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Home , Bulweria, Fiji petrel, Mascarene petrel, Procellaria, Procellariiformes, Pseudobulweria

The Auk 115(1):188-195, 1998

CYTOCHROME-B EVIDENCE FOR VALIDITY AND PHYLOGENETIC RELATIONSHIPS OF AND ()

VINCENT BRETAGNOLLE,•'5 CAROLE A3VFII•,2 AND ERIC PASQUET3'4 •CEBC-CNRS, 79360 Beauvoirsur Niort, France; 2Villiers en Bois, 79360 Beauvoirsur Niort, France; 3Laboratoirede ZoologieMammi•res et Oiseaux,Museum National d'Histoire Naturelie, 55 rue Buffon,75005 Paris, France; and 4Laboratoirede Syst•matiquemol•culaire, CNRS-GDR 1005, Museum National d'Histoire Naturelie, 43 rue Cuvier, 75005 Paris, France

ABSTRACT.--Althoughthe Pseudobulweria was described in 1936for the (Ps.macgillivrayi), itsvalidity, phylogenetic relationships, and the number of constituenttaxa it containsremain controversial. We tried to clarifythese issues with 496bp sequencesfrom the mitochondrialcytochrome-b gene of 12 taxa representingthree putative subspecies of Pseudobulweria,seven in six othergenera of the Procellariidae(, , and ),and onespecies each from the Hydrobatidae(storm-petrels) and Pelecanoidi- dae (diving-petrels).We alsoinclude published sequences for two otherpetrels ( cinereaand Macronectesgiganteus ) and use Diomedeaexulans and Pelecanuserythrorhynchos as outgroups.Based on thepronounced sequence divergence (5 to 5.5%)and separate phylo- genetichistory from othergenera that havebeen thought to be closelyrelated to or have beensynonymized with Pseudobulweria,we conclude that the genusis valid, and that the MascarenePetrel (Pseudobulweria aterrima) and the (Ps. rostrata) are distinct spe- cies.In treesconstructed with maximumparsimony and maximumlikelihood, Pseudobul- weriais the sistertaxon to Puffinusand , and these genera in turn aremost closely relatedto Bulweria(and Procellariain the maximum-parsimonytree). Pseudobulweria is not closelyrelated to Pterodromain either tree. Because Ps. r. trouessartifrom , and Ps.r. rostratafrom Polynesia differ by only0.6%, these taxa do notdeserve species status and shouldbe regardedas valid subspecies.Received 7 October 1996, accepted 23 July1997.

THE GENUSPSEUDOBULWERIA, first proposed (Atti• et al. 1997),and Ps.rupinarum already is by Mathewsin 1936for the (Ps. mac- extinct (Olson 1975). Therefore, systematic gillivrayi),remains one of the least-knowngen- studieson this grouphave relied nearly exclu- era of petrels(Warham 1996, Atti• et al. 1997). sivelyon Ps. r. rostrataand on morphological at- Althoughit hasbeen synonymized with Pter- tributesassessed from museumspecimens (e.g. odroma(e.g. Jouanin and Mougin 1979, Warham Jouanin 1970, 1987; De Naurois and Erard 1979; 1990,Del Hoyo et al. 1992),some systematists Imber 1985). have reinstatedit as a separategenus (Imber Using availabledata as well as new infor- 1985,Warham 1996),either closeto Pterodroma mation provided by DNA sequencing,we ex- (Sibley and Monroe 1990) or to Bulweriaand amined:(1) the validity of the aterrima Procellaria(Imber 1985).In his reappraisalof comparedwith rostrata,because these two taxa the petrels,Imber (1985)also included in Pseu- have been suggestedto be conspecific(e.g. dobulweriathe MascarenePetrel (Ps. aterrima), Jouanin1970); (2) thevalidity of thegenus Pseu- the Tahiti Petrel(Ps. rostrata), and a fossiltaxon dobulweria;and (3) thephylogenetic positions of (Ps.rupinarum). Beck's Petrel (Ps. rostrata becki) Pseudobulweriaand Bulweriawithin the family is knownfrom onlytwo specimensand may be Procellariidae.For this latter aspect,we paid extinct. Similarly, Ps. macgillivrayiis known particularattention to Bulweria,which has been from only two specimens(Watling and Lewa- claimedto be closeto (Kuroda1954) or syn- navanua1985), Ps.aterrima is known from sev- onymouswith Pterodroma(Olson 1975), and to- en specimensand is on the vergeof getherwith Pseudobulweriais thought to be an- cient(Bourne 1975; Imber 1985;Warham 1990, E-mail: [email protected] 1996).We usedthe mtDNA sequence(496 bp 188 January1998] RelationshipsofPetrels 189

