Multiple concordant cytonuclear divergences and potential hybrid speciation within a species complex in Asia

Abstract

Various environmental factors impact the distribution, population structure, demography and evolutionary trajectory of a bird species, leading to genetic and morphological divergences between populations across its distribution. The Paradoxornis webbianus species complex is found throughout much of East Asia, where its geographically distinct populations exhibit dramatic morphological variation. This has resulted in a hotly debated taxonomy. This study intended to identify genetic divergence patterns and their underlying contributing factors for this species complex. We collected 243 birds, whose data was combined with those available in GenBank to perform phylogeographic analyses using one mitochondrial and six nuclear loci. Six mitochondrial clades were observed in the species complex, while individual-based Bayesian clustering using nuclear markers showed multiple congruent breaks. Overall, the six molecular lineages could be recognized as independent species under the lineage species concept in view of genetic divergence, clade-specific morphological changes and distribution: P. webbianus, P. w. bulomachus, P. alphonsianus, P. a. ganluoensis, P. brunneus brunneus and P. b. ricketti. The estimated divergence times range from 0.46 to 3.36 million years ago, suggesting it was likely impacted by paleoclimatic changes. Interestingly, P. alphonsianus carries two divergent mitochondrial lineages shared with P. webbianus and P. a. ganluoensis, respectively, and analyses based on nuclear loci found a similar pattern. We discussed the various hypotheses for this pattern and argued that P. alphonsianus was likely the result of hybridization between P. webbianus and P. a. ganluoensis. Further data on genome, transcriptome and breeding ecology are needed to address the hypothesis of hybrid speciation and its underlying mechanisms.