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'Iolecular Systematics and Biogeography of the I Awaiian Avifauna

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'Iolecular Systematics and Biogeography of the I Awaiian Avifauna iildies in A\.ian Biology No. 22:s 1-60, 2001 'IOLECULAR SYSTEMATICS AND BIOGEOGRAPHY OF THE I AWAIIAN AVIFAUNA 4tst. The Hawaiian avit'auna is exceptio~ialfor it> high proportion of endemic tuxti. its spectac- ular adaptive radiations. and it\ le\el of human induced extinction. Little has been known about the ph>logenetic relationship\. geographical origins, and timing of colonization of indi\idual avian lin- eage> until recently. Here we review the results of niolecular studies that address these topics. Mo- lecular data (rnwtly mitochondrial DNA sequences) are a~ailablefor I4 of the 21 or more lineage5 of Ha~vaiianbirds. We briefly review results of pliylo~,eneticanalyses of these data for lineages that have experienced major and minor rad~ations.and for s~ngledifferentiated species and probable recent coloni\ts. U'hen pos\iblr. we determine the mainland species that are genetically most chely related. We find ev~denccthat roughlq half of the ;,?I linragtx colonixd from North America; not eyen a quarter appear to have come from South Pacitic Islands. Our data also provide little e~idencethat Hawaiian bird lineage\ predate the formation of the cun-ent set of main islands (i.e.. :-5 Ma). a\ has been found for Hawaiian I)t.o\opl~ilr~anti lobeliads. Kc,! Worrls: xlapti~eradiation: biogeography; Hawaiian abifauna: mitochondrial DNA; molecular systematics :I 1943 Ernst Mayr published a short paper in tially mislead on issues of common ancestry \.ia -,Ice Condor summarizing his hypotheses about homoplasy. DNA sequences, on the other hand, he geographic origins and closest living rela- while obviously not evolving in a perfect clock- . I\es of each known lineage in the Hawaiian avi- like fashion (see below), do change over time, I Iuna. Mayr (1943) concluded that half of 14 and evolve more continuously than morphology. !,ypothesized colonizations were of American Also, with the exception of a relatively few non- ,,rigin and only two lineages arose from Poly- synonymous changes within protein sequences, ,csia. Therefore, although Hawai'i is considered they generally evolve via mutation and drift (Nei ,art of the "Polynesian Region" because most 1987, Avise 1994), and are not as subject to ho- )f its biota and its human inhabitants had Pol- moplasy via convergence or stasis as are mor- nesian ancestors. in terms of its birds Hawai'i phological or other characters. Thus major adap- ,s in the Nearctic Region. Since Mayr's paper. tive shjfts in, for example, the bills of Hawaiian ,~~therauthors have posited similar systematic hy- honeycreepers, may occur within some lineages ,)otheses and biogeographic scenarios based on (e.g., to thin and decurved in the nectarivorous unorphological, ecological, and distributional 'I'iwi, Vestiaria coccinea), while not in others ,lata (e.g.. Amadon 1950, Pratt 1979. Berger (e.g., conical and finchlike in the Laysan Finch, 1 98 1 ). Paleontology has offered only minor res- Telc.spiza cantans), in spite of an identical olution of the relationships of ancestral lineages amount of time since evolving from their puta- ~)rthe timing of speciation events; although tively "finch-billed" common ancestor. There there is an excellent Holocene fossil record in are methods for detecting symplesiomorphic Hawai'i (Olson and James 1982a. 1991: James versus synapomorphic characters in phylogenet- and Olson 199 1). 