Aliso: A Journal of Systematic and Evolutionary Botany
Volume 17 | Issue 2 Article 2
1998 Phylogeny and Adaptation in the Encelia Alliance (Asteraceae: Helliantheae) Curtis Clark California State Polytechnic University; Rancho Santa Ana Botanical Garden
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Recommended Citation Clark, Curtis (1998) "Phylogeny and Adaptation in the Encelia Alliance (Asteraceae: Helliantheae)," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 17: Iss. 2, Article 2. Available at: http://scholarship.claremont.edu/aliso/vol17/iss2/2 Aliso. 17(2), pp. 89-98 © 1998, by The Rancho Santa Ana Botanic Garden, Claremont, CA 91711-3157
PHYLOGENY AND ADAPTATION IN THE ENCELIA ALLIANCE (ASTERACEAE: HELIANTHEAE)
CURTIS CLARK Biological Sciences Department California State Polytechnic University Pomona, California 917681
AND Rancho Santa Ana Botanic Garden 1500 N. College A venue Claremont CA 91711-3157 e-mail: [email protected]
ABSTRACT The three related genera Encelia, Enceliopsis, and Geraea comprise the alliance. The first consists primarily of shrubs and the latter two of herbaceous perennials and an annual. With the exception of two Encelia species of arid South America, all inhabit southwestern North America. Enceliopsis and Geraea are sister groups, and together form the sister group to Encelia, which includes two major clades. Especially in Encelia, there are diverse morphologies and a variety of ecological strategies marked by differences in habitat, vestiture, water balance, and photosynthetic parameters. The North American species of all three genera are obligate outcrossers, all with n = 18 chromosomes. Although intergeneric hybrids are largely sterile, interspecific hybrids in Encelia are fertile in the wild and in cultivation. Hybrids in the wild are largely restricted to F ,s, except in areas of human disturbance. Two true-breeding species are of homoploid hybrid origin, and are evidently isolated from the parent species through external ecological barriers involving selection against backcross progeny. Studies of the chloroplast genome and the intercistronic transcribed spacer (ITS) of nrDNA show clear differ entiation of the genera, but much less variation within Encelia, even between phenotypically disparate species, suggesting recent divergence. Because the species are interfertile, it will be possible to study the genetics of the traits that distinguish the species and contribute to their differences. Key words: Asteraceae, Encelia, Enceliopsis, Geraea, phylogeny
INTRODUCTION of species-diagnostic characters. The purpose of this Section 9.3 of Ehleringer and Clark (1987) is titled paper is to outline the state of current knowledge of "Encelia: A model system for the study of adapta the genus and point t6 directions for future research. tion." Fortunately, perhaps, there are no criteria for The "Encelia alliance," as described here, consists "model systems." In many cases, a model system is of the genera Encelia, Enceliopsis, and Geraea. They simply one that has been well studied, but most model are mostly perennials, all with n = 18 chromosomes, systems also have features that lend them to certain and all inhabitants of arid regions, mainly in south western North America. types of research. The lab mouse, Mus musculus, is arguably a case of the former, its primary advantage being that it is amenable to captivity. Drosophila, Cae PHYLOGENY norhabditis elegans, and Arabidopsis thaliana are per Clark (1986) first presented a phylogeny for Ence haps in the latter category; each has aspects of its bi lia, and substantially the same tree was published by ology that strongly favor certain types of studies. In Ehleringer and Clark (1987). The relationships be the study of evolutionary biology of plants, Clarkia tween Encelia, Enceliopsis, and Geraea were explored certainly stands out. by Sanders and Clark (1987), Nishida and Clark Encelia and its relatives certainly aren't the "new (1988), and Nishida (1988). All these studies were Drosophila" or "new Clarkia," but there are features based on phenotypic features: capitulum characters, in of the group that support studies of the phylogeny of cluding UV reflectance (Clark and Sanders 1986), tri ecological adaptation (as explored by Ehleringer and chome type and distribution (Clark et al. 1980; Clark Clark 1987), the nature of hybrid speciation, the role and Clark 1984; Charest-Clark 1984; Charest 1988), of breeding barriers in speciation, and the inheritance and secondary chemistry and associated anatomical features (Budzikiewicz et al. 1984, Proksch and Clark , Address for correspondence. 1984, 1986; Proksch et al. 1988). More recently, Clark 90 Clark ALISO
