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Mitochondrial Analysis of Gene Flow Between New Zealand Mallards (Anas Platyrhynchos) and Grey Ducks (A

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Mitochondrial Analysis of Gene Flow Between New Zealand Mallards (Anas Platyrhynchos) and Grey Ducks (A The Auk 111(4):970-978, 1994 MITOCHONDRIAL ANALYSIS OF GENE FLOW BETWEEN NEW ZEALAND MALLARDS (ANAS PLATYRHYNCHOS) AND GREY DUCKS (A. SUPERCILIOSA) JUDITH M. RHYMER,1'3 MURRAY J. WILLIAMS,2 AND MICHAEL J. BRAUN1 XLaboratoryof MolecularSystematics, Smithsonian Institution, MRC 534, Washington,D.C. 20560, USA; and 2Directorateof Scienceand Research, Department of Conservation, P.O. Box 10-420, Wellington,New Zealand ABSTP,•CT.--Oneof the more well-known examplesof hybridization in birds is the fre- quently documentedoccurrence between sexually dimorphic Mallards (Anasplatyrhynchos) and severalclosely related nondimorphic speciesin the mallard complex.In New Zealand, the Grey Duck (Anas superciliosasuperciliosa) is the indigenous, nondimorphic Mallardlike species,and extensive hybridization with introduced Mallards has been implicated in the populationdecline of Grey Ducks.Individuals from throughoutthe countrywere classified phenotypically as parentals or hybrids based on variation in plumage, bill color, and leg color.We confirmedspecies-specific mitochondrial DNA haplotypesby comparingrestriction- enzymefragment patterns in Grey Ducksand New ZealandMallards to thoseof PacificBlack Ducks (A. superciliosarogersi) from Australia and Mallards from North America, respectively. Our data indicatethat hybridizationhas led not only to introgressionof Grey Duck mtDNA into Mallard populations(the predicteddirection of gene flow), but also to significantin- trogressionof Mallard mtDNA into Grey Duck populations.Thus, the contentionthat hy- bridization between Mallards and nondimorphic speciesinvolves primarily Mallard males with femalesof the other speciesis not upheld for this examplefrom New Zealand. The speciationprocess appears to be undergoingreversal. Received I April 1993,accepted 2 July 1993. THE INCIDENCEOF interspecific and interge- Mallard/Mottled Duck (A. fulvigula)hybrids also neric hybridization in the order Anseriformes are being reportedin someareas of Florida (Ma- is higher than in any other orderof birds,reach- zourek and Gray 1994). In fact, the AOU (1983) ing 30 to 40% by some estimates(Grant and declared the Mexican Duck to be conspecific Grant 1992). In addition, a substantial propor- with the Mallard becauseof extensivehybrid- tion of interspecifichybrids (20%)in this order ization between them. have been reported to be fertile (Scherer and In New Zealand, the Grey Duck (A. superci- Hilsberg 1982),so there is potential for exten- liosa superciliosa)is the indigenous, nondi- sive gene flow and introgressionbetween some morphic, Mallardlike species.Grey Ducks are species. thoughtto have colonizedfrom Australia,like Amongthe morewell-known examples is the much of New Zealand's avifauna (Baker 1991), frequentlydocumented incidence of hybridiza- and the PacificBlack Duck (A. superciliosarogersi) tion betweensexually dimorphic Mallards (Anas in Australiais virtually identicalphenotypical- platyrhynchos)and several closelyrelated, non- ly to the New ZealandGrey Duck (Frith 1982). dimorphic species. For instance, in North Mallards were introduced by the Otago Accli- America,hybridization with Mallards hasbeen matization Societyinto the southern region of implicated as one factor in the population de- South Island, New Zealand in the mid-1800s cline of American Black Ducks (A. rubripes; from Europeangame-farm stock and into North Johnsgard1967, Heusmann 1974, Ankney et al. Island by the Auckland AcclimatizationSociety 1987), Hawaiian Ducks (A. wyvilliana;Griffin et in the 1930s from North America (Williams al. 1989), and Mexican Ducks (A. platyrhynchos 1981). diazi; Hubbard 1977). Increasing numbers of Over the last few decades, Mallard popula- tions have increaseddramatically, while Grey 3 Presentaddress: Department of BiologicalSci- Duck populationshave declined. Extensivehy- ences,Clemson University, Clemson,South Carolina bridization with Mallards, facilitatedby the loss 29634, USA. of natural habitatsto agriculture,has been im- 970 October1994] Mallardand Grey Duck Gene Flow 971 plicatedin the populationdecline of Grey Ducks this study,we soughtspecies-specific markers in a situationanalogous to thosein North Amer- for Mallards and Grey Ducksusing restriction- ica (Williams 1981,Gillespie 1985).By the early enzymeanalysis of mtDNA, a techniquethat is 1980s, levels of hybridization estimated from generallymore sensitivethan allozymeelectro- plumage variation had increasedto over 50%in phoresis.Our study focusedon the analysisof populations on South Island near Dunedin, pure Grey Ducksand Mallards togetherwith while the proportion of pure Grey Ducks had several individuals that