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With an Emphasis on Gooseberries (Subg. Grossularia)

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SystematicBotany (2004),29(1): pp. 77– 96 q Copyright 2004by the AmericanSociety of PlantTaxonomists Molecular Phylogeny and Biogeography of Ribes (Grossulariaceae),with an Emphasis on Gooseberries (subg. Grossularia ) LISA M. SCHULTHEIS1,2,3 and MICHAEL J. DONOGHUE1 1Department ofEcology and Evolutionary Biology,Yale University,P.O.Box 208105, New Haven, Connecticut06520; 2The Arnold Arboretum ofHarvard University,125Arborw ay,JamaicaPlain, Massachuse tts 02130; 3Present address: Biological and Health Sciences Division, Foothill College,12345El Monte Road, Los Altos Hills, California94022 CommunicatingEditor: Matt Lavin ABSTRACT. Gooseberries are oftendistinguishe dfromcurrants as adistinctgenus ( Grossularia )orsubgenus ( Ribes subg. Grossularia ),but recent molecular phylogenetic analyses ofc hloroplast and nuclear data disagree as to the monophylyof this group.Wereport newsequence data fromthe 18–26S nuclear rDNAITSand ETSregions and fromthe chloroplast psbA- trnH intergenicspacer that, incombina tionwith pre viously reported data, suggestsubg. Grossularia ismonophy letic and nested within Ribes.Two main lineages are evident withinsubg. Grossularia ,correspondingto the true gooseberries(subg. Grossularia sect. Grossularia )and aclade ofglabrous-st yledwestern N orthAmerican gooseberries(subg. Grossularia sect. Robsonia, subg. Hesperia, Lobbia).Biogeograp hic analyses based on DIVAoptimizationssuggest a westernN orthAmerican originfor subg. Grossularia ,withsubsequent dispersal to east Asia givingrise to awell-supportedclade ofAsian gooseberry species insect. Grossularia .Thisexample contrastswith the well-documented pattern ofdispersal fromAsia toN orth America, and highlightsthe need toinvestiga te additional groups distributedwidely throughthe NorthernH emisphere. Ribes L. comprises approximately 150species of placedalong aseparatelineage .Asecond study using shrubby plants with strikingly diverse oraland fruit ITSsequence dataalso supported the monophyly of features.The infragenericclassication for Ribes varies the true gooseberries (sect. Grossularia ),but did not among the primary treatments (e.g.,J anczewski 1907; sample glabrous-styled gooseberries or spinycurrants Coville and Britton 1908;Berger 1924;Rehder 1940; (Fenton et al.2000). Given the long tradition ofrec- Sinnott 1985),creating adifcult taxonomy (reviews in ognizing the gooseberries asa distinct genus (e.g.,Co- Spongberg 1972;Sinnott 1985).One ofthe more nota- ville and Britton 1908;Berger 1924)or subgenus (Jan- ble and consistent divisions within the genus is be- czewski 1907;Sinnott 1985),one goalof this study was tween the currants (subg. Ribes)and the gooseberries toclarify the monophyly ofsubg. Grossularia . (subg. Grossularia ).Currants are mostly spineless Arst step towards addressing the monophyly of shrubs bearing multi-ow ered racemes with jointed the gooseberries (subg. Grossularia )is tocombine the pedicels, whereas gooseberries havenodal spines and availablechloropla st (Messinger et al.1999) and ITS sometimes bristly stems, bearfew- ow ered racemes (Senters and Soltis 2003)datasets, and toobtain addi- with non-jointed pedicels, and have highly reexed se- tional datato resolve apparentcon icts evident in pals(Senters and Soltis 2003).The differencesbetween these previous studies. Additional datamay result in gooseberries and currants have led manyresearchers aconvergence onto similar topologies, indicating that torecognize gooseberries atthe subgeneric(subg. the apparentcon ict was w eak or due toinsuf cient Grossularia )(Janczewski 1907;Sinnott 1985)or generic data,or alternatively,may reinforce the apparentcon- (Grossularia )(e.g.,Coville and Britton 1908;Berger ictbetw een the chloroplast and nuclear genomes, in- 1924)le vel. Previous phylogenetic analyses, however, dicating possible hybridization and introgression are atodds regarding the statusof the gooseberries as events in the history ofthe group (Rieseberg and Wen- anaturalgroup (Fig. 1).Sequence datafrom the nu- del 1993;A vise 1994).A dditional datasets reported clear18S– 26S rD NAinternal transcribed spacer(ITS) here include sequence datafrom the nuclearencoded region indicated monophyly ofsubg. Grossularia (Sen- 18S–26S rD NAexternal transcribed spacerregion ters and Soltis 2003),while restriction site datafrom (ETS)and from the chloroplast encoded psbA-trnH in- the 18S–26S n uclearrD NAregion (Messinger et al. tergenic spacerregion. Previous studies reported levels 1993)and from twochloroplas tregions indicated poly- ofv ariation in the ETS similar toor greater than those or paraphyly (Fig. 1;M essinger et al.1999). The chlo- typicalof the ITSregions (Baldwin and Markos 1998; roplastdata strongly resolved the