The Auk 116(4):1093-1106, 1999

HIGH LEVELS OF MITOCHONDRIAL DNA DIFFERENTIATION IN TWO LINEAGES OF ( AND )

JOHN M. BATES?3 SHANNONJ. HACKETT,• AND JAQUELINEM. GOERCK2 •Departmentof Zoology,Field Museum of NaturalHistory, Roosevelt Road at LakeShore Drive, Chicago,Illinois 60605, USA; and 2Departmentof Biology,University of Missouri-St.Louis, 8001 NaturalBridge Road, St. Louis, Missouri 63121, USA

ABSTRACT.--Weassessed levels of geneticdifferentiation based on mitochondrialDNA se- quences(portions of the cytochrome-band ND2 genes)at severaltaxonomic levels in tham- nophilidantbirds. Our focuswas to investigategenetic differentiation among populations of two speciesin the genusDrymophila and to identify the sistergenus to Drymophila.In addition,we presentevidence of highlevels of populationsubdivision in Hypocnemiscantator (WarblingAntbird). This widespread Amazonian taxon co-occurs, on a localscale, with D. devillei(Striated ). Sequencedivergences among populations of D. devilleiand D. cau- data(Long-tailed Antbird), two bamboo-specialists,often exceeded 2% between populations. Divergenceswithin H. cantator,a specieswith moregeneralized habitat requirements and a more"continuous" distribution, were even higher, including 5.7% divergence between sam- plesseparated by 350 km of apparentlycontinuous Amazonian forest. At highertaxonomic levels,genetic distances suggest that antbirdgenera and biological are old. Genetic divergencebetween the two speciesthat comprise the genusHypocnemis was 9.3%, and di- vergencebetween D. devilleiand D. caudataaveraged 7.2%. Weighted parsimony and maxi- mum-likelihoodanalyses supported Hypocnemis asthe sister taxon to Drymophila;the Myrmotherulawas not monophyletic,supporting previous allozyme analyses. In additionto the protein-codingsequences, we foundthat spacerregions between genes also provided phylogeneticallyinformative characters from the levelof suboscinefamilies to within the biologicalspecies that we studied.Received 31 March1998, accepted 7 April 1999.

WITH SOME266 currentlyrecognized biolog- this study and are thoughtto be restricted ical species(Parker et al. 1996), the antbirds largelyto areasof bambooin the upper-tropi- (formerlyFormicariidae) recently have been di- cal zone of the Andes (D. caudata)and in the videdinto theFormicariidae (ground antbirds, westernand southernparts of the Amazonba- 70 species)and Thamnophilidae(typical ant- sin (D. devillei;Fig. 1). The entiregenus is cur- ,196 species) based on DNA-DNA hybrid- rently under study by one of us (JMG) to un- izationdata (Sibleyand Ahlquist1990). Mem- derstandits evolutionaryhistory and how this bersof thesespecies-rich families are distrib- history relatesto current ecologyand distri- uted throughoutthe Neotropics.Antbirds in- bution. habit all levels of tropical forest and many Specializationon bambooexhibited by D. de- different insectivorous niches such that as villei and D. caudatais known for a small guild many as 40 speciescan occurat a singlesite. In of Neotropicalbirds (Parker 1982, Kratter 1997, thispaper, we presentdata on geneticstructure Parker et al. 1997). Bamboo-specialistbirds, within and among three biologicalspecies like theirpreferred habitat, tend to havepatchy (sensuMayr 1963) of thamnophilidantbirds: distributions. In the Andean foothills, D. cau- Drymophiladevillei (), D. caudata data occurs between 1,200 and 2,500 m from (Long-tailedAntbird), and Hypocnemiscantator Venezuelato Bolivia.Three subspecies,with (WarblingAntbird). presumablydisjunct distributions, have been Thegenus Drymophila has been considered to described(Peters 1951), but eventhese subspe- have eight species(Peters 1951), six of which are restricted to the Atlantic forests of eastern ciesprobably are composedof disjunctpopu- South America. The other two are the focus of lations subdividedby deep river valleys and high mountainridges. Based on limited speci- men data, D. devilleishows a similarlypatchy E-mail:[email protected] distribution in the lowlands (Stotz 1990, Rid-

1093 1094 BATES,HACKETT, AND GOERCK [Auk, Vol. 116

10•N oo Attc•zt•,c Ocec•

P•c•.f•.c Ocec•'•.

80"W 75 55

F•G.1. Distribution of Drymophilacaudata (circles) and D. devillei(triangles). In severalplaces both spe- ciesare known from the samesector (closed circles). Sites for samplesof Hypocnemiscantator used in this study are also indicated(open squares);in severalinstances these sites correspond with localitieswhere D. devilleioccurs (dark triangles).Numbers depict localitiesin Appendix. The easternmostopen triangle is where the type of D. devilleisubochracea was collected.Locational data compiledand map preparedby M. and P. Isler. gely and Tudor 1994, Stotz et al. 1997). Two villei and two populationsof D. caudatafrom subspecieshave been described, both of which southernPeru. To establish the outgroup for the were consideredto be probablebiological spe- genus,we also obtainedsequences from indi- ciesby Parkeret al. (1996).The nominateform, vidualsrepresenting a numberof other small D. d. devillei, is known from areas of bamboo in thamnophilids.To provideadditional compar- southeastern Peru and northern Bolivia, but ative data on geneticstructure within biologi- severalspecimen records also exist from as far cal species,we alsoincluded multiple samples north as easternColombia (Stotz 1990).Dry- of both biologicalspecies of Hypocnemis.Al- mophilad. subochraceais known from only a few thoughthese samples cover only a smallpor- localities that lie south of the Amazon, from the tion of the geographicdistribution of thesetwo east bank of the Rio Madeira to a western trib- taxa(particularly for H. cantator),they provide utary of the Rio Xingu in Brazil. more divergencedata from anotherlineage We presentsequences from parts of the mi- from this part of Amazonia.Our resultspro- tochondrialcytochrome-b (cyt b) and NADH vide a clearpicture of thehigh levelsof genetic dehydrogenasesubunit 2 (ND2) genesfor mul- structurewe believeare typical of many forest- tiple populationsof both subspeciesof D. de- dwelling Neotropicalspecies. October1999] GeneticDifferentiation in Antbirds 1095

