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Systematics |
2Department of Biological Science, California State University, Fullerton, California 92834 USA; 3Department of Biology, University of Utah, Salt Lake City, Utah 84112 USA
Received for publication February 6, 2003. Accepted for publication May 9, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: absorptance • adaptation • Asteraceae • brittlebush • desert • drought acclimation • Encelia farinosa • leaf pubescence • maternal family variance • spatiotemporal heterogeneity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Le Houérou et al., 1988
; Frank and Inouye, 1994
). Thus, widely distributed desert species are challenged to adapt to this variability over a broad geographic scale and also on local scales, where unpredictability of limiting resources can be extreme (MacMahon and Schimpf, 1981
; Lajtha and Schlesinger, 1986
; Le Houérou et al., 1988
; Ehleringer, 1994
). The influence of heterogeneous water availability is especially important in the evolution of desert plant species because water is the most limiting resource for productivity in desert ecosystems (Noy-Meir, 1973
; Fischer and Turner, 1978
; Hadley and Szarek, 1981
).
For the widespread desert perennial Encelia farinosa A. Gray (Asteraceae), traits associated with water use and productivity have been shown to vary on local and regional scales (Cunningham and Strain, 1969
; Ehleringer and Cook, 1990
; Monson et al., 1992
; Sandquist and Ehleringer, 1997
, 1998
; Housman et al., 2002
). One of these traits, leaf pubescence, is important for productivity under hot and dry desert conditions because the highly reflective pubescence decreases absorption of solar radiation and decreases the heat load on a leaf (Ehleringer and Clark, 1988
). During drought, each consecutive leaf cohort has a greater density of leaf hairs, which helps maintain leaf temperatures within the narrow range favorable for photosynthesis while also lowering dependence on water for transpirational cooling (Smith and Nobel, 1977
; Ehleringer and Mooney, 1978
; Ehleringer, 1983
). In the absence of water deficit, however, each cohort will maintain approximately the same, low amount of leaf pubescence (Ehleringer, 1982
).
Increasing pubescence during drought is also associated with longer maintenance of the leaf canopy (Sandquist and Ehleringer, 1997
). Although this extended activity can enhance productivity by increasing the longevity of daily and seasonal photosynthesis, there are also productivity trade-offs associated with greater pubescence. These include the additional costs for construction of the pubescence and lower rates of photosynthesis from leaf hairs reflecting photosynthetically active radiation (PAR). There is also an opportunity cost because the degree of pubescence cannot be changed after the leaf has expanded and the plant cannot produce newer primary leaves with higher light absorption (lower pubescence). Highly absorptive leaves can be produced only after a plant has become leafless or as small axillary leaves among the larger pubescent leaves (Ehleringer and Björkman, 1978
; Ehleringer, 1982
). Thus, pubescence constrains maximum PAR absorption if water stress is alleviated in the middle of a drought.
Interpopulation variability of leaf absorptance for E. farinosa may result from the balance between these costs and benefits over regional differences in precipitation and drought. In addition, variation at the intrapopulation level might also be present as a result of the interplay between this trade-off and local climatic heterogeneity. Such predictions are analogous to the density of trichomes being involved in (1) defense, in which variation is related to the presence or absence of herbivores (Levin, 1973
; Becerra and Ezcurra, 1986
), and (2) thermoregulation, in which variation correlates with elevation (Baruch, 1979
). For these two selective factors, evolutionary responses of trichome morphology and density, including heritability, have been well documented (e.g., Levin, 1973
; Baruch, 1979
; Gibson and Maiti, 1983
; Vasek, 1986
). Despite numerous studies that demonstrate the importance of leaf pubescence for productivity in E. farinosa, the genetic basis for phenotypic variation of leaf hair production has not been quantitatively analyzed.
To explore the evolutionary potential of leaf pubescence in E. farinosa, we examined the maternal family variability of pubescence-moderated leaf absorptance for three populations that span a broad gradient of water availability. Previous comparisons among populations of E. farinosa have shown that the leaf absorptance values of the initial leaf flush can be similar (Sandquist and Ehleringer, 1997
, 1998
), but after this stage, discrete differences occur. Leaf absorptance is consistently greater for plants from regions of high rainfall relative to those from lower-rainfall environments (Sandquist and Ehleringer, 1997
; Housman et al., 2002
), and in a preliminary common garden study of E. farinosa plants from nine populations, absorptance was correlated to the mean annual precipitation of the seed source regions (Sandquist, 1995
). These findings suggest that local adaptation and genetic divergence have given rise to variation of absorptance among populations; however, the implied genetic determination for this variation has never been detailed.
