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Madrono, Vol. 58, No. 1, pp. 50-56, 2011 CHROMOSOME COUNTS AND TAXONOMY OF MENTZELIA THOMPSONII (LOASACEAE) Joshua M. Brokaw' School of Biological Sciences, P.O. Box 644236, Washington State University, WA Pullman, 99164-4236 [email protected] Michael D. Windham Department of Biology, Duke University, Durham, NC 27708-0338 Larry Hufford School of Biological Sciences, P.O. Box 644236, Washington State University, WA Pullman, 99164-4236 Abstract The species Mentzelia thompsoniiGlad was published in 1976 based solely on herbarium material, and it is the only species in Mentzelia section Trachyphytum that has not been examined cytogenetically. Here we report that M. thompsonii is diploid {2n = 18), making it the easternmost diploid species in section Trachyphytum and the only one that does not occur in California. The diploid status and edaphic specialization ofM. thompsonii suggest that it is a paleoendemic isolated from other diploids in Trachyphytum by specialization during Pleistocene climate change. Our investigationshavealso uncoveredconfusionintheliteratureandherbaria regardingthetaxonomyof M. thompsoniianditsoverallplacewithinMentzeUa. MentzeUathompsoniihasbeensynonymizedwith Mentzelia humilis (Urb. & Gilg) J. Darl. (a member of section Bartonia) in several prominent databases and herbaria. To the contrary, our studies reveal that M. thompsonii is distinct from M. humilis; furthermore, as a uniquecomponent ofColorado Plateaudiversity, itiscriticalforinferences ofbiogeographic evolution in section Trachyphytum. Key Words: Acrolasia humilis, biogeography, diploid, Mancos Shale, Mentzelia humilis, Mentzelia thompsonii. Pleistocene climate change, polyploidy. Mentzelia thompsonii Glad (Fig. 1) is a small currently lacking a chromosome count. Recent annual confined to the Colorado Plateau of the work has suggested that section Trachyphytum southwestern United States. Its range extends represents a monophyletic group exhibiting from the Four Comers region north along the complicated polyploid evolution (Hufford et al. Utah-Colorado border to the Uinta Basin 2003; Brokaw and Hufford 2010a, b), and (Fig. 2). The species is an edaphic endemic, verification of the ploidal level of M. thompsonii usually occurring on barren, salty soils derived is vital to the interpretation of molecular from the Mancos Shale Formation (Glad 1976; evolution and gene flow in the group. Holmgren et al. 2005; Brokaw 2009). Mentzelia The goals of the study were: 1) to collect thompsonii is one of the most recently described chromosome data for M. thompsonii and 2) to species in section Trachyphytum (Glad 1976), and develop a set of chromosomally vouchered its evolutionary significance within this group is molecular and morphological samples for sys- only now becoming apparent (Brokaw and tematic analyses. While these cytogenetic analy- Hufford 2010a, b). Prior to cytogenetic surveys ses have been essential to determine M. thompso- of the group, only eight North American species niis role in the polyploid complexes of section were recognized in section Trachyphytum (Loa- Trachyphytym, our investigations have also led to saceae) (Darlington 1934). However, the discov- new insights regarding the biogeography of ery ofextensive polyploidy (Zavortink 1966) and Trachyphytum and resolved confusion in the coincident reproductive barriers subsequently led literature and herbaria regarding the taxonomy to the recognition of over 20 species in the and validity of M. thompsonii. southwestern United States alone. Mentzelia thompsonii was described ten years after Zavor- Materials and Methods tink's (1966) biosystematic revision of Trachy- phytum, and it is the only North American species Populations examined in this study were selected to represent the northwestern (Uinta Chr'iPsrteisaenntUnaidvderressist:y,DAebpilaerntem,enTtXo7f96B9i9o-l7o8g6y8,, AUb.iSl.eAn.e JCou.a,n UCTo,.,BrNoMk,aw B2r3o4)kaawnd34s5o)utlhiemaisttsernof(Stahne 2011] BROKAW ET AL.: CHROMOSOME COUNT OF M. THOMPSONII 51 tions of M. thompsonii '\s n = 9. The chromosomes consistently formed nine bivalents during the reductional division (Fig. 3a) and these segregated normally during anaphase H to produce four daughter cells containing nine chromatids each (Fig. 3b). The