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1 U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory, 735 North 500 East, Provo, Utah 84606-1856
Received for publication July 9, 1998. Accepted for publication June 24, 1999.
ABSTRACT
The subgenus Tridentatae of Artemisia (Asteraceae: Anthemideae) is composed of 11 species of various taxonomic and geographic complexities. It is centered on Artemisia tridentata with its three widespread common subspecies and two more geographically confined ones. Meiotic chromosome counts on pollen mother cells and mitotic chromosome counts on root tips were made on 364 populations (
= 3.1 plants per population). These population counts are ~60% of all Tridentatae counts. Some are first records for taxa. The Tridentatae are a polyploid complex (x = 9) with ploidy levels from 2x to 8x, but mostly 2x (48%) and 4x (46%). Polyploidy occurs in nine of the 11 species and in many subspecies as well. Supernumerary or b chromosomes are present only at a low frequency. In the principal species, A. tridentata, 2x plants are larger than 4x ones, which are adapted to drier conditions, probably in consequence of their slower growth rates. Gigas diploidy is a phenomenon shared by some other woody genera, but is in contrast to the gigas polyploid nature of many herbaceous genera. Polyploidy occurs within populations and is essentially autoploid. Hybridization sometimes occurs at taxa interfaces in stable hybrid zones. Stable Tridentatae hybrid zones coupled with the group's inherent propensity for polyploidization has led to the establishment of a geographically and numerically large and successful complex of species.
Key Words: Artemisia • Asteraceae • cytogeography • hybridization • polyploidy • sagebrush • Seriphidium • Tridentatae
The sagebrushes of western North America (= subgenus Tridentatae of Artemisia) are landscape-dominant plants (Küchler, 1964
; West, 1983a, b
). They are among, if not, the most common plants in terms of area occupied and number of individual plants in the United States from Canada to Mexico west of 100° west longitude.
Traditionally, the subgeneric taxonomy of Artemisia follows a system established by Besser (1829)
wherein he separated sections based on various combinations of disc and ray flower occurrences and fertility. Besser's four sections (Abrotanum, Absinthium, Dracunculus, and Seriphidium) have been modified by subsequent workers. Rydberg (1916)
elevated the sections to subgenera and created subordinate sections including section Tridentatae for the North American members of subgenus Seriphidium. Current consensus is to recognize three subgenera: Artemisia L. (= Bessers's Abrotanum + Absinthium), Dracunculus (Besser) Rydb., and Seriphidium (Besser) Rouy. However, McArthur, Pope, and Freeman (1981)
, based on karyotypic, chemotaxonomic, and distributional criteria, elevated Tridentatae to subgeneric status as Tridentatae (Rydb.) McArthur inclusive of 11 species (A. arbuscula, A. argillosa, A. bigelovii, A. cana, A. longiloba, A. nova, A. pygmaea, A. rigida, A. rothrockii, A. tridentata, and A. tripartita). Several authors, e.g., Barker and McKell (1983, 1986)
, Shultz (1983, 1986)
, and Wilt et al., (1992)
, have accepted this proposal. Others, e.g., Kornkven, Watson, and Estes (1998)
, have opted to treat Tridentatae at the sectional level. Big sagebrush (A. tridentata) with its three common subspecies (tridentata, vaseyana, and wyomingensis) and two less common ones (spiciformis and xericensis) is, by far, the most widespread and common species. Several other species and their subspecific entities, e.g., A. arbuscula, A. cana, and A. nova, are also widespread and ecologically important (Beetle, 1960
; Goodrich, McArthur, and Winward, 1985
; Rosentreter and Kelsey, 1991
; Cronquist, 1994
; McArthur, 1994
). The subgenus can be considered as a large species complex (Clausen, 1951
) centered on A. tridentata because hybridization between taxa (species and subspecies) is possible (McArthur et al., 1979
). However, polyploidy in several taxa complicates gene exchange possibilities (Ward, 1953
; Taylor, Marchand, and Crompton, 1964
; McArthur, Pope, and Freeman, 1981
). Evidence from different scientific discipline sources support Tridentatae as a cohesive, monophyletic group, i.e., internal transcribed spacer (ITS) sequences of nuclear ribosomal DNA, and chloroplast DNA restriction site data (Kornkven, 1997
; Kornkven, Watson, and Estes, 1998, 1999
; Torrell et al., in press
), hybridization and karyotypic data (McArthur and Plummer, 1978
; McArthur et al., 1979
; McArthur, Pope, and Freeman, 1981
), randomly amplified polymorphic DNA (RAPD) data (McArthur et al., 1998c
), and flavonoid, terpenoid, and especially sesquiterpene lactone chemical data (Greger, 1978
; Seaman, 1982
; Jeffrey, 1995
). Of the 11 Tridentatae species listed above only two have had their status within Tridentatae questioned: Artemisia bigelovii because its flower heads often include a ray flower within otherwise discoid heads (other Tridentate are uniformly discoid), and A. pygmaea, because of its resinous-glandular, 5–9 lobed leaves and diminutive stature. But the balance of evidence favors inclusion of these species within Tridentatae (McArthur et al., 1998b
, and references therein).
