| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Population Biology |
Department of Ecology and Evolutionary Biology, Brown University, Box G-W, Providence, Rhode Island 02912 USA; and 3Colorado College, Department of Biology, 14 E. Cache La Poudre St., Colorado Springs, Colorado 80903 USA
Received for publication September 10, 2006. Accepted for publication October 23, 2007.
ABSTRACT
Maternal effects can have substantial impacts on plant fitness and plant populations. Stressful environmental conditions can cause a maternal plant to inadequately provision its progeny, resulting in poor seedling growth, low reproductive success, and decreased competitive ability. Maternal effects consist of environmental and genetic load components, but the interactions between these two components have rarely been considered. To determine the effects of maternal drought stress and maternal inbreeding on progeny biomass (a fitness correlate) and physiological responses to drought stress, we conducted a greenhouse experiment with genetic lines from two populations (mesic site vs. dry site) of the herbaceous annual Impatiens capensis (Balsaminaceae). Seeds were collected from cleistogamous flowers of inbred or outcrossed maternal plants that were subject to either a drought or control treatment. These seeds were grown into juvenile plants that were also subject to either a drought stress or a control treatment. Plants from the mesic site had significantly reduced biomass from maternal drought stress, while plants from the dry site maintained biomass despite adverse maternal environmental conditions. Juvenile plants of both populations had reduced biomass only as a result of maternal inbreeding. Interestingly, inbreeding depression was more apparent when maternal environmental conditions were benign.
Key Words: Balsaminaceae • carbon assimilation rate • drought stress • inbreeding depression • maternal effects • stomatal conductance
Plant population persistence may depend upon the ability of plants to withstand environmental stresses such as drought (Hoffman and Parsons, 1991
). Persistence may additionally depend on the degree of inbreeding experienced by a population, particularly among small or fragmented populations (Barret and Kohn, 1991; Lande, 1998
; Oostermeijer et al., 2003
). Therefore, an understanding of the ecological and evolutionary responses to environmental stress and inbreeding is necessary to predict the viability of natural plant populations and the persistence of species in a geographic area. Studies have documented the evolution of strategies for drought stress tolerance in natural populations (e.g., Aronson et al., 1993
; Dudley, 1996
; Heschel et al., 2002
; Heschel and Riginos, 2005
) as well as the fitness disadvantages of inbreeding in field conditions (Schmitt and Gamble, 1990
; Barrett and Kohn, 1991
; Montalvo, 1994
; Heschel and Paige, 1995
) and in greenhouse experiments (Dudash, 1990
; Schmitt and Ehrhardt, 1990
; Agren and Schemske, 1993
; Norman et al., 1995
; Heschel et al., 2005
). Few studies, however, have considered the role of maternal effects in these responses (Wolfe, 1993
; Montalvo, 1994
). Moreover, maternal effects on gas exchange physiology have, to our knowledge, never been examined in the context of inbreeding and drought stress.
Maternal effects in plants are broadly defined as the contribution of the maternal parent to progeny phenotype beyond the equal chromosomal contribution of both parents (Roach and Wulff, 1987
). These effects can arise, for example, because the tissues surrounding the developing embryo are maternal. Maternal effects can be caused by the maternal genotype, the maternal environment, or both (Roach and Wulff, 1987
; Schmitt et al., 1992
). Moreover, they can affect important fitness components such as seed size, dormancy, and hormone levels (see Roach and Wulff, 1987
for review). The consequences of maternal effects on progeny competitive ability and fitness can be substantial; they are most apparent in the seedling stage but often persist over a plant's whole lifetime (Roach and Wulff, 1987
) and even into subsequent generations (Alexander and Wulff, 1985
).
The degree of inbreeding in maternal plants represents a potential cause of genotypic maternal effects. Such genotypic maternal effects may reflect a differential genetic load among maternal lines. For example, del Castillo (1998)
found that the offspring of selfed (inbred) plants had lower fitness relative to the offspring of outcrossed plants and attributed this result to a differential maternal effect in response to inbreeding. In several other studies, however, the effects of maternal environment were found to override the effects of maternal inbreeding (Schaal, 1984
; Wolfe, 1993
; Montalvo, 1994
).
