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A Partial Classification of Waterfowl (Anatidae) Based on Single-Copy Dna

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A PARTIAL CLASSIFICATION OF WATERFOWL (ANATIDAE) BASED ON SINGLE-COPY DNA CORT S. MADSEN, KEVIN P. MCHUGH, AND SIWO R. DE KLOET Instituteof MolecularBiophysics, The Florida State University, Tallahassee, Florida 32306 USA ABSTR^CT.--Single-copyDNA-DNA hybridizationwas used to establishphylogenetic re- lationshipsamong 13 speciesof waterfowl (Anatidae) chosenfrom 10 tribes. On the basisof UPGMA clusteringof ATtodistances, we suggestthat the tribes Anatini, Aythyini, Tadornini, Mergini, and Cairinini diverged more recently than the Anserini, Stictonettini,Oxyurini, Dendrocygnini,and Anseranatini.The FreckledDuck (Stictonettanaevosa, tribe Stictonettini) is only distantlyrelated to the other Anatidae.Presumably the lineage divergedvery early. The sheldgeese(tribe Tadornini) and the true geese(Anserini) are only remotely related. The Oxyurini, consideredto be in the subfamilyAnatinae, is remotely related to the other Anatidae. The Dendrocygnini form an isolatedtribe with no closerelationship to the swans and geese(subfamily Anserinae). We found that the screamers(Anhimidae) are distantly related to the Anatidae. A method to estimate missing cells in a data matrix of pairwise distancesis presented. ReceivedI May 1987,accepted 16 February1988. RECENTLY,nucleic acid sequenceanalysis has up about 10-40% of the total DNA (Eden et al. been usedto estimaterelationships of many or- 1978) but containsonly a small percentageof ganisms. The analysis can include direct se- the total sequencediversity. The remaining60- quencing of individual cloned genes or gene 90%are unique sequencesand representabout products, restriction enzyme analysis of ho- 98% of the total sequencecomplexity (Sibley mologousDNA fragments,and generalanalysis and Ahlquist 1983). of unique DNA by single-copyDNA-DNA hy- The mostconvenient procedurefor sequence bridization. In higher eukaryotes,perhaps only comparisonof total DNA of different species 5-10% of the DNA (including gene-codingre- involves measurementof the thermal stability gions and a small fraction of the single-copy of reannealed heteroduplex single-stranded DNA) is under selection (Britten 1986). The ma- DNA. Becauserepetitive DNA sequencesrean- jor proportion of DNA, unique as well as re- heal first, such sequencesmight contribute in petitive, consistsof nucleotide sequencesthat a disproportionateway to the thermal stability are never expressedas proteins, have no known of resultingduplexes (Sibley and Ahlquist 1983). function, and are therefore presumablyfree to For this reason the repetitive DNA fraction is evolve (Britten 1986). usually removed. Nevertheless, repetitive se- Although both single-copyand repeatedDNA quences,because of rapid evolution, can also comparisonshave been used in studiesof phy- provide valuable data on the relationship of logenetic relationships in birds (Shields and recently evolved species (Gillespie 1977, Ar- Strauss1975; Eden et al. 1978; Sibley and Ahl- nason and Widegren 1986). quist 1982, 1983), the total DNA of higher eu- Although the fossil record of birds is incom- karyotesis composedof many subsetsof DNA plete, that of waterfowl appears better than in that show varying degreesof reiteration (Brit- many other families (Olson and Feduccia1980). ten and Kohne 1968). These include the ex- Paleontological investigations show that the tremes of specific sequences,present as only majorwaterfowl radiation probablytook place one copy per genome through sequencesre- within the last 60 million years (Delacour and peated millions of times. The repeated families Mayr 1945, Olson and Feduccia 1980). These show sequenceas well as copy-number evolu- eventsfall within the sensitivityrange of DNA- tion. Sequencesthat occur only a few times in DNA hybridization proposed by Sibley and one organism may occur many times even in a Ahlquist (1983). closelyrelated species(Zwiebel et al. 1982).De- We propose a phylogeny of the Anatidae pending on reassociationconditions, the re- basedon single-copyDNA relationshipsamong petitive DNA fraction in bird genomes makes samplesfrom 13 of the 148 speciesof waterfowl 452 The Auk 105:452-459. July 1988 July1988] WaterfowlPhylogeny 453 belonging to 10 traditionally defined tribes. after the addition of ammonium acetate to a final Single-copyDNA sequencerelationships among concentrationof 2.5 M. After briefly washing with these waterfowl and three other avian species 70% ethanol, the DNA was dissolved in TE buffer and (Northern Screamer, Chauna chavaria; Spur- the concentrationadjusted to 1.0 mg/ml. winged Plover, Vanellusspinosus; and domestic Isolationof single-copyDNA.