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The Relationships of the Hawaiian Honeycreepers (Drepaninini) As Indicated by Dna-Dna Hybridization

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The Relationships of the Hawaiian Honeycreepers (Drepaninini) As Indicated by Dna-Dna Hybridization THE RELATIONSHIPS OF THE HAWAIIAN HONEYCREEPERS (DREPANININI) AS INDICATED BY DNA-DNA HYBRIDIZATION CH^RrES G. SIBLEY AND Jo• E. AHLQUIST Departmentof Biologyand PeabodyMuseum of Natural History, Yale University, New Haven, Connecticut 06511 USA ABSTRACT.--Twenty-twospecies of Hawaiian honeycreepers(Fringillidae: Carduelinae: Drepaninini) are known. Their relationshipsto other groups of passefineswere examined by comparing the single-copyDNA sequencesof the Apapane (Himationesanguinea) with those of 5 speciesof carduelinefinches, 1 speciesof Fringilla, 15 speciesof New World nine- primaried oscines(Cardinalini, Emberizini, Thraupini, Parulini, Icterini), and members of 6 other families of oscines(Turdidae, Monarchidae, Dicaeidae, Sylviidae, Vireonidae, Cor- vidae). The DNA-DNA hybridization data support other evidence indicating that the Hawaiian honeycreepersshared a more recent common ancestorwith the cardue!ine finches than with any of the other groupsstudied and indicate that this divergenceoccurred in the mid-Miocene, 15-20 million yr ago. The colonizationof the Hawaiian Islandsby the ancestralspecies that radiated to produce the Hawaiian honeycreeperscould have occurredat any time between 20 and 5 million yr ago. Becausethe honeycreeperscaptured so many ecologicalniches, however, it seemslikely that their ancestor was the first passefine to become established in the islands and that it arrived there at the time of, or soon after, its separationfrom the carduelinelineage. If so, this colonist arrived before the present islands from Hawaii to French Frigate Shoal were formed by the volcanic"hot-spot" now under the island of Hawaii. Therefore,the ancestral drepaninine may have colonizedone or more of the older Hawaiian Islandsand/or Emperor Seamounts,which also were formed over the "hot-spot" and which reachedtheir present positions as the result of tectonic crustal movement. The cardueline-drepanininelineage probably diverged from the Fringilla lineage in the late Oligocene, from the New World nine-primaried oscines in the early Oligocene, and from the other oscines in the early Eocene. During this study we also obtained evidence that the vireos (Vireonidae) are not closely related to the New World nine-primaried oscines. Received2 March 1981, accepted1 July 1981. THE volcanic islands of the Hawaiian chain cific Ocean from Hawaii in the southeast to and the Galapagosarchipelago are well-known Midway and Kure atolls at the northwest end as natural laboratories in which to observe the of the Hawaiian Ridge (see Fig. 3). Hawaii is resultsof the processesof colonization,specia- 3,000 km from California and the Aleutian Is- tion, and adaptive radiation. Both island lands, and Kure Atoll is 2,500 km from the groupsare substantialdistances from the near- Aleutians and 3,000 km from Kamchatka. The est continent, are composedof many islands, Hawaiian Ridge makes an elbow bend and ex- various distancesapart, and have a variety of tends northward beyond the islands of the ecologicalconditions. The Galapagosarchipel- Hawaiian chain as a line of submergedvolca- ago includes 10 main islands and 6 smaller nos, the Emperor Seamounts. ones located on the equator about 900 km west Twenty-two species of Hawaiian honey- of Ecuador. Thirteen species of Galapagos creepers(Drepaninini of Sibley 1970: 99) are finches (Geospiza,Cactospiza, Certhidea et al.) known, of which six are recently extinct have evolved from the original emberizine (Greenway 1968, Raikow 1977b). Within his- ancestor (Bowman 1961). toric times only eight of the 25 Hawaiian Is- The Hawaiian Islands extend in a broadly lands have supportedpopulations of Hawaiian linear chain for 2,500 km across the central Pa- honeycreepers. l30 The Auk 99: 130-140. January 1982 January1982] HawaiianHoneycreeper Relationships 131 The 11 genera of drepaninines are character- ian honeycreepers,because there are no ana- ized by a remarkable array of bill types, from tomical characters that preclude the relation- the short, finch-like bills of Psittirostra, Melam- ship and because the carduelines include prosops,and Ciridops and the slender bills of speciesmore capableof colonizing the Hawai- Viridonia (=Loxops), Hirnatione,and Palrneria, ian Islands than do any of the other groups that to the parrot-like structure of Pseudonestorand have been suggested.Bock (1970) also found the long, decurved bills of Hemignathusand that the tongue apparatus of Ciridopsanna re- Drepanis. This variation caused early taxono- sembles that of the carduelines, not that of the mists to distribute the Hawaiian honeycreep- coerebines. Sibley (1970) also supported the ers among