The relative importance of maternal environmental and maternal genotypic effects may depend on the environmental conditions experienced by progeny. Adverse environmental conditions have been shown to exacerbate inbreeding depression in single-generation studies (Pray et al., 1994
; Miller, 1994
; Norman et al., 1995
; Heschel and Paige, 1995
; Byers and Waller, 1999
); thus, maternal inbreeding may result in lower progeny fitness if progeny grow in adverse environmental conditions. At the same time, the effects of maternal environment on progeny fitness may also depend on progeny-generation environmental conditions. Sultan (1996)
found that maternal plants in resource-deprived conditions better provisioned their progeny to withstand similar conditions than did maternal plants in resource-rich conditions. Thus, progeny environmental conditions are likely to play an important role in mediating the separate and net consequences of maternal genotype and environment on progeny fitness.
To investigate the interactions among maternal environmental stress, maternal inbreeding, and progeny environmental stress, we experimentally manipulated the degree of maternal inbreeding and maternal and progeny drought stress among juvenile plants of the annual herb Impatiens capensis Meerb. (Balsaminaceae). Drought is an environmental stress that has been shown to cause maternal effects (Sultan, 1996
; Meyer and Allen, 1999
). Moreover, drought stress can amplify the magnitude of inbreeding depression for fitness as well as gas exchange traits (e.g., Norman et al., 1995
; Hauser and Loeschcke, 1996
; Heschel et al., 2005
). Here, we assess plant performance in terms of drought tolerance via both "drought escape" and "dehydration avoidance." Drought escape traits include faster growth toward earlier reproduction, while dehydration avoidance involves minimizing water loss through decreased stomatal conductance (McKay, 2003
). We chose to examine gas exchange traits because Heschel et al. (2002)
demonstrated that stomatal conductance can be an important component of plant fitness in drought conditions.
Impatiens capensis (jewelweed) provides a good system in which to test the maternal effects of drought stress and inbreeding. Jewelweed populations are common in floodplains, stream banks, and wet woods throughout North America, but populations can also persist in drier woodland sites (Leck, 1979
, 1996
). Studies of natural populations of I. capensis have documented genetic differences in plant responses to drought (Heschel and Hausmann, 2001
) and in stomatal conductance plasticity across drought and irrigated treatments (Heschel et al., 2002
; Heschel and Riginos, 2005
). Jewelweed has a mixed mating system, producing both self-fertilizing cleistogamous and outcrossing chasmogamous flowers, thus facilitating manipulations of inbreeding coefficient. Although purging of deleterious alleles is more likely in highly selfing species (Charlesworth and Charlesworth, 1987
), inbreeding depression is well documented in Impatiens (Waller, 1979
, 1980
, 1984
; Schmitt and Ehrhardt, 1990
; Schmitt and Gamble, 1990
; McCall et al., 1994
; Heschel et al., 2005
). Moreover, because Impatiens populations are highly inbred, natural populations are essentially collections of inbred lines (Paoletti and Holsinger, 1999
). Like our experimental crosses, natural crosses can occur between highly inbred subpopulations, creating a mosaic of homozygosity levels in the field. Thus, examining genetic maternal effects as degrees of inbreeding is relevant to microevolutionary changes in this species.
In this paper we address the following questions: (1) Does maternal drought stress confer higher biomass (a fitness correlate) and reduced gas exchange rates in offspring that undergo drought stress, or, alternatively, does maternal drought stress have a negative impact on progeny biomass and gas exchange? (2) Is there evidence for effects of maternal generation inbreeding on progeny biomass and gas exchange (i.e., physiological performance)? (3) Does inbreeding depression depend upon either maternal or progeny drought stress, or both?
MATERIALS AND METHODS
Organism and study sites
Randomly selected seedlings were collected from each of two natural populations of I. capensis in May 1995. These populations, located on Brown University's Haffenreffer Reserve in Bristol, Rhode Island, are separated by less than 1 km, but the sites differ in light and moisture conditions. One site is moist and sunny, while the other is dry and shaded (see Heschel and Hausmann, 2001
for details). The mesic site experiences soil water potentials from 0 to –0.025 MPa; while the dry site experiences soil water potentials from –0.015 to –0.065 MPa (note: MPa values of less than –0.030 are stressful to I. capensis). In addition, the populations differ in levels of outcrossing. The more mesic population (hereafter referred to as the wet population) has a higher potential for outcrossing than does the "dry" population, as evidenced by the significantly higher rate of chasmogamous flower production within the wet population (Heschel et al., 2005
).