(1995) provided preliminary phylogenetic data from NEVADA UTAH the internal transcribed spacer of nuclear ribosomal DNA (ITS). Although these phylogenetic studies have seemed a "work in progress," since full character support for a specific tree has never been published, they agree in a ARIZONA number of major features. First, they strongly support the monophyly of Encelia (diagnosed by a constricted apical notch of the achene and the general absence of achene awns; the clade has occurred in every tree in every analysis, with 100% bootstrap and jackknife in combined morphology and ITS [Clark 1995]), Ence liopsis sensu stricto (scapose habit and large capitula [Sanders and Clark 1987]; again occurring in all trees), and a sister-group relationship between Enceliopsis and Geraea (thickened unpigmented crown of the achene [Sanders and Clark 1987]; occurring in all trees). They weakly support the monophyly of Geraea o G. canescens and a sister-group relationship between Enceliopsis + Geraea and Encelia. * G. viscida Within Encelia, the presence of two major clades (hereafter called the Jrutescens clade and the califor BAJA CALIFORNIA nica clade) is well supported. Encelia nutans East ~ wood cannot be clearly assigned to either (ITS data are not yet available), and although phenotypic data clearly assign E. ravenii Wiggins to the Jrutescens clade, ITS data less clearly assign it to the californica clade. Within the clades, relationships are less certain. Fig. I. Distribution of Geraea. For example, a stepwise increase in leaf pubescence and congestion of the paniculate capitulescence seem to show relationships among E. Jarinosa A. Gray, E. corolla throat (as contrasted with the bulbous throat of canescens Lam., E. palmeri Vasey & Rose, and E. the relatives). Although Proksch et al. (1986) showed halimifolia Cav. in the californica clade, but their ITS phytochemical similarities between G. canescens and sequences show virtually no differences. Enceliopsis, they found a different set of chemical con Flourensia has been traditionally viewed as an out stituents in G. viscida. ITS sequences are preliminary, group to the Encelia alliance (Clark 1986), and ITS but the clade occurred in 72% of 799 most parsimo data appear to support this. Preliminary sequences sug nious trees in an analysis of ITS 1 (Clark unpubl.). gest that two "misfits" in Encelia, E. stenophylla E. Geraea canescens hybridizes in the wild with E. L. Greene and E. scaposa (A. Gray) A. Gray, are more Jarinosa (Kyhos 1967) and E. Jrutescens A. Gray closely related to Flourensia than to the Encelia alli (Clark unpubl.). Although this has suggested close re ance. Morphology and biogeography provide some lationship, it is important to realize that these two spe support to this view (Clark unpubl.) cies are the only members of the alliance with which G. canescens is sympatric. In cultivation, G. canescens Geraea has been successfully crossed with several other En celia species (Clark unpubl.). Two important facts This genus consists of two species, G. viscida (A. emerge from this study. First, all hybrids between G. Gray) S. F. Blake, an eradiate herbaceous perennial canescens and other species are sterile (Kyhos 1967, with sessile glandular leaves, and Geraea canescens found asynapsis in G. canescens X E. Jarinosa hy Torr. & Gray, a radiate annual with alate-petioled pi brids). Second, G. canescens is always the pollen par lose leaves (Fig. 1). Even though they have long been ent; no other species will successfully pollinate G. ca congeners, they are