several passerine families, includ- carduelines as the ancestors of the drepani- ing the finches (Fringillidae), flower-peckers nines, based on comparisons of the electro- (Dicaeidae), and honeyeaters (Meliphagidae). phoretic patterns of their egg-white proteins. Later, it became obvious that the Hawaiian Raikow studied the muscles of the hind limb honeycreepers are closely related to one (1976) and the forelimb (1977a), and reviewed another and that, as in the Galapagosfinches, and extended the morphological evidence of a single ancestralspecies had given rise to the the origin and evolution of the Hawaiian hon- 22 species,which adapted to the many ecolog- eycreepers(1977b). He concluded(1977b: 116) ical niches that were available to the first col- that the drepaninines "arose from a single onists in these oceanic islands (Areadon 1950, founder species," which "was a primitive Sibley 1970, Raikow 1977b). member of the Carduelines." Raikow suggest- The identity of the ancestral taxon has pro- ed that this ancestral cardueline was a typical duced much debate and speculation, but, be- finch similar to the extant Psittirostra and that cause the Hawaiian honeycreepers are nine- the "nectar-feeding habits arosein Hawaii and primaried oscines,their origin must be sought are merely convergentwith similar conditions among the members of that group. Gadow in other families of birds." (1891) consideredonly the nectar-feeding taxa In this paper we present the results of com- as possible ancestors and concluded that the parisons among the homologous nucleotide neotropical coerebine honeycreepersare the sequences of the single-copy DNAs of a closestrelatives of the Hawaiian honeycreepers Hawaiian honeycreeper(Hirnatione sanguinea) and that the tanagers (Thraupini) are also re- and other taxa of the oscine passerines, using lated to them. Gadow also noted, however, the technique of DNA-DNA hybridization. that the drepaninines and carduelines share The DNA data provide an index to the amount charactersof the horny palate. Lucas (1894) of genetic divergencebetween taxa and to the suggested that the tongues of the Hawaiian time since that divergence began. It is there- honeycreepers could have been derived from fore possible to relate the phylogeny of the that of the New World oriole genus Icterus or birds to the geologicalhistory of the Hawaiian- that of the paruline genus Dendroica.Sushkin Emperor island chain. (1929) proposed that the cardueline finches and Hawaiian honeycreeperswere most closelyre- METHODS lated, because he found similarities between The DNA hybridization technique takes advan- the bills, skulls, and horny palatesof Psittiros- tage of the complementary structure of the double- tra and those of the carduelines. Amadon stranded DNA molecule. When double-stranded (1950: 232) reviewed the earlier proposals but DNA in solutionis heated to ca. 100øC,the hydrogen concluded that the Coerebini or Thraupini bonds between A-T and G-C base pairs dissociate, were the more probable ancestors. Beecher and the two strands separate. Under proper condi- (1953) found that the jaw musculatureof Psit- tions, the two single strands will reassociateas the tirostrais like that of the carduelines(e.g. Car- solution cools, becausethe complementarybases podacus),and he noted (p. 312) "the striking "recognize" one another. If the temperature is main- similarity of the Hawaiian finches to the car- tained at a high enough level, e.g. 60øC, comple- mentary base pairing will occur only between long dueline finches in all but plumage" but con- homologous sequences of nucleotides. This is be- cluded that the similarities are due to "parallel cause only long sequencesof complementary bases developmentfrom . thraupine stock." will have sufficient bonding strength to form stable Bock (1960:477) argued that the carduelines duplexes at that temperature, and only homologous are the most probable ancestorsof the Hawai- sequencespossess the necessarydegree of comple- 132 $t•LEY AtaDA•,QU•ST [Auk, Vol. 99 lO0 such hybrid duplexes will cause them to dissociate at a temperature lower than that required to melt 9O conspecificdouble-stranded DNA. Thus, the prop- erty of sequencerecognition exhibited by homolo- gous sequencesand the decreasedthermal stability 80. of imperfectly matched hybrid sequencesform the basis of the DNA-DNA hybridization technique. 70. The degree of nucleotide sequencehomology be- tween the reassociatedsingle strands of any two DNAs can be determined by measuring the per- z centageof hybridization and the thermal stability of the reassociated duplex molecules. Following is a z synopsis of the technique, which is described in more detail by Sibley and Ahlquist 1981). DNAs were obtained from the nuclei of avian erythrocytesand purified by removing the proteins 30. and RNA according to the procedures of Marmur (1961) and Shields and Straus (1975). The purified
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