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Phylogenetic Reticulation in Subtribe Helianthinae Author(S): Edward E

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Phylogenetic Reticulation in Subtribe Helianthinae Author(S): Edward E Phylogenetic Reticulation in Subtribe Helianthinae Author(s): Edward E. Schilling and Jose L. Panero Source: American Journal of Botany, Vol. 83, No. 7 (Jul., 1996), pp. 939-948 Published by: Botanical Society of America Stable URL: http://www.jstor.org/stable/2446272 . Accessed: 26/12/2010 17:01 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=botsam. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Botanical Society of America is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany. http://www.jstor.org AmericanJournal of Botany 83(7): 939-948. 1996. PHYLOGENETIC RETICULATION IN SUBTRIBE HELIANTHINAE1 EDWARD E. SCHILLING2 AND JOSE L. PANERO3 Departmentof Botany,University of Tennessee, Knoxville, Tennessee, 37996-1100; and Departmentof Botany and Plant Pathology,Michigan State University,East Lansing, Michigan 48824-1312 Incongruencebetween phylogenetic estimates based on nuclearand chloroplastDNA (cpDNA) markerswas used to infer that there have been at least two instances of chloroplasttransfer, presumably through wide hybridization,in subtribe Helianthinae. One instance involved Simsia dombeyana, which exhibited a cpDNA restrictionsite phenotypethat was markedlydivergent from all of the otherspecies of the genus thatwere surveyedbut thatmatched the restrictionsite pattern previouslyreported for South Americanspecies of Viguiera.In contrast,analysis of sequence data fromthe nuclear ribosomal DNA internaltranscribed spacer (ITS) region showed Simsia to be entirelymonophyletic and placed samples of S. dom- beyana as the sistergroup to the relativelyderived S. foetida, a resultconcordant with morphological information. A sample of a South American species of Viguiera was placed by ITS sequence data as the sistergroup to a memberof V. subg. Amphilepis,which was consistentwith cpDNA restrictionsite data. Samples of Tithoniaformed a single monophyleticclade based on ITS sequence data, whereasthey were splitbetween two divergentclades based on cpDNA restrictionsite analysis. The results suggested that cpDNA transferhas occurred between taxa diverged to the level of morphologicallydistinct genera,and highlightthe need forcareful and completeassessment of moleculardata as a source of phylogeneticinformation. Key words: chloroplastDNA (cpDNA); Helianthinae;nuclear ribosomal DNA internaltranscribed spacer (ITS); phy- lopeneticreticulation. Study of phylogeneticreticulation is of particularin- tected,the competinghypothesis that the incongruenceis terestbecause the frequencyof naturalhybridization is the resultof homoplasious changes must also be consid- one of the most distinctiveyet poorly understoodele- ered, and thisis particularlyso when functionaltraits that mentsof floweringplant diversity (e.g., Grant,1981). De- could be subject to selective pressuresare used. The po- spite considerableinterest, the ultimateevolutionary sig- tentialfor homoplasy in such situationsis enhanced by nificanceof naturalhybridization remains uncertain.At the fact thatgroups close enough geneticallyto produce one end of the spectrum,it is possible thatnew genetic hybridswhen crossed will necessarilytend to have sim- combinationsproduced throughhybridization may lead ilar morphologicalor biochemical potentials.Lineage or to novel divergence,and thus be of evolutionarysignif- allelic sorting(Doyle, 1992) is yet anotheralternative hy- icance. In contrast,it has also been hypothesizedthat hy- pothesisthat may account forincongruence between data bridization is an "evolutionary sideshow," producing sets, particularlybetween gene trees. temporaldiversity that may be strikingbut has no trace- Detection of phylogeneticreticulation has been en- able long-termeffects. Phylogenetic reticulation may also hanced greatlyby the availabilityof methodsto analyze be of significanceas a potentialsource of errorfor clas- DNA variationdirectly. Molecular data are readily sub- sificationsystems that are based partlyor solely on in- divided into discrete sets, such as those for individual ferredphylogeny and thatemploy models of divergence genes, that still offerenough variantcharacter states to thatare strictlydichotomous. resolve phylogenetichypotheses. Many