superficially dissimilar. In her nescens. This unilateral incompatibility is not unex study of the genus, Nishida (1988) demonstrated ad pected, since G. canescens is an annual (thus highly ditional differences, but suggested that the genus is disadvantaged by loss of eggs to sterile hybrid prog monophyletic, diagnosed by strongly obcuneate eny) and all the other species are perennials. achenes (common in the Heliantheae, but otherwise Of course, the G. canescens X G. viscida hybrid unknown in the Encelia alliance) and a tapered disk would be very interesting. Is it sterile? How do the VOLUME 17, NUMBER 2 Encelia Alliance 91
Nevada Utah Nevada
~ E. nudicaulis [ill] E. argophylla * E. coviIlei
Arizona Baja California Fig. 2. Distribution of Enceliopsis. contrasting features of the parents sort out? Clark (un publ.) and Nishida (1988) made numerous attempts to form this hybrid. As expected, all attempts using G. canescens as the ovulate parent resulted in no fruit set. When G. viscida was the ovulate parent, all the prog eny were indistinguishable from G. viscida; evidently the G. canescens pollen had overwhelmed the self incompatibility system of G. viscida, allowing self Baja pollination. Attempts to circumvent this by excising California G. viscida anthers resulted in ovule abortion. Thus, no Sur hybrids were ever formed. Fig. 3. Distribution of Encelia farinosa. Enceliopsis Enceliopsis consists of three species of suffrutes Encelia cent, generally scap9se perennials with large capitula (Encelia nutans spent most of its nomenclatural his Encelia comprises 15 species, the aforementioned E. tory in Enceliopsis, but it shares the achene synapo nutans an herbaceous perennial, and the rest shrubs. morphy with Encelia and no synapomorphies with En Two are South American: E. hispida Anderss. from celiopsis, so it is considered here in Encelia, where it some of the Galapagos Islands and E. canescens from was originally described). As mentioned above, the Peru, Chile, and Argentina. The rest inhabit south monophyly of the genus is well established. One spe western North America. cies, E. nudicaulis (A. Gray) A. Nels., is widespread The genus contains two well-marked clades. The across the Great Basin, whereas the other two are re californica clade (Fig. 3, 4), consisting of E. califor stricted endemics, E. argophylla (D.C. Eaton) A. Nels. nica Nutt., E. can esc ens, E. densifolia Clark & Kyhos, occurring on gypsum soils around Lake Mead in Ne E. jarinosa, E. halimifolia, E. h isp ida, E. palmeri, and vada, and E. covillei (A. Nels.) S. E Blake being found E. vento rum Brandegee, is diagnosed by a unique ben only in a few canyons on the west slope of the Pan zopyran-benzofuran dimer (Proksch and Clark 1986) amint Mountains west of Death Valley, California and ultraviolet-reflecting ray corollas (Clark and Sand (Fig. 2). The latter two are similar in appearance, were ers 1986). All but E. densifolia also share brown disk once considered conspecific, and share features that corollas. The jrutescens clade (Fig. 5), comprising E. can best be interpreted as apomorphies (Sanders and actoni Elmer, E. jrutescens, E. resinifera C. Clark, and Clark 1987). However, preliminary ITS data seem to E. virginensis A. Nels., is marked by few or no ben ally E. covillei and E. nudicaulis. zopyrans or benzofurans, a lack of resin ducts Sanders and Clark (unpubl.) formed hybrids, E. nu (Proksch and Clark 1986), and erect fruiting heads dicaulis X E. covillei and E. nudicaulis X E. argoph with expanded paleae (Clark 1986). Encelia ravenii ylla, but neither survived long enough to examine their (Fig. 6) shares these features, but ITS sequences ally fertility (all members of the genus are difficult in cul it instead with the californica clade; both data sets tivation). Like Geraea and almost all Encelia, the spe need to be re-examined. cies of Enceliopsis seem to be self-incompatible. Perhaps because of its unusual habit, Encelia nutans 92 Clark ALISO
Nevada Utah
Nevada Utah
E. nutans Baja California Arizona
Cill E. farinasa ~ E. califarnica ~ E. palmeri illIIII E. halimifalia • E. ventarum Baja California Sur ..