Ling (1982, 1995)
, Weber (1984)
, and Bremer and Humphries (1993)
have recognized Seriphidium (Besser) Fourr. at the generic level with inclusion of members of the Tridentatae. That proposal has not been generally accepted—only one of the numerous references to chromosome counts in Index to Plant Chromosome Numbers list Seriphidium, whereas 514 reference Artemisia (Goldblatt, 1981, 1984, 1985, 1988
; Goldblatt and Johnson, 1990, 1991, 1994, 1996, 1998
).
The Tridentatae have been important in Western North America since the Pliocene (McArthur, Pope, and Freeman, 1981
; Thompson 1991
). Two principal hypotheses are extant in regard to the origin of the Tridentatae. Ling (1991, 1995)
and Bremer and Humphries (1993)
suggest that the group originated from Eurasian Seriphidium species that migrated over the Bering Strait, whereas McArthur and associates (McArthur and Plummer, 1978
; McArthur, Pope, and Freeman, 1981
) suggest that the group evolved from herbaceous members of subgenus Artemisia in situ in North America and differentiated during the extreme climatic fluctuations of the Pleistocene. Subgenus Artemisia species are circumboreal but are centered on the great Eurasian landmass. Both hypotheses remain viable in face of the available molecular (Kornkven, 1997
; Kornkven, Watson, and Estes, 1998
), morphological, anatomical, karyotypical, and chemical data (Rydberg, 1916
; Hall and Clements, 1923
; Ward, 1953
; Carlquist, 1966
; Greger, 1978
; McArthur and Plummer, 1978
; Seaman, 1982
; Shultz, 1983
; Bremer and Humphries, 1993
; Jeffrey, 1995
; Ling, 1995
).
The genus Artemisia has received extensive cytological study, e.g., Index to Plant Chromosome Numbers (nine volumes, 1975–1995, Goldblatt, 1981, 1984, 1985, 1988
; Goldblatt and Johnson, 1990, 1991, 1994, 1996, 1998
) lists 515 records (one as Seriphidium). The genus has two principal base chromosome numbers, x = 8 and x = 9. The Index to Plant Chromosome Numbers database shows x = 9 to be the dominant base number (85.6%) with x = 8 much smaller (9.7%) and with the balance consisting of aneuploids at the diploid or higher levels. Polyploidy, up to 12x, is common, but the vast majority of taxa are 2–6x (Keck, 1946
; Ehrendorfer, 1964
; Estes, 1969
; Persson, 1974
; McArthur and Pope, 1979
; Stahevitch and Wojtas, 1988
; Vallès Xirau and Siljak-Yakovlev, 1997
). The subgenus Tridentatae (x = 9) has been the subject of two major (Ward, 1953
; McArthur, Pope, and Freeman, 1981
) and several smaller scope chromosome studies (Table 1). The current study was initiated to examine more fully Tridentatae cytogeography, especially the extent and nature of polyploidy (McArthur, Pope, and Freeman, 1981
), the incidence of polyploidy within populations, and the interface of ploidy levels between adjacent populations. Although most of the chromosome number data were obtained specifically for this study, additional data collected to aid other research efforts are also included (McArthur and Welch, 1982
; Van Epps, Barker, and McKell, 1982
; Goodrich, McArthur, and Winward, 1985
; McArthur and Goodrich, 1986
; McArthur, Welch, and Sanderson, 1988
; Scott, McCoy, and Wullstein, 1989
; Fairchild, 1990
; Freeman et al., 1991
; Rosentreter and Kelsey, 1991
; Welch et al., 1992
; Downs, Soltis, and Black, 1995
; Graham, Freeman, and McArthur, 1995
; Johnson-Barnard, 1995
; Pounds, 1997
; Wang et al., 1997
; Ayre, 1998
; McArthur et al., 1998a, b, c
; Freeman et al., 1999
).
