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1Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202; 2USDA Forest Service Shrub Sciences Laboratory, 735N 500E, Provo, Utah 84606; and 4Institute of Neuroscience, 1254 University of Oregon, Eugene, Oregon 97403
Received for publication January 6, 1998. Accepted for publication January 14, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Artemisia tridentata • Asteraceae • biological absorption coefficients • elemental concentrations • hybrid zone • niche differentiation • reciprocal transplant experiment • sagebrush
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Lewontin and Birch, 1966
; Grant and Grant, 1994
; Wang et al., 1997
), but it can also reduce fitness by disrupting coadapted gene complexes (Burton, 1990a
, b
; Graham, 1992
; McKenzie and O'Farrell, 1993
). The performance of hybrids in nature has not been well studied, but is beginning to receive some attention (Mallet and Barton, 1989
; Young, 1996
; Wang et al., 1997
; Emms and Arnold, 1997
; Burke, Carney, and Arnold, 1998
). This lack of study is surprising given the importance of hybridization in speciation and microevolutionary processes.
For the past several decades, considerable attention has been given to explaining the persistence of stable hybrid zones, because their existence violates adaptive speciation theory and calls the biological species concept into question (see Harrison [1993]
for a discussion of the importance of stable hybrid zones). While three models have been proposed to account for the existence of stable hybrid zones, they fall into two basic groups. Both the dynamic equilibrium and mosaic hybrid zone models assume that hybrids are relatively unfit when compared to the parental taxa (Barton and Hewitt, 1985
; Harrison, 1986
, 1990
; Howard, 1986
; Hewitt, 1988
; Harrison and Rand, 1989
; Arnold, 1997
). This unfitness is due to the disruption of coadapted gene complexes and is thus independent of the environment. These models differ from one another in that the mosaic hybrid zone model assumes that the parental taxa have adapted to different environments, whereas the dynamic equilibrium model is ecologically neutral (Arnold, 1997
). In contrast, the bounded hybrid superiority model assumes that hybrids are more fit than both parental taxa within the hybrid zone, but less fit than the parental taxa when raised in either parental zone. Accordingly, genotype-by-environment interactions are believed to stabilize the hybrid zone, with the constraint that hybrids have higher fitness only in the hybrid zone. (Note that genotype-by-environment interactions could cause decreased hybrid fitness as presumed by the other two models.)
The factors determining the width and position of the hybrid zone also differ between the two sets of models. According to the dynamic equilibrium and mosaic hybrid zone models, the balance between endogenous selection against hybrids and gene flow determines the width of the zone. Because the dynamic equilibrium model lacks any ecological term there is nothing to link the zone to a particular habitat. Indeed, the zone is believed to move until it encounters an area of low population density where it becomes trapped (Barton and Hewitt, 1985
). In order for the zone to move, the parental taxa must be adapted to the new environment. Thus, this model predicts complete niche overlap by the parental taxa at least within the vicinity of the hybrid zone. This provides another prediction that can be examined independent of hybrid fitness considerations and is the subject of this study. The mosaic hybrid zone assumes only that the parental taxa are adapted to their respective environments, thus the hybrid zone must fall between them with the width being determined by the balance between endogenous selection and gene flow (see Arnold, 1997
).
In contrast, the bounded hybrid superiority model assumes that ecological selection via genotype-by-environment interactions determines both the position and width of the zone. Consequently, it is the nature of the environment that determines the width of the hybrid zone (for a discussion of these models, see Moore, 1977
; Moore and Buchanan, 1985
; Moore and Price, 1993
; Arnold, 1997
). Accordingly, the parental taxa and the hybrids are adapted to their respective environments and must show niche differentiation.
The critical issues that distinguish these models concern the relative fitness of the hybrids (particularly in the hybrid zone), the nature of selection constraining gene flow, and the role of the environment in determining the position and width of the hybrid zone. We have previously resolved fitness issues for the big sagebrush hybrid zone in northern Utah. Using reciprocal transplant experiments, we found significant genotype-by-environment interactions for major life history features (germination, survivorship, growth, and fecundity) in our study of the big sagebrush hybrid zone (Graham, Freeman, and McArthur, 1995
; Wang et al., 1997
). Hybrids were significantly more fit than parental taxa within the hybrid zone and less fit than the native parental taxon when transplanted outside the hybrid zone (Wang et al., 1997
). These findings are clearly consistent with the bounded hybrid superiority model but conflict with the predictions of the other models.
