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Phylogeny of the Cranes (Aves: Gruidae) As Deduced from Dna-Dna Hybridization and Albumin Micro-Complement Fixation Analyses

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Phylogeny of the Cranes (Aves: Gruidae) As Deduced from Dna-Dna Hybridization and Albumin Micro-Complement Fixation Analyses PHYLOGENY OF THE CRANES (AVES: GRUIDAE) AS DEDUCED FROM DNA-DNA HYBRIDIZATION AND ALBUMIN MICRO-COMPLEMENT FIXATION ANALYSES JAMESL. INGOLD?3 JACKC. VAUGHN,1 SHELDON I. GUTTMAN, • AND LINDA R. MAXSON 2 •Departmentof Zoology,Miami University,Oxford, Ohio 45056 USA, and 2Departmentof Biology,Pennsylvania State University, University Park, Pennsylvania 16802 USA ABSTRACT.--Reassociationkinetic analysisof nuclear DNAs from Balearicapavonina (Black- crowned Crane) and Grusleucogeranus (Siberian Crane) shows that the nuclear genome of each containsat least 75%single-copy sequences. The kinetic data show the haploid genome of each speciesto be 1.0-1.5 pg. Neither DNA-DNA hybridization of single-copynuclear sequencesunder conditions of reducedstringency nor albumin micro-complementfixation (MC'F) separatedthe three crane generaGrus, Anthropoides, or Bugeranusin our experiments.These three generawere separable from Balearicaby both techniques.The DNA and MC'F results compare favorably with a parallel electrophoretic study. We conclude that Balearicaand Grusseparated between 10.0 and 6.2 MYBP (million years before present),as determined from MC'F and electrophoretic data, which is consistentwith fossil evidence for cranes.Received 7 November1988, accepted 3 May 1989. THECRANES (Aves: Gruidae) are a widely dis- ecologicalniches. The proper taxonomicposi- tributed group of 15 species in four genera tion of the Siberian Crane is of intense interest (Johnsgard1983). Interest in the craneshas in- (Archibald pers. comm.) because it and the creasedas many natural populations have be- Whooping Crane are endangeredin the wild. come endangered. Recent systematicinvesti- Cross-fosteringand possiblehybridization be- gationsexamined the unisoncall asa taxonomic tween species make information on relation- character (Archibald 1976a, b), a variety of ex- ships important. ternal morphological and skeletal characters There has also been controversyregarding (Wood 1979),and proteinsusing starch gel elec- composition of the genus Balearica(crowned trophoresis(Ingold et al. 1987a,b). cranes).Some investigators(White 1965, Snow Comparison of Wood's and Archibald's taxo- 1978) have suggestedthat Balearicarepresents nomic schemes indicates that the Siberian Crane one specieswith four well-defined subspecies, (Grusleucogeranus) clusters with the genus Bu- whereas Walkinshaw (1964) maintained that geranusand not with Grus.Wood (1979) found there are two species,each of which consistsof the Siberian Crane to be very similar to the two well-defined subspecies.The studiesof Ar- Whooping Crane (G. americana)in external fea- chibald (1976a),Wood (1979), and Ingold et al. tures but more similar to the Wattled Crane (1987b) provide strong support for Walkin- (Bugeranuscarunculatus) in skeletal characters.In shaw's (1964) contention that two speciesof Bal- contrast, the Siberian Crane is more similar earicaare distinct and not subspecies. electrophoreticallyto the WhoopingCrane than The study of this family offersan exceptional it is to the Wattled Crane (Ingold et al. 1987a). opportunity for the comparisonand evaluation Wood (1979) attributed the similarity between of variousmolecular techniques commonly uti- the Siberian and Whooping cranesto conver- lized in studying phylogenetic relationships. gence that resulted from selectionin similar We present data from DNA-DNA hybridization and albumin micro-complementfixation (MC'F) to measuregenetic divergence among 14 species $ Presentaddress: Department of Biology,Franklin of cranes and compare our data with results and Marshall College, Lancaster,Pennsylvania 17604 derived by electrophoretictechniques (Ingold USA. et al. 1987a). We find that all three of these 595 The Auk 106: 595-602. October 1989 596 INGOLDET AL. [Auk, Vol. 106 diverse experimental approachesproduce con- ried out on 0.3 g hydroxylapatite(HAP, Bio-Rad)col- gruent patterns of evolutionary relationships. umnswhich had previouslybeen treatedwith 100 of sonicated,denatured salmon sperm DNA to block all irreversibleDNA binding sites.Single-stranded METHODS single-copyDNAs were eluted with 0.12 M sodium phosphatebuffer (PB)at 60øC,after a 0.03 M PB wash Materials.--We studied 9 speciesof Grus,1 species step. The single-copyprobes were examinedfor pos- of Bugeranus,and 2 specieseach of Balearicaand An- siblecontamination with repetitiveor snap-backse- thropoides(Appendix). Most were captiveindividuals quences(Galau et al. 1976) and for their ability to housed at the International Crane Foundation, Bar- form stableduplexes, by hybridization of probesto aboo, Wisconsin;the specimensof G. americana,how- unlabeledhomoduplex nuclear DNAs in excess(driv- ever, were from the captiveflock at the U.S. Fish and er DNA) at Cotvalues of ca.50-5,000 at a driver/probe Wildlife PatuxentResearch Center, Laurel, Maryland. ratio of about 1000:1. House Sparrows(Passer domesticus) and CommonYel- Hybridization and DNA fractionation by thermal lowthroats(Geothlypis trichas), used as outgroupsfor hydroxylapatitechromatography.