometimes [or maybe often] leading to mitochondrial introgression, wherein one species' mitochondrial genome is entirely replaced by another's (mitochondrial capture). Such processes result in mitonuclear discrepancies, complicating species delimitation and phylogenetic inference. In our study, we used ultraconserved elements (UCE) and mitogenomic data to investigate the evolutionary history of the Ameivula ocellifera complex, a group of South American whiptail lizards widely distributed in arid environments, such as the Caatinga Domain in Brazil. Our focus was on understanding mitonuclear discordances, assessing reticulate evolution, evaluating species limits, and testing for adaptive mitochondrial capture that could explain a higher introgression in the mitochondrial genome compared to nuclear DNA. Our findings support the occurrence of an ancient reticulation event during the diversification of these lizards, driven by introgressive hybridization, leading to mitochondrial capture, and explaining mitonuclear discrepancies. Overall, we did not find clear evidence of positive selection across mitochondrial protein-coding genes suggesting adaptive mitochondrial capture of individuals with introgressed mtDNA. Thus, the genetic diversification and mitogenome evolution could be neutral, with selection against hybridization in the autosomal loci only, or even mediated by mitonuclear incompatibilities. Analyses of mtDNA genomes alongside network and species delimitation methods were crucial for identifying and validating individuals with introgressed mtDNA as a distinct species, demonstrating the potential of wide genome sampling and innovative analytical techniques for elucidating speciation processes in the presence of introgressive hybridization.