Using the elemental concentration of leaves as indicators of niche, we test another prediction of these models, that of niche overlap/differentiation. The bounded hybrid superiority model posits that each parental taxon is adapted to its native environment, and the hybrids are adapted to the hybrid zone, i.e., they have different niches, or at least exhibit some degree of niche separation (Moore, 1977
; Moore and Buchanan, 1985
; Moore and Price, 1993
). In contrast, the dynamic equilibrium model assumes that within the vicinity of the hybrid zone, the taxa do not differentially respond to environmental heterogeneity, i.e., the parental taxa and hybrids should have complete niche overlap. The mosaic hybrid zone presumes that the parental taxa have different niches, but makes no direct prediction about their niche overlap with the hybrids, and thus is not a subject of this study.
Plants make ideal experimental subjects to test these models because all plants require the same 17 essential nutrients (Salisbury and Ross, 1992
). Most of these nutrients are absorbed directly from the soil (Foth, 1992
). Elemental concentrations found in various plant parts can serve as indicators of plant responses to edaphic differences (Shkolnik, 1984
; Jeffrey, 1987
; Rendig and Taylor, 1989
), i.e., they can be used to determine whether there is niche separation or overlap. If elemental concentrations in plants raised in a common garden do not differ significantly among the taxa, then niche overlap is indicated, as suggested by the dynamic equilibrium model. However, if elemental concentrations in plants do differ significantly, particularly when raised in the same garden, then this would indicate at least a partial niche separation, as assumed by the bounded hybrid superiority model.
We examined elemental concentrations of the leaves of basin big sagebrush (Artemisia tridentata ssp. tridentata), mountain big sagebrush (A. tridentata. ssp. vaseyana), and their hybrids in native stands and reciprocally transplanted seedlings raised in common gardens. In particular, we address two questions: (1) Does a taxon have the same elemental concentrations when grown in different gardens, i.e., does it respond to the edaphic differences among gardens? and (2) Do the different taxa exhibit the same elemental concentrations when raised in the same garden? The null hypotheses correspond to the predictions of the dynamic equilibrium model. Significant genotype-by-environment interactions allow us to reject both null hypotheses and, thus, accept the alternative bounded hybrid superiority model. Note that we can accept the bounded hybrid superiority model in this case only because we have previously shown that there are significant genotype-by-environment interactions for fitness components and that hybrids have the highest relative fitness in the hybrid zone (Wang et al., 1997
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Graham, Freeman, and McArthur (1995)
for a more complete description of the study area. Seeds were collected from five plants in each native site, germinated in a greenhouse where the resulting seedlings were raised for a year before being transplanted into the common gardens (see Wang et al. [1997]
for a more complete description of the reciprocal transplant experiments).
Sample collection
Leaves were collected from a total of 130 plant samples: 40 from the five native stands (eight samples per stand) and 90 from the seedling transplant experiments (six leaf samples per seedling source per common garden). For the native plants (hereafter referred to as site indigenous), 
100 g of leaves were collected from each of eight adult plants per stand. To minimize the impact on the transplanted seedlings, only 5 g of leaves were collected from one seedling within each half-sib family in the common gardens.
Sample treatment and digestion
Samples were air dried for at least 30 d, then pulverized using a grinding mill, and temporarily stored in paper bags. A modified dry-ashing procedure (Munter and Grande, 1983
) was used: all pulverized samples were redried in an oven at 85°C for 10 h and stored in a desiccator until weighed. Three-tenths of a gram of each sample were transferred to a 10-mL crucible and ashed in a furnace at 485°C for 14 h. The ashed sample was first soaked with 1 mL of concentrated nitric acid (75%) for 1 h, then transferred to a 50-mL centrifuge tube and diluted to 15-mL with diluted nitric acid (2%). This solution was used to determine elemental concentrations of B, Ca, Cu, Fe, K, Mg, Mn, Mo, Na, and Zn, using a Leeman Lab inductively coupled plasma emission spectrophotometer.