segment) at the cytochrome-blocus because TCCTGTTTCGTGGAGGAAGGT-3').These primers this segmenthas proved valuable for phyloge- amplify a DNA segmentof 496 bases.PCR was per- netic analysisat the species,generic, and fa- formed in a 50-p•Lvolume using ca. 0.3 p•gof tem- milial levelsin (e.g.Lanyon 1994, Baker plateDNA and 50 picomolesof eachof the primers. et al. 1995,Helbig et al. 1995,Arctander et al. The PCRmix (final concentrations)contained 20 mM Tris-HCL, pH 8.55, 16 mM (NH4)2SO•, 2.5 mM 1996, Friesenet al. 1996, Krajewski and King MgC1v 150 p•g/mL BSA, 330 p•M dNTP, and 0.3 1996). (1.5 units) of GoldstarTaq DNA polymerase(Euro- genetec).The PCRprofile for amplificationswas 35 MATERIAL AND METHODS cyclesof 60 s at 93øC,40 s at 50øC,and 40 s at 72øC. PCR productswere openedunder a speciallyde- Speciesand sampling techniques.--We obtained sam- signedhood and checkedby electrophoresisin 1% ples from sevenprocellariid genera as well as one agarose-BETand TBE buffer (Sambrooket al. 1989) speciesof storm-petreland onespecies of diving-pe- with the molecularweight marker VI (Boehringer). trel: Tahiti Petrel (Ps. r. trouessarti;New Caledonia, PCR productswere clonedusing the PCRscriptTM blood sampleand Ps. r. rostrata;Gambier Is., blood), SK(+) cloningkit (Stratagene)according to recom- (R•union I., tissue), Barau'sPetrel mendedspecifications. A classicalwhite/blue selec- (Pterodromabaraui; R•union I., tissue),Black-winged tion (Sambrooket al. 1989) was used for screening Petrel (Pt. nigripennis;New Caledonia,blood), Bul- recombinantclones. Four white coloniesper cloning wer's Petrel (Bulweriabulwerii; Canary Is., blood), were grown overnightin L-broth at 37øC,the pha- Cory's (Calonectrisdiomedea; Malta, gemidic DNA extracted (Sambrooket al. 1989), and blood), Wedge-tailedShearwater ( pacificus; the insertwas checkedby digestionof the recombi- New Caledonia,blood), Northern (Fulmarus nant phagemidicDNA with BssHII.Sequencing on glacialis;Brittany, tissue), (Pagodroma ni- microtiter plates was performed with the T7 se- vea;Ad•lie Land, ,blood), Leach'sStorm- quencingkit (Pharmacia),using the method of ter- Petrel (Oceanodromaleucorhoa; French Guyana, tis- minator dideoxynucleotides(Sanger et al. 1977). sue), and Common Diving-Petrel (Pelecanoidesuri- Two coloniesper cloningwere sequencedwith ex- natrix;,tissue). We also used published ternalvector primers KS and T3 to checkfor artifacts sequencesfrom Procellariacinerea and Macronectesgi- introduced by cloning of PCR products. Differences ganteus(Nunn et al. 1996), making availabledata betweenclones occurred in only two samples(both from9 of the 13genera in thisfamily (sensu Warham one-transitiondifference in the 496 bp), and a third 1996). Diomedeaexulans (Nunn et al. 1996) and Pele- colony was sequencedto confirm the correctse- canuserythrorhynchos (Avise et al. 1994)were used as quence. outgrouptaxa. Bloodsamples (ca. 1 mL) were taken Data ana[ysis.--Sequenceswere read and entered from the tarsusfor the larger speciesand from the twice usingthe computerpackage MUST (Philippe wing for the smallerspecies and preservedin a buf- 1993) and were easily aligned becauseno insertions feredsolution of 4M guanidine-thiocyanate(see Lau- or deletions were found. Relative transitional satu- lier et al. 1995). Tissuesamples (liver) were taken ration was examinedby plotting transitionalagainst from specimensfrozen at -18øC. One specimenwas transversionalpairwise raw differences.Maximum- sampledfor eachspecies. likelihood (ML) analyses(Felsenstein 1981) were DNA extractionand PCR amplification.