The biogeography of mitochondrial and nuclear discordance in animals

Abstract

Combining nuclear (nuDNA) and mitochondrial DNA (mtDNA) markers has improved the power of molecular data to test phylogenetic and phylogeographic hypotheses and has highlighted the limitations of studies using only mtDNA markers. In fact, in the past decade, many conflicting geographic patterns between mitochondrial and nuclear genetic markers have been identified (i.e. mito-nuclear discordance). Our goals in this synthesis are to: (i) review known cases of mito-nuclear discordance in animal systems, (ii) to summarize the biogeographic patterns in each instance and (iii) to identify common drivers of discordance in various groups. In total, we identified 126 cases in animal systems with strong evidence of discordance between the biogeographic patterns obtained from mitochondrial DNA and those observed in the nuclear genome. In most cases, these patterns are attributed to adaptive introgression of mtDNA, demographic disparities and sex-biased asymmetries, with some studies also implicating hybrid zone movement, human introductions and Wolbachia infection in insects. We also discuss situations where divergent mtDNA clades seem to have arisen in the absence of geographic isolation. For those cases where foreign mtDNA haplotypes are found deep within the range of a second taxon, data suggest that those mtDNA haplotypes are more likely to be at a high frequency and are commonly driven by sex-biased asymmetries and ⁄ or adaptive introgression. In addition, we discuss the problems with inferring the processes causing discordance from biogeographic patterns that are common in many studies. In many cases, authors presented more than one explanation for discordant patterns in a given system, which indicates that likely more data are required. Ideally, to resolve this issue, we see important future work shifting focus from documenting the prevalence of mito-nuclear discordance towards testing hypotheses regarding the drivers of discordance. Indeed, there is great potential for certain cases of mitochondrial introgression to become important natural systems within which to test the effect of different mitochondrial genotypes on whole-animal phenotypes.

Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion

“…We can also imagine that the 3 months long teleplanic larvae phase could have permitted the implantation of the A lineage in the Mediterranean Sea by long‐distance colonization of an empty patch. If the Spanish hybrid zone is a stable postglacial contact zone, then the observation that A mtDNA haplogroup carrying individuals tend to sometimes have a high proportion of B lineage ancestry at the nuclear loci would be well explained by the widespread observation of mito‐nuclear discordance in hybrid zones (Toews & Brelsford, 2012). A finer sampling grain along the coast would be required to better describe this phenomenon.…”

Interspecies introgressive hybridization in spiny frogs Quasipaa (Family Dicroglossidae) revealed by analyses on multiple mitochondrial and nuclear genes

“…At present, molecular markers offer an opportunity to reveal gene flow in divergent lineages and infer introgressive hybridization by detecting topological incongruence between gene trees (Choleva et al., 2014). The incongruence may be caused by the overall amount of differentiation (Toews & Brelsford, 2012). In the present study, we analyzed the phylogenetic relationships of mtDNA.…”

“…In addition, the tree topology of the nuclear gene showed that the population of Q. boulengeri was divided into three branches; this result also agrees with the suggestion of four major matrilines of Q. boulengeri (Yan et al., 2012). The incomplete lineage sorting and the ancestral polymorphism were to be considered in Quasipaa ; sex‐biased dispersal, human introductions, hybrid offspring infertility, and low viability or low fertility also resulted in the directional or nondirectional gene introgression pattern in Quasipaa (Toews & Brelsford, 2012). In the present study, introgression between Q. exilispinosa and other species of Quasipaa (e.g., Q. jiulongensis and Q. spinosa ) was not detected.…”

Snails in the desert: Species diversification of Theba (Gastropoda: Helicidae) along the Atlantic coast of NW Africa

“…Furthermore, in cases where species are parapatric advantageous alleles may readily spread across hybrid zones (Barton & Bengtsson, 1986). Such single gene introgressions seem especially common for cytoplasmically inherited genomes and in the past decades, discordant phylogenetic results between mitochondrial and nuclear gene markers were mostly attributed to adaptive introgression of mitochondrial DNA (Harrison, 1989; Rieseberg, 1995; Toews & Brelsford, 2012). Indeed, the highly supported sister group relationship in the COI topology (Figure 2b) along with the small environmental niche overlap between T. sacchii and Theba sp.…”