Seedlings from these sites were used to establish inbred lines that were maintained over six generations of single-seed descent, creating highly homozygous plants. Purging of genetic load was not noticed because lines were not lost over the six generations and seed set was comparable during this time (M. S. Heschel, unpublished data). Lines were grown under uniform conditions in the Brown University greenhouse to minimize maternal environmental effects. Seeds of each generation were stratified at 4°C for 4 mo after collection. Nine lines from each population were used for this experiment. The experimental goal in this and a related study (Heschel et al., 2005
) was to quantify inbreeding effects by comparing highly homozygous individuals (selfed for several generations) and highly heterozygous individuals (crosses between almost completely homozygous lines).
Maternal inbreeding and environments
In the seventh generation, lines were either selfed or crossed with a line representing a neighbor in the natural population (see Heschel et al., 2005
for details). This produced individuals that had the same maternal parent but differed in inbreeding coefficient. Crosses were made with randomly chosen lines whose progenitor in the natural population was 5 m away, a typical pollination distance for I. capensis (Waller, 1984
). Eight selfed and eight outcrossed offspring of each line were randomized over eight blocks, four of which received a drought stress treatment 1 wk in duration (hereafter referred to as "maternal drought") and four of which were kept continually moist (hereafter referred to as "maternal irrigated") (Heschel et al., 2005
). The drought treatment was imposed on these adult plants after 2 mo of growth when plants had already started flowering. This treatment represents the type of drought stress under natural field conditions for I. capensis (M. S. Heschel, unpublished data); in Rhode Island, drought occurs as weeklong pulses early in the growing season. All blocks were bottom-watered daily (except during the drought treatment, during which time maternal drought plants received no water) to insure uniform soil moisture conditions. Beginning 2.5 wk after the drought treatment (mid-May through early June of 1999), cleistogamous seeds from each of the 288 maternal plants were collected.
Progeny experimental design
We conducted a greenhouse experiment to assess the fitness and physiological effects of maternal environment in combination with maternal inbreeding and progeny drought stress. Cleistogamous seeds from the 288 maternal plants of the previous experiment (Heschel et al., 2005
) were collected, weighed, and stratified at 4°C for 4 mo. Seeds were collected from cleistogamous flowers on selfed and outcrossed maternal plants (a distinction hereafter referred to as maternal cross type) in both the irrigated and drought treatments. Thus, progeny were either inbred for one generation (outcrossed parent or "maternally outcrossed") or for eight generations (selfed parent or "maternally selfed"), whereas plants in the maternal generation were inbred for either zero generations or seven generations.
In September 1999, we planted seeds into 8-cm square pots. The soil was composed of two parts perlite and one part Scott's Metromix 360 (Scotts-Sierra Horticultural Products, Marysville, Ohio, USA) to create a slow and uniformly drying soil environment. Eight replicates per maternal treatment per line (576 plants total) were randomized over eight blocks, with four offspring replicates from each maternal plant randomly positioned across four drought treatment blocks (hereafter referred to as progeny drought) and four offspring replicates positioned across four continually watered blocks ( "progeny irrigated"). All plants were grown in the Brown University greenhouse, bottom-watered daily (except during the drought treatment as described next), and fertilized biweekly with Peter's N/P/K (Scotts-Sierra Horticultural Products). Plants were rotated within their blocks every 1.5 wk to reduce neighbor effects.
We applied a drought treatment to four blocks after 5 wk of growth (seedling stage). All water was withheld from progeny drought plants during this time. The treatment lasted for 1 wk, in keeping with the maternal generation drought treatment and stressed the juvenile plants to just before the permanent wilting point. During days 3 through 7 of the treatment, we measured gas exchange (described later) on four blocks, two drought-stressed and two irrigated. Juvenile plants were allowed to recover from the drought treatment and grow for three more weeks. In early December, shoots from all plants and roots from four of the eight blocks (two blocks progeny drought and two progeny irrigated) were harvested, oven-dried at 65°C for 1 wk, and weighed. Because no differences in root : shoot ratios were detected among the experimental treatments, we present results only for aboveground biomass. We harvested juvenile plants at this pre-reproductive stage to increase the likelihood of detecting maternal effects, which can attenuate during a plant's life (Roach and Wulff, 1987
). Aboveground biomass provides a good indicator of overall fitness among I. capensis individuals (Waller, 1979
; Schmitt et al., 1987
).