morphologicallyin- Bena et al.1998; Linder et al.2000). Studies have also termediate spiny currants (subg. Ribes sect. Grossular- reported sufcient variation within the psbA-trnH in- ioides)asa paraphyletic grade subtending only the true tergenic spacerregion forph ylogeneticreconstruction gooseberries (subg. Grossularia sect. Grossularia ), while within genera (e.g.,Sang et al.1997; Mast and Givnish aclade ofglabrous-sty led gooseberries (subg. Hesperia, 2002;M ort et al.2002). Lobbia, and Grossularia sect. Robsonia)were weakly Asecond goalof this study wasto consider Ribes 77 78 SYSTEMATIC BOTANY [Volume 29 FIG.1. Asimplied representation ofprior phylogenetic hypotheses for Ribes.Chloroplast restrictionsite data fromMes- singeret. al.(1999) suggestthat gooseberries(subg. Grossularia )are non-monophyletic.ITS data fromSenters and Soltis(2003) support the monophylyof gooseberries. in the contextof N orthern Hemispherebiogeography. ofSouth America, butis especially diverse in western The Northern Hemisphereproblem has recently at- North America, bothin terms ofth enumber ofspecies tracted attention from aphylogeneticperspective,by and the representationof major subclades.Lik ewise, bothzoologists (e.g.,Sanmart ´‡net al.2001) and bota- subg. Grossularia ,which is the focusof our analysis, nists (e.g.,Manos and Donoghue 2001).It has become occursaround the Northern Hemisphere,butis most clearthat oristic similarities among the major areas diverse in western North America. Specically ,nu- ofendemism ,such aseastern Asia and eastern North merous glabrous-styled gooseberries (subg. Hesperia, America (see Bouffordand Spongberg 1983;W en Lobbia, and sect. Robsonia)are distributed in western 1999),were established in several ways (e.g.,move- North America, while the true gooseberries (sect. Gros- ment through Beringia or the North Atlantic)and at sularia)are foundthroughoutN orth America and Asia different times in different groups (e.g.,Tiffn ey 1985a; (including Taiwanand Japan),with one species in Eu- Manchester1999;W en 1999;Xiang et al.1998, 2000; rope.Better knowledge ofph ylogeneticrelationships in Donoghue et al.2001; Fritsch et al.2001; Manos and Ribes,and especially in Grossularia ,would make it pos- Stanford2001; Tiffney and Manchester 2001;Xiang sible toassess geographic patterns ofdiversi cation and Soltis 2001).Se veral recent studies have highlight- and directions ofmoveme nt in the group. ed plantgroups thatappear to have diversied ini- tially in Asia and subsequently moved toN orth Amer- MATERIALSAND METHODS icavia the Bering Land Bridge,apparently atse veral Samples. New data reported here include 12 ITSsequences , different times (e.g.,Donoghu eet al.2001; Xiang and 73 ETSsequences (from57 species), and 53 psbA-trnH sequences. Soltis 2001).This iterative trans-Beringian movement Previous studies provided an additional 67 ITSsequences (Senters resembles the pattern described formammals earlier and Soltis2003) and restrictionsite data fromtw oamplied chlo- roplast regions( rbcL to accD and rpoC1 to rpoC2)for32 species in the Tertiary (Beard 1998),and generally suggests (Messingeret. al. 1999). Oursampling was weightedtow ards thatAsia has been aprimary source areafor N orthern subg. Grossularia ,the focus ofthis study. Weincluded all ofthe Hemispherediversity.However,this may reect the true gooseberryspecies (sect. Grossularia )recognized bySinnott (1985), all ofthe Asian true gooseberryspecies recognized byBer- sample oftaxa that has been examined todate ,and ger(1924), representatives fromeach ofthe threeglabrous-sty led other patterns, including movement from North Amer- gooseberrytaxa (sect. Robsonia, subg. Hesperia, Lobbia), and both icato Asia, havealsobeen described (see examples in spinycurrant species (sect. Grossularioides ).In total, 82 ofthe ap- ‡ proximately150 species of Ribes were included inthis study (T able Sanmart´net al.2001). It is noteworthythatN orthern 1), representingall ofthe infragenerictaxa recognized byBerger Hemisphereplantgroups thatare especially diverse (1924), but withnomencla ture followingSinnott (1985). Itea, rep- today in western North America haveseldom been the resented by I.virginica and I.ilicifolia ,was chosen as the outgroup focusof ph ylogeneticbiogeographicanalyses. based on previouslyp ublished studies (Soltiset al. 1990, 1993; Morgan and Soltis1993; Soltisand Soltis1997), inwhich Ribes, Ribes is very broadly distributed around the North- Itea,and Saxifragaceae s.s. appeared to be closely related members ern Hemisphere,and extends south in the mountains ofSaxifragales . 2004] SCHULTHEISAND DONOGHUE: PHYLOGENY AND BIOGEOGRAPHY OF RIBES 79 DNAIsolation. Total DNAwas isolated fromfresh, silica-des- ETSprimer (Baldwin and Markos1998) under the followingpa- iccated, and herbariummaterial. Allextractions were performed
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