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Phylogenetic, Morphological, and Chemotaxonomic Incongruence in the North American Endemic Genus Echinacea Lex E

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Phylogenetic, Morphological, and Chemotaxonomic Incongruence in the North American Endemic Genus Echinacea Lex E NCRPIS Publications and Papers North Central Regional Plant Introduction Station 6-2008 Phylogenetic, morphological, and chemotaxonomic incongruence in the North American endemic genus Echinacea Lex E. Flagel Iowa State University Ryan Adam Rapp Iowa State University Corrinne E. Grover Iowa State University, [email protected] Mark P. Widrlechner United States Department of Agriculture, [email protected] Jennifer S. Hawkins UFonilvloerwsit ythi of sGe aondrgi additional works at: http://lib.dr.iastate.edu/ncrpis_pubs Part of the Agricultural Science Commons, Agriculture Commons, Evolution Commons, See next page for additional authors Horticulture Commons, and the Plant Breeding and Genetics Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ ncrpis_pubs/26. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the North Central Regional Plant Introduction Station at Iowa State University Digital Repository. It has been accepted for inclusion in NCRPIS Publications and Papers by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Phylogenetic, morphological, and chemotaxonomic incongruence in the North American endemic genus Echinacea Abstract The tudys of recently formed species is important because it can help us to better understand organismal divergence and the speciation process. However, these species often present difficult challenges in the field of molecular phylogenetics because the processes that drive molecular divergence can lag behind phenotypic divergence. In the current study we show that species of the recently diverged North American endemic genus of purple coneflower,Echinacea, have low levels of molecular divergence. Data from three nuclear loci and two plastid loci provide neither resolved topologies nor congruent hypotheses about species-level relationships. This lack of phylogenetic resolution is likely due to the combined effects of incomplete lineage sorting, hybridization, and backcrossing following secondary contact. The poor er solution provided by molecular markers contrasts previous studies that found well-resolved and taxonomically supported relationships from metabolic and morphological data. These results suggest that phenotypic canalization, resulting in identifiable morphological species, has occurred rapidly within Echinacea. Conversely, molecular signals have been distorted by gene flow and incomplete lineage sorting. Here we explore the impact of natural history on the genetic organization and phylogenetic relationships of Echinacea. Keywords Asteraceae, chloroplast DNA, Echinacea, incomplete lineage sorting, phylogenetics, single-copy nuclear DNA Disciplines Agricultural Science | Agriculture | Evolution | Horticulture | Plant Breeding and Genetics | Plant Sciences Comments This article is from American Journal of Botany 95, no. 6 (June 2008): 756–765, doi:10.3732/ajb.0800049. Rights Works produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted. Authors Lex E. Flagel, Ryan Adam Rapp, Corrinne E. Grover, Mark P. Widrlechner, Jennifer S. Hawkins, Jessie L. Grafenberg, Inés Álvarez, Gyu Young Chung, and Jonathan F. Wendel This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/ncrpis_pubs/26 American Journal of Botany 95(6): 756–765. 2008. P HYLOGENETIC, MORPHOLOGICAL, AND CHEMOTAXONOMIC INCONGRUENCE IN THE NORTH AMERICAN ENDEMIC GENUS ECHINACEA 1 Lex E. Flagel, 2 Ryan A. Rapp, 2 Corrinne E. Grover, 2 Mark P. Widrlechner, 3 Jennifer Hawkins,4 Jessie L. Grafenberg, 2 In é s Á lvarez, 5 Gyu Young Chung, 6 and Jonathan F. Wendel 2,7 2 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa 50011 USA; 3 USDA-ARS North Central Regional Plant Introduction Station, Ames, Iowa 50011 USA; 4 Department of Genetics, University of Georgia, Athens, Georgia 30602 USA; 5 Departamento de Biodiversidad y Conservaci ó n, Real Jard í n Bot á nico, CSIC, Madrid 28014 Spain; and 6 School of Bioresource Science, Andong National University, Andong Gyeongbuk, 760-749 South Korea The study of recently formed species is important because it can help us to better understand organismal divergence and the speciation process. However, these species often present diffi cult challenges in the fi eld of molecular phylogenetics because the processes that drive molecular divergence can lag behind phenotypic divergence. In the current study we show that species of the recently diverged North American endemic genus of purple conefl ower, Echinacea , have low levels of molecular