base chromosome number of Mentzelia section Trachyphytum is x = 9, making M. thompsonii a diploid. It is the easternmost diploid in the section and the only one that does not occur in California (Fig. 2). Further, it is the only diploid species whose current distribution does not overlap with any other diploid in Trachyphytum. Evolutionary Ecology The discovery that Mentzelia thompsonii is diploid has important implications for our understanding of biogeography and evolution in section Trachyphytum. The lineage of M. thompsonii is nested within the section Trachyphytum clade (Brokaw and Hufford 2010a) leading to the most parsimonious hypothesis that M. thompsonii represents a range extension far from the California origin of the Trachyphytum diploids. The section has its greatest species richness and representatives ofall its major clades in southern California. The polyploid taxa generally have larger distributions, extending further north and east than those of diploids (Zavortink 1966). Prior to our investigation of M. thompsonii, only Fig. 1. Habit of Mentzelia thompsonii Glad. Photo- polyploid taxa were known to have gotten as far graph courtesy of W. A. Weber (University of east as the Colorado Plateau. Given that Colorado). polyploids are derived from diploids and thus more recently evolved, analyses of Trachyphytum distribution of M. thompsonii. Chromosome lacking M. thompsonii would suggest that range counts were made from field-collected microspo- expansions were associated novel trait combina- rocytes fixed in Farmer's solution (3 parts 95% ttiioonn.s Haocwqueivreerd,dtuhreinggeoogrrafoplhlyowoifngthpeoldyippllooiiddizMa.- ethanol: 1 part glacial acetic acid) at the time of thompsonii represents a major exception to this voucher collection. Following the procedures generalization, suggesting that other factors must outlined byWindham(2000), fixed materialswere stored at —20'C and transferred to 70% ethanol be considered. Patterns of edaphic specialization in Trachy- immediately before making slides. Dissected phytum may partly explain the disjunct range of anthers were macerated in a drop of 1% M. thompsonii. Only two other species in acetocarmine stain, which was mixed 1:1 with Trachyphytum, the tetraploid M. mollis M. Peck Hoyer's solution priorto settingthecoverslipand and the octoploid M. packardiae Glad, occur squashing. SlideswereexaminedwithanOlympus entirely outside California; both are limited to BH-2 phase contrast microscope, and representa- unusual soils (Glad 1975, 1976). Although soils tive cells were photographed using Kodak Tech- were not available to her for chemical analyses. nical Pan 2415 film. The voucher specimens, Glad (1976) first noted that shales and grey clays Brokaw 234 (WS375612) and Brokaw 345 of the Mancos Formation were commonly listed (WS375773), have been deposited at the Marion as substrates on specimen labels for M. thompso- vOowuncbheerys Hhearvebabreieunmse(nWtS)t.o AAdCdUitiaonndalCOduLpOli.cate nniio.wWeivtihdenatwtihdaetrMs.amthpoHmnpgsonoifipiospulilmaittieodnsa,lmiotsits exclusively to the Mancos Shale and other Results and Discussion Cretaceous marine sediments of the Colorado Plateau (Holmgren et al. 2005; Brokaw 2009). Analyses of microsporocytes undergoing mei- Thus, all three Trachyphytum species absent from osis revealed that the chromosome number of California appear to be associated with substrate both the northwestern and southeastern popula- specialization. MADRONO 52 [Vol. 58 120° 115° 110° 105° Fig. 2. Range ofMentzelia thompsoniiin eastern Utah, western Colorado, and Four Comers region (white) and combined ranges ofall other diploid species in Mentzelia section Trachyphytum in California, southern Oregon, southwestern Idaho, western Nevada, southwestern Arizona, and northwestern Mexico (black). These observations suggest that the simplest populations could have been driven by dramatic biogeographic hypothesis (a one-way expansion shifts in vegetation during Pleistocene climate from California) may be insufficient to fully change (Dynesius and Jansson 2000; Thompson explain species distributions in Trachyphytum. and Anderson 2000; Minnich 2007). During The range of M. thompsonii shows that diploids vegetational shifts, theancestorsofM. thompsonii have accomplished substantial