Mitonuclear co-introgression opposes genetic differentiation between phenotypically divergent songbirds

Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the relative effective population sizes of these genomic components. Differential introgression can cause some species pairs to deviate dramatically from this pattern. The yellowhammer (Emberiza citrinella) and the pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance but show no mtDNA differentiation. This discordance might be explained by mtDNA introgression-a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). We investigated genome-wide nuclear differentiation between yellowhammers and pine buntings and compared it to what was seen previously in the mitochondrial genome. We found clear nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further tested for preferential introgression of mitonuclear genes and detected evidence for such biased introgression in yellowhammers. Mitonuclear co-introgression can remove post-zygotic incompatibilities between species and may contribute to the continued hybridization between yellowhammers and pine buntings despite their clear morphological and genetic differences. As such, our results highlight the potential ramifications of co-introgression in species evolution.

Extraordinary variation in a simple song: No geographical patterns in initial phrase variation of the Yellowhammer, a passerine with pronounced dialects

Geographical variation of birdsong is used to study various topics from cultural evolution to mechanisms responsible for reproductive barriers or song acquisition. In species with pronounced dialects, however, patterns of variation in non-dialect parts of the song are usually overlooked. We focused on the individually variable initial phrase of the song of the Yellowhammer (Emberiza citrinella), a common Palearctic passerine which became a model species for dialect research. We used a quantitative method to compare the similarity of initial phrases from the repertoires of 237 males recorded at different spatial scales in a central European country covering all main dialect types. We hypothesized that patterns of initial phrase sharing and/or phrase similarity are affected by dialect boundaries and geographical proximity (i.e. that birds from the same dialect regions use more similar phrases or share them more often). Contrary to our expectations, initial phrase variation seems unrelated to dialects, as we did not find higher similarity either among recordings from the same dialect areas or among those from the same locality. Interestingly, despite the immense variability of phrase types detected (only 16% of 368 detected initial phrase types were shared between at least 2 males), a relatively high proportion of males (45%) was involved in sharing, and males using the same initial phrase were located anywhere from tens of meters to hundreds of kilometers apart. The patterns of variation suggest that precise copying during song learning as well as improvisation play important roles in forming individual repertoires in the Yellowhammer. Our data also confirm previous indications that the repertoires of Yellowhammer males (i.e. the composition of initial phrases) are individually unique and temporally stable. This makes the species a good candidate for individual acoustic monitoring, useful for detailed population or behavioral studies without the need for physical capture and marking of males.