METHODS Biosystems,Inc. [ABI]). Cycle-sequencingreactions were Nh4OAcprecipitated, rinsed in ethanol, dried, DNA sequencing.--Samplesof the 34 individuals resuspendedin a formamide-EDTA solution, and used in this study were obtainedfrom tissuecollec- run on an ABI 377 Automated DNA Sequencer.Se- tions of the LouisianaState University Museum of quenceswere obtained from both strandsof DNA, NaturalScience (LSUMNS), the Academyof Natural checkedusing the programSequencher 3.0 (Gene Sciencesin Philadelphia(ANSP), and the Di- CodesCorp.), aligned to the chicken(Gallus gallus) vision of the Field Museum of Natural History sequence(Desjardins and Morais 1990) to ensure (FMNH; Appendix).Voucher specimens are housed there were no insertions or deletions of bases in the at these institutions, the Museu Paraense Emilio antbird sequences,and submitted to GenBank Goeldi, Be16m,Brazil (MPEG), and Museu de Zoo- (AFl18154 to AFl18221; Appendix). logia da Universidadede S•o Paulo,Brazil (MZUSP). The followingprotocol was undertakento ensure All DNA work was carried out in the Field Museum's that the smallfragments of DNA weremitochondrial PritzkerLaboratory for the Studyof MolecularSys- in origin (not nuclear copies).(1) Sequencesof se- tematicsand Evolution.Samples were from the two lectedindividuals were verified by amplifying(with speciesof Drymophilaand eight other speciesof L14990 and H16065 for cyt b and L5215 and H6313 thamnophilids( humeralis [Chestnut-shoul- for ND2; sequencesin Hackett [1996], except for dered Antwren]; Myrmotherulalongipennis [Long- H6313 [CCTTTATTTAAGGCTTTGAAGGC]) and se- winged Antwren]; M. leucophthalma[White-eyed quencinga larger pieceof mtDNA using the primers Antwren]; M. hauxwelli [Plain-throated Antwren]; above.(2) Both DNA strandswere sequencedto en- Formicivorarufa [Rusty-backedAntwren]; E grisea sure accurate sequences.(3) Sequenceswere used [White-fringed Antwren]; Hypocnemishypoxantha only if they gave clean sequence(i.e. little back- [Yellow-browed Antbird]; and H. cantator).We in- ground and no double peaks), and sequenceswere cludedmultiple individuals of speciesin Hypocnemis inspectedfor insertions,deletions, or stop codohs becausethe genushas been hypothesizedto be the that would indicatethat the sequenceswould result closestrelative of Drymophila(Ridgely and Tudor in a nonfunctionalprotein. (4) Partition-homogene- 1994:293).At the genericlevel, the goal of this sam- ity testswere performed to assessif thephylogenetic pling schemewas to confirma suitableoutgroup for contentof thesetwo partial genesequences was sim- geneticand ecologicalresearch on Drymophila,and ilar; nuclearcopies would not necessarilybe expect- not to reconstructa phylogenyof thamnophilidgen- ed to havesimilar phylogenetic content to mitochon- era. As a result, higher-levelrelationships among drial genes.(5) Genetic-distancematrices were gen- thamnophilidsshould be viewed as tentative.We eratedseparately for the two genefragments and in- also included a ground antbird (Formicariuscolma spectedfor differences.(6) Sequencesof individuals [Rufous-capped Antthrush], Formicariidae), a from the samecollecting locality, population, or geo- woodcreeper(Lepidocolaptes angustirostris [Narrow- graphicregion were expected to be geneticallymore billed Woodcreeper],Dendrocolaptidae), an ovenbird similarthan thoseof otherpopulations or regions.If (Synallaxisalbescens [Pale-breasted Spinetail], Fur- not, the sequencesmay not be mitochondrialand are nariidae), and a manakin (Pipra pipra [White- in needof furtheranalysis (e.g. cloning to assessthe crownedManakin], Pipridae). Using the phylogeny number of sequencesrepresented in an individual). of Sibley and Ahlquist (1990), we designatedthe Phylogeneticanalyses.--All phylogenetic analyses manakin as the outgroup. were conducted with version 4.0d64 of PAUP*, writ- DNA wasextracted using either G NOME© or Pure- ten by David L. Swofford.We performeda partition- gene (Gentra Systems,Inc.) extractionkits. Piecesof homogeneitytest using 1,000random partitions to two mitochondrialgenes, cyt b and ND2, were am- determine if these partial gene sequenceswere in- plified usingthe primersL15656 and H16065for cyt congruentwith respectto their phylogeneticcontent b and L5215and H5578 for ND2 (primersequences (Farris et al. 1995, Cunningham 1997). In addition, are given in Hackett 1996).Fragments were PCR-am- we performed another partition-homogeneitytest plified using standardconditions (available from the (1,000random partitions)comparing third positions authorsupon request;denaturation at 94øC,anneal- with first and secondpositions to determineif third ing between 45 and 54øC,and extensionat 72øCin positionsgave a differentphylogenetic signal (pos- MJResearchPCR machines).A small aliquotof each sibly becauserate variation acrosscodon positions ampiiconwas electrophoresedon an agarosegel to may lead to saturation).After assessingthe degree checkfor the correctfragment size and to verify the of saturationat all three codonpositions (following presenceof a singleclean PCR product. The remain- Hackett 1996 and Griffiths 1997), we constructed der of the reaction was cleaned and concentrated us- maximum-parsimonytrees on bothunweighted and ing Microcon 100 tubes (Amicon) or Geneclean weightedsequence data. We present strict-consensus (BIO101). Cleaned double-strandedamplifications treeswhen more than one most-parsimonioustree were cycle-sequencedusing fluorescentdye termi- wasfound. We exploredthe sensitivityof parsimony nator chemistryand the FS Taq enzyme (Applied trees to the weighting schemeby down-weighting 1096 BATES,HACKETT, AND GOERCK [Auk, Vol. 116 transitionsin saturateddata partitions 2, 5, 10, 100, RESULTS and 1,000times. Weighted analyses based on results of saturationwere accomplished using step matrices Mitochondrialor nuclearcopies.--Only one in- in PAUP*.For example, if transitionsat third andfirst stanceoccurred where a sequenceamplified positionswere down-weightedby a factorof 10, a fromthe small fragment differed from the larg- weightof 10 was givento secondpositions to make their weight equivalentto a transversionat first or er one.The small fragmentof cyt b from Hy- third positions.We assessedthe amountof support pocnemishypoxantha REAJ232 resulted in a se- for nodesusing 100 bootstrapreplicates (Felsenstein quencethat wasmissing a few basescompared 1985).All searcheswere heuristic,with default op- with the sequencesfrom the larger amplified tions (keep best trees only, stepwiseaddition, swap fragment.The larger fragment sequencedif- on besttree only,quick swap enabled, hold 1 tree at feredby onlytwo nucleotidesfrom the otherH. eachstep, TBR branch-swapping,MULPARS, swap hypoxanthaindividual that we had in our data on besttrees only) exceptfor performing100 random set and thereforewas hypothesizedto be mi- addition sequencereplicates. Maximum-likelihood (ML) analyses have been tochondrial.Sequences of all otherindividuals were from both strands of DNA, had little suggestedto performbetter under long-branchat- traction conditions (Huelsenbeckand Hillis 1993); backgroundor double peaks, and translated therefore, we used PAUP* to estimate ML trees to without stop codons.Partition-homogeneity comparewith parsimonyanalyses. Because of time testsand genetic-distancematrices revealed no constraintsassociated with ML analyses,individuals significantdifferences between the two partial differingonly slightlyfrom eachother were exclud- genesequences. Individuals from the same col- ed from the analysis(e.g. only one individual from lectinglocality or geographicregion were ge- the Rond6niasample of D. devillei[DEVIl wasused). neticallymore similar to eachother than to in- The ML data setcontained 20 individuals.Using the suggestedprocedure of Huelsenbeckand Rannala dividuals from other geographicregions or (1997),likelihood-ratio tests (LRTs) were performed species.Therefore, we believethat thesese- to select the model of evolution for the detailed ML quenceswere mitochondrial in origin. treesearch. A preliminaryneighbor-joining (NJ) tree Informativevariation.--The gene regionswe was generatedusing Kimura 2-parameterdistances, studiedare positions5241 to 5577in ND2 and and the likelihood score for that tree was noted un- 15664to 16035in cyt b (numberscorrespond to der a simple HKY (Hasegawaet al. 1985) model (two the chickensequence; Desjardins and Morais substitutiontypes, all sitesassumed to evolveat the 1990).We alsoreport sequences of the spacer same rate, molecular clock not enforced).LRTs were regionbetween cyt b and the threoninet-RNA performedby adding parametersto the model and testing for a significantimprovement in likelihood (bases 16036 to 16038 of chicken;Table 1). scoreson this neighbor-joiningtree. In this analysis, Lengthvariation occurs in thisspacer (ranging the HKY model, which assumesonly two substitu- from two to four bases in different suboscine tiontypes, was compared with a generaltime-re- families). Therefore,the data set contains713 versiblemodel (Yang1994) that has six substitution characters(337 ND2, 372 cyt b, 4 spacer).Par- types.These models were comparedboth with and simony-informativesites are evenlydistributed without rate heterogeneity(proportion of invariant in both genes(119 ND2 [35.3%of total bases], sitesand gamma distributionshape parameters es- 133 cyt b [35.8%]).Both geneshave a similar timated). Finally, the assumption of a molecular clockwas assessedusing ML analyses.A lack of sig- proportion of informative sites acrosscodon nificant difference in likelihood scores with the ad- positionsexcept that ND2 has proportionally dition of parametersdictated that the lessparameter- twice as many informative second-position rich model would be used in further ML searches. sitescompared with cyt b (10.7%vs. 4.0%). ML searcheswere then performed with themodel of Neitherpartition-homogeneity test was sig- evolutionsuggested by theLRTs and the startingpa- nificant,suggesting that differencesin phylog- rameters(empirical base frequencies, matrix of sub- eniesfrom thesepieces of cyt b and ND2 (P = stitution types, proportion of invariant sites, and 0.16)can be attributedto samplingerror, as can shapeof gamma distribution)estimated from the original NJ tree. Ten addition sequencereplicates differencesbetween first and secondcodon po- were performedusing heuristicsearches. Only one sitionscompared with third (P = 0.65). Thus, addition sequencereplicate was performedfor each sequencedata from all regions(cyt b, ND2, and of the 100bootstrap replicates because of time limi- spacerregions) were combined for phylogenet- tations. ic analyses. October1999] GeneticDifferentiation in Antbirds 1097

