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Molecular Systematics and Biogeography of the Hawaiian Avifauna

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Molecular Systematics and Biogeography of the Hawaiian Avifauna Studies in Avian Biology No. 22:51-60, 2001. MOLECULAR SYSTEMATICS AND BIOGEOGRAPHY OF THE HAWAIIAN AVIFAUNA ROBERT C. FLEISCHER AND CARL E. MCINTOSH Abstract. The Hawaiian avifauna is exceptional for its high proportion of endemic taxa, its spectac- ular adaptive radiations, and its level of human induced extinction. Little has been known about the phylogenetic relationships, geographical origins, and timing of colonization of individual avian lin- eages until recently. Here we review the results of molecular studies that address these topics. Mo- lecular data (mostly mitochondrial DNA sequences) are available for 14 of the 21 or more lineages of Hawaiian birds. We briefly review results of phylogenetic analyses of these data for lineages that have experienced major and minor radiations, and for single differentiated species and probable recent colonists. When possible, we determine the mainland species that are genetically most closely related. We find evidence that roughly half of the >21 lineages colonized from North America; not even a quarter appear to have come from South Pacific Islands. Our data also provide little evidence that Hawaiian bird lineages predate the formation of the current set of main islands (i.e., >5 Ma), as has been found for Hawaiian Drosophila and lobeliads. Key Words: adaptive radiation; biogeography; Hawaiian avifauna; mitochondrial DNA; molecular systematics. In 1943 Ernst Mayr published a short paper in tially mislead on issues of common ancestry via The Condor summarizing his hypotheses about homoplasy. DNA sequences, on the other hand, the geographic origins and closest living rela- while obviously not evolving in a perfect clock- tives of each known lineage in the Hawaiian avi- like fashion (see below), do change over time, fauna. Mayr (1943) concluded that half of 14 and evolve more continuously than morphology. hypothesized colonizations were of American Also, with the exception of a relatively few non- origin and only two lineages arose from Poly- synonymous changes within protein sequences, nesia. Therefore, although Hawaii‘ is considered they generally evolve via mutation and drift (Nei part of the “Polynesian Region” because most 1987, Avise 1994), and are not as subject to ho- of its biota and its human inhabitants had Pol- moplasy via convergence or stasis as are mor- ynesian ancestors, in terms of its birds Hawaii‘ phological or other characters. Thus major adap- is in the Nearctic Region. Since Mayrs’ paper, tive shifts in, for example, the bills of Hawaiian other authors have posited similar systematic hy- honeycreepers, may occur within some lineages potheses and biogeographic scenarios based on (e.g., to thin and decurved in the nectarivorous morphological, ecological, and distributional I‘ iwi,‘ Vestiaria coccinea), while not in others data (e.g., Amadon 1950, Pratt 1979, Berger (e.g., conical and finchlike in the Laysan Finch, 1981). Paleontology has offered only minor res- Telespiza cantans), in spite of an identical olution of the relationships of ancestral lineages amount of time since evolving from their puta- or the timing of speciation events; although tively “finch-billed” common ancestor. There there is an excellent Holocene fossil record in are methods for detecting symplesiomorphic Hawaii‘ (Olson and James 1982a, 1991; James versus synapomorphic characters in phylogenet- and Olson 1991), the pre-Holocene record is ex- ic analysis, but the higher variance in rates of tremely limited (though one excellent fauna change of morphological characters remains a dates to >0.12 Ma ago; James 1987). problem for phylogenetic reconstruction (Hillis In recent years, molecular methods have prov- et al. 1996). en extremely useful for inferring evolutionary While there have been significant molecular relationships among taxa and the relative time investigations of particular Hawaiian plant and frames during which taxa evolved (Avise 1994, invertebrate taxa (especially Drosophila; e.g., Hillis et al. 1996). Inference from molecular data Hunt and Carson 1983, DeSalle and Hunt 1987, may be the best available way to reconstruct DeSalle 1992), few molecular studies detailing phylogenetic relationships and determine geo- evolutionary histories of the Hawaiian avifauna graphical origins and evolutionary time frames have been made until recently (e.g., Tar-r and for Hawaiian taxa. In part this is because mor- Fleischer 1993, 1995; Feldman 1994, Cooper et phological or behavioral changes are often adap- al. 1996; Fleischer et al. 1998, 2000, this vol- tive responses subject to natural or sexual selec- ume; Paxinos 1998, Sorenson et al. 1999, tion (i.e., as part of the process of adaptive ra- Fleischer et al. in press, Rhymer this volume; C. diation), and they do not usually show constancy Tarr, E. Paxinos, B. Slikas, H. James, S. Olson, in their rates of change. Thus they can poten- A. Cooper, and R. Fleischer, unpubl. data). 