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Phylogenetic Analysis Reveals Multiple Cases of Morphological Parallelism and Taxonomic Polyphyly in Lomatium (Apiaceae)

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Phylogenetic Analysis Reveals Multiple Cases of Morphological Parallelism and Taxonomic Polyphyly in Lomatium (Apiaceae) Systematic Botany (2014), 39(2): pp. 662–675 © Copyright 2014 by the American Society of Plant Taxonomists DOI 10.1600/036364414X680843 Date of publication 04/23/2014 Phylogenetic Analysis Reveals Multiple Cases of Morphological Parallelism and Taxonomic Polyphyly in Lomatium (Apiaceae) Emma E. George,1 Donald H. Mansfield,1,6 James F. Smith,2 Ronald L. Hartman,3 Stephen R. Downie,4 and Cody E. Hinchliff5 1Department of Biological Sciences, College of Idaho, 2112 Cleveland Boulevard, Caldwell, Idaho 83605, U. S. A. 2Department of Biological Sciences, Boise State University, 1910 University Drive, Boise, Idaho 83725, U. S. A. 3Department of Botany, University of Wyoming, 1000 E University Avenue, Laramie, Wyoming 82071-3165, U. S. A. 4Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, U. S. A. 5Department of Ecology and Evolutionary Biology, University of Michigan, 2071A Kraus Natural Sciences Building, 830 N University, Ann Arbor, Michigan 48109-1048, U. S. A. 6Author for correspondence ([email protected]) Communicating Editor: Benjamin van Ee Abstract—The genera Lomatium and Cymopterus, along with many others, form a group that has been referred to previously as the perennial endemic Apiaceae subfamily Apioideae of western North America. This group of ecologically important and widespread species has been the target of numerous systematic studies, but the evolutionary relationships among these species remain elusive. Here we show that this confusion is due to high levels of morphological parallelism and homoplasy in the characters that have traditionally been used to define them, a result that is concordant with previous studies of the group. We explore patterns of evolution in traditionally important morphologi- cal characters using Bayesian stochastic character mapping on a phylogeny constructed from novel nrDNA and cpDNA sequence data for 96 specific and infraspecific taxa of the estimated 200 species in the group. We consider the implications of these results for taxonomic classification, the evolution of morphologies, and the utility of these morphologies to delimit small and large clades. Lomatium concinnum is newly combined as Cymopterus glomeratus var. concinnus and the new combination Cymopterus glomeratus var. greeleyorus is made. Keywords—Classification, convergent evolution, Cymopterus, homoplasy, morphology. One of North America’s largest endemic plant radiations comparable to others such as Lupinus L. (Drummond 2008; is also one of its least understood: the perennial, endemic Eastwood et al. 2008) and Castilleja Mutis ex L. f. (Tank North American clade of Apiaceae subfamily Apioideae and Olmstead 2008, 2009; Tank et al. 2009). Like other such (hereafter, the PENA clade). The PENA clade contains radiations, the PENA clade is known for its high propor- approximately 200 species in 20 currently recognized genera tion of narrowly endemic species, many of which are of (Table 1), and the proper circumscription of these genera conservation concern (Cronquist 1992; Grimes and Packard has been the subject of much debate (Mathias 1928, 1930, 1981; Carlson et al. 2011a). New species continue to be 1938; Theobald et al. 1964; Downie et al. 2001, 2002). The described on an almost yearly basis (Darrach et al. 2010; largest of the PENA genera are Lomatium and Cymopterus, Helliwell 2010; Carlson et al. 2011a, b; McNeill 2012). together containing over half of the group’s species. Both Morphological evolution in the PENA clade is remark- are taxonomically challenging because of high levels of able, resulting in a great deal of variation both within and species sympatry and extreme morphological variability among populations. Efforts to untangle the intricacies of within many species. species relationships based on this morphology have met Species of the PENA clade are ecologically important with limited success (Coulter and Rose 1900; Mathias 1928, across much of western North America. Most species (espe- 1930, 1938; Schlessman 1984). The taxonomic boundary cially Lomatium and Cymopterus) occur in open habitats of between Lomatium and Cymopterus, for instance, has tra- the Intermountain and Pacific West, and many are xeric- ditionally been defined by a morphological macrofeature: adapted geophytes (Hartman 2000). Several related eastern Lomatium fruits are dorsally flattened with lateral wings, North America genera including Zizia, Taenidia, and Polytaenia, whereas Cymopterus fruits generally are terete to dorsally are associated with more mesic meadow environments. The compressed with dorsal wings in addition to lateral ones. combined