TABLE1. Sequencevariation of spacerbetween cyt-b and threonine t-RNA genes.

Taxon Family Spacersequence Piprapipra Pipridae CT Formicarius colma Formicariidae CT Lepidocolaptesangustirostris Dendrocolaptidae AC Dendrocolaptescerthia Dendrocolaptidae ACa Synallaxisalbescens Furnariidae AACC Smithornissharpei Eurylaimidae CGCAa Herpsilochmusrufimar ginatus Thamnophilidae CGT Myrmotherulaleucophthalma Thamnophilidae CGT Hypocnemiscantator (Mato Grosso) Thamnophilidae CGT Drymophiladevillei devillei (La Paz,Pando, Acre) Thamnophilidae CGT Drymophilacaudata Thamnophilidae CGT Hylophylaxnaevia Thamnophilidae CGTø Hylophylaxpunctulata Thamnophilidae CGTb Hylophylaxnaevioides Thamnophilidae CGTø Formicivoragrisea Thamnophilidae CGC Formicivorarufa Thamnophilidae CAC Teremura humeralis Thamnophilidae CAC Myrmotherulalongipennis Thamnophilidae CAC Phlegopsisnigromaculata Thamnophilidae CAC Hypocnemishypoxantha Thamnophilidae CAC Hylophylaxpoecilinota Thamnophilidae CACb Hypocnemoidesmaculicauda Thamnophilidae CACb Drymophiladevillei "subochracea" (Rond6nia, Santa Cruz) Thamnophilidae CAC Hypocnemiscantator (Rond6nia, Santa Cruz) Thamnophilidae CAT Myrmotherulahauxwelli Thamnophilidae CAT Thamnophilusdoliatus Thamnophilidae CCCa

Mindell et al. 1998. j. M. Bates unpubl. data.

Equallyweighted parsimony analyses.--Equally grouprelationship between the two Drymophila weightedparsimony analyses resulted in a sin- species.Deep mitochondrialdivergences also gle most-parsimonioustree (length997; CI = occur among populationsof Hypocnemiscanta- 0.41,excluding uninformative characters; RI = tor (up to 6% sequencedivergence), and some 0.67;Fig. 2). The formicariidantbird (Formicar- relationshipsreceive strong support. Satura- ius colma)is separatedfrom the thamnophilid tion analysessuggest that substitutionswithin antbirds, and Formicariusis in a clade with the and among both Drymophilaand Hypocnemis woodcreeper (Lepidocolaptes)and ovenbird speciesare not saturated.Therefore, relation- (Synallaxis).This relationshipis not supported shipswithin thesegenera as suggestedby the by bootstrapanalyses, nor is a sisterrelation- equal-weightanalyses are preferred. ship betweenthe woodcreeperand ovenbird. Weightedparsimony analyses.--Although sat- Monophyly of thamnophilidsreceives only urationdoes not appearto be a problemwithin 56% bootstrapsupport. Among higher-level and amongantbird species, when other antbird antbird relationships,bootstrap values (Fig. 2) generaare included,transitions at first and indicatestrong support for monophylyof For- third positionsare saturated (plots not shown). micivoraand for a cladeincluding We applied step matricesto thesedata parti- longipennisand (although these taxa tions that counted 2 to 1,000 stepsfor a trans- are not very similarto eachother genetically, version and only one step for a transition, differing by 11% uncorrectedsequence diver- thereby down-weightingthe transitions.Be- gence;Table 2). Hypocnemisis not monophyletic causesecond positions were not saturatedin in equally weightedanalyses, and Hypocnemis this analysis,they were given a weightof 2 to cantatoris the sister taxon to Drymophila(al- 1,000to make them equalto the transversions though this relationshipis not supportedby at first and third positions. bootstrapanalyses). Strong support existsfor The 2x weightedanalysis resulted in four nodeswithin Drymophilaspecies, monophyly most-parsimonioustrees (length 1,294; strict- of each speciesof Drymophila,and a sister- consensustree shown in Fig. 3A). A sister- 1098 BATES,HACKETT, AND GOERCK [Auk,Vol. 116