Previously, we had determined the concentrations of eight of these elements (Ca, Cu, Fe, K, Mg, Mo, Na, and Zn) in soils from the same area (Wang, 1996
; Wang et al., 1998
). The majority of these elements (B, Ca, Cu, Fe, K, Mg, Mn, Mo, and Zn) are essential to angiosperms. Sodium is often required by plants in arid regions (Brownell, 1979
; Salisbury and Ross, 1992
).
Analytic precision
Duplicate digestions were conducted for each plant sample, and the concentrations of each element were measured twice per digestion. Further, one empty control was done for each batch of digestions. The corresponding control value (if any) was subtracted from each measurement. All concentrations are expressed in milligrams per kilogram of dry matter.
Data analysis
Because we collected multiple data points from the same plant, we used a MANOVA (Zar, 1984
; Norusis, 1988
). We used univariate ANOVAs and post hoc Student-Newman-Keuls multiple comparison tests to analyze for differences among means. We examined the relationships between elemental concentrations of plants and soils in two ways. First, correlation analyses were conducted between the concentrations of the same element in plants and soils, and secondly, we calculated the Biological Absorption Coefficient (BAC) for each element (Brooks, 1983
). BAC = Cp /Cs, where Cp is the concentration of the element in plants and Cs is the concentration of the same element in soils. BACs have been used to examine the differential response of plants (Shkolnik, 1984
; Jeffrey, 1987
) and thus are appropriate for our purposes.
Correspondence analysis (CA) (CANOCO; Ter Braak, 1992
; Randerson, 1993
) was used to analyze the pooled elemental concentrations and BACs, following a square-root transformation (to improve normality), for leaves from both site-indigenous plants and seedlings in the reciprocal transplant gardens. We used CA rather than principal components analysis because CA better reflects changes across gradients (Randerson, 1993
). Sample scores of the first two axes from CA were used for ordination. To conserve space we only report the result for the BACs. The patterns for the elemental concentrations accounted for a lower percentage of the variance, but were remarkably similar to those for the BACs (Wang, 1996
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
Biological Absorption Coefficients (BACs) of elements by site-indigenous plants and transplanted seedlings
The biological absorption coefficients of the elements in the site-indigenous taxa and transplanted seedlings have the following order: BACMo > BACNa 
BACK > BACZn BACMg BACFe2 > BACCu > BACCa. BACs of the eight elements are all greater than one, suggesting that the big sagebrush taxa concentrate these elements. The MANOVA showed a significant site effect (Wilks' lambda = 0.0006, P << 0.001). Univariate analyses showed that BACK, BACMg, BACFe, BACCu, BACMo, and BACNa differed significantly among plants from the five native sites, while BACCa and BACZn did not (Table 3).
For the transplanted seedlings, the MANOVA showed that BACs differed significantly among seedling origins (Wilks' lambda = 0.296, P < 0.001) and among the gardens (Wilks' lambda = 0.005, P < 0.001). There was also a significant garden by seedling origin interaction Wilks' lambda = 0.193, P < 0.001). Univariate analyses showed that all BACs differed significantly among the gardens, while BACCa, BACFe, BACZn, and BACNa varied significantly among seedling sources and BACFe and BACNa had significant garden site-by-seedling source interactions (Fig. 2, Table 4).
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). Here, we report only the results for the BACs and note any discrepancies between the two analyses. BACs of site-indigenous plants from the five sites clearly differed from each other because they ordinate into separate groups, although the BACs of the mountain and near-mountain taxa can be classified into one group (Fig. 3).
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; Wang et al., 1998
). The element with the highest relative contribution to the first axes in CA of elemental concentrations in the transplanted seedlings is either Na or B (Wang, 1996
), while the BAC with the highest relative contribution to the first axes in CA of BACs in the transplanted seedlings is either BACNa or BACZn (see legends of Figs. 4 and 5). As the first axis has the most information in correspondence analysis and different groups can ordinate along the first axis in most of our analyses, the different amounts of a few elements (e.g., Na, B, and Zn) may reflect the niche differentiation among the big sagebrush taxa.