--A DNA fraction en- riched for single-copymaterial was isolatedas de- chicken, Gallusgallus) were investigated. scribed by Sibley and Ahlquist (1983). DNA was shearedby sonicationinto fragmentswith an average MATERIALS AND METHODS length of 500 nucleotides.Fragment size was deter- minedby electrophoreticcomparison with calibrated Material camefrom Mergus Waterfowl Farms(Tal- markers. The DNA was denatured by immersion in lahassee, Florida). Species were the White-faced boiling water for 10 min and reannealedat 50øCin Whistling-Duck(WW) (Dendrocygnaviduata), Plumed 0.48 M sodium phosphatebuffer (pFI 7.0) to a Cot of Whistling-Duck (D. eytoni),Bar-headed Goose (BG) 1,000.A single strandedfraction was isolatedby hy- (Anserindicus), Red-breasted Goose (Branta ruficollis), droxyapatitechromatography at 50øC.The fraction RuddyDuck (RD) (Oxyurajamaicensis), Orinoco Goose wasdialyzed against TE buffer,concentrated with iso- (OG) (Neochenjubata), Hooded Merganser(HM) (Lo- butanol (Maniatis et al. 1982), and precipitated with phodytescucullatus), Wood Duck (WD) (Aix sponsa), ethanol. After washing with 70% ethanol the DNA White-eyed Pochard(WP) (Aythya nyroca),Mallard was dissolved in TE buffer and the concentration ad- (ML) (Anasplatyrhynchos), White-cheeked Pintall (WC) justed to 1.0 mg/ml. (Anasbahamensis), and the nonanatidSpur-winged Radio-labelingofsingle-copy DNA.--Single-copy DNA Plover and domesticchicken. Northern Screamer(SC) was labeledwith 32P at the 5' terminusby incubation materialcame from Mary Dam (HainesCity, Florida), with polynucleotidekinase and gamma-labeledATP 32. the Magpie Goose(MG) (Anseranassemipalmata) and A 5' terminuslabeling kit wasobtained from Bethesda Trumpeter Swan (TS) (Cygnusbuccinator) from Mi- ResearchLaboratories and used accordingto the in- chaelLubbock (Sylva, North Carolina),and the Freck- structionsprovided by the manufacturer.The specific led Duck (FD) (Stictonettanaevosa) from the Wildfowl activity of the radio-labeledDNA preparedby this Trust (Slimbridge,United Kingdom). Gamma-labeled procedureaveraged 5 x 106counts/•g of DNA. The ATP 32was obtained from ICN (Irvine, California). labeled DNA was freed of unincorporated labeled Isolationof DNA.--DNA was isolatedfrom blood ATP by the spin-column technique (Maniatis et al. cells by a procedure modified from Blin and Stafford 1982). The maximum amount of unincorporated la- (1976). Blood was obtained from a wing vein and beled ATP contamination was less than 3%. Terminal collectedin a heparinizedsyringe. After one-folddi- labeling was substitutedfor iodination (Sibley and lution with 0.15 M NaC1 containing 0.05 M EDTA at Ahlquist 1983) for safety reasons. pH 7.6 (buffer A), cells were collectedby centrifu- Hybridizationof single-copytracer DNA with driver gation, resuspendedin 25 volumes of buffer A, and DNA.--Hybrids were formed from a mixture com- lysedby the additionof 0.3%sodium dodecyl sulfate. posed of 1 part (=200 ng) radio-labeled single-copy An equal volume (with respectto the total lysate)of DNA and 1,000parts (=200 •g) sheared,whole DNA redistilled phenol, equilibrated with 0.1 M Tris-HCL (Sibleyand Ahlquist 1983).Hybrids were denatured buffer pH 9.0, was added, and the mixture was shaken by immersion in boiling water for 10 min, precipi- in a gyrotory waterbathovernight at room tempera- tated with ethanol, and redissolved in 0.5 M sodium ture (25øC).After the addition of one-half volume of phosphate(pH 7.0). Reannealingwas carried out at chloroform,the phaseswere separatedby centrifu- 60øC until a Cot of 8,000 was reached. The formation gation, the aqueous phase collected, and the crude of double-strandedhybrid DNA was analyzed by DNA precipitatedby the addition of an equal volume thermal elution from hydroxyapatite.Thermal elu- of absolute ethanol. The DNA was washed with 70% tion columns were submergedwithin an insulated ethanol and dissolvedin TE (0.01 M Tris-HCL buffer column box connectedto a Haacke temperature-con- pH 7.6, 0.001 M sodium EDTA) (5 ml/ml original trolled (ñ0.1øC) circulating waterbath. After appli- blood). After completesolution was obtained,0.5 ml cationof the samplesto the column (200 •g of DNA/ of 1.0 M Tris-HCL buffer pH 8.0 was added followed ml of hydroxyapatite)at 55øCin 0.03 M sodiumphos- by 100 •g of pancreaticribonuclease. The mixture was phate, the column was washed with 40 ml of 0.12 M incubated for 30 min at 37øC,5 mg of pronasewas sodium phosphate (pH 7.0) to remove the unbound added,followed immediately by 0.2ml of 10%sodium tracer. The last fraction of the wash (5 ml) was counted dodecyl sulfate, and the solution was incubated for 2 in a liquid-scintillationcounter, and radioactivitywas h at 60øC.The mixturewas againdeproteinized by determined to be no higher than the normal back- shaking overnight with an equal volume of phenol ground,indicating that the unboundtracer was elut- saturatedwith 0.1 M Tris-HCL buffer pH 9.0, the ed from the column.At eachof
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