range expansion may have persisted in northeastern portions of outside of California. The current abundance of the diploid ranges by specializing for edaphically polyploids in intervening regions of the Great stressful habitats where most competing vegeta- Basin and western Colorado Plateau suggest that tion was excluded. a similar distribution of ancestral diploids is at It is likely that shifting diploid ranges during least plausible. It is possible that diploid popu- the Pleistocene facilitated hybridization, leading lations formerly in this region have been dis- to the extensive generation of allopolyploids in placed by competition. This line of reasoning, Trachyphytum documented by Brokaw and coupled with observed edaphic specialization, Hufford (2010b). Mentzelia thompsonii is one of suggests that M. thompsonii may be a paleoen- the few diploids in Trachyphytum lacking allo- demic, i.e., a species isolated through extinctions polyploid descendents (Brokaw and Hufford of close relatives (Stebbins and Major 1965). 2010b), which is not surprising considering its Major migrations and extinctions of diploid current isolation from other extant diploids. The 2011] BROKAW ET AL.: CHROMOSOME COUNT OF M. THOMPSONII 53 Fig. 3. Chromosomes of Mentzelia thompsonii {Brokmv 234) at: A) Metaphase I cell showing nine pairs of chromosomes; B) Anaphase II cell showing four daughter nuclei each containing nine chromatids. Scale bars = 5 (im. species almost certainly had fewer opportunities phytum (Brokaw and Hufford 2010a, b). These than most diploids for allopolyploid hybridiza- provide intriguing evidence that Pleistocene tions in Pleistocene ice age refugia. However, migrations have contributed to complicated molecular data have implicated M. thompsonii in patterns of molecular evolution, ecological spe- one introgressional event without polyploidiza- cialization, and a burst of allopolyploid speciation (Brokaw and Hufford 2010a, b). Brokaw tion (Brokaw and Hufford 2010a, b). The and Hufford (2010a) showed evidence of recom- discovery that M. thompsonii is diploid adds bination between nuclear genes ofM. thompsonii another piece to the puzzle, allowing us to view and the Sonoran Desert diploid M. affinis our biogeographic hypotheses in a new light and Greene, suggesting gene flow between these critically examine the effects of geographic species. Although M. thompsonii and M. affinis isolation on speciesevolutionin Mentzelia section are not currently sympatric, populations of M. Trachyphytum. affinis approach the range ofM. thompsoniimore closely than those of any other diploid in Taxonomic Status Trachyphytum. Mentzelia affinis occurs in southern and western Arizona, separated from the Mentzelia thompsonii is a poorly known taxon, nearest M. thompsonii populations (in the Four rarely collected and confined to unusual sub- Corners region) by less than 400 km. The strates in a region of the United States that is suitability of the intervening habitat during the only now receiving the botanical exploration it Pleistocene is unclear, but it is interesting to note deserves (Heil et al. in press). This largely that a similar geographic pattern has been explains why it was overlooked by both previous observed in the genus Boechera (Brassicaceae). monographic treatments of Trachyphytum (Dar- In this instance, microsatellite data (Windham lington 1934; Zavortink 1966). Not only has this et al. unpublished) reveal that B. perennans (S. led to the delayed cytogenetic study of M. Watson) W. A. Weber (with a southern Arizona thompsonii, but it has also contributed to a range similarto M. affinis) has hybridized with B. complicated nomenclatural history and, ultimate- paUidifolia (Rollins) W. A. Weber, a Colorado ly, to the synonymization of the taxon in Plateau endemic that reaches its southern limit prominent databases and herbaria. In fact, M. near the Four Corners (like M. thompsonii). The thompsonii is still listed as ''not accepted" by the striking similarity ofthese two cases suggests that Integrated Taxonomic Information System (ITIS genetic interactions between species occupying 2011) and the PLANTS Database (USDA- the warm deserts of southern Arizona and the NRCS 2011). cool deserts of the Four Corners region may be Through a series of nomenclatural and