Physiological measurements
Carbon assimilation rate (A = µmol CO2·m–2·s–1) and stomatal conductance (gst = mol H2O·m–2·s–1) were measured with an LCA 4 (ADC Bioscientific Ltd., Hoddesdon, UK) infrared gas analyzer (IRGA). All IRGA measurements were taken between 0900 and 1500 hours. The LCA 4 had an adjustable PAR light source, and light levels were kept between 790 and 800 µmol·m–2 ·s–1. A Parkinson leaf chamber was kept over ice, and a fan was used to push air over the chamber. Chamber temperature was kept between 20 and 25°C, with variations within each day in the range of 2–3°C. Ambient humidity, varying from 40 to 50%, was used for all measurements. We estimated boundary-layer conductances using leaf mimics made with moist filter paper (Parkinson, 1985
). To correct for different leaf areas in the Parkinson leaf chamber, we calculated an individual's leaf area for each gas exchange measurement. Carbon assimilation rate and stomatal conductance were adjusted for date and time of measurement with residuals from regression models that included date and time as fixed factors and carbon assimilation rate or stomatal conductance as response variables (Farris and Lechowicz, 1990
; Dudley, 1996
; Heschel et al., 2002
).
Statistical analysis
All statistical analyses were performed with version 3.1 of JMP (SAS Institute, 1994
). We used four-way ANOVAs to test for population, maternal treatment, maternal cross type, and progeny treatment differences in carbon assimilation rate, stomatal conductance, and biomass (a fitness correlate). Population, maternal treatment, maternal cross type (i.e., selfed progeny derived from inbred or outcrossed maternal plants), and progeny treatment were fixed factors, while line (nested within population) and block (nested within progeny treatment) were random factors. Because of significant higher order interactions in the four-way ANOVAs, data were sorted by maternal treatment and progeny treatment and analyzed using two-way ANOVAs with population and maternal cross type as fixed factors and line and block as random factors. A sequential Bonferroni adjustment was applied to each of the two-way ANOVAs (Tables 1–3); for each model, the adjusted, initial P value for rejecting the null hypothesis was 0.008. Because of the overly conservative nature of the Bonferroni adjustment, we discuss the unadjusted P values in the Results section (Moran, 2003
). Several F tests are constructed in each ANOVA model; however, they each test a priori hypotheses so accepting a P value of 0.05 seems appropriate. Models initially included a block by line interaction term, but we removed this interaction to reduce the size of our linear models because it had no effect on line significance for any of the traits examined and was not significant in any case. To examine the role of seed mass in mediating the observed differences in final biomass, we analyzed biomass data both with and without seed mass as a covariate. Seed mass had no effect on the predictive nature of treatment or on population differences in biomass, so the biomass analysis is not presented as an ANCOVA. Planned linear contrasts were calculated on model least-square means to ascertain where differences lie within interaction terms; the contrasts presented were intended to address a priori experimental questions. We used planned contrasts in the context of model interaction terms rather than a complete set of multiple contrasts to avoid an excess of statistical tests. All models were examined for normality of residuals and homoscedasticity.
|
|
Maternal environmental effects
A maternal generation drought resulted in reduced biomass among progeny, independent of maternal cross type. This maternal drought effect was population-dependent (significant population by maternal treatment interaction in a four-way ANOVA, F = 5.34, df = 1, P = 0.03) (Fig. 1). Contrasts within this interaction revealed that biomass in the wet population was greater in the maternal irrigated treatment than in the maternal drought treatment (t = 3.28, df = 1, P = 0.005), while biomass in the dry population did not differ across maternal treatments (t = 0.008, df = 1, P = 0.994) (Fig. 1). The negative effects of maternal drought on progeny biomass in the wet population were independent of maternal drought effects on seed mass. When the effect of seed mass was held constant, the effect of maternal drought on biomass within the wet population was still significant (contrast within population by maternal treatment term of a four-way ANCOVA: t = 2.84, df = 1, P = 0.012).
|
|
|
|
). No significant interactions between the progeny treatment and maternal treatment, however, were detected for any of the traits measured (progeny by maternal treatment interactions in four-way ANOVAs, carbon assimilation rate: F = 0.39, df = 1, P = 0.53; stomatal conductance: F = 0.03, df = 1, P = 0.86; biomass: F = 0.02, df = 1, P = 0.88). This absence of interaction indicates that progeny responses to drought stress did not depend on the environment experienced by the maternal generation.
