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Affinities of the Hawaiian Goose Based on Two Types of Mitochondrial Dna Data

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Affinities of the Hawaiian Goose Based on Two Types of Mitochondrial Dna Data AFFINITIES OF THE HAWAIIAN GOOSE BASED ON TWO TYPES OF MITOCHONDRIAL DNA DATA THOMAS W. QUINN, • GERALD F. SHIELDS,2 AND ALLAN C. WILSON • •Divisionof Biochemistryand Molecular Biology, University of California,Berkeley, California 94720 USA, and 2Instituteof ArcticBiology, University of Alaska,Fairbanks, Alaska 99775-0180 USA ABSTRACT.--Wecompared restriction fragments of mitochondrial DNA and sequencesof portionsof the cytochromeb gene of the following: the Hawaiian Goose(Nesochen sandvi- censis),five subspeciesof the CanadaGoose (Branta canadensis), the PacificBlack Brant (B. berniclanigricans), and the Emperor Goose(Chen canagica). Both comparisonssupport the association of the Hawaiian Goose and the Canada Goose as sister taxa as well as the association of all four large-bodiedsubspecies of CanadaGeese as separatefrom the one small-bodied subspeciesanalyzed here. Bootstrapand winning-sitestests show theseassociations to be statisticallysignificant. The amountof sequencedivergence implies that Hawaiian andCanada Geesediverged from a common ancestorless than three million years ago and that this divergencepreceded the divergenceof large- and small-bodiedCanada Geese only slightly, if at all. Therefore,we suggesta North American origin for the Hawaiian Goose.Received 2 July 1990,accepted 27 December1990. THE H^W^nAN Goose (Nesochensandvicensis), Both restriction and sequencingmethods of or Nene as it is called locally,is the only extant characterizingmtDNA yield traits that can be speciesof gooseendemic to Hawaii, yet its an- subjectedto parsimony analysis (e.g. Edwards cestry and geographicorigin have never been and Wilson 1990), allowing branching orders established.Within the present century, the to be testedwithout strict assumptionsof clock- goosesubfamily Anserinae has routinely been like rates of change.We comparedrestriction divided into at least five genera (Anser,Branta, fragmentsof whole mtDNA and DNA sequenc- Chen,Nesochen, and Philacte)(Johnsgard 1978, es of portions of a specificmitochondrial gene Bellrose 1980, Palmer 1976). There is disagree- of the HawaiianGoose with thoseof othergeese. ment as to whether Anser should be split into Geographic considerations influenced our several genera (e.g. Anser,Chen, and Philacte). choice of the other geese. Becauseour intent Moreover, taxonomistshave been equivocalre- was to determine the sister taxon of the Ha- garding the allocation of the Hawaiian Goose. waiian Goose and to estimate when and where Some have emphasizedmorphological differ- it may have arisen, we centered attention on encesfrom the other geeseby placing it in Ne- those geesethat inhabit western North Amer- sochen.Others have emphasizedobvious simi- ica, the Aleutian Islands, and northeastern Asia, laritiesby placingit in Branta.Berger (1972) has and that had not alreadybeen studiedby Shields proposed that Nesochenis closely related to and Wilson (1987a, b). Branta and that it arose specifically from the Canada Goose (Branta canadensis)after one or MATERIALS AND METHODS more migration events from North America. We obtainedapproximately 20 g of hearttissue from This hypothesishas awaited testing with mod- an adult Hawaiian Goose that had died at the Ho- ern methods of phylogenetic analysis. nolulu Zoo. The tissuewas immediatelyminced and Information preserved in the DNA of this maintained in cold (4øC) buffer (mannitol, sucrose, speciesmay be used to infer its relatednessto Tris-EDTA) during subsequenttransport to Fair- other extant speciesof geese. Mitochondrial banks. The combined methods of Shields and Wilson DNA (mtDNA) has been valuable for phylo- (1987a) and Carr and Griffith (1987) were used to ob- genetic reconstructionsbecause of its ease of tain purified mtDNA from this tissueand from hearts isolation, rapid evolutionary change, maternal and kidneys of a single small-bodiedCanada Goose (Taverner's Canada Goose,Branta canadensis taverneri); inheritance and apparent lack of recombination four large-bodiedCanada Geese (the LesserCanada (Wilson et al. 1985). This approach has been Goose,B.c. parvipes;the Dusky Canada Goose,B.c. particularly useful for studiesof phylogeny of occidentalis;the VancouverCanada Goose, B.c. fulva; maternal lineages in waterfowl (Kessler and the WesternCanada Goose, B.c. moffitti);the Pacific Avise 1984; Shields and Wilson 1987a, b; Van BlackBrant, B. bernicla nigricans; and the Emperor Goose, Wagner and Baker 1990;also see Discussion). Chencanagica (also known as Philactecanagica). We 585 The Auk 108:585-593. July 1991 586 QUINN,SHIELDS, AND WILSON [Auk, Vol. 108 TABLE1. Fragmentpatterns of mtDNAs from eight taxa of geese:Nesochen sandvicensis, Branta canadensis taverneri,B.c. parvipes,B.c. occidentalis,B.c. fulva, B.c. moffitti,B. bernicla,and