Abstract:

Aims: This study aims to investigate the evolutionary origin and molecular mechanisms underlying homoploid hybrid speciation in the golden-crowned manakin (Lepidothrix vilasboasi), a hybrid bird species distributed in the Amazon Basin. 

Methods: Using genome-wide SNP data from L. vilasboasi and its two parental species, the snow-capped manakin (L. nattereri) and the opal-crowned manakin (L. iris), we conducted population genetic analyses with ADMIXTURE and principal component analysis (PCA) to infer genetic structure, and employed D-statistics (ABBA-BABA tests) to examine gene flow patterns. We further applied a recently proposed molecular model of homoploid hybrid speciation to explore how hybridization contributes to reproductive isolation. Finally, gene family analyses of those positively selected genes were carried out using BLASTP, MAFFT alignments, and phylogenetic reconstruction to assess gene duplication and evolutionary constraint. 

Results: Our results supported the hypothesis that L. vilasboasi has an ancient hybrid origin. The establishment of reproductive isolation in this hybrid species may have been facilitated by the inheritance of alternate parental premating isolation-related candidate genes from both parental species. Genes related to skin pigmentation and reproductive system development were identified as potential contributors to both prezygotic and postzygotic isolation mechanisms. Gene family analysis revealed that ADAMTS10, ASTL, and ALX4 underwent multiple duplication events; ESRRG showed extensive gene expansion; and OCA2 exhibited strong evolutionary constraint and high sequence conservation. 

Conclusion: This study highlights the important role of hybridization in avian speciation and phenotypic diversification, providing new molecular evidence for the genetic basis of reproductive isolation in homoploid hybrid species. Our findings further support the applicability of the proposed molecular model of homoploid hybrid speciation across different lineages and suggest that the inheritance of alternate parental genomic components associated with reproductive isolation may facilitate the origin of new species.

Key words: hybrid speciation, reproductive isolation, golden-crowned manakin, avian species, speciation genes