Interspecific hybridization causes long‐term phylogenetic discordance between nuclear and mitochondrial genomes in freshwater fishes

Abstract

Classification, phylogeography and the testing of evolutionary hypotheses rely on correct estimation of species phylogeny. Early molecular phylogenies often relied on mtDNA alone, which acts as a single linkage group with one history. Over the last decade, the use of multiple nuclear sequences has often revealed conflict among gene trees. This observation can be attributed to hybridization, lineage sorting, paralogy or selection. Here, we use 54 groups of fishes from 48 studies to estimate the degree of concordance between mitochondrial and nuclear gene trees in two ecological grades of fishes: marine and freshwater. We test the hypothesis that freshwater fish phylogenies should, on average, show more discordance because of their higher propensity for hybridization in the past. In keeping with this idea, concordance between mitochondrial and nuclear gene trees (as measured by proportion of components shared) is on average 50% higher in marine fishes. We discuss why this difference almost certainly results from introgression caused by greater historical hybridization among lineages in freshwater groups, and further emphasize the need to use multiple nuclear genes, and identify conflict among them, in estimation of species phylogeny.

Comparative phylogeography of trans‐Andean freshwater fishes based on genome‐wide nuclear and mitochondrial markers

“…However, the species trees estimated from multilocus nuclear data were well resolved for three of the five species. In addition, general concordance analyses of the mtDNA data set exhibited well‐supported clades for those without resolution in the nuclear data set, further providing evidence of multilocus concordance (Avise, ; Wallis et al, ). A few instances of mitonuclear discordance arising from mitochondrial introgression were also identified (e.g.…”

The puzzling phylogeography of the haplochromine cichlid fishAstatotilapia burtoni

“…On the other hand, evidence is accumulating that the replacement of mtDNA across large geographic distances, without apparent signatures of nuclear genomic admixis is more common than previously thought (e.g., Good, Vanderpool, Keeble, & Bi, 2015; Melo‐Ferreira, Seixas, Cheng, Mills, & Alves, 2014; Nevado, Fazalova, Backeljau, Hanssens, & Verheyen, 2011; Tang, Liu, Yu, Liu, & Danley, 2012). More general, discordance between nuclear and mtDNA phylogenetic inferences is known from many freshwater fish taxa and attributed to their high propensity to hybridize (see Wallis et al., 2017). In particular, in stenotopic, littoral cichlids from Lake Tanganyika—such as Eretmodus cyanosticus , Tropheus moorii and Variabilichromis moorii —such mtDNA/ncDNA discordance patterns due to introgression/hybridization have been linked to lake‐level fluctuations leading to past contact zones between otherwise isolated populations and large‐scale migration events (Koblmüller et al., 2011; Nevado, Mautner, Sturmbauer, & Verheyen, 2013; Sefc, Baric, Salzburger, & Sturmbauer, 2007; Sturmbauer et al., 2001).…”

“…More general, discordance between nuclear and mtDNA phylogenetic inferences is known from many freshwater fish taxa and attributed to their high propensity to hybridize (see Wallis et al, 2017).…”

Bidirectional mitochondrial introgression between Korean cobitid fish mediated by hybridogenetic hybrids

“…Surprisingly, the Cyt b locus exhibited insignificant genetic differentiation between C. hankugensis and I. longicorpa populations within each of the hybrid localities (Tables and ). Genetic discordance between mitochondrial and nuclear loci can be attributed to genetic introgression through hybridization (Toews & Brelsford, ; Wallis et al, ). Therefore this observation indicates the existence of mitochondrial introgression between the two parental species.…”