Reticulated adaptive radiation and phylogenomic diversity loss in the Hawaiian honeycreepers.

Abstract

The Hawaiian honeycreepers, one of the world's most iconic adaptive radiations, are facing a human-mediated extinction crisis. More than 60 Hawaiian honeycreepers (Fringillidae: Carduelinae: Drepanidini) evolved from a single rosefinch-like ancestor that colonized the Hawaiian Islands. Only 17 Hawaiian honeycreeper taxa are known to be extant, of which only the common 'amakihi (<i>Chlorodrepanis virens</i>) and 'apapane (<i>Himatione sanguinea</i>) are classified as "Least Concern." Using mitogenome, whole-genome, and hybridization-capture data, we present a comprehensive phylogeny of the historically known Hawaiian honeycreeper radiation. We also place two taxa known only from paleontological specimens (<i>Vangulifer neophasis</i> and <i>cf. Xestospiza conica</i>) in their phylogenomic context. We demonstrate that most Hawaiian honeycreeper lineages diversified in a "Big Bang" of adaptive radiation correlating with the formation of O'ahu and that interspecies introgression likely played a role in this process. Using whole-genome data, we confirm putative interspecies admixture [N. A. S. Przelomska <i>et al.</i>, <i>Biol. Lett.</i> <b>21</b>, 20250265 (2025)] between the 'ō'ū (<i>Psittirostra psittacea</i>) and Lāna'i hookbill (<i>Dysmorodrepanis munroi</i>) and document ongoing gene flow across the 'amakihi species complex. Furthermore, we reject the synonymization of <i>Vestiaria</i> ('i'iwi) and <i>Drepanis</i> (Hawai'i and black mamo). Instead, the mamo species form an extinct clade with no close extant relatives, demonstrating a greater loss of phylogenomic diversity than previously understood.