51 52 STUDIES IN AVIAN BIOLOGY NO. 22 TABLE 1. THE ELEMENTS OF THE HAWAIIAN AVIFALINA TaXOn Family No. of species” Geographic ori& Comments‘ Non-passeriformes: Ibises Plataleidae 22 N.A. minor radiation, flight- less, Apteribist Night Heron Ardeidae 1 N.A. recent colonist, Nyctico- rax nycticorax Moa-nalos Anatidae 24 W. Hemisphere minor radiation?, 3 flightless duck gen- eral Trne Geese Anatidae 23 N.A. minor radiation, Bran- ta,te Modem Ducks Anatidae 2 N.A. and Asia 1 Z differentiated, 1 re- cent colonist, Anas e Porzana Rails Rallidae 212 Pacific/unknown major radiation?, ~2 colonizationsl Large rallids Rallidae 2 N.A.? recent colonists?, coot and moorhen Black-necked Stilt Recurvirostridae 1 N.A. recent colonist, Himan- topus knudseni e Eagle Acciptridae 1 Asia recent colonist, Haliaee- tus leucophryst Buteo Acciptridae 1 N.A. differentiated, Buteo so- litarius e Harrier Acciptridae Unknown differentiated, Circus dossenust Long-legged Owls Strigidae Unknown minor radiation, Grullis- trix spp. 4t Short-eared Owl Strigidae Unknown recent colonist, Asio flammeus sandwichen- sis Passeriformes: crows Corvidae 24 Unknown minor radiation?, Corvus SPP., 3t, 1 e Millerbird Sylviidae 1 South Pacific differentiated, Acroce- phalus familiaris e Elepaio‘ Myiagridae 21 Australasia differentiated, Chasiem- pis sandwichensis Thrushes Muscicapidae 5 W. Hemisphere minor radiation, Myad- estes spp., 37, 1 e Honeyeaters Meliphagidae ~6 South Pacific minor radiation, Moho spp., Chaetoptila, alli_ Honeycreepers Fringillidae 250 Asia or N.A.? major radiation, drepani- dines, most? or e >21 lineages 13 families 2 IO2 species a Number of species within each lmeagelfamily, based on James and Olson (1991). Olson and James (1991), and H. James (pers.comm.). h N.A. = North America; W = West ’ ’ t denotes at least some members extinct; e denotes at least some members endangered. Components of the Hawaiian avifauna vary flightless waterfowl (moa-nalos) show extreme greatly in the degrees to which they have spe- morphological modification in their apparent ciated and become modified morphologically shift into a ratite/grazing mammal/tortoise niche and ecologically (Table 1). For example, the Ha- (Olson and James 1991; Sorenson et al. 1999). waiian drepanidines (Hawaiian finches or hon- Other avian lineages have not speciated and eycreepers) have evolved incredible morpholog- have changed morphologically little or not at all ical, ecological, and behavioral diversity across from putative mainland relatives (e.g., Black- more than 50 species and are one of the most crowned Night Heron, Nycticorax nycticorax often cited cases of adaptive radiation (Roths- hoactli; Short-eared Owl or Pueo, Asioflammeus child 1893-1900, Perkins 1903, Amadon 1950, sandwichensis). Is this variance in levels of spe- Raikow 1977, Freed et al. 1987a, James and Ol- ciation and phenotypic differentiation related son 1991, Tarr and Fleischer 1995, Fleischer et merely to the lengths of time that lineages have al. 1998). Several species of extinct, large, been evolving in the islands (Simon 1987, Car- HAWAIIAN BIRD MOLECULAR SYSTEMATICS--Fleischer aizd Mclntosh 53 FIGURE 1. Map of the main Hawaiian Islands (plus inset map of main and leeward Hawaiian Islands). Ages of the oldest rocks from the main islands based on K-Ar dating are noted. Maui-Nui is composed of the islands of Maui, Lgna‘i, Kaho‘olawe, and Moloka‘i, all of which were connected until about 0.3-0.4 Ma ago and again during more recentperiods of low sea level. son and Clague 1995)? Or are there other factors 1993, Fleischer et al. 1998). We then consider that have promoted stasis in some lineages and the origins and phylogenetic histories of each change in others, regardless of length of time in lineage within the avifauna, addressing exten- the islands? As noted above, the fossil record sive and minor radiations, well-differentiated provides little resolution of this question. Thus, single species, and undifferentiated (and likely estimates of the age of separation from ancestors recent) colonists. We also apply a molecular outside of the Hawaiian Archipelago, or the age clock approach to obtain rough estimates of the of a radiation within the islands, can only be maximum period of time that a lineage could inferred from molecular data. have existed in the Hawaiian Islands. The Hawaiian Islands and its avifauna are ex- tremely isolated from continental and other Pa- GEOLOGICAL HISTORY AND THE cific island avifaunas. This is likely the primary CALIBRATION OF MOLECULAR reason for the relatively low number of indepen- EVOLUTIONARY RATES dent taxonomic avian lineages that occur in the The Hawaiian Islands have an unusual geo- islands (Mayr 1943, Pratt 1979). While the total logical history (Clague and Dalrymple 1987, number of such lineages has been increased (and Walker 1990, Carson and Clague 1995; Fig. 1). continues to increase) from recent fossil findings They form as the Pacific Plate drifts northwest (Olson and James 1982a, 1991; James and Olson over a “hot spot” where magma extrudes from 1991), the islands still appear to have far fewer the earths’ mantle through the crust to build independent avian lineages than one might ex- huge shield volcanos (often to >4 km above sea pect for a tropical archipelago of this size and level).
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