range of the PENA genera covers most of North This pattern, however, is not without exception. These incon- America. The greatest species density, however, is concen- sistencies have led some authors to question the value of trated west of the Mississippi River. Lomatium and Cymopterus fruit characters for classification in this group (Cronquist contain many species that are well-documented food sources et al. 1997; Sun and Downie 2004, 2010a, b; Sun et al. for animals including insects, gophers, sage grouse, and 2004). Vegetative and floral characters show essentially grizzly bears (Mattson et al. 1990; Barnett and Crawford similar patterns, though often with even greater degrees of 1994; Thompson 1998), and both the tuberous roots and fruits variation (Hitchcock and Cronquist 1973; Schlessman 1984; of some species were also once an important part of many Cronquist et al. 1997). Native American diets (Hunn and French 1981). Several spe- Previous phylogenetic studies have confirmed suspi- cies of Lomatium are of interest to modern medicine for cions that the current morphological classification does not their antimicrobial and antiviral properties (McCutcheon reflect monophyletic groups within the PENA clade. Sev- et al. 1997; Chou et al. 2006; Mukhtar et al. 2008). eral genera, including Cymopterus and Lomatium as they In addition to its ecological and cultural significance, the are currently circumscribed, appear to define para- or poly- PENA clade is also of interest for its biodiversity. With its phyletic assemblages (Downie et al. 2002; Sun and Downie approximately 200 species, this group represents one of the 2004, 2010a, b; Sun et al. 2004; Carlson et al. 2011a). In fact, most extensive endemic plant radiations on the continent, previous studies have indicated high levels of homoplasy 662 2014] GEORGE ET AL.: POLYPHYLY IN LOMATIUM 663 Lomatium, 11 from Cymopterus, 21 from other PENA genera, and six Table 1. Genera of the perennial endemic North American (PENA) from a clade containing species of Angelica L., which is an outgroup of clade of Apiaceae subfamily Apioideae. Species counts follow Mabberly the PENA clade (Sun and Downie 2004, 2010a). Samples collected for (2008), except as otherwise referenced in the case of recent taxonomic this study were preserved in silica gel whenever possible; vouchers revisions. for these silica-dried specimens have been deposited at the College of Idaho herbarium (CIC; herbarium acronyms according to Thiers Genus Number of constituent species 2012). Those samples taken directly from pre-existing specimens were Aletes J. M. Coult & Rose 15–20 obtained from vouchers in the collections of CIC, RM, ID, and SRP. Cymopterus Raf. 32 DNA was extracted from dried leaf samples using a Qiagen DNeasy Eurytaenia Torr. & A. Gray 2 plant mini kit (Qiagen, Valencia, California). We used the polymerase Harbouria J. M. Coult. & Rose 1 chain reaction (PCR), following the methods of Smith et al. (2004), to Lomatium Raf. 74 amplify the nuclear ribosomal marker ITS and the chloroplast markers Musineon Raf. 3 rpl32-trnLUAG (Shaw et al. 2007), rps16 intron (Shaw et al. 2005), and matK Neoparrya Mathias 1 (Wolfe et al. 1992). Amplification products were sequenced by Genewiz Oreonana Jeps. 3 (South Plainfield, New Jersey). Oreoxis Raf. 4 Alignment and Phylogeny Estimation—Sequences were checked for Orogenia S. Watson 2 mislabeled base pairs and manually aligned using PhyDE 0.9971 (Mu¨ ller Podistera S. Watson 4 etal.2005).Foranalyseswhereindelswerescored,thesimpleindelcoding Polytaenia DC. 2 of Simmons and Ochoterena (2000) as implemented in the program Pseudocymopterus J. M. Coult. & Rose 2 (Sun et al. 2006) SeqState (Mu¨ller 2005) was used. Regions of ambiguous alignment, as Pteryxia (Nutt. ex Torr. & A. Gray) 5 well as the beginning and end of each marker sequenced (which were gen- J. M. Coult. & Rose erally of poor quality), were excluded from final nucleotide data matrices. Shoshonea Evert & Constance 1 Phylogenetic trees were estimated from these alignments using Taenidia (Torr. & A. Gray) Drude 2 maximum parsimony (MP), maximum likelihood (ML), and Bayesian Tauschia Schldl. 31 inference (BI) methods. The exception to this was the data matrix that Thaspium Nutt. 3 rescored indels which was analyzed only with MP. Following Sun Vesper Hartman & Nesom 6 (Hartman and Nesom 2012) and Downie (2004, 2010a), trees were rooted manually using a clade Zizia W. D. J. Koch 4 containing species from the genus Angelica. The MP analyses were per- formed using PRAP2 (Mu¨ller 2007) in conjunction with PAUP* v4.0 b10 (Swofford 2002). Bootstrap support (BS; Felsenstein 1985) was estimated from 1,000 heuristic replicates using PRAP2 (Mu¨ller 2007). in essentially every morphological character ever used for The Akaike information criterion (AIC), as implemented in Modeltest higher classification in this group (Sun et al. 2004, 2005,
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