OUTGROUP(Pipra pipra) Formicarius colma so23 Synallaxisalbescens 47 Lepidocolaptesangustirostris Terenura humeralis 58 Myrmotherulalongipennis 9526 396•24Formicivora grisea 26 t• 15 Formicivoratufa

47 Myrmotherulaleucophthalma Herpsilochmusrufimarginatus Myrmotherulahauxwelli E Hypocnemishypoxantha, Madre de Dios(118161, 118195) 23 2 Hypocnemishypoxantha, Acre (118162, 118196) Hypocnemiscantator, Loreto (118167,118201) Hypocnemtscantator, Mato Grosso(118165, 118199) 21 Hypocnermscantator, Mato Grosso(118164, 118198) '20•14 97 52 1110••06Hypocnemiscantator, RondOnia (118168, 118202) ioo1- 17 6/[•_•--Hypocnemis cantator, Santa Cruz (118163,118197) Hypocnermscantator, Santa Cruz (118166,118200) caudata,Pasco (118173, 118207) caudata,Pasco (118172, 118206) 98 15 caudata,Napo (118170,118204) 11 caudata,Puno (118171,118205) devillei, Acre (118174,118208) 92 devillei, Pando (118178,118212) devillei, Pando ( 118177,118211) devillei,Santa Cruz (118183,118217) devillei, Santa Cruz (118184,118218) devillei,Rond6nia (118180,118214) devillei, Rond6nia (118182,118216) devillei,Rond6nia (118179,118213) devillei, Drymophila Rond6nia (118181,118215) devillei,La Paz (118176,118210) , Z devillei,La Paz (118175,118209)

parsimonyanalysis with equalweights of characters one most parsimonioustree length997, CI = 0.41,RI = 0.67

FIG.2. Parsimonyanalysis with equalweights of mitochondrialcytochrome-b and ND2 characters.Num- bersabove the branchesare bootstrapvalues for nodeswith 50%support or better.Numbers below the branchesare branch lengths. grouprelationship between the ovenbird (Syn- The relationshipbetween Myrmotherula longi- allaxis)and the woodcreeper(Lepidocolaptes) pennis and Formicivorawas found with this was supportedin 77% of the bootstraprepli- weightingscheme as well (98%bootstrap). cates.Monophyly of the thamnophilidswas The5x weightingresulted in onemost-par- supportedby a 90% bootstrapvalue. Relation- simonioustree (length2,178; Fig. 3B) and dif- shipswithin Drymophila and Hypocnemis were feredfrom 2x weightingin supportinga basal unchangedfrom equal weightingwith this positionfor the woodcreeper/ovenbirdclade weightingscheme (not shown). However, a sis- with the formicariid(Formicarius colma) as sis- ter-taxonrelationship between the two Hypoc- ter to the thamnophilids.Hypocnemis is mono- nemisspecies was recoveredin three of the four phyletic(88% bootstrap) and sisterto Drymo- most-parsimonioustrees (bootstrap support of phila(89% bootstrap), as in the 2x weighted 55%),and thesespecies are placedas sisterto analysis.Relationships among other antbird Drymophilawith highbootstrap support (82%). generavary dependingon weightingscheme. October1999] GeneticDifferentiation in Antbirds 1099

Relationshipswithin Drymophilaand Hypoc- Two clades are supported, one containing nemisremained unchanged from unweighted birds from sites in northern Bolivia (DEVI La analyses. Paz, DEVI Pandoand DEVI Acre; Fig. 3) and Analysesdown-weighting first- and third- another of birds from sites in eastern Bolivia position transitionsby 10, 100, and 1,000x re- and western Brazil (DEVI Santa Cruz and DEVI suitedin the sametopology (Fig. 3C) with rel- Rond6nia). Both populationsfrom northern atively similar bootstrapvalues. These trees Bolivia have white breasts and are referable to differ in the placementof Terenurahumeralis; all nominate D. d. devillei. However, substantial otherrelationships are unchanged from the 5 x differentiation exists between samples from weightedanalysis. thesetwo localities(2.5% sequence divergence; Maximum-likelihoodanalyses.--Likelihood-ra- Table 2), whichare separatedby about370 km. tio testssuggested a modelof evolutionwith The taxonomicidentity of birds from eastern the following properties:(1) generaltime-re- Bolivia(DEVI SantaCruz) and the RioJiparanfi versible (six substitution types; substitution (westernBrazil, DEVI Rond6nia)is more prob- matrix estimated from original NJ tree); (2) lematic.Parker et al. (1997)described the Jipar- proportion of invariant sites estimatedusing anti birds as also being the nominateform. maximum likelihood (on NJ tree); (3) rates for However,a recentreexamination of thesespec- variablesites follow a gammadistribution with imensby JMB (in MPEG), in which malesof shapeparameter estimated by maximumlike- nominatedevillei were comparedwith a male lihood (on NJ tree); (4) empirical nucleotide from the Rio Jiparanfiand a male identifiedas frequencies;and (5) no assumptionof a molec- D. d. subochraceafrom the Rio Aripuanfi(ca. 350 ular clock.The followingparameters were de- km east-southeastof the Rio Jiparanfisite [No- rived from the initial NJ tree and were input vaes 1976]), revealed that the Jiparanfimale into the maximum-likelihoodalgorithm of was buffy below and thus more like the Ari- PAUP*prior to searches:empirical base fre- puanfibird thannominate devillei. Although no quencies,A = 0.31086, C = 0.32217, G = comparativematerial was available,three fe- 0.10711,T = 0.25987;proportion of invariant malesfrom the Rio Jiparanfisite alsowere buf- sites,0.539972; rates for variablesites following fy below(matching the originaldescription of a gamma-shapedistribution, 1.39454 (four rate D. d. subochracea;Chapman 1921). The speci- categories,average represented by mean); and mens from the Jiparanfihave not been directly a substitution-ratematrix (whichcan be recon- comparedwith Santa Cruz specimens;how- structedfrom the original data or obtained ever, JMB has seen both series and considers from the authorsupon request). Using these in- them to be identical. An additional problem put parameters and 10 addition sequencerep- arises becauseD. E Stotz (pers. comm.) notes licates, one tree resulted (-In likelihood score that the Rio Jiparanfiand Santa Cruz birds = 4779.89182;Fig. 4). This tree has relation- could representa distinctpopulation of D. de- ships among generaexactly as 10 to 1,000x villei.The typelocality of D. d. subochraceais the weighted analyses,including monophyly of Rio Curufi, a tributary of the Rio Iriri and sub- Hypocnemisand its sisterrelationship to Dry- sequentlythe Rio Xingu (Fig.1; Chapman 1921, mophila. specimensin the Museu Nacional,Rio de Ja- neiro,Brazil; no tissuesavailable for genetican- DISCUSSION alyses).Thus, this sitelies in a differentarea of endemismfrom the Jiparanfiand Santa Cruz Geneticstructure in Drymophiladevillei, Dry- sites(the Parfiarea of endemismrather than the mophila caudata,and Hypocnemiscantator.-- Rond6nianarea, followingCracraft [1985]). As Our datademonstrate high levelsof geneticdif- a result,it is conceivablethat populationsfrom ferentiationbetween the two Drymophilaspe- the Rond6nian area of endemism (DEVI Ron- cies(7.2%) and substantialgenetic differentia- d6nia and DEVI Santa Cruz) may representan tion among differentpopulations of all three undescribedtaxon. They are clearlygenetically biologicalspecies that we examined.For D. de- and morphologicallydistinct from populations villei, multiple individuals were available for west of the Madeira (DEVI La Paz and DEVI most localities, and individuals from the same Pando). localitiesexhibited little, if any,differentiation. Althoughadditional sampling and specimen 1100 BATES,HACKETT, AND GOERCK [Auk, Vol. 116

