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Dryad

Phylogenomics of the tetraploid Hawaiian lobeliads: Implications for their origin, dispersal history, and adaptive radiation

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Apr 18, 2025 version files 78.51 MB

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Abstract

Hawaiian lobeliads exhibit extensive adaptive radiations and are considered the largest plant clade (143 species) endemic to any oceanic archipelago. Rapid insular radiations are prone to reticulate evolution, yet detecting hybridization has been limited by species sampling or inadequate nuclear data in previous Hawaiian studies. We analyzed 633 nuclear loci (including tetraploid duplications) and whole plastomes for 89% of extant species to derive phylogenies for the Hawai­ian lobeliads. Nuclear data provide strong support for nine major clades in both likelihood and ASTRAL analyses. All genera/sections are monophyletic except Clermontia and Cyanea. Nuclear and plastome phylogenies conflict on short, deep branches; the nuclear tree resolves a fleshy-fruited clade of Hawaiian Clermontia/Cyanea-Brighamia/Delissea, sister to Polynesian Sclerotheca, with both sister to a capsular-fruited Hawaiian clade. Incomplete lineage sorting in a rapid radiation starting 8.5-11.3 million years ago is sufficient to explain uncertainty and cytonuclear discordance along the backbone; sequence data strongly supports reticulation within Clermontia and especially Cyanea. Nuclear data identify 42 inter-island dispersal events, of which 89% accord with the progression rule, involving movement to the next younger, formerly unoccupied islands in the hotspot chain, consistent with ecological theory; plastid data overestimate such dispersals by 17%. Clermontia and Cyanea have undergone parallel adaptive radiations in elevational distribution and flower length on all major islands, but with some inter-island divergence. Within-island adaptive radiation and ecological speciation in these traits within Clemontia/Cyanea, combined with widespread single-island endemism, frequent inter-island dispersal, and occasional hybridization drove Hawaiian lobeliad diversification, together with early intergeneric divergence in habitat.