Stress-independent inbreeding effect
Maternal generation inbreeding had significantly negative effects on progeny biomass independent of maternal or progeny environmental stress. Juveniles derived from cleistogamous flowers of outcrossed maternal plants were larger than those derived from cleistogamous flowers of maternally selfed plants, regardless of population, among plants not subjected to drought in either generation (significant cross type effect, Table 3; Fig. 1). This lack of an interaction between inbreeding level and drought suggests that both populations underwent stress-independent maternal inbreeding depression for final biomass; moreover, this inbreeding depression was only experienced in benign conditions.
Conversely, no effects of the type of maternal generation cross were seen for carbon assimilation rate (Table 1), regardless of treatment; that is, no effects of maternal generation inbreeding were detected in stressful or benign conditions for this trait. However, carbon assimilation values did depend on genotype because significant genetic variation for the effect of cross type on this trait (significant line by maternal cross type interaction term) was detected among plants not subjected to drought in either generation (Table 1). This result indicated that, like biomass, inbreeding depression for carbon assimilation was only experienced in benign conditions.
Stress-dependent inbreeding effects
Stomatal conductance was the only trait for which there was an interaction between maternal generation inbreeding and drought treatment. Maternal cross type was a significant predictor of stomatal conductance when both maternal and progeny generations experienced drought stress (Table 2). Individuals derived from maternally selfed plants from both populations had substantially higher stomatal conductance in this treatment combination than did individuals derived from maternally outcrossed plants (maternally outcrossed LSM = 0.048 mol H2O·m–2·s–1, maternally selfed LSM = 0.075 mol H2O·m–2·s–1, SE = 0.008). There was no effect of maternal cross type on stomatal conductance for any other maternal and progeny treatment combination, indicating that inbreeding depression for stomatal conductance was only experienced in stressful conditions.
DISCUSSION
Although maternal effects are known to have both environmental and genetic load components, few studies have examined the interactions between these two components or their ramifications in the context of progeny environmental conditions. In this study of I. capensis, the maternal effects of drought stress may have obscured the effects of maternal generation inbreeding for some traits. Significant inbreeding effects were only detected in benign conditions for biomass, which is strongly correlated with fitness in this species (Fig. 1, Table 3) and for carbon assimilation rate (Table 1), but were not detected for stomatal conductance (Table 2). Moreover, some maternal genotypes had the ability to maintain offspring biomass despite the drought stress in the maternal generation.
Maternal drought effects on progeny
Our results suggest that biomass may be maintained in the face of maternal drought stress among dry population genotypes but not among wet population genotypes. Nevertheless, the dry population was more sensitive to maternal treatment in terms of physiology; juveniles had decreased stomatal conductance in response to maternal drought. This result is consistent with the greater sensitivity of the dry population than the wet population to abscisic acid (ABA) (Heschel and Hausmann, 2001
); in response to increased levels of ABA (characteristic of drought conditions), dry population plants had lower stomatal conductance than wet population plants. Taken together, the increased physiological sensitivity of the dry population to maternal drought stress as well as the known population differences in ABA sensitivity suggest that maternal drought has a developmental effect, perhaps via ABA, on gas exchange physiology (Sawhney and Naylor, 1982
; Hansen, 2000
). Moreover, this developmental effect may precondition dry population juveniles to better avoid dehydration and to tolerate stress because decreased stomatal conductance can decrease water loss in this population (Heschel et al., 2002
).
In summary, adverse maternal environmental conditions had negative, neutral, and potentially positive effects on progeny biomass, depending on the source population. These results support previous findings wherein progeny fitness was reduced (Donohue and Schmitt, 1998
), maintained (Sultan, 1996
; Donohue and Schmitt, 1998
), or enhanced (Sultan, 1996
) as a consequence of maternal generation stress. Here the maternal effects of drought may confer functional homeostasis to drought stress among progeny of the dry population but not the wet population. These genetic differences between responses of the wet and dry populations to maternal drought stress may have adaptive significance. For the dry population, which is frequently subject to drought conditions (Heschel and Hausmann, 2001
), the ability to maintain progeny fitness in the face of maternal drought stress may have been selected for in the past.