TABLE2. Uncorrectedsequence divergence between taxa. Numbers in parenthesesare the lastthree digits of GertBank accession numbers.

Taxon I 2 3 4 5 6 7 8 9 10 11 12 13

1 Pipra -- 2 Lepidocolaptes 0.223 3 Synallaxis 0.217 0.153 -- 4 Formicarius 0.219 0.180 0.165 -- 5 Herpsilochmus 0.218 0.176 0.178 0.180 -- 6 Formicivoragrisea 0.214 0.190 0.180 0.179 0.142 -- 7 Formicivorarufa 0.224 0.187 0.183 0.173 0.152 0.055 8 Terenura 0.215 0.193 0.190 0.181 0.169 0.154 0.166 -- 9 Myrmotherulalongipennis 0.215 0.197 0.185 0.200 0.147 0.111 0.101 0.167 -- 10 MyrmotheruIaleucophthalma 0.219 0.198 0.170 0.181 0.150 0.149 0.147 0.159 0.145 -- 11 Myrmotherulahauxwelli 0.245 0.205 0.174 0.196 0.146 0.153 0.153 0.162 0.152 0.153 -- 12 H. hypoxantha(161, 195) 0.224 0.184 0.160 0.159 0.140 0.138 0.138 0.160 0.132 0.136 0.129 13 H. hypoxantha(162, 196) 0.224 0.183 0.159 0.162 0.143 0.135 0.135 0.162 0.132 0.135 0.129 0.003 -- 14 H. cantatorLoreto (167, 201) 0.232 0.186 0.166 0.172 0.129 0.132 0.125 0.163 0.126 0.136 0.135 0.093 0.093 15 H. cantatorRend (168, 202) 0.229 0.186 0.175 0.165 0.128 0.125 0.121 0.162 0.135 0.140 0.139 0.089 0.089 16 H. cantatorS. Cruz (166, 200) 0.227 0.185 0.173 0.168 0.131 0.123 0.121 0.162 0.135 0.142 0.141 0.090 0.090 17 H. cantatorS.Cruz (163, 197) 0.231 0.186 0.174 0.165 0.132 0.126 0.122 0.159 0.136 0.143 0.139 0.093 0.093 18 H. cantatorM.Gros(164,198) 0.220 0.197 0.166 0.162 0.132 0.125 0.124 0.162 0.139 0.138 0.136 0.089 0.087 19 H. cantatorM. Gres (165,199) 0.219 0.197 0.166 0.162 0.132 0.125 0.124 0.162 0.139 0.138 0.136 0.088 0.087 20 D. devilleiLa Paz (175, 209) 0.245 0.203 0.180 0.166 0.142 0.139 0.148 0.176 0.163 0.148 0.136 0.125 0.128 21 D. devilleiLa Paz (176, 210) 0.245 0.201 0.176 0.169 0.139 0.136 0.149 0.176 0.160 0.146 0.136 0.125 0.125 22 D. devilleiPando (177, 211) 0.253 0.211 0.187 0.170 0.143 0.140 0.145 0.178 0.167 0.156 0.145 0.125 0.128 23 D. devillei Pando (178, 212) 0.249 0.208 0.184 0.167 0.140 0.140 0.145 0.176 0.164 0.153 0.142 0.122 0.125 24 D. devilleiAcre (174, 208) 0.250 0.208 0.184 0.167 0.140 0.138 0.142 0.176 0.164 0.153 0.142 0.122 0.125 25 D. devilleiRend (179, 213) 0.245 0.207 0.181 0.169 0.145 0.136 0.140 0.166 0.154 0.154 0.138 0.121 0.124 26 D. devilleiRend (180, 214) 0.243 0.205 0.180 0.167 0.143 0.138 0.142 0.164 0.156 0.153 0.136 0.119 0.122 27 D. devilleiRend (181, 215) 0.243 0.205 0.180 0.167 0.143 0.138 0.142 0.164 0.156 0.153 0.136 0.119 0.122 28 D. devilleiRend (182, 216) 0.243 0.205 0.180 0.167 0.143 0.138 0.142 0.164 0.156 0.153 0.136 0.119 0.122 29 D. devilleiS. Cruz (183, 217) 0.242 0.204 0.178 0.166 0.143 0.136 0.140 0.163 0.152 0.152 0.136 0.118 0.121 30 D. devilleiS.Cruz (184, 218) 0.245 0.207 0.181 0.169 0.146 0.139 0.143 0.166 0.154 0.154 0.139 0.121 0.124 31 D. caudataPune (171, 205) 0.238 0.203 0.169 0.167 0.150 0.140 0.152 0.170 0.160 0.154 0.131 0.112 0.115 32 D. caudataPasco (172, 206) 0.242 0.204 0.169 0.163 0.150 0.143 0.152 0.164 0.164 0.153 0.129 0.101 0.104 33 D. caudataPasco (173, 207) 0.239 0.200 0.169 0.160 0.146 0.138 0.146 0.159 0.162 0.150 0.125 0.098 0.101 34 D. caudataNape (170, 204) 0.243 0.204 0.174 0.167 0.149 0.140 0.153 0.159 0.166 0.154 0.131 0.107 0.110

