Mitochondrial introgression and replacement between yellowhammers (Emberiza citrinella) and pine buntings (Emberiza leucocephalos) (Aves: Passeriformes)

Abstract

In studies of phylogeography and taxonomy, strong emphasis is usually placed on the study of mitochondrial (mt)DNA. In the present study, we present a remarkable case in which highly phenotypically divergent species have almost no divergence in mtDNA. Yellowhammers (Emberiza citrinella Linnaeus) and pine buntings (Emberiza leucocephalos S. G. Gmelin) differ noticeably in appearance and song but hybridize in some areas of contact. They share a variety of closely-related mtDNA haplotypes, with little divergence in frequencies, indicating a mitochondrial divergence time sometime during or after the last major glacial period. By contrast, nuclear DNA (amplified fragment length polymorphism markers and CHD1Z gene sequences) differs more strongly between the species, and these differences can be used to identify intermediate genetic signatures of hybrids. The combined amount of mitochondrial diversity within yellowhammers and pine buntings is very low compared to other Emberiza species pairs, whereas the level of variation at the nuclear gene CHD1Z is comparable to that within other species pairs. Although it is difficult to completely reject the possibility that the two species split extremely recently and experienced rapid nuclear and phenotypic differentiation, we argue that the evidence better supports another possibility: the two species are older and mtDNA has recently introgressed between them, most likely as a result of a selective sweep. Mismatches between mitochondrial and nuclear phylogeographic patterns may occur more commonly than previously considered, and could have important implications for the fields of phylogeography and taxonomy.

Extensive mitochondrial introgression in North American Great Black-backed Gulls (Larus marinus) from the American Herring Gull (Larus smithsonianus) with little nuclear DNA impact

“…Females being the heterogametic sex in birds, Haldane's rule would also predict that mitochondrial haplotypes show patterns of reduced introgression compared with nuclear alleles (Carling and Brumfield, 2008). However, several cases of interspecific gene flow documented in birds depicted the reverse pattern; no nuclear introgression is detected while the maternally transmitted mtDNA exhibits high levels of introgression (Tejedor et al, 2007;Bellemain et al, 2008;Irwin et al, 2009). This is the same pattern we observed between the North American L. marinus and the sympatric L. smithsonianus.…”

“…Indeed, one general pattern that emerges from recent studies is that introgression rates among loci may greatly vary according to their location in the genome. In particular, several studies have reported cases of mitonuclear discordances with introgression of mitochondrial DNA and low or even apparent absence of nuclear introgression (fish: Wilson and Bernatchez, 1998, birds: Bellemain et al, 2008;Irwin et al, 2009, mammals: Roca et al, 2005Good et al, 2008;Melo-Ferreira et al, 2009, amphibians: Zieliń ski et al, 2013. The reverse situation, high nuclear introgression with low mitochondrial introgression or lack of mitochondrial introgression has also been observed in butterflies, a primate species and birds species (Steeves et al, 2010, see also Petit and Excoffier, 2009 for a review).…”

The biogeography of mitochondrial and nuclear discordance in animals

“…In these cases, significantly less mtDNA divergence compared with nuclear differentiation can implicate mitochondrial introgression between taxa (e.g. Cathey et al 1998;Bachtrog et al 2006;Irwin et al 2009). …”

Contact zone dynamics during early stages of speciation in a chorus frog (Pseudacris crucifer)

“…For example, asymmetrical mtDNA introgression may be caused by local adaptation, mtDNA-nDNA coevolution or selective sweeps of universally favoured mutations (Irwin et al, 2009). The lack of obvious environmental gradients geographically coincident with this zone of secondary contact (Williams, 2009) and our use of putatively neutral loci does not support the local adaptation hypothesis.…”