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Phylogeny of Cranes (Gruiformes: Gruidae) Based on Cytochrome-B Dna Sequences

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Phylogeny of Cranes (Gruiformes: Gruidae) Based on Cytochrome-B Dna Sequences The Auk 111(2):351-365, 1994 PHYLOGENY OF CRANES (GRUIFORMES: GRUIDAE) BASED ON CYTOCHROME-B DNA SEQUENCES CAREY KRAJEWSKIAND JAMESW. FETZNER,JR. • Departmentof Zoology,Southern Illinois University, Carbondale,Illinois 62901-6501, USA ABS?RACr.--DNAsequences spanning 1,042 nucleotide basesof the mitochondrial cyto- chrome-b gene are reported for all 15 speciesand selected subspeciesof cranes and an outgroup, the Limpkin (Aramusguarauna). Levels of sequencedivergence coincide approxi- mately with current taxonomicranks at the subspecies,species, and subfamilial level, but not at the generic level within Gruinae. In particular, the two putative speciesof Balearica (B. pavoninaand B. regulorum)are as distinct as most pairs of gruine species.Phylogenetic analysisof the sequencesproduced results that are strikingly congruentwith previousDNA- DNA hybridization and behavior studies. Among gruine cranes, five major lineages are identified. Two of thesecomprise single species(Grus leucogeranus, G. canadensis), while the others are speciesgroups: Anthropoides and Bugeranus;G. antigone,G. rubicunda,and G. vipio; and G. grus,G. monachus,G. nigricollis,G. americana,and G. japonensis.Within the latter group, G. monachusand G. nigricollisare sisterspecies, and G. japonensisappears to be the sistergroup to the other four species.The data provide no resolutionof branchingorder for major groups, but suggesta rapid evolutionary diversification of these lineages. Received19 March 1993, accepted19 August1993. THE 15 EXTANTSPECIES of cranescomprise the calls.These behavior patternsinclude both ste- nominate family (Gruidae) of the order Grui- reotyped movements and vocalizations, and are formes,and are currentlydivided into two sub- mostelaborately developed in gruines.Notable families, Balearicinae and Gruinae (Brodkorb among Archibald's conclusionsis the postulat- 1967).Balearicine cranes are anatomicallyun- ed closerelationship between the Siberian(Grus specializedrelative to gruines and are repre- leucogeranus)and Wattled (Bugeranuscaruncula- sentedby only two extant speciesin the genus tus) cranes.Both specieslack the elaboratetra- Balearica(the crowned cranesof Africa). Gruines cheal coiling found in other gruines, although share derived anatomical features such as an both show the characteristicsculpted keel. Ar- anteriorly sculpted sternum (often associated chibald'sfindings were generally supportedby with trachealcoiling inside keel) in which the the anatomical-pheneticstudy of Wood (1979) furcular processis fused to the anteroventral and the recent allozyme survey of Dessaueret tip of the keel. Three extant gruine generaare al. (1992). recognized: Grus (10 species),Anthropoides (2 Ingold et al. (1987b)examined allozyme vari- species),and Bugeranus(1 species).These genera ation among cranes, and Ingold et al. (1989) are defined on the basis of soft anatomical fea- reportedthe resultsof selectedcomparisons us- tures,although their monophyly has not been ing microcomplement fixation and DNA-DNA addressedby phylogeneticanalysis. Fossil bal- hybridization.Both these studies, however, were earicines are known from the lower Eocene and inadequatelydesigned for phylogeneticrecon- later depositsin Eurasia,whereas Gruines date struction (Krajewski 1989). from the late Miocene (Brodkorb 1967). Crane phylogeny was estimatedfrom a com- Evolutionaryrelationships among cranes have plete matrix of DNA-DNA hybridization com- been addressedwith a variety of different ap- parisonsby Krajewski (1989; for a refinement proachesduring the past two decades.Archi- of the analysis,see Krajewskiand Dickerman bald (1976) derived the speciesgroups shown 1990). DNA-DNA hybridization (Fig. 1) con- in Table 1 on the basis of similarities in unison firmedthe distinctnessof balearicineand gruine cranes,and supportedArchibald's (1976) gruine speciesgroups. An exception is the placement • Present address:Alaska Department of Fish and of G. leucogeranusas an isolatedlineage among Game,333 RaspberryRoad, Anchorage, Alaska 99518, gruines, perhaps representing the oldest phy- USA. logeneticbranch within the subfamily. Among 351 352 KRAJEWSKIAND FETZNER [Auk, Vol. 111 T^BLEI. Crane speciesand subspeciesstudied. Spe- s• ciesgroups are thoseidentified by Archibald(1976) on basis of unison-call similarities. •. Japonensts G. ntgrtco111s Family Gruidae (Cranes) Subfamily Balearicinae Genus Balearica B. pavonina(Black Crowned Crane) A. virgo B. regulorum(Gray Crowned Crane) A. paradlsea Subfamily Gruinae Genus Bugeranus G. antigone B. carunculatus(Wattled Crane) ß a. vtpto Genus Anthropoides G. rubicunda A. virgo(Demoiselle Crane) 't A. paradisea(Stanley Crane) Genus Grus