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 >().I2 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., Tarr 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 1~11- tive responses subject to natural or sexual selec- ume; E'axinos 1998, Sorenson et al. 1999, tion (i.e.. as part of the process of adaptive ra- Fleischer et al. in press, Rhymer this \wlurnr; C. diation), and they do not usually show constancy Tam, E. Paxinos. B. Slikas, H. James, S. Olson. in their rates of change. Thus they can poten- A. Cooper. and R. Fleischer, unpubl. data). 52 STUDIES IN AVIAN BIOLOGY NO. 22 TABI,E 1. THEELEMENTS OF THE HAWAIIANAVIFAUNA Non -pnsserifortrre.s: Ibises Plataleidae N.A. minor radiation, flight- less. Apterihist Night Heron Ardeidae N.A. recent colonist, .Vytic.o- rux nycticwrux Moa-nalos Anatidae W. Hemisphere minor radiation?, 3 flightless duck gen- era* True Geese Anatldae 23 N.A. minor radiation, Brcrn- tci,te Modern Ducks Anatldae 2 N.A. and Asia 1 -t differentiated. 1 re- cent colonist, Anns e Porxuztr Ralls Rallldae 2 12 Pacifichnknown major radiation?, 22 colonizationsf Large rallld5 Rallidae 2 N.A.? recent colonists", coot and moorhen Black-necked S trlt Recurv~rostndae 1 N.A. recent colonist, Himun- topus knudsrni e Eagle Acciptridae I Asia recent colonist. Hcrliuee- tus Iruc~ophr~st Buleo Acciptridae N.A. differentiated. B~cteo.so- litarius e Harrier Acciptridae Unknown differentiated. Circus dos.venust Long-legged Owls Strigidae Unknown minor radiation, Grril1i.r- tri.x spp. 4i Short-eared Owl Strigidae Unknown recent colonist. Asio Pas.ser~fi-,rmes: Crows Corvidae Unknown minor radiation'?, Conus spp., 3t, 1 e Mi llerbird Sylviidae South Pacific differentiated, Acrnce- phalus familiaris e 'Elepaio M yiagridae Australasia differentiated, C'hnsiem- pis sandwichensis Thrushes Muscicapidae W. Hemisphere minor radiation, Myt~d- estes spp.. 3+, 1 e Honeyeaters Meliphagidae 26 South Pacific minor radiation, Moho spp.. Chcietoptila. allt Honeycreepers Fringillidae 250 Asia or N.A.? major radiation, drepani- dines, most? or e >21 lineages 13 ,filmilies 2 102 species " Sumber of specles w~thmeach Iineagelfnm~ly.based on James and Ol~on(1991). Olson and Jameh (1991). and H. Jamv (per\, comm.) N.A. = North Arnenca; W = West. :denotes at least wme member\ extmct. e denotes at least wrne 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 ratitelgrazing 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- hoacrli; Short-eared Owl or Pueo, AsioJarnrneus child 1893-1900, Perkins 1903, Amadon 1950, sandwichensis). Is this variance in levels of spe- Raikow 1977, Freed et al. 1987a, James and 01- 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-Fleischrr atd Mcltzto.slz 111Main Hawaiian Islands v !-IGURE 1. Map of the main Hawaiian Islands (plus inset map of main and leeward Hawaiian Islands). Apes the oldest rocks from the main i4lands based on K-Ar dating are noted. Maui-Nui is composed of the i5lancls '1 Maui. Liina'i. Kaho'olnwe. ancl Moloka'i. 311 of uhich were connected ~~ntilabout 0.3-0.4 Ma ago and again ii~~~ngmore recent perlocis of 10%' ae't level anand Clague 1995)? Or are there other factors 1993, Fleischer et al. 1998). We then consider !hat have promoted stasis in some lineages and the origins and phylogenetic histories of each .hange in others. regardless of length of time in lineage within the avifauna, addressing exten- ihe islands'? As noted above, the fossil record sive and minor radiations, well-differentiated ;~rovideslittle resolution of this question. Thus, single species, and undifferentiated (and likely $:.;timates of the age of separation from ancestors recent) colonists. We also apply a molecular ,wtside 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 ~nferredfrom 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 citic 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 earth's mantle through the crust to build independent avian lineages than one might ex- huge shield volcanos (often to >4 krn above sea pect for a tropical archipelago of this size and level).
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