comparisonsare needed, our findings demon- bamboo-associatedspecies would be morelike- stratethat D. devilleipopulations from eastand ly candidatesthan other forest birds to cross west of the Rio Madeira (Fig. 1) are substan- large rivers. With respectto D. devilleiand the tially differentiatedfrom one another geneti- Rio Madeira, this does not seem to be the case. cally,whereas populations from the samesides As with many specieshaving narrow distri- of the river are more similar.The geneticdif- butionsalong the easternslopes of the Andes, ferentiationacross the river is matchedby it is unknownwhether D. caudatais truly dis- plumagedifferences. Many otheravian taxa are continuouslydistributed (as shownin Ridgely separatedby the Rio Madeira (Hellmayr1910), and Tudor 1994), or incompletelysampled in a pattern that is in contrastto recent genetic manyareas. Our datasuggest that considerable studiesof rodentsand marsupialsalong the differentiation exists between sites in central smallerand more meanderingRio Jurua(Silva and southernPeru (2.4% divergencebetween and Patton1994). Drymophila devillei is the only Pascoand Puno). The foothills of the Andes are bamboospecialist with describedforms on op- amongthe mostbisected regions in the world, positebanks of the Rio Madeira. Becausebam- and a numberof deepriver valleysseparate the boo is considered a successional habitat occur- populationswe studied (mostnotably the Rio ring primarily along rivers, these patches Urubamba).As a result, we suspectthat ge- would be predictedto be temporary.As a re- netic differentiationamong these populations suit, one might expect that birds associated results from population subdivision (lack of with bamboowould require good dispersal ca- geneflow) and not from variationwithin a sin- pabilitiesin order to moveto new patchesas gle population. old ones disappeared through succession. Genetic differentiationin our limited geo- Also, bamboo patches can be quite small graphicsampling of Hypocnemiscantator was which might necessitatedispersal to new higherthan that found within eachspecies of patchesonce a patch becamesaturated with Drymophila.The highest divergencewas for territories.This leads to the predictionthat samplesseparated by the (5 to October1999] GeneticDifferentiation inAntbirds 1101

TABLE 2. Extended.

14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33

0.057 0.058 0.003 -- 0.060 0.006 0.006 -- 0.051 0.044 0.046 0.049 -- 0.051 0.045 0.046 0.049 0.000 -- 0.124 0.128 0.128 0.131 0.122 0.122 -- 0.119 0.126 0.127 0.129 0.121 0.121 0.007 0.119 0.115 0.116 0.115 0.113 0.112 0.025 0.025 -- 0.117 0.112 0.113 0.112 0.110 0.110 0.025 0.025 0.006 -- 0.117 0.112 0.113 0.112 0.110 0.110 0.022 0.022 0.003 0.003 -- 0.117 0.114 0.114 0.114 0.114 0.114 0.031 0.032 0.021 0.021 0.018 -- 0.115 0.112 0.113 0.112 0.113 0.112 0.030 0.031 0.020 0.020 0.017 0.001 -- 0.115 0.112 0.113 0.112 0.113 0.112 0.030 0.031 0.020 0.020 0.017 0.001 0.000 -- 0.115 0.112 0.113 0.112 0.113 0.112 0.030 0.031 0.020 0.020 0.017 0.001 0.000 0.000 -- 0.114 0.111 0.111 0.111 0.108 0.108 0.034 0.035 0.024 0.024 0.021 0.006 0.004 0.004 0.004 0.117 0.114 0.114 0.114 0.111 0.111 0.034 0.035 0.024 0.024 0.021 0.006 0.004 0.004 0.004 0.003 -- 0.114 0.115 0.118 0.118 0.108 0.108 0.076 0.079 0.080 0.079 0.077 0.079 0.077 0.077 0.077 0.079 0.081 -- 0.111 0.105 0.107 0.107 0.103 0.103 0.075 0.079 0.073 0.073 0.070 0.072 0.070 0.070 0.070 0.072 0.074 0.024 -- 0.108 0.104 0.104 0.104 0.100 0.100 0.072 0.074 0.069 0.069 0.066 0.067 0.066 0.066 0.066 0.067 0.070 0.024 0.006 -- 0.117 0.112 0.113 0.112 0.111 0.111 0.072 0.074 0.069 0.069 0.066 0.067 0.066 0.066 0.066 0.067 0.070 0.027 0.017 0.011

6%);however, the moststriking finding was an micariidand thamnophilid split. Second, three apparentlysubstantial genetic break (4.5% di- membersof the large genusMyrmotherula are vergence)between populationsoccurring in not monophyletic,which is consistentwith re- the interfluvium between the Rio Madeira and sultsof earlier allozymestudies (Hackett and the Rio Tapaj6s.This divergencepossibly is Rosenberg1990). Also consistentwith the al- predictedby the describedsubspecies (follow- Iozymeresults is theclustering of Myrmotherula ing Peters1951), Hypocnemis c.implicata (for the longipenniswith Formicivora relative to theother Mato Grossobirds) and H. c.ochrogyna (for the taxa surveyed.Using Kishinoand Hasegawa Jiparan• and easternBolivian birds). Haffer (1989)maximum-likelihood tests to compare (1997)has noted other avian taxa with similar the unweightedor weightedtree topologies contactzones in this region.This level of ge- with topologiesthat includeMyrmotherula as a netic divergence,over 350 km of essentially monophyleticgroup, the sequencedata reject continuousforest with no largerivers or shifts monophylyof Myrmotherula(P < 0.01).Third, in habitat,warrants additional study. thehigh level of sequencedivergence (9.3%) be- Relationshipsof Drymophila to otherantbird tween the congenersHypocnemis cantator and genera.--Allof our analysessupport a sisterre- H. hypoxanthasuggests that speciationevents lationshipbetween Hypocnemis and Drymophi- betweenthese two took place severalmillion la. Becauseof high levelsof divergenceamong yearsago. This levelof divergenceis slightly antbirdgenera (Table 2), incompletetaxon sam- higher than the averagefor avian congeners pling, and low numbersof characters,we cau- (Johnsand Avise 1998), althoughit doesnot tionagainst over-interpretation ofother higher- reach levels of divergenceobserved in some level antbird relationshipssuggested by our otherNeotropical birds suchas potoos(Nycti- data.However, some aspects of theserelation- biusspp.; Mariaux and Braun1996). shipsare worth noting.First, all analysessug- Utility ofgene spacer regions for systematicques- gesta separationof Formicariuscolma from the tions.--Genespacer regions in mitochondrial other antbirdgenera, consistent with the for- DNA are often sequencedbecause of primer 1102 BATES,HACKETT, AND GOERCK [Auk,Vol. 116

OUTGROUP(Pipra pipra) A • Formicariuscolma Lepidocolpatesangustirostris Synallaxisalbescens

Terenura huraeralis 2x weightedparsimony strict consensus 98 10•oMyrmotherula longipennis 4 mostparsimonious trees length 1294,CI = 0.44, RI = 0.68 Formicivoraspp. Myrmotherulaleucophthalraa Herpsilochmusrufimarginatus Myrmotherulahauxwelli 100 Hypocnemishypoxantha 82I 100Hypocnemis cantator 100Dryraophila spp.