or most molec- Assessmentof the evolutionaryimportance of natural ular variantsmay be selectively neutral.Rieseberg and hybridizationis complicatedby the factthat the evidence Soltis (1991) summarize 36 examples of chloroplast forphylogenetic reticulation is based on patternsof char- DNA (cpDNA) "capture" involving 17 genera. A num- acter distributionswhose detectionis difficultand which ber of these examples involve cases in which phyloge- can be explained by alternativehypotheses. Evidence for netic reticulationhad not been anticipatedfrom other phylogeneticreticulation comes primarilyfrom incongru- types of data. ence of phylogeneticestimates based on differentchar- Detection of phylogeneticreticulation does not ensure acter sets. The existenceof discretesubsets of characters thatit is of evolutionarysignificance, but it does forma that are incongruentmay be overlooked when morpho- necessary foundationfor further examination of the phe- logical or chemical data are employed. Even when de- nomenon. In this respect,the documentationthat phylo- genetic reticulationhas occurred in a group prior to its 1 Manuscript received 3 May 1995; revision accepted 26 January. subsequentdivergence would be of particularimportance 1996. The authorsthank P. B. Cox and M. L. Schmid for technicalassis- by providingthe possibilitythat genetic materialtrans- tance, J. La Duke and D. Spooner for plant samples, and the staffof ferredthrough hybridization had alteredthe evolutionary MEXU for logistical support.Automated fluorescentsequencing was potentialof the group. Many of the examples cited by performedby the MSU-DOE-PRL Plant BiochemistryFacility using Rieseberg and Soltis (1991) involve single species within the ABI Catalyst 800 for Taq cycle sequencing and the ABI 373A a genus, or closely related species where the reticulation Sequencer forthe analysis of products.This researchwas supportedby may not differ substantiallyfrom regular gene flow NSF grantsDEB-9019158 to EES and DEB-9496174 to JLP. 2 Authorfor correspondence. throughoutcrossing. A notable exception is an example 3Current address:Department of Botany,University of Texas, Austin, involvingintergeneric cpDNA transferthat was reported Texas 78713-7640. by Soltis et al. (1991) fromSaxifragaceae. 939 940 AMERICAN JOURNAL OF BOTANY [Vol. 83 SubtribeHelianthinae has been the subject of several TABLE 1. List of samples of Helianthinaeused for chloroplastDNA previousmolecular studies,and phylogeneticreticulation restrictionstudies or for sequence studies of the nuclearribosomal internaltranscribed spacer region. * sample newly analyzed for in the subtribehas been documentedwithin a single sec- chloroplastDNA data. tion of one genus. The subtribeis a memberof the As- teraceae, tribeHeliantheae, and is well definedmorpho- Genus and logically (Robinson, 1981; Bremer,1994). Results of sur- sample number Species Geographicalorigin veys of cpDNA restrictionsite variationhave added ev- Heliomeris idence that the subtribe is monophyletic (Schilling, 1001 H. multiflora USA Panero, and Eliasson, 1994). The cpDNA studies have Pappobolus 720 P. lehmannii Ecuador also helped to confirmthat Viguiera, the core genus of Simsia the subtribe,is paraphyletic,and to refinethe circum- 4223*, 4230*, scriptionof, and suggest relationshipsfor, infrageneric 4272* S. amplexicaulis Mexico groups of the genus (Schilling and Jansen,1989; Schil- 443*, 2416* S. annectens Mexico 84-1 S. calva USA ling and Panero, 1991). Detailed studies of Helianthus 193*, 306* S. dombeyana Argentina,Ecuador sect. Helianthus have shown that phylogeneticreticula- 2434*, 2699 S. foetida Mexico, Honduras tion has been a significantevolutionary factor in thisdip- 1099* S. fruticulosa Ecuador loid, annual group (Rieseberg, Carter,and Zona 1990; 1803* S. ghiesbreghtii Mexico Beckstrom-Sternberg,and Doan, 1990; Rie- 2268* S. lagascaeformis Mexico Rieseberg, 2406*, 2468* S. sanguinea Mexico seberg, 1991; Rieseberg et al., 1991; Rieseberg and 88-43* S. spooneri Mexico Brunsfeld,1991). A broadersurvey has failed, however, 88-35* S. sylvicola Mexico to detectany evidence of intersectionalreticulation in the 2789* S. villasenorii Mexico genus (E. E. Schilling,unpublished data). Tithonia 2213*, 2862* T. calva Mexico Although application of data from molecular studies 2452* T. diversifolia Mexico has greatlyadvanced
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