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

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 morphological 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 is also one of its least understood: the perennial, endemic North American clade of Apiaceae subfamily Apioideae (hereafter, the PENA clade). The PENA clade contains approximately 200 species in 20 currently recognized genera (Table 1), and the proper circumscription of these genera has been the subject of much debate (Mathias 1928, 1930, 1938; Theobald et al. 1964; Downie et al. 2001, 2002). The largest of the PENA genera are Lomatium and Cymopterus, together containing over half of the group’s species. Both are taxonomically challenging because of high levels of species sympatry and extreme morphological variability within many species. Species of the PENA clade are ecologically important across much of western North America. Most species (especially Lomatium and Cymopterus) occur in open habitats of the Intermountain and Pacific West, and many are xericadapted geophytes (Hartman 2000). Several related eastern North America genera including Zizia, Taenidia, and Polytaenia, are associated with more mesic meadow environments. The combined range of the PENA genera covers most of North America. The greatest species density, however, is concentrated west of the Mississippi River. Lomatium and Cymopterus contain many species that are well-documented food sources for animals including insects, gophers, sage grouse, and grizzly bears (Mattson et al. 1990; Barnett and Crawford 1994; Thompson 1998), and both the tuberous roots and fruits of some species were also once an important part of many Native American diets (Hunn and French 1981). Several species of Lomatium are of interest to modern medicine for their antimicrobial and antiviral properties (McCutcheon et al. 1997; Chou et al. 2006; Mukhtar et al. 2008). In addition to its ecological and cultural significance, the PENA clade is also of interest for its biodiversity. With its approximately 200 species, this group represents one of the most extensive endemic plant radiations on the continent, comparable to others such as Lupinus L. (Drummond 2008; Eastwood et al. 2008) and Castilleja Mutis ex L. f. (Tank and Olmstead 2008, 2009; Tank et al. 2009). Like other such radiations, the PENA clade is known for its high proportion of narrowly endemic species, many of which are of conservation concern (Cronquist 1992; Grimes and Packard 1981; Carlson et al. 2011a). New species continue to be described on an almost yearly basis (Darrach et al. 2010; Helliwell 2010; Carlson et al. 2011a, b; McNeill 2012). Morphological evolution in the PENA clade is remarkable, resulting in a great deal of variation both within and among populations. Efforts to untangle the intricacies of species relationships based on this morphology have met with limited success (Coulter and Rose 1900; Mathias 1928, 1930, 1938; Schlessman 1984). The taxonomic boundary between Lomatium and Cymopterus, for instance, has traditionally been defined by a morphological macrofeature: Lomatium fruits are dorsally flattened with lateral wings, whereas Cymopterus fruits generally are terete to dorsally compressed with dorsal wings in addition to lateral ones. This pattern, however, is not without exception. These inconsistencies have led some authors to question the value of fruit characters for classification in this group (Cronquist et al. 1997; Sun and Downie 2004, 2010a, b; Sun et al. 2004). Vegetative and floral characters show essentially similar patterns, though often with even greater degrees of variation (Hitchcock and Cronquist 1973; Schlessman 1984; Cronquist et al. 1997). Previous phylogenetic studies have confirmed suspicions that the current morphological classification does not reflect monophyletic groups within the PENA clade. Several genera, including Cymopterus and Lomatium as they are currently circumscribed, appear to define paraor polyphyletic assemblages (Downie et al. 2002; Sun and Downie 2004, 2010a, b; Sun et al. 2004; Carlson et al. 2011a). In fact, previous studies have indicated high levels of homoplasy