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Redefining Phrymaceae: the Placement of Mimulus, Tribe Mimuleae, and Phryma1

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Redefining Phrymaceae: the Placement of Mimulus, Tribe Mimuleae, and Phryma1 American Journal of Botany 89(7): 1093±1102. 2002. REDEFINING PHRYMACEAE: THE PLACEMENT OF MIMULUS, TRIBE MIMULEAE, AND PHRYMA1 PAUL M. BEARDSLEY2 AND RICHARD G. OLMSTEAD Department of Botany, Box 355325, University of Washington, Seattle, Washington 98195 USA Chloroplast trnL/F and nuclear ribosomal ITS and ETS sequence data were used to analyze phylogenetic relationships among members of tribe Mimuleae (Scrophulariaceae) and other closely related families in Lamiales. The results of these analyses led to the following conclusions. (1) The Australian genera Glossostigma and Peplidium and the taxonomically isolated Phryma join four genera of tribe Mimuleae to form a well-supported clade that is distinct from other families in the Lamiales. We refer to that clade as the subfamily Phrymoideae. (2) The genera Mazus and Lancea (tribe Mimuleae) together form a well-supported clade that we recognize as the subfamily Mazoideae. Mazoideae is weakly supported as sister to Phrymoideae. We assign Mazoideae and Phrymoideae to a rede®ned family Phrymaceae. (3) Mimulus is not monophyletic, because members of at least six other genera have been derived from within it. In light of the molecular evidence, it is clear that species of Phrymaceae (about 190 species) have undergone two geograph- ically distinct radiations; one in western North America (about 130 species) and another in Australia (about 30 species). Phylogenetic interpretations of morphological evolution and biogeographical patterns are discussed. Key words: ETS; ITS; Mimuleae; Mimulus; Phryma; Phrymaceae; Scrophulariaceae; trnL/F. Species in the genus Mimulus have become model systems Mimulus, though in subsequent works, Pennell placed Mimu- for the study of evolutionary processes in nature. The most leae in tribe Gratioleae (Pennell, 1935, 1947). Pennell (1935) intensely studied species are part of the radiation of Mimulus also transferred Hemichaena and Berendtiella to tribe Grati- in western North America. North American Mimulus was es- oleae, noting a similarity in ¯oral structure to Mimulus. Burtt tablished for the study of evolution by the classic work of (1965) reestablished Mimuleae as a tribe, diagnosed on the scientists at the Carnegie Institution. They investigated bio- presence of two characters: (1) tubular, toothed calyces and (2) systematics, genetics, and physiological ecology in sect. Ery- bilamellate stigmas that are receptive only on the inner surface thranthe (Hiesey, Nobs, and Bjorkman, 1971). Research on and that close together with contact. Thieret (1954, 1967) sug- Mimulus has continued with studies of inbreeding depression gested the removal of Melosperma and Monttea to Melosper- (Carr and Dudash, 1996; Carr, Fenster, and Dudash, 1997; meae. This left tribe Mimuleae sensu Argue (1984) composed Karron et al., 1997; Dudash and Carr, 1998; Willis, 1999) the of Mimulus (125 species), Berendtiella (5 species), Hemichae- genetics of speciation (Bradshaw et al., 1995, 1998), mating na (1 species), Leucocarpus (1 species), Dodartia (1 species), system evolution (Leclerc-Potvin and Ritland, 1994), and the Lancea (2 species), and Mazus (25 species). The relationships ecological effects of hybridization (Beeks, 1962; Waayers, among Mimulus and other members of Mimuleae are poorly 1996). understood. In his analysis of pollen, Argue (1980, 1984) As currently described, Mimulus contains approximately found no character or combination of characters that separates 120 species, of which some 75% occur only in western North Dodartia, Lancea, Leucocarpus, Mazus,orMimulus. America. However, Mimulus is worldwide in distribution. Four Barker (1982) considered the Australian genera Glossostig- species exist in Australia (Grant, 1924; Barker, 1982) (one of ma, Peplidium, and Elacholoma (subtribe Limoselleae of tribe them also occurs in South Africa and India), 10 in Chile (von Gratioleae, sensu Bentham [1876]) to be members of Mimu- Bohlen, 1995a), approximately 19 in Mexico (Grant, 1924; leae. Similar to the traditional members of Mimuleae, these Vickery, 1997), 4 in the Himalayas (Yamazaki, 1993), 1 in Australian genera possess tubular, toothed calyces, though in Madagascar, and 2 in eastern North America. The relationships Glossostigma the calyx has three or four lobes instead of the among western North American Mimulus, Mimulus species typical ®ve lobes. The stigmas of these Australian genera are distributed outside western North America, and several genera structurally different from those of species traditionally as- putatively closely related to Mimulus remain uncertain. signed to Mimuleae. In the monotypic Elacholoma, the stigma Dumortier (1829) ®rst