--Asmall performedwith program FastDNAml (Olsen et al. amount of tissue or blood (ca. 0.1 g) was powdered 1994).The optionsF (empiricalfrequencies) and G in liquid nitrogenand suspendedwithin CTABbuff- (global rearrangements)were used, and 10 random- er containing proteinaseK (Doyle and Doyle 1987, input of specieswere done for eachmodel to Winnepenninckxet al. 1993). was at 60øC minimize input-order bias. We used three models for 1 h, and protein isolationwas carried out with differingin the numberof categoriesof substitution chloroform-isoamylalcohol. In addition,0.5 unitsof rates(CSR). In 1-CSR,the threecodon positions had RNAasewere added to the secondaqueous phase equal substitution rates; in the 2-CSR model, first and incubated at 37øC for 30 min to remove RNA. To- and secondcodon positions had equalrates whereas tal genomicDNA wasprecipitated with isopropanol. the third differed; and in the 3-CSR model, each co- DNA concentrationand qualitywere evaluated with don positionhad a differentrate of substitution.Two a spectrophotometer.Extracted DNA was amplified sets of relative codon-positionevolutionary rates with thefollowing two primers,whose numbers cor- (lst:2nd for the 2-CSRmodel, and lst:2nd:3rdfor the respondto the locationof the 3' end of the primer 3-CSR model) were used: 1:5 and 1:10, and 2:1:5 and respectivelyin the full sequenceof human mtDNA 2:1:10, respectively.Three transition-transversion (Andersonet al. 1981, in bold) and chickenmtDNA ratios(TS:TV) were used and thusdefined a prioriin (Desjardinsand Morais 1990):L14841/L14990 (5'-CA- the likelihoodcomputations: 2:1, 5:1, and 10:1.The TCCAACATCTCTGCTTGATGAAA-3')defined by best likelihood values were obtained for 2-CSR and Kocher et al. (1989), and H15338/H15487 (5'-GA- 3-CSR models with TS:TV=5:I, and with - 190 BRETAGNOLLE,ATTIf:, AND PASQUET [Auk, Vol. 115 ary categoryrates being respectively1:10 or 2:1:10. Theseparameters produced two treesthat differed in the positionof Procellariacinerea, with eithera ba- sal positionto the cladePterodroma-Fulmarus-Pago- droma-Macronectes(Model 2-CSR), or an inner posi- tion in thisclade, as sister-group of fulmarines(Mod- el 3-CSR).However, because three shortbranches did not significantlydiffer from zero,these two treesef- fectivelygave the sametopology, and thuswe have presentedonly this tree beyond. We also performed maximum-parsimony (MP) analyseswith PAUP3.1.1 (Swofford 1991) with unor- dered characters. Branch and bound searches were performedwith the completedata set of 14 taxa. Weightswere given to the transversionsvia a step matrix. The two optimizationsused, Accelerated Transformation (ACCTRAN) and Decelerated Transformation(DELTRAN), yielded similar topo- logicalresults. Likelihoods of the MP treeswere cal- culatedand comparedwith thoseof ML trees.Boot- strapping (Felsenstein1985) was performed using FastDNAml and PAUP. For the MP trees, heuristic searches were used for 100 and 1,000 iterations. Pe- lecanuserythrorhynchos was used as an outgroupin all analyses.