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Chromosome counts
Both meiotic and mitotic chromosome counts were made. Meiotic counts were used as the preferred technique, therefore avoiding the possibility of scoring endomitosis. However, when flower buds were not available mitotic counts were performed. For some populations both meiotic and mitotic counts were made. We usually made chromosome counts for several plants per population because an earlier study (McArthur, Pope, and Freeman, 1981
) demonstrated that more than one ploidy level was present in some populations. Mitotic tissue was examined from root tips pretreated overnight in cold water (~3°C) and fixed in 5% aqueous acetic acid, hydrolyzed in 1 mol/L HCl for 5 h at room temperature (~20°C), stained in acetocarmine, and squashed in a drop of corn syrup. Meiotic material (pollen mother cells) was obtained from the field on appropriate dates, during August or early September. Flowering times of plants growing at higher altitudes and latitudes are generally earlier than those growing at lower altitudes and latitudes. Because of high reactivity of phenolics in sagebrush tissue, the customary use of acidic fixatives was replaced by the dehydrating solvents methanol or acetone (usually methanol) in order to obtain clear chromosomal preparations. Buds were collected in 100% methanol (or acetone) and kept up to 1.5 yr in refrigeration (~3°C), and pollen mother cells were squashed in acetocarmine for examination. Meiotic and mitotic slide preparations were made semipermanent by replacing the stain sequentially by 45% acetic acid and then corn syrup. Representative voucher specimens were collected and deposited in the Shrub Sciences Laboratory Herbarium (SSLP), some duplicates are also deposited in other herbaria (BRY, ID, MO, NY, OGDF, RENO, RM, UC, UT, UTC) (Holmgren, Holmgren, and Barnett, 1990
).
Plant identification
As we collected buds and worked with populations of Tridentatae taxa we used the taxonomic keys of Beetle (1960)
, McArthur (1983)
, Shultz (1986)
, and Cronquist (1994)
with fine tuning of newly recognized taxa from Goodrich, McArthur, and Winward (1985)
, Rosentreter and Kelsey (1991)
, and Winward and McArthur (1995)
. Identification of A. tridentata ssp. vaseyana was confirmed by subjecting leaves or fixed bud solutions to a long-wave (364 nm) ultraviolet light test (Winward and Tisdale, 1969
; Stevens and McArthur, 1974
; McArthur, Pope, and Freeman, 1981
). This taxon, in contrast to ssp. tridentata and ssp. wyomingensis, contains substantial concentrations of coumarin glycosides that are water and methanol soluble. These water and methanol solutions glow a bright iridescent blue color under an ultraviolet light. For many populations we scored the intensity of these compounds on a 0–5 scale, where 0 = no color and 5 = bright, blue color.
Measurements and analyses
Plants of several of the taxa have relative size differences even when growing in uniform gardens or in mixed stands (Beetle and Young, 1965
; Marchand, McLean, and Tisdale, 1966
; Winward and Tisdale, 1977
; McArthur and Welch, 1982
, Barker and McKell, 1986
; Shumar and Anderson, 1986
). We collected maximum height and crown diameter data (in centimetres) from individual mature plants from several populations where taxa co-occurred. Population means and comparisons between populations for height and crown were obtained using Proc Means and Proc GLM procedures of SAS statistical packages (SAS, 1989
). T tests were used to compare the color intensity values of ultraviolet visible coumarin glycosides (Woolf, 1968
). We accepted significant differences between means when P < 0.05.