Stress-dependent and -independent effects of maternal inbreeding
Both theoretical and empirical studies have emphasized that inbreeding depression is more likely to occur under harsh environmental conditions (Lloyd, 1980
; Dudash, 1990
; Wolfe, 1993
; Miller, 1994
; Pray et al., 1994
; Heschel and Paige, 1995
; Normal et al., 1995; Byers and Waller, 1999
). However, in the present study, significant maternal generation inbreeding depression for carbon assimilation rate and biomass (a fitness correlate) was only detected under benign conditions (Tables 1, 3). The soil moisture levels for the irrigated treatment were not at stressful levels (C. Riginos and M. Heschel, unpublished data), indicating that maternal inbreeding depression for biomass and carbon assimilation was stress-independent. Stress-dependent inbreeding effects, i.e., inbreeding depression detected under drought conditions, were found only for stomatal conductance (Table 2). Interestingly, this effect was seen in juvenile plants from both the wet and dry populations in the present study, whereas in the maternal generation (a separate study; Heschel et al., 2005
), adult plants from the dry population had minimal effects of inbreeding for gas exchange traits, while wet population plants had stronger inbreeding depression for physiological traits. These contrasting results may be due to differences in the expression of inbreeding depression over the lifetime of the plants. Higher stomatal conductance results in increased water loss, and thus a potential fitness decrease for more inbred individuals, during late-season drought among the same populations of I. capensis (Heschel et al., 2002
). In early-season drought, however, increased stomatal conductance and high water loss is selectively advantageous because it increases short-term carbon gains, resulting in faster growth and higher reproductive output for inbred plants (Heschel and Riginos, 2005
). Thus, the higher stomatal conductance of maternally selfed plants observed here might translate into inbreeding depression during late-season drought and outbreeding depression during early-season drought.
Whereas the maternal generation did not show any consequences of inbreeding in terms of biomass (and, by extension, fitness) (Heschel et al., 2005
), the progeny generation did. That is, even though maternal generation plants were able to maintain their own biomass, the offspring of more inbred plants had lower biomass; biomass differences were detected between progeny cleistogamously derived from inbred vs. outcrossed maternal plants. These biomass differences suggest that cryptic effects of inbreeding in plant populations may have fitness consequences in subsequent generations via maternal effects.
Conservation implications
The results presented here inform both theoretical considerations, such as how fitness is maintained or reduced in natural plant populations, as well as applied considerations, such as which seeds to collect for restoration or experimental purposes in order to minimize the chances of negative maternal effects. For instance, negative maternal environmental effects may be more likely to occur within a population without a history of stress exposure or within a population that has recently experienced a novel environmental stress. Moreover, for populations that have experienced stress in the past, it may be important to consider the time of year that these populations have typically experienced stress. Here, maternal stress effects were beneficial for progeny only if offspring would be expected to receive a late-season drought. Generally, because maternal effects can persist for multiple generations (Alexander and Wulff, 1985
; Campbell, 1997
), these effects have the potential to play a significant role in maintaining or accelerating a decline in fitness within natural plant populations.
FOOTNOTES
1 The authors thank F. V. Jackson for maintaining the greenhouse environment in excellent condition, M. Bertness for use of his IRGA, and D. Murray for laboratory assistance. N. Hausmann, N. Kane, K. Gravuer, E. Hane, and Y. Toyonaga were invaluable in assisting with experimental measurements and setup. This paper benefited from comments by K. Donohue, K. Holsinger, P. Ewanchuk, J. Boggs, two anonymous reviewers, and C. Fenster. This work was supported by a Sigma Xi grant to M.S.H. and a Howard Hughes Medical Institute Advanced Research grant to C.R. 