Fig. 4. Distribution of other members of the californica clade, overlapping the distribution of E. Jarinosa. Baja California Sonora (Fig. 6) has no clear-cut synapomorphies tying it to either clade, and no molecular data are yet available. ~ It perennates as a thick underground semisucculent rootstock, emerging during the winter and spring to flower and fruit, with the above-ground parts withering in the summer. Its biology is in need of detailed study. E. densifolia
Fig. 6. Distributions of Encelia nutans, E. ravenii, and E. den sifolia. California Because it is difficult in cultivation, no data pertaining to self-incompatibility or hybridization are available. With the exception of E. canescens, and the prob able exception of E. hispida, all the species are self ESJ E. resinifera incompatible. Even E. can esc ens does not ordinarily ~ E. fruteseens spontaneously self. Pollination is generalist, involving subsp. fruteseens • E. fruteseens butterflies, solitary bees, occasional honeybees, and ssp. gumdulosa beetles (Clark, unpubl. observations). Baja All the species of Encelia are interfertile in culti California vation, and their Fls are fertile, as well as all studied F2s and backcrosses. Spontaneous natural hybrids are Fig. 5. Distribution of the Jrutescens clade. common in areas of sympatry. E. actoni X E. Jrutes- VOLUME 17, NUMBER 2 Encelia Alliance 93 cens, E. Jarinosa X E. asperijolia, E. Jarinosa X E. 20+-----~----~----~----~----~~--__+ Jrutescens, E. Jarinosa X E. halimijolia, E. Jarinosa X '1 E. palmeri, E. virginensis X E. Jrutescens, E. vento rum E. Jrutescens X E. asperijolia, and E. vento rum X E. palmeri have ~ 10 ov'V '1 been documented. ~ III E. acton; Because E. vento rum has dissected leaves with lin ')( ~ ear lobes, natural hybrids between it and E. palmeri
8 4.0 -r------, E./rutesce:s I I -E E 3.5 -J:.... "C § 3.0 +E. virginensis E. actoni Q) c::: mE. virginensis Q) ~ E. frutescens J: o 2.5 « I I I Baja California E. actoni 2.0 +----..------r-----r-----! Fig. 10. Encelia virginensis, E. actoni, and E. frutescens, geo 6.0 6.5 7.0 7.5 8.0 graphic distribution Achene Length (mm) phenotypic autapomorphies, E. virginensis shares none with it. However, it shares several random amplified 9 polymorphic DNA (RAPD) markers with both parents 30 (Allan et al. 1993, 1997). 6 In addition, the internal transcribed spacers of nu - clear rONA (ITS) of several individual E. virginensis e combine the sequences of both parents in a manner 25 .a En celia frutescens " strongly suggestive of hybrid origin. The parent spe ~ Q) a. cies differ by 9 bases; at each site, every sampled E. E v~v virginensis has either the E. actoni base, the E. jrutes Q) 20 I- cens base, or a polymorphism consisting of both bases. cu Furthermore, few of the individuals are identical to ::I "0 ~ c: each other, suggesting a "sorting out" of parental lin c: eages (Clark in prep.). « 15 o ~. c: 0 Encelia asperifolia is less precisely intermediate to C'II <0 Encelia virginensis Q) its parents, and in fact was originally described as a ~ subspecies of E. californica (Clark and Kyhos 1980). 10~E~n~c~e~h,a~a~c~~~o~n~i~~~~~~ Its achenes are smaller in both length and width than 10 15 20 25 30 either parent (Fig. 12). It has capitula similar to those of E. californica, with long ray florets (as contrasted Mean Annual Range of Temperature (C) with the eradiate condition of E. jrutescens), but leaves Fig. 8, 9. Encelia virginensis, E. actoni, and E. frutescens-8. more like those of E. jrutescens, so much so that sterile Length and width of achenes (error bars represent the 95% confi specimens are occasionally identified as that species, dence level)- 9. Climatic distribution. leading to the incorrect distribution of E. jrutescens in Baja California provided by Wiggins (1980). able from F\ hybrids between E. actoni and E. jrutes Unlike E. virginensis, E. asperifolia is allopatric to cens. (Prior to molecular studies, only the presence of one of its parents (E. jrutescens) and only parapatric populations of similar and apparently true-breeding E. to the other (Fig. 14). It occupies climates, however, virginensis plants hundreds of kilometers from either that are intermediate between the climates of the par parent supported the idea that E. virginensis was a spe ent species (Fig. 13). Encelia asperifolia plants are not cies, rather than a named hybrid.) Figure 11 shows the especially similar to F\ hybrids, the latter being more leaf trichomes of all three species and the F\. or less intermediate to the parents. Encelia virginensis shares apomorphies with both With E. jrutescens, E. asperifolia shares broad mul parents. With E. jrutescens it shares broad multicel ticellular-based uniseriate leaf hairs (Clark et al. 1980, lular-based uniseriate leaf hairs (Clark et al. 1980, Eh Ehleringer and Cook 1986), and an absence of ben leringer and Cook 1986). Since E. actoni has no clear zopyrans or benzofurans (Proksch and Clark 1986), as VOLUME 17, NUMBER 2 Encelia Alliance 95
Fig. II . Leaf trichomes: (a) Encelia virginensis, (b) E. jrutescens, (c) E. actoni, and (d) E. actoni x jrutescens.
