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Phylogenetic Classification of Subtribe Castillejinae (Orobanchaceae)

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Phylogenetic Classification of Subtribe Castillejinae (Orobanchaceae) Systematic Botany (2009), 34(1): pp. 182–197 © Copyright 2009 by the American Society of Plant Taxonomists Phylogenetic Classification of Subtribe Castillejinae (Orobanchaceae) David C. Tank, 1,3, 4 J. Mark Egger, 2 and Richard G. Olmstead 1,2 1 Department of Biology, University of Washington, Box 355325, Seattle, Washington 98195 U.S.A. 2 Herbarium, Burke Museum of Natural History, University of Washington, Box 355325, Seattle, Washington 98195 U.S.A. 3 Present Address: Department of Forest Resources and Stillinger Herbarium, University of Idaho, PO Box 441133, Moscow, Idaho 83844-1133 U.S.A. 4 Author for Correspondence ( [email protected] ) Communicating Editor: Lena Struwe Abstract— Recent molecular systematic research has indicated the need for a revised circumscription of generic boundaries in subtribe Castillejinae (tribe Pedicularideae, Orobanchaceae). Based on a well-resolved and well-supported phylogenetic hypothesis, we present a for- mal reclassification of the major lineages comprising the Castillejinae. Prior to this treatment, subtribe Castillejinae included Castilleja (ca. 190 spp.), Cordylanthus (18 spp.), Orthocarpus (9 spp.), Triphysaria (5 spp.), and the monotypic genera Clevelandia and Ophiocephalus. In the clas- sification presented here, Orthocarpus and Triphysaria retain their current circumscriptions, Castilleja is expanded to include Clevelandia and Ophiocephalus , and Cordylanthus is split into three genera; a key to the genera as they are recognized here is provided. Two new combinations, Castilleja beldingii and Castilleja ophiocephala , are proposed within the expanded Castilleja . The concept of Cordylanthus is restricted to the 13 species formerly recognized as subg. Cordylanthus , while subg. Dicranostegia and subg. Hemistegia are elevated to genus level ( Dicranostegia and Chloropyron , respectively). We resurrect the generic name Chloropyron for the halophytes previously recognized as subg. Hemistegia . Five new combinations are proposed for Chloropyron ( Chloropyron maritimum subsp. canescens, Chloropyron maritimum subsp. palustre, Chloropyron molle subsp. hispidum, Chloropyron palmatum, and Chloropyron tecopense ). In addition to the formal classification, we provide phylogenetic clade definitions for Castillejinae, each of the genera, and two additional clades that are not assigned formal ranks. Morphological characteristics used to recognize traditional groups are evaluated, and synapomorphies are discussed. Finally, the current infrageneric classifications for Castilleja and Cordylanthus are evaluated in light of the recent molecular phylogenetic analyses. Keywords— former Scrophulariaceae , hemiparasites , Lamiales , Lamiidae , revision , western North America. With the explosion of molecular phylogenetic studies in the monotypic genus Gentrya did not differ enough from Castilleja last two decades, systematists have been better able to evaluate to warrant generic status, and it was reassigned to Castilleja traditional classifications in the context of an explicit phylo- as subg. Gentrya . Therefore, Castillejinae (sensu Chuang and genetic hypothesis. A molecular systematic study investigat- Heckard 1991 ) included six genera: Castilleja (ca. 190 mostly ing phylogenetic relationships within subtribe Castillejinae perennial species), Clevelandia (1 annual species), Cordylanthus G. Don (tribe Pedicularideae Duby, Oroban chaceae Vent.), (18 annual species), Ophiocephalus (1 annual species), Orth- based on data from chloroplast (cp) and nuclear ribosomal ocarpus (9 annual species), and Triphysaria (5 annual species). (nr) DNA regions, indicates the need for a revision of the clas- Traditional classifications place subtribe Castillejinae in sification of this group ( Tank and Olmstead 2008 ). Scrophulariaceae Juss. (e.g. Bentham 1846 , 1876 ; Wettstein As it is currently circumscribed, Castillejinae comprises 1891 ; Cronquist 1981 ; Takhtajan 1997 ). However, numer- ca. 220 hemiparasitic species in six genera distributed pri- ous molecular systematic studies have demonstrated that marily in western North America. The group was originally Scrophulariaceae, as it is traditionally recognized, represents proposed to include Castilleja Mutis ex L.f., Cordylanthus an unnatural assemblage of plants comprising more than seven Nutt. ex Benth., and Orthocarpus Nutt. ( Bentham 1846 ). Three distinct lineages of Lamiales (reviewed in Tank et al. 2006 ). monotypic Mexican genera, Clevelandia Greene, Gentrya One of these lineages, now recognized as Orobanchaceae s.l. Breedlove & Heckard, and Ophiocephalus Wiggins, were (APG II 2003), contains the obligately parasitic Orobanchaceae subsequently added