The goals of the present investigation were to (1) determine if differences for leaf absorptance values and responses to drought result from genetic differentiation among populations, (2) examine the degree of family-level variance (VG) present within populations to see how it might be related to the differences of climatic heterogeneity, and (3) provide insights about the potential selective processes operating within and among populations. We made use of three E. farinosa populations from a broad gradient of annual precipitation amount and maximum drought length. At one end of the gradient, where rainfall is low and drought is long, selection should strongly favor leaf pubescence, thereby reducing genetic variance, specifically, additive genetic variation (VA), for this trait (Falconer, 1989
). However, this environment is also unpredictable, being temporally heterogeneous on both an inter- and intra-annual basis. Thus, a high degree of genetic variability (VA) may be maintained if disruptive selection is strong and alternative genotypes can survive through unfavorable years (Ellner and Hairston, 1994
). At the other end of the gradient, rainfall is high and drought duration is short. Here, pubescence should play a less important role in productivity, and selection for high leaf pubescence should be weaker. However, this expectation does not preclude the possibility of finding reduced variance resulting from either consistency of this selection or via selection for higher PAR absorption (i.e., against high leaf pubescence) (Falconer, 1989
).
Knowledge of the genotypic basis for variation of leaf pubescence is necessary so that we may better understand the potential for adaptation and adaptability of E. farinosa over its broad geographic range and within highly variable local environments.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). This geographic variability is accompanied by variability of temporal patterns in precipitation and drought. Annual and seasonal rainfall is most unpredictable where average rainfall is lowest (Hastings and Turner, 1965
; Ehleringer, 1985
; Comstock and Ehleringer, 1992
), while drought length varies in relation to the termination of spring rainfall and the onset of summer monsoon rain (Ehleringer, 1994
). The most unpredictable drought length is found where summer monsoons die out in weak years but continue to advance in strong monsoon years. This region is roughly along the boarder of Arizona and California in North America.
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)—a greater CV value indicating higher year-to-year unpredictability.
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Plants were watered to pot capacity every day for 1 mo, after which the first leaf absorptance measurements were made (designated "predrought"). Watering was then reduced to once every 5 d for the next 3 wk, with natural precipitation providing additional water on two dates. After this 3-wk period, the "early drought" measurements of leaf absorptance were made. Light rain showers on five of the next 13 d, plus one final water supplement during this period, was the only water input for the next month. By the final date of leaf absorptance measurements ("mid-drought"), plants had not received any water for 20 d. Temperature conditions during the course of the study were within the normal range experienced by all populations, but were most similar to those experienced by plants of the Superior population.
Absorptance, the percentage of light absorbed relative to a MgO standard that absorbs <1%, was measured using an Ulbricht-type integration sphere and a monochromatic wavelength of 625 nm (Ehleringer, 1981
). This method closely approximates the integrated absorptance of all photosynthetically active radiation (400–700 nm) and is highly correlated with total solar radiation absorption (400–3000 nm).
On each sample date, one leaf of the most recently matured leaf cohort was removed for determination of leaf absorptance. Leaves were kept in plastic bags and refrigerated until measured. All leaves were measured within 72 h (<72 h), so that the time since leaf removal would not influence absorptance values (Sandquist, 1995
). Plants were measured at random among populations.
Among populations analyses
Analysis of variance with repeated measures (ANOVAR; JMP 3.1 statistical package, SAS Institute, 1994
) was used to test the overall differences in leaf absorptance among populations (population effect, P), differences in responses to drought (population by drought stage effect, P x D), and effects based on drought stage (D). The recommendations of Potvin et al. (1990)
were used for ANOVAR tests. All data conformed to the assumption of compound symmetry based on the Mauchly criterion or had a Huynh-Feldt epsilon (H-F 
) that neared unity (>0.95). In the latter cases, drought stage and population by drought stage effects were tested using the Huynh-Feldt epsilon correction for F values and probabilities (Potvin et al., 1990
). Pillai's trace was always used for population effects and for D and P x D effects when H-F = 1.0.
Differences among populations for mean leaf absorptance at a single drought stage were tested by the Kruskal-Wallis nonparametric rank test (JMP 3.1, SAS Institute, 1994
). This test was chosen because the assumption of homogeneity among group variances was occasionally violated depending on the method used for its determination (see JMP 3.1; SAS Institute, 1994
). Note, however, that these differences of variance only slightly influenced, if at all, the assumption of compound symmetry for the ANOVARs.