RESULTS

Sequencevariation.--Sequences were deposit- ed in GenBank under accession numbers U70482to U70493.Within the 14 speciesana- lyzed, 174 sites (35% of the 496 sites) were foundto be variable,and 126(25.4%) were phy- logeneticallyinformative, i.e. were present in two or morestates in morethan one species. Of the 174variables sites, 32 (18%)were at the first positionof the codon,seven (4%) at the second, and the remaining135 (75.6%)at the third po- sition,representing at eachposition 19.4, 4, and 81%, respectively,of all suchsites. These are similar proportionsto those found for alba- trosses(Nunn et al. 1996) and are typical pro- portionsin cytochrome-bgene of vertebrates (seeCicero and Johnson1995, Arctander et al. 1996). Sequencedivergence.--Among taxa within the samegenus, uncorrected sequence divergences rangedfrom 0.6%between the two subspecies of the Tahiti Petrel to 7.1% between the two speciesof Pterodroma(Table 1), valuesthat are within the rangefound for othernonpasserine genera(Cicero and Johnson 1995, Helbig et al. 1995, Nunn et al. 1996).The sequenceof the Mascarene Petrel differed from that of the two subspeciesof the TahitiPetrel by an averageof 5.3%, typical of levels of divergenceamong January1998] Relationshipsof Petrels 191

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$ 10 •S 20 25 30 35 40

Transversions

FIG.1. Pairwiseplots of transitionsversus transversions (between Procellariidae, triangle; between the Procellariidaeand otherProcellariiformes or Pelecanus,circle). congenericspecies of birds. Among genera was near 10:1 (Fig. 1; see also Austin 1996, within the family Procellariidae,sequence di- Nunn et al. 1996),whereas the unweightedMP vergencesranged from 8.1 to 14.3% (Table 1). analysisindicated that the relativefrequencies Divergence between the Procellariidae se- of TS:TV was 5:1. Therefore, we used both of quencedin this studyand otherpublished se- theseratios for subsequentconstruction of MP quencesof procellariiformsranged from 11.5to trees. 17.3%. Lastly,among the 14 taxa studied, the Phylogeneticposition of Pseudobulweriaand proportions of transversionalsubstitutions in Bulweria.--Althoughthe topologiesof the ML pairwisecomparisons among taxa were highly and MP trees(Figs. 2 and 3) differ somewhatin variable,ranging from 0 to 0.49. their placementof genera,in both treesPseu- Saturation effects.--Relative saturation of dobulweriais the sistergroup to Puffinusand Ca- transitions appeared fairly rapid (Fig. 1), lonectris,and these genera in turn are most which indicatedthat using transitionsand closelyrelated to Bulweria(and Procellariain the transversionswith equal weightfor phyloge- MP tree). Pseudobulweriais not closelyrelated to neticanalysis was not acceptable.The verybe- Pterodromain either tree.Bootstrap support is ginningof thecurve, corresponding to themost strongonly for the monophylyof Pseudobulwer- closelyrelated taxa, indicated that TS:TV ratio ia on the one hand and for the monophylyof 192 BRETAGNOLLE,ATTIla, AND PASQUET [Auk, Vol. 115

Pel. erythrorhynchos Pel. erythro rhynehos O. leucorhoa D.exulans D. exulans _• Pc. urinatrix O.leucorhoa Pc. urinatrlx .•pB. bulwerii PS.aterdma C.diomedea Ps.rostrata trouessarti Pu.pacific us Ps.rostrata rostntta Ps.aterrima 48 Pu.pacific us C.dlomedea ulwedi • Pr.cinema P.cinerea Pa.nivea I 60•..•-•,• Pa'nivea F.glacialis [ •- F.glacialls • 1V•glgante us M.giganteus I 100 • Pt. bamul Pt.bamPu• nigripennis [• PLnigrtpennis 10