Correlations between elemental concentrations and plant size
We previously measured a number of parameters on the same plants that we used in this study and thus can correlate the elemental concentrations reported here with these prior measurements. However, in doing so we are limited by the degrees of freedom. Consequently, we report only correlations with plant size (the product of height and crown diameter) as we have the most degrees of freedom for that analysis. Overall, Fe (R = -0.25, P < 0.05) and Mn (R = -0.35, P < 0.05) were negatively correlated with plant size, while B (R = 0.17, P < 0.053) and Cu (R = 0.15, P < 0.073) showed weak positive correlations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Given the essential nature of the elements studied, it is not surprising that BACs are all greater than one, suggesting that big sagebrush taxa concentrate them, but they do so differently. Thus, it is probably not surprising that linear correlations between soil and leaf concentrations were not strong (only four of the eight correlations were significant, and these did not account for a high fraction of the variance). Nevertheless, the concentrations of elements in the soils probably contribute to the structuring of the hybrid zone, because the relative contributions of the eight elements to the first axes in both the soil and leaf analyses are highly correlated.
Based upon our examination of life history features (Wang et al., 1997
), each parental taxon was most fit within its native habitat, and hybrids were overwhelmingly more fit than either parental taxon in the hybrid zone. Thus, our life history data also show significant genotype-by-environment interactions. Here, we found that the same taxon responded differentially when transplanted into different gardens and that the different taxa concentrate minerals to different extents. Thus, it is not surprising that the different taxa responded differentially when transplanted into the same garden. These findings indicate that genotype-by-environment interactions influence the concentrations and BACs of essential elements from the soil. However, because of our limited degrees of freedom we have not identified which elements are responsible for the fitness differentials. Nevertheless, we find it most interesting that Fe showed significant genotype-by-environment interactions, was a major component of the CA axes, and was negatively correlated with plant size. However, it may be naive to suppose that there should be a simple correlation between fitness and elemental concentration or BACs. Often it is the ratios or proportions among elements that influence the outcome of competition (Tilman, 1985
). While we have not identified which elements, or combination of elements, limit the fitness of each taxon in each environment and believe such studies would be very useful and informative, we do not think they are necessary to establish niche differentiation. What is necessary is to show that the taxa utilize essential aspects of the environment differently (see, for example, Lack, 1944
) which we have done.
We have shown that the parental and hybrid taxa have different niches as they differentially use available resources. That such microevolution (the width of the zone is 1 km) can occur despite high gene flow (big sagebrush is wind pollinated with wind-dispersed seeds) is testament to the strong selection required to stabilize this zone. We estimate selection coefficients on the order of 10-1 (Wang et al., 1997
). We raised seedlings from three sites within the hybrid zone in our common gardens. In no case was the common garden in the hybrid site >250 m from the native location of any hybrid seedling. Yet, the hybrids exhibited some degree of niche separation among plants from the three hybrid sites. This indicates that extremely powerful local selection is operating to structure this hybrid zone.
Our evidence indicates that each taxon is adapted to the local environment in which it occurs naturally. We have tried to identify the nature of that adaptation. Accordingly, we have also examined water stress and respiration rates of plants in the common gardens (McArthur et al., 1998a
). In that study we found significant differences among the gardens and taxa, but not genotype-by-environment interactions. Thus, the physiological evidence, at this time, indicates that adaptations to the different environments encountered across the hybrid zone probably involves the active uptake of the elements described in this study. Because fitness does not readily map onto the elemental concentrations or BACs, further work is required to elucidate the precise adaptive features.
Our study of soil chemistry (Wang et al., 1998
) indicates that the sites have markedly different soil chemistry and, within the hybrid zone, soils are spatially more variable than corresponding sites in either parental zone. It appears that hybridization provides the enhanced genetic variance required to successfully occupy such sites (see Lewontin and Birch, 1966
; Grant and Grant, 1994
).
While the taxa do differ for a number of traits (e.g., morphology, secondary compounds, and PCR markers; (McArthur, Welch, and Sanderson, 1988
; Freeman et al., 1991
; McArthur et al., 1998b
), they apparently have not diverged to the point that hybridization disrupts coadaptation (see Graham, 1992
). Freeman et al. (1995)
found no evidence of enhanced developmental instability among native hybrids compared to the parental taxa. Thus, it appears that strong exogenous selection stabilizes the sagebrush hybrid zone and sifts among the phenotypic variants, adapting hybrid populations to unique microhabitats within the hybrid zone.
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FOOTNOTES |
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3 Author for correspondence (cfreeman@sun.science.wayne.edu).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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