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A MOLECULAR PHYLOGENY of the DOVE GENERA <I>

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A MOLECULAR PHYLOGENY of the DOVE GENERA <I> The Auk 118(4):874-887, 2001 A MOLECULAR PHYLOGENY OF THE DOVE GENERA STREPTOPELIA AND COLUMBA KEVIN P. JOHNSON,L3,s SELVINO DE KORT,2 KAREN DINWOODEY,3 A. C. MATEMAN,4 CAREL TEN CATE,2 C. M. LESSELLS,4 AND DALE H. CLAYTON3 •IllinoisNatural History Survey,Champaign, Illinois 61820, USA; 2Instituteof Evolutionaryand Ecological Sciences, Leiden University, Leiden, The Netherlands; 3Departmentof Biology,University of Utah,Salt Lake City, Utah84112, USA;and 4NetherlandsInstitute of Ecology,Heteren, The Netherlands ABSTRACT.--Evolutionaryhistory of the dove genus Streptopeliahas not been examined with rigorousphylogenetic methods. We presenta study of phylogeneticrelationships of Streptopeliabased on over3,600 base pairs of nuclearand mitochondrialgene sequences. To testfor monophylyof Streptopelia,we usedseveral other columbiform taxa, including Colum- ba(Old and New World),Macropygia, Reinwardtoena, and the enigmaticPink Pigeon(Nesoenas mayeri).On the basisof our analyses,Streptopelia (as currently defined) is not monophyletic; Nesoenasmayeri is the sisterspecies to S.picturata, resulting in paraphylyof Streptopelia.Three main cladesof Streptopeliaare identified: (1) S. chinensisplus S. senegalends,(2) S. picturata plus Nesoenasmayeri, and (3) all other speciesof Streptopelia.It is unclearwhether thoseclades form a monophyleticgroup to the exclusionof Old World Columba,but severalanalyses pro- ducethat result.Species of Old World Columbaare closelyrelated to Streptopelia,with species of New World Columbaclustering outside that group.Taxonomic changes suggested by our resultsinclude merging Nesoenaswith Streptopeliaand changingthe genericname for New World Columbaspecies to Patagioenas.Vocal similarities between S. picturata and N. mayeriare striking, given the generaldiversity of vocalizationsin other species.Received 20 September 2000, accepted27 March 2001. SPECIESOF DOVES in the genusStreptopelia are lationshipswithin the genusare uncertain.No- important model systemsfor studiesof physi- wak (1975)examined morphological character- ology (Walker et al. 1983, Janik and Buntin istics within Streptopeliaand produced a 1985, Cheng 1986,Ramos and Silver 1992, ten classificationthat grouped speciesinto several Cate et al. 1993,Lea et al. 1995,Georgiou et al. subgenera.However, he did not producean ex- 1995) and behavior (Lade and Thorpe 1964, plicit phylogenetictree. Goodwin (1983) de- Zenone et al. 1979, Cheng et al. 1981, Cheng picts a tree of "presumed relationships" 1992, Slabbekoorn and ten Cate 1998, Slabbe- among speciesof Streptopelia,and that tree dif- koornet al. 1999).The 16 speciesof Streptopelia fers from Nowak's classification, but Goodwin's historically had an African and Eurasian dis- tree is not based on a rigorous phylogenetic tribution, but some specieshave been intro- analysis.Johnson and Clayton (2000a)showed duced to the New World and Australia. Several that speciesof Old World Columbaform the sis- speciesof Streptopeliaseem highly adaptableto ter group to Streptopelia,with speciesof New human-altered environments and have ex- World Columbabeing more distantly relatedto panded their ranges considerably(e.g.S. de- both groups. However, the authors included caocto;Bijlsma 1988, Hengeveldand van den only single representativesof Streptopeliaand Bosch1991, Hengeveld 1993, Kasparek 1996). Old World Columbain their study.The goal of Other specieshave remarkably localized distri- the presentstudy is to assessmonophyly of the butions(e.g.S. hypopyrrha).An understanding genus Streptopeliaand identify relationships of historical relationshipswould provide an within the genus.We alsouse this study to test importantcontext for work on physiology,be- Nowak's (1975) classification and Goodwin's havior,and biogeographyof this genus. (1983)proposed relationships of specieswithin Eventhough species of Streptopeliahave been the genus.We include severalrepresentatives well studiedin manyrespects, phylogenetic re- of New and Old World Columba, as well as the endangered,enigmatic Pink Pigeon (Nesoenas E-mail: [email protected] mayeri)of Mauritius. We alsoinclude represen- 874 October2001] Phylogeny0f Streptopelia 875 tatives of Macropygiaand Reinwardtoena,which of individual variation within each species,we se- togetherwith Columbaand Streptopeliaform a quenced (when available) multiple individuals for distinct clade within Columbiformes (Johnson the COI gene (see Table 3 for list of those multiple and Clayton 2000a). The entire phylogenetic individuals and GenBank accessionnumbers). Mi- tochondrial genes tend to evolve at similar rates at analysisis rooted on Geotrygon,Leptotila, and low levelsof sequencedivergence in birds (Johnson Zenaida,which