FIG.2. Maximum-likelihoodtree based on 496 bp FIG. 3. Single most-parsimonioustree obtained of cytochrome-bDNA sequenceswith transition/ using a TV:TS = 5:1 weighting schemewith boot- transversionratio (TS:TV = 5:1) and two categories strapproportions (percentages) shown to the left of of substitutionrates (1:10; see Methods). The branch- internal branches.The same topologywas found es markedwith a star are not significantlypositive. with the 10:1weighting scheme (see text for method Data for Pelecanuserythrorhynchos are from Aviseet and parameters). Bootstrap proportions are given al. (1994); data for Diomedeaexulans, Macronectes gi- onlywhen >40%. Similarvalues were obtained with ganteus,and Procellariacinerea are from Nunn et al. maximum-likelihoodanalysis. (1996). imprecisedue to low bootstrapvalues and/or sequencesthat are too short. Pterodromaon the other. Weakersupport for Subspeciesof Pseudobulweria rostrata.-- othernodes is a commonresult when shortcy- Three subspeciesof the Tahiti Petrel currently tochrome-bsequences are analyzedat thisphy- are recognized: rostrata,trouessarti, and becki logeneticlevel (e.g.Wink 1995). (Jouaninand Mougin 1979, Warham 1990). However,the validity of the first two subspe- DISCUSSION cies is controversial(Murphy and Pennoyer 1952,De Naurois and Erard 1979),as is the tax- Validity and phylogeneticposition of Bulweria onomicstatus of becki,which may require full andPseudobulweria.--The genus Pseudobulwer- species status (e.g. King 1978, Collar and An- ia has long beenthought to be closelyrelated drew 1988,Sibley and Monroe 1990),although to, or evenincluded within, Pterodroma.Our ge- all recentsystematic studies of the Procellari- neticanalyses do not supportthis belief;Pseu- iformes regard it as a subspecies(Jouanin and dobulweria and Pterodroma are not members of Mougin 1979,Imber 1985,Warham 1990). This the sameclade within the Procellariidae(Figs. latter taxon could not be included in our anal- 2 and 3), and they are quite divergent. The ysis becausebreeding coloniesare undiscov- sameconclusion applies to Bulweria.Therefore, ered,but the othertwo subspecieswere consid- we concludethat Pseudobulweria,as suggested ered.Moreover, we sampledbirds from the two by Mathews(1936), is a valid genus,consisting geographicextremes: (1) New Caledonia,the of four to five species.Imber (1985)reached the westernmostbreeding locationof the species; sameconclusion based on nongeneticevidence, and (2) the GamblerIslands, a newly discov- and he further suggestedthat Pseudobulweriaered breedingsite for this species(2,000 km was linked to Procellaria and Bulweria, and more east of its previousknown range; Bretagnolle distantly,to Puffinus.In the ML tree (Fig. 2), and Thibaultunpubl. data). Our DNA sequence Pseudobulweriaand Bulweriawere linked to Puf- data showthat populationsfrom New Caledo- finus (and Calonectris)but apparentlynot to Pro- nia and Gambler are closelylinked, differing cellaria,although the phylogeneticpositions of by only three transitionsand leading to the Bulweria and Procellaria within the remain smallestpercentage of differenceamong the January1998] RelationshipsofPetrels 193 taxa we analyzed(0.6 %). This is at the lower cial thanks to A. J. Baker for extensive revision of the end of sequencedivergence found at the sub- manuscript,and to R. Dawson, S. J. G. Hall, A. Pat- specificlevel amongbirds in general(see Hel- erson, and two anonymousreferees for improving a big et al. 1995), and petrelsin particular (e.g. previous draft. Randi et al. 1989; Wink et al. 1993a, b), al- thoughBrooke and Rowe (1996)recently split LITERATURE CITED a speciesof petrelwith only 1% difference. ANDERSON,S., A. T. BANKIER,B. G. BARRELL,M. H. Accordingto our