Rapid divergence with gene flow creates intractable nodes in the tree of life: An empirical demonstration in the Buzzing Flowerpecker (Dicaeum hypoleucum)

The avian tree of life contains a series of famously intractable nodes and controversial relationships whose resolution varies between studies depending on both data type and the analytical approach used for phylogenetic reconstruction. Here we present an empirical case study of the Buzzing Flowerpecker (Dicaeum hypoleucum), documenting how these challenging nodes can be generated by rapid divergence with subsequent gene flow across an island archipelago. In our study, a phylogeographic approach revealed the presence of three discrete genomic lineages corresponding to the three phenotypic lineages. Yet phylogenetic reconstructions repeatedly generated conflicting topologies with high levels of uncertainty, and significant ABBA/BABA tests imply uneven patterns of allele sharing that cannot be explained without invoking gene flow. Overall, the most supported genome-wide topology was only recovered in 34.4% - 36.7% of gene trees. This high level of phylogenomic discordance explains the inconsistent and conflicting results recovered across phylogenetic reconstructions. Finally, multispecies coalescent modeling revealed that a polytomy (i.e., simultaneous three-population split) with ongoing gene flow between adjacent lineages provides the best fit to the empirical data. Our thorough investigation of this deceptively simple three-taxa group demonstrates why investigators should take extreme care to resolve the conflicting and misleading results that can arise in cases where phylogenomic discordance is pervasive. Further, these results demonstrate that rapid divergence and gene flow facilitated by colonization across island archipelagoes may play an outsized role in generating phylogenomic discordance and recalcitrant nodes across the tree of life.