4 Present address: Department of Plant Sciences, University of California, Davis, Mail Stop 1, One Shields Avenue, Davis, CA 95616 USA
5 Author for correspondence (e-mail: shane.heschel{at}coloradocollege.edu
)
LITERATURE CITED
Agren J. Schemske D. W.. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125-135..[CrossRef][ISI]
Alexander H. M. Wulff R.. 1985. Experimental ecological genetics in Plantago. X. The effects of maternal temperature on seed and seedling characters in Plantago lanceolata. Journal of Ecology 73: 271-282..[CrossRef][ISI]
Aronson J. Kigel J. Schmida A.. 1993. Reproductive allocation strategies in desert and Mediterranean populations of annual plants grown with and without water-stress. Oecologia 93: 336-342..[CrossRef][ISI]
Barrett S. C. H. Kohn J. R.. 1991. Genetic and evolutionary consequences of small population size in plants: implications for conservation. In D. A. Falk, K. E. Holsinger [eds.], Genetics and conservation of rare plants, 2-30. Oxford University Press, Oxford, UK..
Byers D. L. Waller D. M.. 1999. Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics 30: 479-513..[CrossRef][ISI]
Campbell D. R.. 1997. Genetic and environmental variation in life-history traits of a monocarpic perennial: a decade-long field experiment. Evolution 51: 373-382..[CrossRef][ISI]
Charlesworth D. Charlesworth B.. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268..[CrossRef][ISI]
del Castillo R. F.. 1998. Fitness consequences of maternal and nonmaternal components of inbreeding depression in the gynodioecious Phacelia dubia. Evolution 52: 44-60..[CrossRef][ISI]
Donohue K. Schmitt J.. 1998. Maternal environmental effects in plants: adaptive plasticity?. In T. A. Mousseau, C. W. Fox [eds.], Maternal effects as adaptations, 137-158. Oxford University Press, New York, New York, USA..
Dudash M. R.. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129-1139..[CrossRef][ISI]
Dudley S. A.. 1996. Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50: 92-102..[CrossRef][ISI]
Farris M. A. Lechowicz M. J.. 1990. Functional interactions among traits that determine reproductive success in a native annual plant. Ecology 71: 548-557..[CrossRef][ISI]
Hansen M.. 2000. ABA treatment and desiccation of microspore-derived embryos of cabbage (Brassica oleracea ssp. capitata L.) improves plant development. Journal of Plant Physiology 156: 164-167..[ISI]
Hauser T. P. Loeschcke V.. 1996. Drought stress and inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae). Evolution 50: 1119-1126..[CrossRef][ISI]
Heschel M. S. Donohue K. Hausmann N. J. Schmitt J.. 2002. Population differentiation for water-use efficiency in Impatiens capensis (Balsaminaceae). International Journal of Plant Sciences 163: 907-912..[CrossRef][ISI]
Heschel M. S. Hausmann N. J.. 2001. Population differentiation at the hormonal level in response to drought in Impatiens capensis (Balsaminaceae). International Journal of Plant Sciences 162: 1253-1260..[CrossRef][ISI]
Heschel M. S. Hausmann N. J. Schmitt J.. 2005. Testing for stress-dependent inbreeding depression in Impatiens capensis. American Journal of Botany 92: 1322-1329..
Heschel M. S. Paige K. N.. 1995. Inbreeding depression, environmental stress, and population size variation in scarlet gilia (Ipomopsis aggregata). Conservation Biology 9: 126-133..[CrossRef][ISI]
Heschel M. S. Riginos C.. 2005. Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminaceae). American Journal of Botany 92: 37-44..
Hoffman A. A. Parsons P. A.. 1991. Evolutionary genetics and environmental stress. Oxford University Press, Oxford, UK..
Lande R.. 1998. Anthropogenic, ecological and genetic factors in extinction and conservation. Researches on Population Ecology 40: 259-269..[CrossRef][ISI]
Leck M. A.. 1979. Germination behavior of Impatiens capensis. Meerb. Bartonia 46: 1-14..
Leck M. A.. 1996. Germination of macrophytes from a Delaware River tidal freshwater wetland. Bulletin of the Torrey Botanical Club 123: 48-67..[CrossRef][ISI]
Lloyd D. G.. 1980. Demographic factors and mating patterns in angiosperms. In O. T. Solbrig [ed.], Demography and evolution in plant populations, 67-88. University of California Press, Berkeley, California, USA..