divergence. Data from three nuclear loci and two plastid loci provide neither resolved topologies nor congruent hypotheses about species-level relationships. This lack of phylogenetic resolution is likely due to the combined effects of incomplete lineage sorting, hybridiza- tion, and backcrossing following secondary contact. The poor resolution provided by molecular markers contrasts previous studies that found well-resolved and taxonomically supported relationships from metabolic and morphological data. These results suggest that phenotypic canalization, resulting in identifi able morphological species, has occurred rapidly within Echinacea . Conversely, molecular signals have been distorted by gene fl ow and incomplete lineage sorting. Here we explore the impact of natural history on the genetic organization and phylogenetic relationships of Echinacea . Key words: Asteraceae; chloroplast DNA; Echinacea ; incomplete lineage sorting; phylogenetics; single-copy nuclear DNA. Species of the genus Echinacea are geographically circum- tantly, the disruption of natural processes of intraspecifi c and scribed within a region of North America that has undergone interspecifi c gene fl ow and the attendant increase in population repeated rounds of glaciation ( Clayton and Moran, 1982 ), with fragmentation and genetic bottlenecks. the last such round, the Wisconsinan, ending roughly 10 000 yr Taxonomically, Echinacea is delimited into nine species before the present. Presently, the genus ranges from southern ( Table 1 ), including two, E. angustifolia DC and E. paradoxa Alberta, Canada to near the coast of the Gulf of Mexico in (Norton) Britton, that each are further divided into two varietals Texas and Louisiana and from the oak savannas of Ohio, the ( McGregor, 1968 ; Flora of North America Editorial Commit- glades of Tennessee, and open habitats in the Carolinas west to tee, 1993 +; McKeown, 1999 ). These species are all diploid with the foothills of the Rocky Mountains ( Urbatsch et al., 2006 ). the exception of E. pallida , which is putatively a polyploid Much of this range was under ice during the last glacial epoch, ( Mechanda et al., 2004 ). This taxonomic treatment was devised signifying that Echinacea survived in southerly refugia. De- by McGregor (1968) , who spent 15 years studying the genus spite the expansive aggregate range of the genus, much of this while making controlled, common-garden crosses, noting that range has been converted into agricultural production, resulting many hybrids have high levels of stability, fecundity, and via- in an extremely fragmented modern population structure. This bility in parental backcrosses. In a recent morphological study, distributional history has many potential implications for the four species with eight subspecies were proposed ( Binns et al., genetic architecture of a perennial plant species, most impor- 2002, 2004 ), but McGregor ’ s classifi cation continues to be widely used by botanists and herbalists (see discussion in 1 Manuscript received 11 February 2008; revision accepted 7 April 2008. Blumenthal and Urbatsch [2006 ]) and serves as the basis for the This journal paper of the Iowa Agriculture and Home Economics Experiment recent Flora of North America treatment ( Urbatsch et al., 2006 ). Station, Ames, Iowa, Project No. 1018, was supported by Hatch Act and State McGregor ’ s results regarding the ease of formation and fer- of Iowa funds and was made possible by grant number P01ES012020 from the tility of interspecifi c hybrids suggest that Echinacea may either National Institute of Environmental Health Sciences (NIEHS) and the Offi ce be a young genus in which rapid speciation has occurred of Dietary Supplements (ODS), NIH. Its contents are solely the responsibility (McKeown, 2004) or one in which, for reasons other than rela- of the authors and do not necessarily represent the offi cial views of the NIEHS, tive youth, genetic barriers have incompletely formed. In either NIH. Mention of commercial brand names does not constitute an endorsement case, gene fl ow between species has been historically common; of any product by the U. S. Department of Agriculture or cooperating agencies. McGregor noted hybrid swarms in natural sympatric settings, J.-A. McCoy and other members of the Center for Research on Botanical and in more recent molecular work, Mechanda et al. (2004) Dietary Supplements at Iowa State University were helpful in providing feedback and comments throughout the research. L. Urbatsch kindly provided found evidence of natural hybrid individuals. DNA samples for sequence analysis. Assessment and maintenance of Echinacea genetic diver- 7 Author for correspondence (e-mail: [email protected])
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