Finding complexity in complexes: Assessing the causes of mitonuclear discordance in a problematic species complex of Mesoamerican toads

Abstract

Mitonuclear discordance is a frequently encountered pattern in phylogeographic studies and occurs when mitochondrial and nuclear DNA display conflicting signals. Discordance among these genetic markers can be caused by several factors including confounded taxonomies, gene flow, and incomplete lineage sorting. In this study, we present a strong case of mitonuclear discordance in a species complex of toads (Bufonidae: Incilius coccifer complex) found in the Chortís Block of Central America. To determine the cause of mitonuclear discordance in this complex, we used spatially explicit genetic data to test species limits and relationships, characterize demographic history, and quantify gene flow. We found extensive mitonuclear discordance among the three recognized species within this group, especially in populations within the Chortís Highlands of Honduras. Our data reveal nuclear introgression within the Chortís Highlands populations that was most probably driven by cyclical range expansions due to climatic fluctuations. Though we determined introgression occurred within the nuclear genome, our data suggest that it is not the key factor in driving mitonuclear discordance in the entire species complex. Rather, due to a lack of discernible geographic pattern between mitochondrial and nuclear DNA, as well as a relatively recent divergence time of this complex, we concluded that mitonuclear discordance has been caused by incomplete lineage sorting. Our study provides a framework to test sources of mitonuclear discordance and highlights the importance of using multiple marker types to test species boundaries in cryptic species.

The toad’s warts: Discordance creates bumpy expectations of mitochondrial‐nuclear evolution between species

“…Studies like Firneno et al. (2020) provide strong empirical evidence that patterns of mito‐nuclear coevolution vary through space and among species. They also suggest that species‐specific idiosyncrasies are more important to consider than generalized expectations of cytonuclear coevolution.…”

“…An important, but often underappreciated point discussed by Firneno et al. (2020), is the role that taxonomy may play in causing mito‐nuclear discordance. In a phylogenetic sense, the evolutionary entities we decide represent ‘species’ can operationally introduce mito‐nuclear discordance (sensu Ivanov et al., 2018).…”

“…Nonetheless, the phylogeographical literature offers a plethora of empirical examples where multiple divergent mtDNA genomes persist within a single animal species, as demonstrated in this issue by Firneno et al. (2020).…”

“…Dai, Wang, & Lei, 2013), introgression (e.g. Ivanov et al., 2018; Phuong, Bi, & Moritz, 2017) or incomplete lineage sorting (Firneno et al., 2020); however, many studies are unable to distinguish between them, which has become a major challenge in the field (Toews & Brelsford, 2012). In this issue, Firneno et al.…”

“…In this issue, Firneno et al. (2020) identify between these mechanisms, highlighting a complex biogeographic history in a group of cryptic Mesoamerican toad species, which revealed both mito‐nuclear and nuclear–nuclear patterns of genome discordance. The Incilius coccifer complex (containing three species: I. coccifer , I. ibarrai and I. porter, Figure 1) belong to the ‘true toad’ family (Amphibia: Anura: Bufonidae) that occur across a heterogeneous (highland versus lowland) landscape.…”