taxo- more common than previously supposed. nomic errors, M. thompsonii (Fig. 4) has been Molecular data have revealed that unexpected incorrectly synonymized with M. humilis (Urb. & interactions between species (like those inferred Gilg) J. Darl. (Fig. 5), a distantly related member between M. thompsonii and M. affinis) are of section Bartonia. The initial confusion in the relatively common in Mentzelia section Trachy- taxonomy of M. thompsonii stems from a long- MADRONO 54 [Vol. 58 Fig. 4. Holotype ofMentzelia thompsonii Glad. running disagreement between authors who ton (1934) raised M. pumila var. humilis Urb. & recognize Trachyphytum as a section ofthe genus Gilg ofsection Bartonia to the rank ofspecies as Mentzelia (Torrey and Gray 1840; Urban and M. humilis. Unfortunately, she also treated A. Gilg 1900; MacBride 1918; Darlington 1934; humilis and M. humilis as homotypic and Thompson and Roberts 1974; Hufford et al. incorrectly synonymized the name Aerolasia 2003) and authors who segregate the group as the humilis under Mentzelia humilis. genus Aerolasia (Presl 1831; Rydberg 1903; When Glad (1976) named M. thompsonii, she Davidson 1916; Weber and Wittman 2001). did not mention Aerolasia humilis, a name that, Following Rydberg's (1903) recircumscription of nevertheless, could not have been transferred to Aerolasia, theentity now known as M. thompsonii Mentzelia because of Darlington's (1934) earlier was first described and published as Aerolasia elevation of M. pumila var. humilis to species humilis by Osterhout in 1922. The epithet humilis status. Thus, M. thompsonii became the accepted had been used previously in Mentzelia fora taxon name (in treatments recognizing Traehyphytum as treated by Urban & Gilg (1900) as a variety ofM. a section ofMentzelia; e.g., Holmgren et al. 2005) pumila Torr. & A. Gray. Subsequently, Darling- for the species originally described as Aerolasia 2011] BROKAW ET AL.: CHROMOSOME COUNT OF M. THOMPSONII 55 humilis. Subsequently, the nomenclatural combi- Our reconstruction ofthe taxonomic history of nation A. thompsonii (Glad) W. A. Weber, was M. thompsonii indicates that a failure to consult proposed to accommodate use of Acrolasia in type specimens has played a major role in the treatments of the Rocky Mountain flora (Weber current taxonomic confusion surrounding this 1984). However, rediscovery of the original species. Even cursory examination of types of description and holotype of A. humilis led to M. thompsonii and M. humilis (Figs. 4 and 5, synonymization ofA. thompsonii and a return to respectively) reveals that these names do not the use of A. humilis in later treatments (Weber represent the same taxon. Given the new evidence and Wittman 1992). The final taxonomic error from cytology and molecular phylogenetics (Bro- occurred when Kartesz (1999) repeated Darling- kaw and Hufford 2010a) we hope that earher ton's(1934)incorrectsynonymyofA. humiliswith taxonomic misinterpretations will be put to rest. M. humilis and went on to designate M. thompso- Mentzelia thompsonii is a distinct species with a nii and A. thompsonii as synonyms ofM. humilis. unique phylogenetic history and ecological niche. MADRONO 56 [Vol. 58 and it is an important piece of the evolutionary Kartesz,J.T. 1999. AsynonymizedcheckHstandatlas puzzle that is Mentzelia. with biological attributes for the vascular flora of the United States, Canada, and Greenland, 1st ed. Acknowledgments In J. T. Kartesz and C. A. Meacham. Synthesis of We thank B. A. Prigge, J. J. Schenk, and J. L. tChaerolNionrathBotAamniecrailcaGnardfelnor,a,ChvaepreslioHnill1,.0N.C.North MSternottzheelriafaonrdhWe.lpfAu.lWdeibsecrusfsoironproovfidtihnegtaapxhoontoomgyrapohf MacBTrriaedhey,phJ.ytFu.m.191C8o.ntarirbeuvtiisoinosn offroMmenttzheeliGar,aysecHteiro-n of Mentzelia thompsonii. The following herbaria pro- barium 56:24-28. TtCvhriOiudsLsetdpOr,aoajncedNcceYtts,hsweatRHsoaMpr,srdpoevmUciaNidnmeMedN,nabstyiUuvtTshe,eedPBlaeanitnndttytWAhWSwi.s.arHsdFtiuugidninydn:BibonoAtgtCahnUfayo,m.r MiNNpKiaeCleelHoe,vre-gWReo.tlaft,Ai.oann.2d0P0Ap7... 4AC.3l-iS7mc0ahtoiene,nMh.eparlrGe.o(ecdBlsai.r)m.baotTueerr,raenTsd.- trial vegetation ofCalifornia, 3rd ed. University of Literature Cited California Press, Berkeley, CA. OsTERHOUT, G. 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