to Castillejinae ( Greene 1885 ; Wiggins and all of the hemiparasitic Scrophulariaceae traditionally 1933 ; Breedlove and Heckard 1970). With the exception of placed in tribes Buchnereae Benth. and Pedicularideae Duby Ophiocephalus , all of these taxa possess anthers with unequal of subfamily Rhinanthoideae Link (sensu Wettstein 1891 ). anther sacs that are unequally attached (i.e. the larger anther Furthermore, molecular systematic studies (e.g. Young et al. sac attached to the filament medially, and the smaller by its 1999 ; Wolfe et al. 2005 ; Bennett and Mathews 2006 ) place sub- apex), and this character was used by Bentham (1846) to tribe Castillejinae within a clade of New World taxa distributed define the group. Throughout the history of the subtribe, in North and South America. defining generic boundaries has been problematic, especially The evolutionary relationships of the major lineages com- between Castilleja and Orthocarpus , where numerous spe- prising subtribe Castillejinae was the focus of a recent molec- cies have been shuffled between the two genera (e.g. Gray ular phylogenetic investigation ( Tank and Olmstead 2008 ). 1862 ; Watson 1871 ; Eastwood 1909 ; Jepson 1925 ; Keck 1927 ; This study explicitly addressed evolutionary hypotheses Chuang and Heckard 1991 , 1992 ). The most recent treatment presented by Chuang and Heckard’s (1991) realignment of of Castillejinae ( Chuang and Heckard 1991 ), based on exten- Castillejinae, based on sequences from two cpDNA regions sive morphological and cytological study, departed from the (trnL/F and the rps16 intron) and two nrDNA regions (ITS traditional generic boundaries of Castilleja and Orthocarpus . In and the 3¢ end of ETS; Tank and Olmstead 2008 ). Sequences of this treatment, Orthocarpus subg. Triphysaria was restored to the four DNA regions were obtained from a broad sampling its original status as a genus and 12 other Orthocarpus spe- of all six genera comprising subtribe Castillejinae sensu cies were moved to Castilleja , forming sect. Oncorhynchus of Chuang and Heckard (1991), including 46 species of Castilleja , subg. Colacus ( Chuang and Heckard 1991 , 1992 ), and reducing complete sampling of Orthocarpus and Triphysaria , and 14 of Orthocarpus from 25 species (sensu Keck 1927 ) to only nine. the 18 species of Cordylanthus (Appendix 1), as well as three In addition, Chuang and Heckard (1991) concluded that the outgroups. In this study, Orthocarpus and Triphysaria each 182 2009] TANK ET AL.: CLASSIFICATION OF CASTILLEJINAE 183 formed well-supported monophyletic groups, representing the two monotypic genera Clevelandia and Ophiocephalus two separate evolutionary lineages within Castillejinae ( Fig. 1 ). were derived from within Castilleja ( Fig. 1 ). The major- Chuang and Heckard (1991) were correct in their interpreta- ity of Castilleja species are perennial (ca. 170 species), and tion that Castilleja subg. Colacus sect. Oncorhynchus , which, these taxa, along with Clevelandia and Ophiocephalus , formed like Triphysaria , comprises species previously recognized a well-supported clade derived from a grade of annual as Orthocarpus , belonged with Castilleja ; however, these lineages belonging to subg. Colacus sect. Oncorhynchus . annuals did not represent a distinct clade within Castilleja This clade also included the enigmatic species Castilleja rac- ( Fig. 1 ). Although all three of these groups were previ- emosa , which, prior to Chuang and Heckard’s (1991) revision, ously included in Orthocarpus (sensu Keck 1927 ), they were was isolated in the monotypic genus Gentrya . The final genus confirmed to be more closely related to other members of Castillejinae, Cordylanthus, was polyphyletic in all molec- of the subtribe than they were to each other, as suggested ular analyses; two of the subgenera (subg. Cordylanthus and by Chuang and Heckard (1991). Separate and combined subg. Hemistegia ) were each monophyletic, and the mono- analyses of the cpDNA and nrDNA regions also indicated typic subg. Dicranostegia formed the sister group to subg. that the large genus Castilleja was not monophyletic, because Hemistegia ( Fig. 1 ). In the present study we develop a revised classification of Castillejinae and reevaluate the morphological charac- ters traditionally used to recognize genera. The congruence of the independent data sets from both the chloroplast and nuclear genomes strongly supports the revised classification of Castillejinae proposed here. In an explicitly phylogenetic classification, only monophyletic taxa are recognized ( Hennig 1966 ; Wiley 1979 ; de Queiroz 1988 ; de Queiroz and Gauthier 1990 , 1992 , 1994 ); however, under the traditional Linnaean system, as governed by the International Code of Botanical Nomenclature (ICBN), taxa are ultimately defined by types and the ranks to which they are assigned, with no explicit ref- erence
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