well as two RAPD markers (Clark unpubl.). With E. brid speciation (Arnold 1993; Gallez and Gottlieb californica it shares UV-refiective ray corollas (Clark 1982) involve similar mechanisms. and Sanders 1986), brown disk corollas, moniliform Hybrid speciation in Encelia differs from this model hairs (Clark et al. 1980, Ehleringer and Cook 1986), in many respects. In Encelia, F1s are fully fertile, and and five RAPD markers (Clark unpubl.). there are few or no chromosomal differences between Like E. virginensis, the single sequenced E. asper parent species. Backcrosses are formed as readily as ifolia appears to have chimeric ITS. The parent species F2s, but are strongly selected against, and seldom occur differ by 21 bases. Encelia asperifolia has E. califor- as mature plants in the wild. This corresponds to an . nica bases at eight sites, E. Jrutescens at seven, unique other model proposed by Grant (1981), hybrid speci bases at four sites (including a site for which the par ation with external barriers. Although he included such ents are identical), and ambiguous bases at three. Its mechanisms as pollinator fidelity in "external barri unique ITS mutations, its lack of precise intermediacy, ers," the strong selection against backcross progeny and its disjunct distribution suggest that E. asperifolia serves the same purpose. is an older species than E. virginensis. XEROPHYTIC ADAPTATIONS Theoretical Mechanisms All species of the three genera Encelia, Enceliopsis, Riesberg (1991) and Riesberg et al. (1990, 1995) and Geraea inhabit arid regions, and all have adapta have outlined a mechanism for hybrid speciation in tions to the seasonal lack of water that characterizes Helianthus that agrees with the "recombinational spe them. These adaptations have been extensively studied ciation" model proposed by Grant (1981). In these ex by Ehleringer and his colleagues (summarized in Eh amples from Helianthus, F1s have reduced fertility. leringer and Clark 1987). Four different mechanisms The F2s are often more fertile than backcrosses, and serve different species in the group. repeated crossing among F2 and later generations re Geraea canescens is an annual, and thus a drought stores fertility in the new hybrid species through re avoider. Although annuals are very common in the combination of chromosome segments (in essence, the regions inhabited by members of the Encelia alliance, entire genome becomes chimeric). Thus, the newly they are uncommon among the group of Heliantheae forming species is isolated from the parents by internal to which it belongs. reproductive barriers. Other documented cases of hy- Encelia Jarinosa exemplifies leaf shading by thick 96 Clark ALISO
12 4
E. frutescens -E E SSp. glandulosa + -J: +'" 3 ~ E. californica §" D E. asperifolia CI) E. cali/ornica s::: + • E. frutescens Q) J: subsp. glandulosa (J 2 tit « ~ E. asperi/olia Baja
4 5 6 7 8 9 California Achene Length (mm) Fig. 14. Encelia asperifolia, E. californica, and E. frutescens subsp. glandulosa, geographic distribution. 13 25 reflective when dry than when wet with fog (Harring 0- ton and Clark 1989). -e Within the alliance, reflective pubescent leaves :::s E. asperifolia E." frutescens would seem to be ancestral, but the outgroup Flour l'!! ssp. glandulosa ensia has generally glabrous glutinous leaves, a con -CI) dition not found in the Encelia alliance. An under Q. • standing of the relationships of these two groups E 20 CI) •• t. r among the rest of the Heliantheae will clarify the an I- • cestral condition in the Encelia alliance . cu :::s ~, " Encelia californica is an example of a drought-de c: . c: ciduous species; it loses its glabrous leaves in the dry « season. It inhabits