Complex histories of gene flow and a mitochondrial capture event in a non-sister pair of bird

Hybridization, introgression, and reciprocal gene flow during speciation,
specifically the generation of mitonuclear discordance, are increasingly
observed as parts of the speciation process. Genomic approaches provide
insight into where, when, and how adaptation operates during and after
speciation and can measure historical and modern introgression. Whether
adaptive or neutral in origin, hybridization can cause mitonuclear
discordance by placing the mitochondrial genome of one species (or
population) in the nuclear background of another species. The latter,
introgressed species may eventually have its own mtDNA replaced or
“captured” by other species across its entire geographical range.
Intermediate stages in the capture process should be observable. Two
non-sister species of Australasian monarch-flycatchers, Spectacled Monarch
(Symposiachrus trivirgatus) mostly of Australia and Indonesia and
Spot-winged Monarch (S. guttula) of New Guinea, present an opportunity to
observe this process. We analysed thousands of single nucleotide
polymorphisms (SNPs) derived from ultraconserved elements of all
subspecies of both species. Mitochondrial DNA sequences of Australian
populations of S. trivirgatus form two paraphyletic clades, one being
sister to and presumably introgressed by S. guttula despite little nuclear
signal of introgression. Population genetic analyses (e.g., tests for
modern and historical gene flow and selection) support at least one
historical gene flow event between S. guttula and Australian S.
trivirgatus. We also uncovered introgression from Maluku island subspecies
of S. trivirgatus into an island population of S. guttula, resulting in
apparent nuclear paraphyly. We find that neutral demographic processes,
not adaptive introgression, are the most likely cause of these complex
population histories. We suggest that a Pleistocene extinction of S.
guttula from mainland Australia resulted from range expansion by S.
trivirgatus.