molecularevidence, troues- L. DE BRUIJN,A. R. COULSON,J. DROUIN, I. C. sarti from New Calect•onia and rostrata from EPERON,D. P. NIERLICH, B. A. ROE, E SANGER,P. Polynesiado not deservespecies status, and H. SCHREIER,A. J. H. SMITH, R. STADEN,AND I. they shouldbe regardedas valid subspecies. YOUNG.1981. Sequence and organization of the This conclusionis supportedboth by morpho- humanmitochondrial genome. Nature 290:457- metrics and vocalizations (De Naurois and Er- 465. ard 1979,Bretagnolle unpubl. data), although ARCTANDER,P., O. FOLMER, AND J. FJELDSA.1996. dataon rostratafrom Vanuatuand Fiji currently The phylogeneticrelationships of Berthelot's are lacking,and thesebirds may prove to be in- Pipits Anthusberthelothii illustrated by DNA se- termediate between the two forms. quencedata, with remarkson the geneticdis- Taxonornicstatus of Mascareneand Tahiti pet- tancebetween Rock and Waterpipits Anthus spi- noletta. Ibis 138:400-415. rels.--Using external morphology, Jouanin Attila, C., J.-C. STAHL,AND V. BRETAGNOLLE.1997. (1970)suggested that the Mascareneand Tahiti New data on the endangeredMascarene Petrel petrelsmight be conspecific(along with becki). Pseudobulweriaaterrima: A third 20th century Our results from mtDNA show that the differ- specimenand distribution.Colonial Waterbirds encebetween the two petrels (5 to 5.5% se- 20: in press. quencedivergence; Table 1) involves 3 trans- AUSTIN,J. 1996. Molecularphylogenetics of Puffinus versionsand 20 to 22 transitions.This is clearly shearwaters:Preliminary evidencefrom mito- outsidethe rangefound between subspecies in chondrialcytochrome b genesequences. Molec- birds, but within the range of divergencefor ular Phylogeneticsand Evolution6:77-88. congenericspecies (Helbig et al. 1995). Boot- AVISE, J. C., W. S. NELSON,AND C. G. SIBLEY. 1994. strapvalues also were high, and thereforeit can DNA sequencesupport for a closephylogenetic be concluded that Ps. aterrirna and Ps. rostrata relationship between some storks and New World vultures. Proceedingsof the National are indeedvalid congenericspecies. Although Academyof SciencesUSA 91:5173-5177. nothingis known aboutthe breedingecology BAKER,A. J., C. H. DAUGHERTY,R. COLBOURNES,AND of Ps. aterrirna(Atti• et al. 1997), studiesof ex- J.L. MCCLENNAN.1995. FlightlessBrown Kiwis ternalmorphology have convincingly reached of New Zealand possessextremely subdivided the sameconclusion of speciesstatus (see Im- populationstructure and cryptic specieslike ber 1985). small .Proceedings of the National Academyof SciencesUSA 92:8254-8258. ACKNOWLEDGMENTS BOURNE,W. R. P. 1975.The lacrymal bone in the ge- nus Bulweria. Ibis 117:535. Field work was facilitated by J. Broudissou,M. BROOKE,M. DE L., AND G. ROWE. 1996. Behavioural Pandolfi,and S. Sirgouanton New Caledonia;by M. and molecular evidencefor specificstatus of Atti• on R•unionIsland; and by J.R. Kingon theCa- light anddark morphs of the HeraldPetrel Pter- nary Islands.WWF-France provided a grant to C.A. odroma heraldica. Ibis 138:420-432. in 1995for researchon the endangeredMascarene CICERO,C., ANDN. K. JOHNSON.1995. Speciationin Petrel.N. Hyde and J.-C.Stahl kindly providedtis- Sapsuckers(Sphyrapicus): III. Mitochondrial- suesamples from The NationalMuseum of Welling- DNA sequencedivergence at the cytochrome-b ton, New Zealand, as well as E Siorat (LPO, Station locus. Auk 112:547-563. ornithologiquede l'ile Grande).Y. Bigot(Tours Uni- COLLAR,N.J., ANDP. ANDREW. 1988. Birdsto watch. versity)kindly allowedus to usehis techniquefor ICBP TechnicalPublication No. 8. Cambridge, blood preservation,and J.-E Murail and E Fond•re United Kingdom. helpedwith processingFastDNAml on UNIX com- DEL HOYO, J., A. ELLIOTT,AND J. 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