coastal climates that are wetter than c: <>~&~ cu the typical desert haunts of the other species, but its CI) :i: 15 ~ E. cali/ornica range is characterized by no precipitation during the six warm months. Geraea viscida and Encelia nutans are also drought-deciduous, in both cases losing the 5 10 15 20 above-ground parts of the plant. Encelia halimifolia is Mean Annual Range of Temperature (C) nearly as glabrous as E. californica, but the nature of its adaptation is not well understood. Fig. 12, 13. Encelia asperifolia, E. californica, and E. frutescens Encelia frutescens exhibits the other adaptation used subsp. glandulosa-12. Length and width of achenes (error bars represent the 95% confidence level)-l3. Climatic distribution. by glabrous-leaved species: transpirational cooling. It lives primarily in desert washes and other areas with water at depth, and thus can continue to transpire into reflective pubescence. This shading reduces leaf tem the dry season. (It, too, loses its leaves when the water peratures, preventing leaf damage even when there is runs out, but that does not always happen.) Encelia inadequate water for transpirational cooling. Encelia ventorum lives on coastal sand dunes, another habitat palmeri, E. can esc ens, E. actoni, E. raven ii, and the with deep water, and most likely uses the same mech three species of Enceliopsis all have reflective pubes anism. cent leaves, and although they have not been studied as extensively as E. farinosa, the same mechanism can ECOTYPES OF ENCELIA FARlNOSA be inferred. Encelia densifolia is especially interesting Encelia farinosa is the most widespread species in in that its pubescence is wettable, and is much more the genus (Fig. 3). It contains three infraspecific taxa, VOLUME 17, NUMBER 2 Encelia Alliance 97 two (f. farinosa and f. phenicodonta S. F. Blake) dif lecular evidence clearly support a branching clado fering only by disk color (Kyhos 1971), and the third gram. There is no evidence of introgression in the ge (var. radians Brandegee) lacking the characteristic leaf nus, and excepting the two species of hybrid origin, pubescence. no evidence of reticulation. Clearly the mechanisms Other variation is not taxonomically distinguished. that restrict backcrosses in the natural environment The plants of cismontane southern California (in west thus restrict gene flow between the species. ern San Bernardino and Riverside counties) differ in This divergent evolution has led to clear morpho vegetative appearance from those of the adjacent Col logical and ecological differentiation among the spe orado Desert, being taller and less "dome-shaped." cies. Because the species are so easily grown and hy These " ecotypes" meet and to some extent intergrade bridized in cultivation, Encelia provides a great op in the San Gorgonio Pass. portunity to directly study the inheritance of traits that Miller (1988) grew plants from both areas in com distinguish species. mon gardens in both areas. He found that the leaves of desert-origin plants were significantly more reflec ACKNOWLEDGMENTS tive (around 50% reflectance) at 670 nm (the red ab sorption peak of the photosynthetic action spectrum) Many people have provided assistance over the than cismontane-origin plants (30-40%) in both test years in the studies described here. I especially want gardens. Cismontane-origin plants had significantly to thank Gery Allan, Daniel Axelrod, Gerald Braden, longer peduncles (20-22 cm) than desert-origin plants Stephen Bryant, Nancy Charest, Emily Clark, Don (10-15 cm) in both test gardens. These results imply Delano, Daniel F. Harrington, Michael Kinney, Donald a genetic difference between the two "ecotypes" for W. Kyhos, Gregory