McCall C. Waller D. M. Mitchell-Olds T.. 1994. Effects of serial inbreeding on fitness components in Impatiens capensis. Evolution 48: 818-827..[CrossRef][ISI]
McKay J. K. Richards J. H. Mitchell-Olds T.. 2003. Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12: 1137-1151..[CrossRef][Medline]
Meyer S. E. Allen P. S.. 1999. Ecological genetics of seed germination regulation in Bromus tectorum L. II. Reaction norms in response to a water stress gradient imposed during seed maturation. Oecologia 120: 35-43..[CrossRef][ISI]
Miller P. S.. 1994. Is inbreeding depression more severe in a stressful environment?. Zoo Biology 13: 195-208..[CrossRef]
Montalvo A. M.. 1994. Inbreeding depression and maternal effects in Aquilegia caerulea, a partially selfing plant. Ecology 75: 2395-2409..[CrossRef][ISI]
Moran M. D.. 2003. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100: 403-405..[CrossRef][ISI]
Norman J. Sakai A. K. Weller S. G. Dawson T. E.. 1995. Inbreeding depression in morphological and physiological traits of Schiedea lydgatei (Caryophyllaceae) in two environments. Evolution 49: 297-306..[CrossRef][ISI]
Oostermeijer J. G. B. Luijten S. H. den Nijs J. C. M.. 2003. Integrating demographic and genetic approaches in plant conservation. Biological Conservation 113: 389-398..[CrossRef][ISI]
Paoletti C. Holsinger K. E.. 1999. Spatial patterns of polygenic variation in Impatiens capensis, a species with an environmentally controlled mixed mating system. Journal of Evolutionary Biology 12: 689-696..[CrossRef][ISI]
Parkinson K. J.. 1985. A simple method for determining the boundary layer resistance in leaf cuvettes. Plant, Cell and Environment 8: 223-226..
Pray L. A. Schwartz J. M. Goodnight C. J. Stevens L.. 1994. Environmental dependency of inbreeding depression: implications for conservation biology. Conservation Biology 8: 562-568..[CrossRef][ISI]
Roach D. A. Wulff R. D.. 1987. Maternal effects in plants. Annual Review of Ecology and Systematics 18: 209-235..[CrossRef][ISI]
SAS.. 1994. JMP user's guide, version 3.1. SAS Institute, Cary, North Carolina, USA..
Sawhney R. Naylor J. M.. 1982. Dormancy studies in seed of Avena fatua. 13. Influence of drought stress during seed development on duration of seed dormancy. Canadian Journal of Botany 60: 1016-1020..
Schaal B. A.. 1984. Life history variation, natural selection, and maternal effects in plant populations. In R. Dirzo, J. Sarukhan [eds.], Perspectives in plant population ecology, 188-206. Sinauer, Sunderland, Massachusetts, USA..
Schmitt J. Eccleston J. Ehrhardt D. W.. 1987. Dominance and suppression, size-dependent growth, and self-thinning in a natural Impatiens capensis population. Journal of Ecology 75: 651-666..[CrossRef][ISI]
Schmitt J. Ehrhardt D. W.. 1990. Enhancement of inbreeding depression by dominance and suppression in Impatiens capensis. Evolution 44: 269-278..[CrossRef][ISI]
Schmitt J. Gamble S. E.. 1990. The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution 44: 2022-2030..[CrossRef][ISI]
Schmitt J. Niles J. Wulff R. D.. 1992. Norms of reaction of seed traits to maternal environments in Plantago lanceolata. American Naturalist 139: 451-466..[CrossRef][ISI]
Sultan S. E.. 1996. Phenotypic plasticity for offspring traits in Polygonum persicaria. Ecology 77: 1791-1807..[CrossRef][ISI]
Waller D. M.. 1979. The relative costs of self- and cross-fertilized seeds in Impatiens capensis (Balsaminaceae). American Journal of Botany 66: 313-320..[CrossRef][ISI]
Waller D. M.. 1980. Environmental determinants of outcrossing in Impatiens capensis (Balsaminaceae). Evolution 34: 747-761..[CrossRef][ISI]
Waller D. M.. 1984. Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers in Impatiens capensis. Evolution 38: 437-440..
Wolfe L. M.. 1993. Inbreeding depression in Hydrophyllum appendiculatum: role of maternal effects, crowding, and parental mating history. Evolution 47: 374-386..[CrossRef][ISI]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