RESULTS
Chromosome counts
Our chromosome counts are summarized in Table 1 with all other known counts for subgenus Tridentatae of Artemisia. Chromosome counts reported as a result of our current study are listed in Table 2. The counts there constitute ~60% of all counts that have been made (Figs. 1–6); adding those counts to those reported in McArthur, Pope, and Freeman (1981)
the cumulative contribution from our laboratory is nearly 80% of total Tridentatae counts. First records are presented here: for A. arbuscua ssp. longicaulis, uniformly n = 27 (foreshadowed by Winward and McArthur, 1995
); A. cana ssp. cana, n = 36 (previously mistakenly reported as n = 9 and n = 18); and A. bigelovii, n = 36 (one population, other populations are n = 9 and n = 18) (Table 2, Figs. 4–6). The distribution of ploidy levels shown in Tables 1 and 2 demonstrates that Tridentatae species are mostly 2x and 4x with 6x limited to two species (A. arbuscula and A. rothrockii) and 8x common in only one species (A. cana). We recorded the presence of a low frequency of supernumerary or b chromosomes [ten of the 366 populations (2.8%) representing five taxa in Table 2].
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). The two less common subspecies of A. tridentata, ssp. spiciformis and xericensis, reveal contrasting patterns (Fig. 4). Subspecies spiciformis has both 2x and 4x populations in its high elevation habitats, whereas ssp. xericensis is 4x in its restricted range in west-central Idaho (Fig. 4). This is the first report for a chromosome number for ssp. xericensis, although Winward (1970)
speculated that it might be a 2x taxon.
The subspecies of A. cana like those of A. tridentata have contrasting polyploid patterns (Fig. 4). There are two common subspecies of A. cana; ssp. cana is mostly a Great Plains taxon and ssp. viscidula is a high-elevation, mountain taxon. The third subspecies, ssp. bolanderi grows in alkaline basins. Subspecies cana is 8x, a discovery we report for the first time. The solitary 4x report by Stahevitch and Wojtas (1988)
is suspect since numerous plants in 24 other populations were all 8x. Subspecies viscidula, on the other hand, includes populations at both the 2x and 4x levels. The only populations of ssp. bolanderi reported is 2x (Fig. 4).
The widespread species A. nova and A. arbuscula, sometimes treated as conspecific (Ward, 1953
), include populations at different ploidy levels (Fig. 5). Populations of A. nova are about two-thirds 4x and one-third 2x. Populations of A. arbuscula ssp. arbuscula are 2x and 4x in relatively even proportions. Populations of A. arbuscula ssp. longicaulis are uniformly 6x (Fig. 5).
The remaining Tridentatae species are less common and more geographically restricted (Fig. 6). Many of these species also include polyploid cytotypes. Artemisia tripartita, A. rigida, and A. longiloba all have 2x and 4x populations. Artemisia bigelovii has 2x and 4x populations as well as a single 8x population; A. rothrockii has 4x and 6x populations and perhaps one 8x population (Clausen, Keck, and Hiesey [1940]
recorded a single 8x plant but neither Ward [1953]
nor McArthur, Pope, and Freeman [1981]
confirmed an 8x presence). Artemisia pygmea populations are 2x, although individual plants in one population were 4x (McArthur, Pope, and Freeman, 1981
). The single report for A. argillosa is 4x.
Sympatric or tightly parapatric distribution of cytotypes
Since we usually counted chromosomes from several plants per population (Table 2; = 3.1, range 1–27), we confirmed the earlier account of populations with mixed ploidy levels (McArthur, Pope, and Freeman, 1981
). Several populations include both 2x and 4x plants, i.e., one population of A. arbuscula ssp. arbuscula, ten populations of A. tridentata ssp. vaseyana, and a hybrid population of A. t. ssp. tridentata x A. t. ssp. vaseyana. One A. t. ssp. vaseyana population had a 6x plant in an otherwise 2x population (Table 2). Three of the A. t. ssp. vaseyana population samples that had 2x and 4x plants were near Pine Valley Mountain in Washington County, Utah (Fig. 7). In several other locations that taxon has tightly parapatric 2x and 4x populations, e.g., locations in Washington, Sevier, and Utah counties, Utah (Table 2 and illustrated in Fig. 7).