Chencanagica. Fragment patternsa Restriction B.c. B. C. enzyme N. sand. B. c. tav. B. c. par. B. c. occ. B. c. ful. moff. bernicla canagica AvaI A A A A A A B C AvaII A A A A A A B C BamHI A A A A A A A B BanI A B C/D/E C C C F G BglII A A A A A A B A BstUI A B C C D C E F ClaI A A A A A A B C EcoRI A A A A A A B C HhaI A B A A A A C D HincII A A A A A A B C HindIII A B A A A A C A HinfI A B B B B B C D NarI A A A / B B B B C D NciI A A A A A A B C NcoI A B B B B B C D PvuII A B A A A A C D SpeI A B B B B B C D StyI A B C C C C D E XbaI A A B B B B A C completelist of all fragmentsizes is availableupon request. were not concernedabout larger samplesizes because (northern Atlantic and Eurasia,respectively) and past intrasubspecificvariation in CanadaGeese and Brant distributions(never in easternAsia) make it unlikely is extremelylow (Shieldsand Wilson 1987b;Shields that they could have flown to Hawaii. 1990; Van Wagner and Baker 1990). Moreover, the mtDNA diversity among Hawaiian Geesemust have RESTRICTION FRAGMENT ANALYSIS beenreduced drastically when its populationcrashed to only 17 individualsin the 1940s(Kear and Berger We comparedfragment patterns of mtDNA of the 1980).While two other extant geeseof the genusBran- Hawaiian Goose(Table 1) to those of the other taxa ta (the BarnacleGoose, B. leucopsis,and the Red-breast- of geesein severalways. We firstcompared restriction ed Goose,B. ruficollis)could have been included in fragmentsof mtDNA from the Hawaiian Goosein the this study, they are poor candidatesas ancestorsof samegels with thoseof the geeseidentified above. the Hawaiian Goosebecause their breeding ranges Thenwe comparedthese fragment patterns with those TABLE2. Extent of sequencedifference (percent) for taxa of geesebased on restriction fragment analysisof mtDNA. a Species:Nesochen sandvicensis, Branta canadensis ssp., Branta bernicla, and Chencanagica. 1 2 3 4 5 6 7 8 9 10 11 1. N. sandvicensis -- 1.44 a 1.44 a 1.44 1.60 1.64 1.64 1.64 1.64 5.85 4.87 2. B.c. leucopareia -- 0.06c 0.11c 1.28a 1.31a 1.27 1.00c 1.30c 6.14 5.77 3. B.c. minima -- 0.05 c 1.28 a 1.31 a 1.27 0.80 c 1.10 • 6.14 5.77 4. B.c. taverneri -- 1.28 1.31 1.27 0.90 1.12 c 6.14 5.77 5. B.c. parvipes -- 0.08 0.20 0.16 0.26a 6.02 5.54 6. B.c. occidentalis -- 0.14 0.17 0.26 a 6.05 5.33 7. B.c. fulva -- 0.14 0.26a 6.11 5.32 8. B.c. moffitti -- 0.26c 6.05 5.33 9. B.c. maxima -- &10 b 5.33 10. B. bernicla -- 5.99 11. C. canagica -- • Overall thesevalues tend to be lower than comparableestimates (Van Wagner and Baker1990), probably because the presentanalysis uses mainly 6-basecutters. bValue computedin Shieldsand Wilson (1987a). cValues computedin Shieldsand Wilson (1987b). a Values averaged. July1991] HawaiianGoose Mitochondrial DNA 587 found by Shieldsand Wilson (1987a,b) for the Aleu- tian CanadaGoose (B.c. leucopareia),the Cackling Can- ada Goose (B.c. minima), Taverner's Canada Goose, the Western Canada Goose, the Giant Canada Goose (B.c. maxima),and the Pacific Black Brant. The 19 enzymesAval, Avail, BamHI, BanI, BglII, BstUI, ClaI, EcoRI, HhaI, HinclI, HindIII, HinfI, NarI, NciI, NcoI, PvuII, SpeI,StyI and XbaI were used in the first seriesof fragment comparisons.Restriction en- donucleasedigestions were carried out under the con- ditions specifiedby the vendor (New England Bio- labs.). Five of these enzymes (BstUI, HhaI, HindIII, I PvuII, and XbaI) unequivocally differentiate large- bodied from small-bodied Canada Geese (Shields and 4260 Wilson 1987b),and thus they were included here as potential phylogenetically informative enzymes rel- ative to the Hawaiian Goose. The 22 restrictionenzymes used in the secondcom- parison are listed in Shields and Wilson (1987a, b); 12 of thesecoincide with enzymesused in the first 2250 comparison.Divergence values for both data setswere computedfrom the fraction of sharedfragments ac- 1960 cording to equation 20 of Nei and Li (1979). In cases where pairwise comparisonswere not possible,we usedaverage values among small-bodied Canada Geese (first comparison)and among large-bodied Canada Geese(second comparison) to accountfor missingdata (Table 2). For phylogeneticanalysis, we inferred re- striction sites from the fragment data for the taxa studied here and used the exhaustive search algo- rithm of the PAUP (PhylogeneticAnalysis Using Par- simony) computerprogram (Swofford 1989). Finally, bootstrap (Felsenstein 1985) and winning-sites tests were applied to the tree arrangementsto test for sig- nificance(Shields and Wilson 1987b,Prager and Wil- son 1988). 600 GENE AMPLIFICATIONSAND DIRECT SEQUENCING We usedthe methodsof Gyllenstenand Eriich (1988) and Kocheret al. (1989) to amplify and sequencepor- tionsof the cytochromeb genesof the Hawaiian Goose, Taverner's Canada Goose, the Lesser Canada Goose, the Dusky Canada Goose, the Vancouver Canada Goose, the Western Canada Goose, the Pacific Black Brant, and the Emperor Goose.Two primer pairs were Fig.
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