OUTGROUP(Pipra pipra) B Lepidocolpatesangustirostris 85[ Synallaxisalbescens Formicarius colma 5x weightedparsimony Terenura huraeralis 1 mostparsimonious tree length2178, CI = 0.45, RI = 0.70 94 Myrmotherulahauxwelli Myrmotherulaleucophthalraa

Myrmotherulalongipennis 99 Formicivoraspp. 8• Hypocnemishypoxantha 89 •- Hypocnemiscantator I 95 Drymophilaspp.

OUTGROUP(Pipra pipra)

c Lepidocolpatesangustirostris

ß Synallaxl'salbescens

Formicaflus colma 10,100, 1000x weighted parsimony strict consellSUS Terenura huraeralis 2 mostparsimonious trees . Myrmotherulaleucophthalma

Myrmotherulalongipennis

Formicivoraspp.

Herpsilochmusru)qmarginatus

ß Myrmotherulahauxwelli

Hypoc'nemishypoxantha

H!rpocnemiscantator

Drymophilaspp. F•G.3. Weightedparsimony analyses. (A) 2x; (B) 5x; (C) 10, 100,and 1,000x. Boostrap values shown abovebranches. In 3C,bootstrap values for 10,100, and 1,000x are listed from top to bottom,respectively. October1999] GeneticDifferentiation in Antbirds 1103

OUTGROUP(Pipra pipra) Lepidocolatesangustirostris Synallaxisalbescens

Formicaflus colma

Terenura humeralis

-- Myrmotherulaleucophthalma -- Formicivorarufa Formicivoragrisea Myrmotherulalongipennis -- Herpsilochmusrufimarginatus Myrmotherulahauxwelli Hypocnemishypoxantha (118161, 118195) -- Hypocnemiscantator (118167, 118201) Hypocnemiscantator (118163,118197) -- devillei,La Paz (118176, 118210)

100 ß devillei,Pando (118178,118212) devillei,santa Cruz (118183, 118217)

ß devillei,Rond6nia (118182, 118216) -- caudata,Puno (118171,118205)

Drymophila[ caudata,Napo (118170, 118204)

maximumlikelihood analysis onemost likely tree -In likelihood = 4779.89182

Ftc. 4. Maximum-likelihoodtree shownwith bootstrapvalues indicated above branches. placementin generegions adjacent to thegenes can showthat both the lengthand basecom- beingstudied. However, the phylogeneticutil- positionof the spacervary acrossthe group. ity of spacerDNA sequencesbetween sequenc- Based on limited sampling, suboscineout- esof knownfunction has not beenexplored of- groupshave either two bases (CT, Pipridae and ten (but seeMcKnight and Shaffer1997), and Formicariidae;AC, Dendrocolaptidae)or four these sequencesare not usually reported in bases(AACC, Furnariidae;CGCA, Eurylaimi- data bases such as GenBank. Inclusion or exclu- dae),whereas all thamnophilidssampled have sionof the smallspacer region between cyt b three bases. We found five different spacer and the threoninet-RNA did not changeany of typeswithin thamnophilids(Table 1). Within the resultsof our study,but the spacerregion Drymophiladevillei, populations from eastern did containphylogenetic information at all lev- Bolivia and western Brazil (DEVI Santa Cruz elsof thetaxonomic hierarchy that we surveyed and DEVI Rond6nia,respectively) have a dis- (Table1). By combiningour data with those tinct spacerfrom La Paz and Pandopopula- from other suboscines(Mindell et al. 1998),we tions.Different spacersalso occurred in Hypoc- 1104 BATES,HACKETT, AND GOERCK [Auk,Vol. 116 nemiscantator samples. In both cases,these CRACRAFT,J. 1985. Historical biogeography and pat- charactersare consistentwith phylogenetic terns of differentiation within the South Amer- patternsin the protein-codingsequences (see ican avifauna:Areas of endemism.Pages 49-84 above).This alsosuggests that thereis homo- in Neotropicalornithology (P. A. Buckley,M. S. plasyin thesesequences. For example, the spac- Foster, E. S. Morton, R. S. RidRely, and F. G. Buckley,Eds.). OrnithologicalMonographs No. er CAC occursin somepopulations of Drymo- 36. phila devillei(DEVI Santa Cruz and DEVI Ron- CUNNINGHAM,C. W. 1997. Is congruencebetween d6nia) and in six other generaof thamnophil- data partitionsa reliablepredictor of phyloge- ids. Although these spacerregions contain netic accuracy?Empirically testing an iterative homoplasyand present character-coding prob- procedurefor choosingamong phylogenetic lemstypical of all non-codingDNA, theyclear- methods.Systematic Biology 46:464-478. ly containphylogenetically informative infor- DESJARDINS,P., ANDg. MORALS.1990. Sequence and mationas well, and we advocatereporting the geneorganization of the chickenmitochondrial sequencesof theseregions and incorporating genome.Journal of Molecular Biology 212:599- thesedata into phylogenetic reconstructions. In 634. our study,including these characters did not FARRIS, J. S., M. K.•LLERSJ•),A. G. KLUGE, AND C. affectthe phylogenies,but they couldin other BULT. 1995. Testing significanceof incongru- ence. Cladistics 10:315-319. situations. Thehigh levels of geneticdivergence that we FELSENSTEIN,J. 1985. Confidence limits on phyloge- nies:An approachusing the bootstrap.Evolu- foundwithin thesebiological species of Ama- tion 79:783-791. zonianbirds suggest that multiple distinct evo- GRIFFITHS, C. S. 1997. Correlation of functional do- lutionary lineagesoccur within many other mainsand ratesof nucleotidesubstitution in cy- Amazonian species. It remains to be seen tochromeb. MolecularPhylogenetics and Evo- whether this geneticdiversity is consistent lution 7:352-365. with other character sets such as vocalizations HACKETT,S. J. 1996. Molecular phylogeneticsand (e.g.Isler et al. 1998),but thesedata suggest biogeographyof tanagersin the genusRampho- that our current species-levelclassification celus(Aves). Molecular Phylogenetics and Evo- greatlyunderestimates the diversityof Ama- lution 5:368-382. zonian birds. HACKETT, S. J., AND K. V. ROSENBERG.1990. A com- parisonof phenotypicand geneticdifferentia- ACKNOWLEDGMENTS tion in South American antwrens (Formicari- idae). Auk 107:473-489. We thank the LSUMNS, ANSP, MPEG, and HAFFER, J. 1997. Contact zones between birds of MZUSP for accessto specimensand tissues and southernAmazonia. Pages 281-306 in Studiesin gratefullyacknowledge the field effortsof manycol- Neotropicalornithology honoring Ted Parker (J. leagueswho helped collectthis material. We also V. Remsen,Jr., Ed.). OrnithologicalMonographs thank the variouspermit-granting agencies in Ec- No. 48. uador, Peru, Bolivia, and Brazil for their support. HASEGAWA, M., H. KISHINO, AND K. YANO. 1985. Specialthanks go to the Museode Historia Natural Dating of the human-apesplitting by a molec- "Noel Kempff Mercado," SantaCruz, Bolivia. M. L. ular clock of mitochondrial DNA. Journalof Mo- Isler preparedthe map. This researchwas carried out lecular Evolution 22:160-174. in the PritzkerLaboratory for MolecularSystematics HELLMAYR,C. E. 1910. The birds of the Rio Madeira. and Evolutionoperated with supportfrom thePritz- NovitatesZoologicae 17:257-428. ker Foundation.We thank Lee Weigt,researchers in HUELSENBECK,J.P., AND D. M. HILLIS. 1993. Success the Field Museum's Pritzker Lab, and Bette Loiselle of phylogeneticmethods in the four-taxoncase. for their assistance.Support for this projectcame from Academic Affairs and the Ellen Thorne Smith SystematicBiology 42:247-264. Fund of FMNH and a Universityof Missouri-St.Lou- HUELSENBECK,J.P., AND B. RANNALA.1997. Phylo- is ResearchAward (to B. Loiselle).The manuscript geneticmethods come of age:Testing hypothe- was improvedby the commentsof D. F. Stotz,Allan sesin an evolutionarycontext. Science 276:227- 232. Baker,and three anonymousreviewers. ISLER, M. L., E R. ISLER, AND B. M. WHITNEY. 1998.