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). Similarly, essentially 2x ssp. vaseyana and 4x ssp. wyomingensis interface, e.g., north of Harper, Oregon (M&S 2329A, 2329B), Nash Wash, Utah (M&S 2038, 2036), near Cove Fort, Utah (M&S s.n., August 24, 1984).
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The central species of Tridentatae, A. tridentata, has numerous inter- and intraspecific contacts, some detailed in the previous section. The three common subspecies, tridentata, vaseyana, and wyomingensis, occasionally tightly co-occur, e.g., Clear Creek Canyon–Cove Fort area, Utah (M&S 1484, 1488, 2085, 2086, 2087, 2088, 2089, s.n., August 24, 1984, August 20, 1992), Martin's Draw, Utah (M&S 1597, 1599, 1603, 1604), and Rio Grande Drainage, Idaho (M&S 2098, 2100, 2102, s.n., July 27, 1992); see also reports from Beetle and Young (1965
; Daniel, Wyoming) and Harniss and McDonough (1975
; Dubois, Idaho). We did chromosome counts from 69 different plants over a 31 km transect on the Clear Creek and Cove Creek drainages across the Cove Fort Summit of the Pahvant-Tushar Mountain Range axis in south-central Utah (Table 2). On that transect we recorded 12 2x ssp. tridentata, 22 2x, one 4x, and one 6x ssp. vaseyana, and 33 4x ssp. wyomingensis plants.
In several locations, 2x ssp. tridentata and ssp. vaseyana essentially interface, e.g., Hatch, Utah (U-070, U-031), Salt Creek Canyon, Utah (U-109, M&S 2503, 2504, 2505, 2506, 2507), and north of Kemmerer, Wyoming (M&S 1736, 1737) (Table 2). Several other interfaces from information presented in Table 2, our personal observations, and the literature are: A. arbuscula ssp. arbuscula and A. nova (M&S 2107A, 2107B; Table 2), A. arbuscula ssp. arbuscula and A. tridentata ssp. wyomingensis (Young s.n., August 24, 1984; Table 2), A. arbuscula ssp. arbuscula and A. tridentata ssp. vaseyana (Ward, 1953
; McArthur and Sanderson personal observations, head of Logan Canyon, Utah), A. arbuscula ssp. longicaulis and A. tridentata ssp. wyomingensis (footnote d, Table 1; Winward and McArthur, 1995
), A. cana ssp. cana and A. tridentata ssp. wyomingensis (M&S 2113, 2114; 2483, 2484; 2495, 2493), A. tridentata ssp. wyomingensis and A. tripartita ssp. tripartita (M&S 2337, 2341, s.n., August 31, 1994, Table 2), A. tridentata ssp. wyomingensis and A. nova (McArthur and Sanderson personal observations, Gabbs, Nevada, Desert Experimental Range, Utah), A. tridentata ssp. vaseyana and A. tridentata ssp. spiciformis (several locations in Utah; McArthur and Goodrich, 1986
), A. tridentata ssp. vaseyana and A. cana ssp. viscidula [Soldier Summit area, Utah (M&S 2132, 2195, 2146), Strawberry Valley, Utah, and other locations; McArthur and Goodrich, 1986
; Winkel, 1986
].
Coumarin concentrations by ploidy level in A. tridentata
Coumarin concentrations in the three common subspecies of A. tridentata reveal some interesting patterns (Table 3). Subspecies vaseyana has high concentrations, whereas ssp. tridentata and vaseyana do not. Within ssp. vaseyana 2x plants have significantly higher (P < 0.01) coumarin concentrations than 4x plants. Conversely, within ssp. tridentata 4x plants have significantly higher (P < 0.05) concentrations than 2x plants.