--Homoduplex and the DNA-DNA hybridization and MC'F, respectively, heteroduplexhybrids were formedby mixing labeled were collectednear Oxford, Butler County, Ohio. and unlabeledDNA at a driver/probe ratio of 1,000: DNA isolation.--Blood was collected from two in- 1. Two-hybridizationreactions were performed for dividuals in each of 15 species(Table 1). High mo- each speciespair comparison(30 comparisons).We lecularweight DNA wasobtained from the combined were limited to small sample sizes becauseof the erythrocytenuclei of both individuals using a phenol small amounts of DNA available from these endan- extractionprocedure (Vaughn et al. 1982),which in- gered birds. Reactionmixtures were sealedin glass cludedRNAase and pronasedigestions. The purified capillary tubes,denatured for 3 min in a boiling water DNA was sonicatedto obtain short fragments,which bath, incubated in 0.50 M PB at 55øC to a driver Cot weresized by agarosegel electrophoresisusing pBR322 of 5,000 and frozen quickly at -20øC until samples DNA cut with HaeIII as a standard (Southern 1979). could be fractionated on HAP columns. The 55øC in- This procedureyielded fragmentsaveraging 380 nu- cubation temperaturerepresents a condition of low- cleotide pairs in length (range: 250-500 nucleotide ered stringencyand was used to detect the more di- pairs).Sample purity was determinedby the 260/230 vergent cross-reactiveDNA sequencesexpected to be absorptionratio. A samplewith a ratio that is greater present in heteroduplex reactions (Rice 1972), and than or equal to 2/1 is consideredto be pure. The permittedcomparison of a greaterpercentage of each purity of our samplesranged from 2.16/1 to 2.45/1. genome.Samples were adjustedto 0.03 M PB prior DNA reassociation kinetics.--Kinetics of reassociation to loadingDNAs onto water-jacketedcolumns equil- were determined for genomic DNA of the two species ibrated to 0.03 M PB and 55øC.The 0.3 g HAP bed to be usedas probes,B. pavoninaand G. leucogeranus,was determinedpreviously to be more than sufficient utilizing standardtechniques (Britten et al. 1974,Laird to bind all the DNA contained in each reaction tube. and McCarthy 1969).We have previouslydescribed Very short DNA fragments incapable of binding to in detail our modifications of these methods, and our HAP were eluted with 0.03 M PB; the column was second-orderreaction kinetic calculationprocedures equilibrated to 0.12 M PB prior to thermal elution. (Vaughn 1975). Balearicaand Gruswere selectedbe- Column temperaturewas raisedin 5øCincrements cause they represent two different subfamiliesof to a final temperatureof 95øC.Once each new tem- cranes(Brodkorb 1967); G. leucogeranuswas used in perature was reached, the column was allowed to anticipation of clarifying its questionablephyloge- equilibrate for 2 min before the fractionswere eluted. netic position within the family. Column temperature was monitored with a therm- DNA labelingand preparationof single-copycompo- istor probe (Bailey) rated to be linearly sensitiveto nent.--We labeled sonicated total nuclear DNA of B. the nearest 0.1øC.At each temperature, two 2.5-ml pavoninaand G. leucogeranuswith 3H-dCTP (23 Ci/ fractionswere collected manually by elution with mmole, 1 mCi/ml; New England Nuclear) by the nick 0.12 M PB. After the 95øCelution step, the column translationtechnique (Rigby et al. 1977) to a specific was washed with three 1.2-ml fractions of 0.50 M PB activity of 1,200 cpm/ng and 630 cpm/ng, respec- to removeany remaining double-strandedDNA. Each tively, as determinedby liquid scintillation counting fraction was mixed with 15 ml of scintillation cocktail in Scinti-verseII cocktail(Fisher). Single-copy nucle- (Scinti-verseII, Fisher) and countedin a liquid scin- ar DNA probesfor the two specieswere isolatedby tillation counter to an error of < 10%. We determined denaturing and renaturing the labeled DNAs of each that, under theseconditions, quenching was propor- speciesto a Cotof 200. Prior kinetic analysisshowed tional for all samples. this to be sufficientto permit renaturationof virtually DNA data analysis.--Hybridizationdata were ana- all repeated sequencesbut very little of the single- lyzed by the T5oHstatistic (Kohne 1970,Bonner et al. copycomponent (Fig. 1). Becausethe labeledDNAs 1981).T50H and Tmvalues were obtainedby plotting were in small quantity, DNA fractionation was car- the cumulativecounts per minute eluted vs. temper- October1989] CranePhylogeny 597 atureon normalprobability paper (Knittel et al. 1968) 10-1 10¸ 101 102
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