LITERATURE CITED Useof vocalizationsto establishspecies limits in antbirds(Passeriformes: Thamnophilidae). Auk CHAPMAN,F. M. 1921. Descriptionsof apparently 115:577-590. new birds from Bolivia, Brazil, and Venezuela. JOHNS,G. C., AND J. C. AVISE.1998. A comparative American Museum Novitates 2:1-8. survey of genetic distancesin vertebratesfrom October1999] GeneticDifferentiation in Antbirds 1105

the mitochondrialcytochrome b gene.Molecular patrick, T A. Parker Ill, and D. A. Moskovits, Biology and Evolution 15:1481-1490. Eds.).University of ChicagoPress, Chicago. KISHINO, H., AND M. HASEGAWA.1989. Evaluation of PARKER,t. A. III, D. F. STOTZ, AND J. W. FITZPATRICK. the maximum likelihood estimate of the evolu- 1997. Notes on avian bamboo specialistsin tionary tree topologies from DNA sequence southwesternAmazonian Brazil. Pages543-548 data, and the branchingorder in Hominoidea. in Studiesin Neotropicalornithology honoring Journal of Molecular Evolution 29:170-179. TedParker (J. M Remsen,Jr., Ed.). Ornithological KRATTER,A. W. 1997.Bamboo specialization by Am- MonographsNo. 48. azonianbirds. Biotropica29:100-110. PETERS,J. L. 1951. Check-list of birds of the world, MARIAUX, J., AND M. J. BRAUN. 1996. A molecular vol. 7. Museum of ComparativeZoology, Cam- phylogeneticsurvey of the nightjarsand allies bridge,Massachusetts. (Caprimulgiformes)with specialemphasis on RIOGELY,R., AND G. TUDOR.1994. The birds of South the potoos(Nyctibiidae). Molecular Phylogenet- America.Vol. 2, The suboscinepasserines. Uni- ics and Evolution 6:228-244. versity of TexasPress, Austin. SIBLEY,C. G., ANDJ. E. AHLQUIST.1990. Phylogeny MAYR,E. 1963. speciesand evolution.Belk- and classificationof birds. YaleUniversity Press, nap Press,Cambridge, Massachusetts. New Haven, Connecticut. MCKNIGHT,M. L., ANDH. B. SCHAFFER.1997. Large SILVA, M. N. F., AND J. L. PATTON. 1994. Amazonian rapidly evolvingintergenic spacers in the mi- phylogeography:MtDNA sequencevariation in tochondrial DNA of the salamander family arborealechimyid rodents (Caviomorpha). Mo- Amystomatidae(Amphibia: Caudata).Molecu- lecularPhylogenetics and Evolution2:243-255. lar Biologyand Evolution14:1167-1176. STOTZ,D. E 1990.First specimensof Drymophilade- MINDELL, D. P., M.D. SORENSON,AND D. E. DIM- villei from Colombia. Bulletin of the British Or- CHEFF.1998. Multiple originsof mitochondrial nithologists'Club 110:37-38. geneorder in birds.Proceedings of the National STOTZ,D. E, S. M. LANYON, t. S. SCHULENBERG,D. E. Academyof SciencesUSA 95:10693-10997. WILLARD, A. t. PETERSON,AND J. W. FITZPAT- NOvAES,F. C. 1976.As avesdo rio Aripuana, Estados RICK.1997. An avifaunal surveyof two tropical de Mato Grosso e Amazonas. Acta Amazonica 6: forestlocalities on the middleRio Jiparana,Ron- 61-85. d6nia, Brazil. Pages763-781 in Studies in Neo- PARKER,T. A. Ill. 1982. Notes on some unusual rain tropicalornithology honoring Ted Parker(J. V. forest birds and marsh birds in southeastern Remsen,Jr., Ed.). OrnithologicalMonographs Peru. Wilson Bulletin 104:173-178. No. 48. PARKER,T. A. III, D. F. STOTZ, AND J. w. FITZPATRICK. YANG,Z. 1994.Estimating the patternof nucleotide 1996. Ecologicaland distributional databases. substitution. Journal of Molecular Evolution 39: 105-111. DatabaseA. Pages131-291 in Neotropicalbirds: Ecologyand conservation(D. E Stotz,J. W. Fitz- AssociateEditor: A. J. Baker 1106 BATES,HACKETT, AND GOERCK [Auk, Vol. 116

zzz