DISCUSSION
Polyploidy
Tridentatae species exhibit abundant polyploidy. All the major species (A. tridentata, A. cana, A. arbuscula, and A. nova), as well as several less common or more geographically restricted ones (A. bigelovii, A. longiloba, A. rigida, A. tripartita, and A. rothrockii) include diploid and polyploid populations (Tables 1, 2). Several of the prominent subspecies, e.g., A. tridentata ssp. tridentata, A. t. ssp. vaseyana, A. cana ssp. viscidula, and A. arbuscula ssp. arbuscula, also include polyploid populations, but others do not or have only limited cytotypic differentiation, e.g., A. tridentata ssp. wyomingensis, A. arbuscula ssp. longicaulis, and A. cana ssp. cana. Other Artemisia subgenera also include species with high frequencies of polyploidy (Keck, 1946
; Ehrendorfer, 1964
; Estes, 1969
; Persson, 1974
; Stahevitch and Wojtas, 1988
). A summary of the literature on intraspecific dicot polyploidy through 1974 (Lewis, 1980a
) placed Artemisia with 47 cases, second only to Potentilla with 60 cases (N = 758 genera). It appears that polyploidy is an important mechanism in the differentiation and adaptation of Artemisia species in general and Tridentatae species in particular. Tridentatae species not only exhibit broad general polyploid patterns (Table 1, Figs. 1–6) but also patterns that are evident at ecotonal interfaces and within populations (Table 2, Figs. 7–9).
The low frequency of supernumerary or b chromosomes present in ten populations (2.8%) of the sampled populations (Table 2) is similar to results reported earlier by Ward (1953)
and McArthur, Pope, and Freeman (1981)
. These results do not appear to be systematically meaningful.
The 2x–4x population interfaces are quite common. Notable examples are between 2x A. tridentata ssp. tridentata or ssp. vaseyana with 4x A. t. ssp. wyomingensis. What might the biological significance of these frequent contacts be? Hagerup (1932)
suggested that polyploids were better adapted to extreme ecological environments than were their diploid relatives (= Hagerup's hypothesis). This hypothesis has been supported by several investigators and reviewers working over a broad geographical range (Tischler, 1935
; Wulff, 1937
; Löve and Löve, 1943
; Johnson and Packer, 1965
) but disputed by others (Bowden, 1940
; Gustafsson, 1948
; Stebbins, 1950, 1971
; Powell and Sloan, 1975
). Stebbins (1950)
suggested that increasing polyploid frequencies have resulted from a selective advantage to heterozygous polyploids in unstable environments. Grant (1971)
and Lewis (1980b)
recognized the validity of Stebbins' suggestion that increased polyploid frequencies do result from unstable environments, but both also acknowledged possible merit in Hagerup's hypothesis. It has been shown that both diploid and polyploid species can have broad ecological adaptation (Stebbins, 1971
), of which diploid and octoploid Fragaria species are examples (Hancock and Bringhurst, 1978, 1979
). In the Tridentatae case under consideration, the essential autoploid nature of the group (McArthur, Pope, and Freeman, 1981
) is, we believe, consequential. Levin (1983)
suggested that "autopolyploidy alters cytologic, biochemical, genetic, and physiological, and developmental character which (may) provide tolerance beyond limits of diploid progenitors" and further suggested that metabolism and growth are retarded in polyploid cells, which would lower growth rates and increase drought tolerance. Wentworth and Gornall (1996)
with work on Parnassia give additional support for wide ecological amplitude of polyploids. Artemisia tridentata ssp. wyomingensis is smaller and slower growing (McArthur and Welch, 1982
; Barker and McKell, 1986
; Shumar and Anderson, 1986
), grows on drier sites (Winward, 1980
; Barker and McKell, 1983
; Shumar and Anderson, 1986
; Swanson, Simonson, and Buckhouse, 1986
) and is subject to greater water stress (Ayre, 1998