proposed tribe Mimuleae (Scrophu- lobes are relatively long and are receptive over most of their lariaceae). Von Wettstein (1891) placed Mimulus with Mazus, length (Barker, 1982). The stigmas of Glossostigma and Pe- Dodartia, Monttea, Melosperma, and Lancea in subtribe Mi- plidium contain one large and one vestigial stigma lobe. The mulinae of tribe Gratioleae. Leucocarpus, Hemichaena, and large lobe covers the mouth of the corolla and is receptive Berendtiella were placed in tribe Scrophularieae. Pennell only on the outer surface (Barker, 1982). Upon being touched, (1920) rede®ned tribe Mimuleae to contain Leucocarpus and this large stigma lobe moves from covering the mouth to pressing against the upper corolla lip, exposing the anthers. In 1 Manuscript received 3 August 2001; revision accepted 19 February 2002. order to assess the homology of these stigmatic movements to The authors thank W. Barker, P. Cantino, D. Crawford, L. McDade, B. the touch-sensitive stigmatic movements in traditional Mimu- Oxelman, K. Ritland, S. Schoenig, and J. Willis for providing plant material leae, a sound phylogenetic hypothesis is needed. or DNA and P. Cantino, L. McDade, P. Reeves, J. Reveal, and D. Schemske Though much has been learned about processes of evolution for helpful discussions. Funding was provided by grants to PMB from ASPT, Sigma Xi, and the University of Washington Department of Botany and NSF in Mimulus, the systematic placement of the genus and the awards to RGO #DEB-9509804 and #DEB-9727025. relationships among species within it remain unresolved. Mo- 2 Author for reprint requests (e-mail: [email protected]). lecular studies have demonstrated that the traditionally rec- 1093 1094 AMERICAN JOURNAL OF BOTANY [Vol. 89 ognized Scrophulariaceae are not monophyletic (Olmstead and two reasons: (1) to compare phylogenetic hypotheses from dif- Reeves, 1995; Olmstead et al., 2001). In their analysis of Scro- ferent genomes and (2) to help resolve more distal portions of phulariaceae using three chloroplast genes, Olmstead et al. the phylogeny. Our expectation in starting this project was that (2001) found that the single representative of Mimulus formed the substitution rate of trnL/F, ETS, and ITS would overlap, the sister group to Orobanchaceae and Paulownia in some but overall the trnL/F region would have more slowly evolv- trees and to Lamiaceae in others. Additional taxa were not ing sites. This information would be useful for resolving the sampled within Mimulus or tribe Mimuleae. Olmstead et al. deeper nodes in the phylogeny. The ETS and ITS would show (2001) dismembered the traditional Scrophulariaceae but did higher overall substitution rates that would aid in resolving the not reassign Mimulus to any clade of family rank. distal portions of the phylogeny. An additional intriguing result of molecular analyses of Lamiales is the close relationship between Mimulus and the MATERIALS AND METHODS taxonomically isolated Phryma (Phrymaceae) (R. G. Olm- stead, unpublished manuscript). Phryma is monotypic with a Taxon samplingÐAll genera within the traditionally described tribe Mi- disjunct distribution in eastern Asia and eastern North Amer- muleae were sampled except Dodartia, a monotypic genus from Russia, and ica. The taxonomic position of Phryma has been unsettled for the monotypic Australian genus Elacholoma (Table 1). The Australian genera Glossostigma and Peplidium were sampled, as was Phryma from eastern years: some authors place it in Verbenaceae (e.g., Cronquist, North America and China. Within Mimulus, we included at least two repre- 1981) and others in its own family Phrymaceae (e.g., Schauer, sentatives of each of the seven major sections. An attempt was also made to 1847; Moldenke, 1971; Lu, 1990). Phryma has a distinctive sample broadly across the geographical distribution of Mimulus. Species from pseudomonomerous gynoecium, which develops into a one- western North America, eastern North America, Chile, Australia, and China seeded fruit (Chadwell, Wagstaff, and Cantino, 1992). A close were included. Molecular systematic analyses of nearly every species of Mi- relationship between Phryma and Mimulus has never been mulus currently underway (P. Beardsley, unpublished data) indicate that our suggested. sample of species within Mimulus results in the same pattern of relationships Relationships within Mimulus have also been a source of as denser sampling. Also represented are members of the clades identi®ed by taxonomic controversy. Grant (1924) divided the approxi- Olmstead et al. (2001) as most closely related to Mimulus, including Pau- mately 120 species into two subgenera and ten sections. Sub- lowniaceae, Lamiaceae, Orobanchaceae, Pedaliaceae, and Acanthaceae. Some genus Mimulus (Synplacus sensu Grant) is based on the char- of the trnL/F and ITS sequences for the preceding families were obtained acter of
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