Within populations analyses
Analysis of variance with repeated measures was also used as one test of the genetic and environmental components of variance for absorptance within populations. Effects due to family (F), drought stage (D), and family by drought stage (F x D) were determined (JMP 3.1, SAS Institute, 1994
). This intrapopulation, family-based partitioning of seasonal variances for leaf absorptance provides broad estimates of the genetic variation corresponding to overall leaf absorptance and changes caused by drought (i.e., reaction norms).
In addition, an estimate of quantitative genetic variance (VG) for leaf absorptance within each population was determined for each drought stage. The least squares method, Model II ANOVA, was used to determine family-based variance components (VG) (Falconer, 1989
; JMP 3.1, SAS Institute, 1994
). From these, maximum and minimum values of broad-sense heritabilities were calculated based on the possible range of individual relatedness being half-sib to full-sib (E. farinosa is an obligate outcrosser). In the strictest sense, this estimate of VG includes one-fourth additive genetic variance (VA) plus 1/16 of the epistatic effects, if any. However, dominance variance (VD) and maternal effects confound this strict interpretation of VA, and our design, unfortunately, does not allow for the determination of these factors. Therefore, our calculation of the intraclass correlation (t) is based only on family variance (VG) divided by the total variance. This value is then used to estimate the broad-sense heritability (H2) as 4t (Falconer, 1989
).
Intrapopulation phenotypic correlations of leaf absorptance (pairwise comparisons among drought stages) were determined with the Pearson product-moment correlation (JMP 3.1, SAS Institute, 1994
). Estimates for family mean correlations among drought stages were based on the Pearson product-moment correlation among mean leaf absorptance values for each family (Via, 1984
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Intrapopulation variation of leaf absorptance
Leaf absorptance variation due to family effect was significant within the Oatman and Death Valley populations, but not the Superior population (Table 2). All three populations had significant differences in leaf absorptance due to drought stage, but the family by drought stage effect was not significant within any population (Table 2). The latter result suggests that differentiation is low among families for leaf absorptance changes through drought; however, some variation may exist because family-level reaction norms for absorptance response to drought occasionally crossed (data not shown).
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Within all three populations, predrought leaf absorptance did not correlate with values at later drought stages (Table 4). All three populations, however, had significant phenotypic correlations between early and mid-drought leaf absorptance. Significant family mean correlations (P < 0.05) were also observed among these periods for the Superior and Death Valley populations, while for the Oatman population this family correlation was significant at P = 0.059 (Table 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Leaf pubescence and environmental variability
A consistent pattern observed in comparisons among Encelia species is that plants from regions of high precipitation always have greater leaf absorptance than those of drier regions (Ehleringer, 1985
). This pattern has also been found within E. farinosa (Sandquist and Ehleringer, 1997
, 1998
; Housman et al., 2002
), and because leaf absorptance variation affects differences in productivity (Ehleringer, 1983
; Ehleringer and Cook, 1990
), divergence among populations may represent local adaptation to soil-water availability.
This conclusion implies that strong selective pressures have given rise to differences in leaf absorptance among populations, but such selection should reduce the genetic variance within populations (Falconer, 1989
). Our results, however, indicate that family-based (genetic or maternal) variation may persist within some populations (Tables 3 and 4), suggesting that either (1) selection has not been strong enough or consistent enough to eliminate genetic variance for leaf absorptance, (2) prevalence of dominance and maternal effects overwhelm selective influences, or (3) local spatial/temporal heterogeneity is great enough to support polymorphic populations (e.g., Ellner and Hairston, 1994
). Furthermore, the amount of this genetic variance appears to be related to the unpredictability of the environments from which these populations originated. Family-level variance was greatest where temporal (and presumably spatial) heterogeneity of precipitation is high (Death Valley) and least where heterogeneity of precipitation is low (Superior) (Tables 1 and 4). This result is consistent with predictions based on the relationship between genetic variance and environmental heterogeneity, but it must also be viewed with caution because of the small maternal family-level sample size of the Superior population. Nonetheless, because broad-scale differentiation among populations is correlated with soil-water availability, one might also predict that the same mechanisms of selection could contribute to variation within populations, especially where precipitation is highly variable. That is, within a population some plants may be adapted to low levels of water availability and others adapted to higher levels. This suggestion seems to contradict a general evolutionary pattern in which genotypes that do well across all climates (high plasticity), but do best in neither extreme, should be favored in heterogeneous environments based on a greater geometric mean fitness (Marshall and Jain, 1968
; Cooper and Kaplan, 1982
; Seger and Brockmann, 1987
). However, diverse genotypes within a population could persist if disruptive selection is strong enough and the genotypes that are not favored in a given year have some means of surviving through those unfavorable years (Ellner and Hairston, 1994
).