; Kolb and Sperry, in press) than are ssp. tridentata and ssp. vaseyana. Another more limited example is on the foothills of Mt. Borah, Idaho, where 2x A. nova and 4x A. arbuscula are tightly parapatric. There, A. nova is found in the shallow drainages, ~15 cm deep, dissecting the bajadas, which are covered with A. arbuscula. This is a fine-scale environmental gradient but as in the case of 4x A. tridentata ssp. wyomingensis interfaces with 2x A. t. ssp. tridentata and vaseyana the 4x plants are in the drier habitat. Stutz (1989)
suggested that woody polyploids might have reduced stature because of the slowed tempo of cell divisions with consequential additional cellulose deposition in meristematic cells—cells of polyploids in comparison to those of diploids tend to have slower mitotic cycles (Stebbins, 1950, 1971
; Grant, 1971
). Li, Berlyn, and Ashton (1996)
ascribe the drought tolerance of polyploid Betula to physiological and morphological adaptations. The subgenus Seriphidium species, Artemisia santonicum, includes fast-growing diploids and slower growing polyploids (Persson, 1974
). Several shrubby genera in addition to Artemisia display the syndrome of smaller, drought-tolerant polyploids in comparison to diploids. These include Atriplex, Chrysothamnus, and Larrea (Yang, 1970
; Stutz, Melby, and Livingston, 1975
; Sanderson, McArthur, and Stutz, 1989
). The condition of smaller polyploids is a reversal of the gigas growth habit of polyploid herbaceous plants (Smith, 1946
; Lewis, 1980b
). We believe the reversal of the traditional gigas syndrome of large, robust polyploids in herbaceous lineages to large robust diploids and smaller polyploids in some shrubby lineages is a consequence of slower woody plant cellular growth. Two exceptions to the gigas diploid shrub syndrome are instructive. Both Grayia brandegei and Gutierrezia sarothrae are suffrutescent shrubs with larger polyploids than diploids, thus conforming to the traditional herbaceous gigas syndrome (Solbrig, 1977
; Stutz and Sanderson, 1983
; Stutz et al., 1987
).
Mixoploidy in the form of some plants at higher ploidy levels, usually 4x, in otherwise diploid populations but occasionally minority 2x plants in predominant 4x populations, is quite common in Tridentatae populations (McArthur, Pope, and Freeman, 1981
; Table 2). We suspect there is a relatively high frequency of unreduced gametes formed, thus producing the higher euploid plants (few odd-ploid, 3x, 5x, etc. plants have been discovered, but see McArthur, Pope, and Freeman, 1981
). Unreduced gametes are the most common mechanism for the production of polyploidy either by direct fusion or self-fertilized progeny of tetraploid chimeras in floral structures (Lewis, 1980b
). Unreduced gametes have been shown to be relatively common in the polyploid Anthemideae genus Achillea, an Artemisia relative (Tyrl, 1975
; Vetter et al., 1996
). Additional support for the in situ de novo production of 4x plants in 2x populations is found in the sympatric distributions of plants of these cytotypes in populations of Artemisia tridentata ssp. vaseyana (Fig. 7). The recent origin of these plants is supported by randomly amplified polymorphic DNA analysis (RAPD). In the same general area shown in Fig. 7, McArthur et al. (1998b)
demonstrated that 2x and 4x plants had the same RAPD profile in addition to being indistinguishable morphologically and chemically (coumarin compound content). The close indistinguishable relationship of the sympatric 2x and 4x ssp. vaseyana plants in the Pine Valley Mountain area (Fig. 7) by RAPD analysis together with overall close relationships of ssp. vaseyana from all locations and indeed of all A. tridentata and of subgenus Tridentatae in hierarchical order support the autopolyploid nature of the Tridentatae (McArthur et al., 1998b,c
). Previous work in our laboratory supported the autopolyploid nature of Tridentatae based on similarity of 2x karyotypes and the 4x karyotypes being approximate doubles of the 2x ones, a high frequency of multivalents in pollen mother cells of polyploids, and mixed ploidy populations (McArthur, Pope, and Freeman, 1981
).