together consitute the sister and Sorenson1998, Johnsonand Lanyon 1999) and group to the Columba/Streptopelia/Macropygiamore specificallyfor cyt b, ND2, and COI in Col- clade (Johnsonand Clayton 2000a). umbiformes (Johnson and Clayton 2000b). Mito- For our current study, we use sequencesof chondrial divergencesare also highly correlated both mitochondrial and nuclear genesto con- with divergencesin FIB7 in Columbiformes(Johnson structa phylogenyfor Streptopelia,Columba, and and Clayton 2000a, b). Thus, within-speciesvaria- relatedtaxa. We comparerelative usefulness of tion in COI sequencesis likely to be representativeof nuclearand mitochondrialgenes for phyloge- other mitochondrialand nuclear genes.In general, netic resolutionat that level.Using the phylog- individualsof the samespecies differed only slightly, if at all, in thoseCOI sequences(see below), so single eny we recommendsome changes in taxonomic exemplar individuals are reasonablefor the multi- classification,and comparephylogeny to vocal gene data set. similarities and diversity in Streptopelia. Where possible,we used tissueor feathersamples to avoid risk of nuclear copies of mitochondrial METHODS genes (Sorensonand Quinn 1998). In caseswhere blood sampleswere used,we verified sequencesfor Sequencing.--Weobtained samplesof muscle tis- COI using multiple individuals. We also checked sues,feathers, or blood from representativesof 14 of chromatogramsfor signsof doublepeaks, as well as the 16 describedspecies of Streptopelia(Table 1). We checkingfor indels and stop codons.By sequencing also sampled members of New and Old World Co- several mitochondrial genes, we were also able to lumba,Macropygia, Reinwardtoer•a, Nesoenas, Geotry- te•t for any incongruencein phylogeniesresulting gon,Leptotila, and Zenaida.We extractedDNA from from thosegene regions, which would likely occurif those samplesusing a Qiagen Tissue Kit (Valencia, some of the sequencesrepresented nuclear copies. California) with the manufacturer'sprotocols. For We found no evidence of nuclear copies in our feather samples(-2 mm of the tip of the shaft) we sequences. alsoadded 30 btLof 10% DTT to the digestionbuffer. Phylogeneticanalysis.--Relative rates of substitu- Using PCR we amplifiedportions of three mitochon- tion can be examined by plotting pairwise sequence drial genes:cytochrome-b (cyt b), cytochromeoxi- divergences for various substitution types and dase I (COI), and NADH dehydrogenasesubunit 2 genes.For the nuclear gene(FIB7), we estimatedthe (ND2). We also amplified the nuclear gene [3-fibrin- "native" transition:transversionratio by plotting ogen intron 7 (FIB7). Table 2 lists primers used for pairwise transition differences against pairwise those reactions. Protocols for reactions follow John- transversiondifferences. Slope of the linear portion son and Clayton (2000a). of that curve estimates the transition:transversion ra- Direct sequencingof PCR products and determi- tio (Sturmbauer and Meyer 1992). We do not fit re- nation of sequenceswas performed as describedby gressionsthrough those points because they are non- Johnsonand Clayton (2000a).We aligned sequences independent, rather we use slopes as a rough acrossspecies using Sequencher(GeneCodes, Mad- indicator of relative rates. For mitochondrialgenes, ison, Wisconsin).The three mitochondrialgenes to- we plotted transition differenceat third positions taled 2,520 bp and the nuclear intron included 1,150 against transversionsat third positionsto estimate aligned base pairs (GenBankaccession numbers in that ratio. To estimate relative rates of mitochondrial Table 1). In the caseof mitochondrialprotein coding versusnuclear substitution, we plotted pairwise di- genes,alignment was straightforward.We noted sev- vergencesfor mitochondrialgenes against those for eral insertion-deletion (indel) events in the nuclear FIB7. We also plotted pairwise divergencesfor in- intron, but for those taxa, divergenceswere so low dividual mitochondrialgenes against each other and that manual alignment was straightforward.Gaps againstFIB7 to determinewhich genesare more sub- were treated as missingdata in phylogeneticanaly- ject to multiple substitution. ses. For Streptopeliatranquebarica and S. bitorquata, PAUP* (Swofford2000) was used for all phyloge- only partial FIB7 sequenceswere availablebecause of netic analyses.We used the partition homogeneity amplificationfailures. Thus, we repeatedanalyses test (Farris et al. 1994, 1995; Swofford 2000) to ex- involving the nuclearintron both with and without aminewhether the generegions could be considered thosespecies. samples of the same underlying phylogeny, or For each species,we included single representa- whether there was evidencefor different phyloge- tives for all sequences.However, to assessthe level netic signal between gene regions.Even though that 876 JOHNSONETAL.
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