A slight variation of this same mechanism is evident when populations of highly heterogeneous environments never reach equilibrium because there is greater incidence of catastrophic events (e.g., drought) during which genotypes that are at a competitive disadvantage under normal climatic conditions could realize greater relative fitness. It is also possible that strong selection, based on microclimatic variation, could maintain highly localized population structuring over short distances (Levin, 1973
; Monson et al., 1992
), and if gene flow is not constrained by such localization, the genetic variation of the progeny from a maternal plant (as used in this study) may be greater than that of the natural population (in which variance is reduced by selection within each microclimate). In this case, our results would instead represent the possible evolutionary potential of the population.
Finally, measurements of genetic variance must also take into consideration genotype-by-environment interactions because the observed genetic variance can be dependent on the environment (Gupta and Lewontin, 1982
; Mitchell-Olds and Rutledge, 1986
). Indeed, our study was done in only one environment, one that had fairly high water availability and cooler temperatures than the drier populations might experience during normal years. It was, therefore, more similar to the selective regime of the wetter population (Superior) and thus may have lowered the observed family variance for this population. However, it should also be recognized that higher-than-average water availability is also an important component for selection in dry regions and may be one of the agents that maintains genetic variance within populations like Oatman and Death Valley.
Our investigation was not designed to determine the mechanism responsible for maintenance of genetic variance within these populations, but it does demonstrate the following for leaf absorptance of E. farinosa: (1) genetic variance potentially does exist, (2) it may be related to the degree of environmental heterogeneity, and (3) from this variation there may be the potential for local adaptation.
In contrast to the variation in mean leaf absorptance, family variation for the slope of leaf-absorptance reduction during drought was very low at both the inter- and intra-population levels. This low variability might result from the importance of coupling leaf absorptance changes with other physiological and developmental characters that also change in response to reduced soil water. Indeed, Ehleringer and Cook (1984)
showed that reductions in both leaf absorptance and stomatal limitations were correlated to the rate of decrease in water availability (i.e., water potential). Strong selection for drought-response trait associations could indirectly reduce the variance of the leaf absorptance response. Such low genetic variability would still allow among-environment difference as seen in field observations (Sandquist and Ehleringer, 1998
; Housman et al., 2002
), but it would preclude strong differentiation in a common environment unless maternal effects are rather strong.
The observation that leaf absorptance reduction rates are invariable while mean leaf absorptance values are distinctly different raises the question as to when leaf absorptance differentiation takes place? Results from the interpopulation comparison suggest that this departure must occur very early in development because differentiation had already taken place prior to the earliest measurements. This implies that the interpopulation differences resulted from a genetically controlled divergence of leaf absorptance during the initial leaf flushes, or if populations start with the same leaf absorptance values (as in Sandquist and Ehleringer, 1997
), the differences would result from leaf absorptance changes that take place very early and under generally favorable conditions.
Intrapopulation patterns may also indicate that differentiation takes place during early development, albeit at a slightly later period than among populations, which might be expected for more closely related plants. We found that family-level genetic variation in leaf absorptance was present only after the predrought stages, and there were no correlations between predrought and early drought leaf absorptance values. These two patterns imply that changes of leaf absorptance that take place between pre- and early drought result in the differences among genotypes and support the proposal that the leaf absorptance variation is manifested during early canopy development or very early within a drought.
In summary, this study has shown that the interpopulation variation of mean leaf absorptance may result from genetic differences among population (although maternal effects can not be ruled out completely). This variation also conforms to expected differences based on geographic variation of water availability, higher leaf absorptance values being found in wetter environments. However, there appeared to be no variation for the rate of leaf absorptance reduction during drought. These findings suggest that selection based on soil-water availability may have given rise to genetic differences for leaf absorptance in E. farinosa, but that the rate of leaf absorptance reduction during drought is constrained, perhaps due to correlations between leaf absorptance and other drought-response traits.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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P < 0.06; * P < 0.05; ** P < 0.01; *** P < 0.001