Tridentatae evolution
The differentiation of Tridentatae taxa by polyploidy and hybridization has apparently led to a widely successful plant group consisting of a large species complex. Polyploidization has apparently provided new genetically isolated material for selective forces to mold. Hybridization is widespread in the Tridentatae (Hall and Clements, 1923
; Ward, 1953
; Beetle, 1960
; McArthur, Welch, and Sanderson, 1988
; Weber et al., 1994
). Several extant taxa are thought to be the products of hybridization events, some also involving polyploidization as well (Ward, 1953
; Beetle and Young, 1965
; McArthur and Goodrich, 1986
; Winward and McArthur, 1995
). Kornkven (1997)
and Kornkven, Watson, and Estes (1998)
suggest that the non-Tridentatae species A. filifolia (subgenus Dracunculus) may have a reticulate relationship with the Tridentatae. They suggest that the Tridentatae chloroplast genome has been captured by A. filifolia. McArthur and Pope (1979)
reported that the karyotype of A. filifolia is similar to the Tridentatae karyotype, more similar, in fact, than it is to A. spinescens, a member of subgenus Dracunculus as is A. filifolia. Torrance and Steelink (1974)
reported that the sesquiterpene lactone colartin common in several Tridentatae species is present in A. filifolia. Perhaps the relationship of A. filifolia is closer to the Tridentatae than has been previously assumed.
In a series of studies on hybrid zones (Harrison, 1993
; Arnold et al., 1999
), McArthur, Freeman, Graham, and colleagues have shown that the A. tridentata ssp. tridentata—A. t. ssp. vaseyana hybrid zone is stable and contains a reservoir of fit hybrid plants (Freeman et al., 1991, 1995, 1999
; Graham, Freeman, and McArthur, 1995
; Messina, Richards, and McArthur, 1996
; Wang et al., 1997, 1998, 1999
; McArthur et al., 1998a
; McArthur and Sanderson, 1999
). Such Tridentatae hybrid zones could have been the source for differentation of new genetic combinations that were able to exploit new habitats available as climates changed in the Pliocene and Pleistocene when the Tridentatae apparently differentiated and became important landscape dominants (McArthur and Plummer, 1978
; McArthur et al., 1981
; Thompson, 1991
). Couple the successful and stable Tridentatae hybrid zone formation with the group's inherent propensity for polyploidization and, we believe, a formula for success has been achieved: the landscape dominant subgenus Tridentatae.
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1 The authors thank K. K. Ayre, J. R. Barker, G. K. Brackley, J. N. Davis, J. L. Downs, J. Happ, J. Johnson-Barnard, J. A. Fairchild, G. P. Jones, G. L. Jorgensen, R. M. McCoy, S. E. Meyer, S. B. Monsen, G. L. Noller, A. P. Plummer, M. A. Pounds, L. F. Scott, J. S. Sperry, B. L. Sillitoe, G. A. Van Epps, B. L. Welch, A. H. Winward, L. H. Wullstein, and J. A. Young for providing plant materials (seeds or buds) or directing us to study sites; Joan Vallès for kindly sharing unpublished ITS data with us; and J. L. Downs, A. B. Kornkven, N. L. Shaw, and three referees selected by the editor of the American Journal of Botany for thoughtful review of earlier versions of the manuscript. The work was funded, in part, by U.S. Department of Agriculture CSREES competitive grant 91-98300-6157 and facilitated by Pittman-Robertson Agreement W-82-R for wildlife habitat enhancement (Rocky Mountain Research Station and Utah Division of Wildlife Resources, cooperating). 
2 Author for correspondence (e-mail: dmcarthur/rmrs_provo{at}fs.fed.us
).
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= 4x) based on all known chromosome counts (see Table 1 for references).
Fig. 2. Distribution of cytotypes of Artemisia tridentata ssp. vaseyana (• = 2x, 
= 4x, 
= 8x; and ssp. bolanderi—* = 2x), A. tridentata ssp. xericensis (
= 4x) and A. t. ssp. spiciformis (
= 2x, 
= 4x) based on all known chromosome counts (see Table 1 for references)