had been classified as declined to lessthan 5% (Gillespie 1985). This hybrids on the basisof their morphological hasled to concernthat the Grey Duckmay even- characteristics. tually disappearas a separatespecies from New We also used the results to infer the direc- Zealand (Weller 1980,Gillespie 1985),as it has tionality of hybridization.If hybrid matingsoc- from the Marianas Islands. The so-called Mar- cur primarily between colorful Mallard males iana Mallard (A. oustaletiSalvadori) is generally and Grey Duck females,then the majority of consideredto be a hybrid betweenstray Mal- hybrid individuals should have a Grey Duck lard Ducksand A. superciliosa(Delacour and Mayr mitochondrial haplotype, since avian mtDNA 1945, Yamashina 1948; but see Reichel and is maternally inherited (Giles et al. 1980, Wa- Lemke 1994). tanabe et al. 1985). Although assortativemating appearsto pre- vail between Mallards and American Black METHODS Ducks in North America (E. Morton unpubl. data), and betweenMallards and A. superciliosa Samplecollection.--We sampled Mallard, Grey Duck, in Australia (Braithwaite and Miller 1975) and and hybridindividuals from North and SouthIslands New Zealand (Hitchmough et al. 1990), there of New Zealand. We also analyzed Mallards from is some experimental evidence that more col- North America(as part of a largerstudy of the mallard orful Mallard males outcompetedull-colored complexof waterfowl) and PacificBlack Ducks from males for mates(Brodsky et al. 1988). Ankney Australiato ensurethat we couldunequivocally iden- et al. (1987)also suggested that the majorityof tify the species-specificmtDNA haplotypesof the pa- hybrid matingsin North America may result rental species. Birdsshot by hunterswere collectedin May 1991 from forcedcopulations between Mallard males from localitiesthroughout the country, as part of a and BlackDuck femalesduring renesting. largerstudy by M.J.W. to assessthe extentof hybrid- Several studies have tried to estimate the ex- ization in New Zealand. Samplesfrom six areas on tent of hybridization and introgressionbe- North Island(Lake Whangape, Cambridge, Ohakune, tween Mallards and one or another of the non- Wairoa, Wanganui, Lake Wairarapa)and one area on dimorphicspecies by qualitativeassessments of South Island (Lake Ellesmere) were selected for anal- phenotypic variation (Braithwaite and Miller ysisin thisinitial study(Fig. 1).Samples were selected 1975, Gillespie 1985, Heusmann 1974; Kirby, on the basisof phenotypiccharacters to include 12 U.S. Fishand Wildlife Serviceunpubl. report), Grey Ducks,9 Mallards,8 Grey Duck-like hybrids, but it is difficult to distinguishhybrids mor- and 14 Mallardlike hybrids.It hasbeen observedthat hybridstend to be Grey Duck-like or Mallardlike in phologicallyafter more than one generationof appearance(Yamashina 1948, Weller 1980). backcrossingto a parentalspecies (Williams and Heart tissue from these birds was stored in 70% Roderick1973, Rhymer unpubl. data). In ad- ethanol and shipped at room temperature. We also dition to the use of phenotypiccharacters to analyzedheart and liver tissuefrom additionalbirds estimatelevels of gene flow, somebiochemical that had been collected between 1986 and 1991 and techniqueshave been applied to the Mallard storedat -80øC. Thesesamples included seven Grey group. However, no species-specificmarkers Ducks(Pohangina River; Apiti, Orua River), six Mal- have been found to distinguishMallards from lards (Apiti), and two Grey Duck-like hybrids (Ron- American BlackDucks using allozyme electro- gotea;Apiti), all from North Island.We alsoanalyzed phoresis(Ankney et al. 1986) or restriction-en- tissueand blood samplesof North AmericanMallards and blood samplesof 10 Pacific Black Ducks. The zyme analysisof mitochondrialDNA (mtDNA; Pacific Black Ducks were chosen from an area near Avise et al. 1990). Canberra in eastern Australia (where no Mallards are Allozyme studiesalso have been unsuccess- found) to comparewith our pure Grey Duck samples. ful in separatingMallards from A. superciliosa Phenotypicscoring.--Variation in some phenotypic both in Australia and New Zealand (Braithwaite charactersof each bird was quantified, using criteria and Miller 1975, Hitchmough et al. 1990). In similar to those outlined by Gillespie (1985) and 972 R•M•, WILLIAMS,.•_ND BP,•UN [Auk, Vol. 111 TASLE1. Phenotypiccriteria used to scorehead, wing and leg characteristicsof Grey Ducksand Mallards. NORTH ISLAND Face (0) Two black stripes,the upper superciliarystripe of uniform width and extending well beyond eye; lower stripe tapering from gape to below eye and Cambridge giving way to mottled cheek;clean creamstripe be- tween eye and crown, throat and face cream. Dhakune (1) Two blackstripes, upper stripe as described above, Wanganui lower stripe merging with mottled face midway be- tween bill and eye, clean cream stripe between eye Rongotea -- Apiti and crown; face and cheek
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