Genetic Evidence for the Origin and Relationships of Hawaiian Honeycreepers (Aves: Fringillidae)

Abstract

Using starch gel electrophoresis of proteins, we examined variation at 36 genetic loci in nine species (eight genera) [Telospiza cantans, Loxioides bailleui, Hemignathus parvus, Oreomystis bairdi, Paroreomyza montana, Loxops coccineus caeruleirostris, Vestiaria coccinea, Himatione sanguinea sanguinea, Hemignathus virens virens, H. v. wilsoni, H. v. chloris and H. v. stejnegeri] of Hawaiian honeycreeprs (Class Aves; Family Fringillidae; Subfamily Drepanidinae). Two species of cardueline finches and two emberizids [Piranga ludoviciana, Sicalis flaveola pelzelni, Carpodacus purpureus californicus, and Loxia curvirostra grinnelli] served as outgroup taxa. Twenty-three loci (64%) were either polymorphic within taxa and/or were fixed at alternative alleles among taxa. In seven of nine species, low levels of mean Hobs (0.05), percentage of polymorphic loci (4.16), and average number of alleles per polymorphic locus (2.03) may reflect population bottlenecks that occurred either during or after initial colonization. Phenograms, distance Wagner trees, F-M trees, and a cladistic analysis provided hypotheses for the evolutionary relationshps of taxa and suggest that: (1) The drepanidines are monophyletic. (2) The Hawaiian honeycreepers are more similar genetically to the two species of emberizids than to the two species of carduelines, a result that conflicts with a recent consensusus of opinion based on morphologic and other biochemical data. (3) The species ancestral to modern drepanidines colonized the Hawaiian Archipelago at an estimated 7-8 million years before present (MYBP). This date agrees generally with the timing of emergence of Nihoa, now largely submerged, but antedates the appearance of Kauai (5 MYBP), the oldest of the present high Hawaiian Islands. (4) The creepers Oreomystis and Paroreomyza represent the oldest and most divergent lineage of living drepanidines. (5) The youngest lineages are represent by the nectar feeders (Himatione and Vestiaria), the thick-billed "finch types" (Loxioides and Telespiza), and a diverse array of other forms (Loxops and Hemignathus), (6)Hemignathus "virens" stejnegeri is a full species, possibly allied to Loxops coccineus. Our genetic data conflict with the two major phylogenetic hypotheses that have been proposed for the radiation of the drepanidines: (1) origin from tubular-tongued, nectar-feeding ancestors; and (2) origin from thick-billed and thick-tongued, seed- and fruit-eating ancestors. Instead, the evidence suggests that the earliest Hawaiian honeycreepers had generalized bills, tongues, and diets. This ancestral group gave rise to the lineages that eventually led to both (1) modern Paroreomyza and Oreomystis and (2) a complex group of (a) nectar feeders (Himatione, Vestiaria, and relatives); (b) seed and fruit eaters (Loxioides, Telespiza, and relatives); and (c) a diverse group of species that feed on both arthropods and nectar (Loxops, Hemignathus, and relatives). We speculate that the most immediate ancestor of all of the heavy-billed species was a thin-billed tubular-tongued, nectarivorous form and that this major morphologic shift was expendiated by the alteration of developmental patterns and rates.