Fig. 1. Bootstrapconsensus tree for DNA-DNA SpeciesGroup Leucogeranus• hybridization distancesamong cranes (redrawn from G. leucogeranus(Siberian Crane) Krajewski and Dickerman 1990). Nodal value shows SpeciesGroup Canadensis frequency eachputative clade representedamong 100 G. canadensis(Sandhill Crane) b bootstrap pseudoreplicates.Bifurcating nodes with- G. c. canadensis(Lesser Sandhill Crane) out bootstrapvalues appear in 100%of pseudorepli- G. c. tabida(Greater Sandhill Crane) cates;polytomies have bootstrap values less than 50%. G. c. rowani (Canadian Sandhill Crane) G. c. pratensis(Florida Sandhill Crane) prevented phylogenetic resolution. Poor reso- SpeciesGroup Antigone lution between groupsmay indicatea relatively G. antigone(Sarus Crane) rapid evolutionaryradiation of the majorgruine G. a. antigone(Western SarusCrane) G. a. sharpei(Eastern Sarus Crane) lineages (Krajewski 1989, 1990). Further reso- lution of crane relationships, as well as testing G. rubicunda(Brolga) G. vipio(White-naped Crane) the DNA-DNA hybridization results, requires an additional and independent type of com- SpeciesGroup Americanac G. monachus(Hooded Crane) parative genetic data. G. grus(Common Crane) In this study we report sequencesof the mi- G. americana(Whooping Crane) tochondrial cytochrome-bgene for all crane G. japonensis(Japanese Crane) species and selected subspecies.A mitochon- G. nigricollis(Black-necked Crane) drial sequencewas chosen to complement the "Archibald(1976) placed Siberian Crane in Bugeranus.Species Group nuclear data derived from DNA-DNA hybrid- Leucogeranuswas suggested by Krajewski(1989). • Mississippi(G. c. pulla)and Cuban (G. c, nesiotes)Sandhill Cranes ization, as well as to exploit the advantagesof were not included in study. mitochondrialDNA (mtDNA) for phylogenetic ßKrajewski (1989) suggested that this group be renamedSpecies Group inference (Moritz et al. 1987). We chosethe cy- Grus. tochrome-bgene becausepreliminary compar- isons indicated that divergences were in the other gruines,Anthropoides and Bugeranusform range of 1 to 10%. Such divergencesare suffi- a clade,as do three Australasianspecies of Grus cient to distinguish species,but not so large as (G. antigone,G. rubicunda,and G. vipio).The larg- to be distortedby multiple substitutions(Moritz est assemblageof Grusincludes four Eurasian et al. 1987). species(G. grus,G. japonensis,G. monachus,and G. nigricollis),as well as the North American METHODS WhoopingCrane (G. americana).The Sandhill Laboratoryprocedures.--DNA was extracted from Crane (G. canadensis)shows no close affinities whole blood samplesusing standardmethods of cell with other gruine groups. lysis,Proteinase K and RNaseA digestion,extraction DNA-DNA hybridization, however, was un- with phenol and chloroform, and ethanol precipita- able to resolve relationships either within or tion (Sambrook et al. 1989). Voucher information for betweenmajor clades. Within groups,small in- the specimensemployed is given in Appendix A. We terspecificgenetic distances (< 1% divergence) included subspeciesrepresentatives for the polytypic April 1994] CranePhylogeny 353 TABLE2. Cytochrome-bprimer sequencesand sources. Primer name' Sequence Source L14841 5'~CCATCCAACATCTCAGCCATGATGAAA-3' Kocher et al. (1989) L15087 5'-TACTTAAACAAAGAAACCTGAAA-3' Edwardset al. (1991) L15136 5'-ATAGCAACAGCATTTGTAGG-3' Krajewskiet al. (1992) L15418 5'-GATAAAATCCCATTCCACCCCTA-3' This study L15615 5'-GTTCAATCCCAAACAAACTAGGA-3' This study H15149 5'-TGCAGCCCCTCAGAATGATATTTGTCCTCA-3' Kocher et al. (1989) H15498 5'-GGAATAAGTTATCTGGGTCTC-3' Krajewskiet al. (1992) H15767 5'-ATGAAGGGATGTTCTACTGGTTG-3' Edwardset al. (1991) H15915 5'-AACTGCAGTCATCTCCGGTTTACAAGAC-3' Edwards et al. (1991) • H and L refer to heavyand light strandsof mtDNA, respectively,and numberscorrespond to positionof eachprimeKs 3' basein human mitochondrialgenome (Anderson et al. 1981).Corresponding positions in chickenmitochondrial genome (Desjardins and Morals1990) can be obtainedby adding149 to humanposition number. Primer H15915 lies in threoninetRNA gene3' to cytochrome-b. Sarus(G. antigone)and Sandhill (G. canadensis)cranes graphwere aligned manually with previousoverlap- in order to assessthe effect, if any, of intraspecific ping sequencesfrom the sameDNA sampleto ensure polymorphism on phylogenetic inferences (Smouse accuracy.After resolutionof base-callingerrors and et al. 1991).A Limpkin (Aramusguarauna, Aramidae) sequencingartifacts, sequences for eachspecies were served as an outgroup. aligned with one another. Manual alignment pre- Portionsof the cytochrome-bgene were isolated sentedno difficultiesbecause the sequencesare high- and amplifiedvia the polymerasechain reaction (PCR; ly similar,and no gapsare requiredto maintainthe Innis and Gelfand 1990). PCR reactions were done in reading frame. 100 #1 volumesusing 1.5 mM Mg2+. 1.0 #M concen- Dataanalysis.--Methods
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