J. Lee, Linda Maepo, Joy Nishida, these traits. However, even though cismontane plants Jose Panero, Mima Parra, Mark Patterson, Peter growing in habitat had a significantly greater height! Proksch, Loren Riesberg, Eloy Rodriguez, Barbara K. width ratio than desert plants (a measure of the Rugeley, Stephanie Saccoman, Donald L. Sanders, Ed "dome" -shape of the latter), this difference did not ward Schilling, William C. Thompson, Jeff Weiler, Ka persist in the test gardens, suggesting phenotypic plas thy Weisman, and Charles Wisdom. ticity. The maintenance of these differences across a nar LITERATURE CITED row geographic region suggests substantial selection pressures, and indeed the contact between the two ALLAN, G. 1., C. CLARK, AND L. H . RIESEBERG. 1993. Encelia vir forms in San Gorgonio Pass also marks a transition ginensis (Asteraceae): Origin and genetic composition of a diploid from a generally coastal flora to a desert flora. This species of putati ve hybrid ori gin. Amer. 1. Bot. 80(6), Supplement, p. 129. region most likely represents a secondary contact be ---, ---, AND ---. 1997. Distribution of parental DNA tween the forms. The cismontane form is otherwise markers in Encelia virginensis (Asteraceae: Heliantheae), a dip isolated from the bulk of the species. loid species of putative hybrid origin. Pl. Syst. Evo/. 205: 205- 22 1. ARNOLD, M. L. 1993. Iris nelsonii (Iridaceae): origin and geneti c EVOLUTION OF ENCELIA composition of a homoploid hybrid species. Amer. 1. Bot. 80: 577-583. Although the species show some striking differences B UDZIKIEWICZ, H ., G. LAUFENBERG, C. CLARK, AND P. PROKSCH. 1984. in morphology and ecology, the low levels of variation New benzofuran deri vatives fro m Enceliopsis argophylla. Phyto in ITS and the chloroplast genome and the ability of chemistry 23: 2625-2627. all the species to interbreed suggest a recent origin, CHAREST, N. A. 1988. A scanning electron microscopic study of the peduncle, phyllary, and palea trichomes of Encelia (Asteraceae: especially as compared to the sister group comprising Heliantheae). M .S. Thesis, California State Polytechnic Univer Enceliopsis and Geraea. Despite the recent origin, and sity, Pomona. vii + 83 p. despite the potential for hybridization, the species are CHAREST-CLARK , N. 1984. Preliminary scanning electron microscop easily distinguished. Most taxonomic confusion has re ic study of the peduncle, phyllary, and pale trichomes of Encelia sulted from the overrepresentation of hybrids in her (Asteraceae: Heliantheae). Crossosoma 10(4): 1-6. barium collections (the, "1 don't recognize that plant CLARK, C. 1986. The phylogeny of Encelia (Asteraceae: HeIi an theae). Amer. 1. Bot. 73: 757. so I'll put one in the press," syndrome). ---. 1995. Reconciling phenotypic and ITS sequence phyloge More important, the basic pattern of evolution in the nies in the Encelia alliance (Asteraceae: Heliantheae) to study group appears to be divergent. Grant (1981) charac character evolution. Amer. 1. Bot. 82(6), Supplement, p. 120. terized similar situations in other genera as "synga ---. 1998. New names and combinations in Encelia Jrutescens mea" ; by this reckoning, the genus Encelia would be sensu lato (Asteraceae: Heli antheae). Aliso 16: ##-##. ---, AND G. 1. ALLAN. 1997. Hybrid speciation with external a syngameon, equivalent to a single " biological" spe barriers: Encelia (Asteraceae: Heli antheae), a case study. Amer. 1. cies, and the individual taxonomic species would be Bot. 83(6), Supplement, p. 249. "semispecies." However, both morphological and mo- ---, AND D. W. KYH OS. 1979. Origin of species by hybridizati o n 98 Clark ALISO
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