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Population Biology |
Department of Ecology and Evolutionary Biology, Brown University, Box G-W, Providence, Rhode Island 02912 USA
Received for publication August 1, 2000. Accepted for publication December 21, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: dormancy • genetic variation • maternal effect • photoperiod • plasticity • recombinant inbred • stratification
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Masuda and Washitani, 1992
). However, it may be advantageous to delay germination until spring if the risk of winter mortality is high. Breakage of seasonal dormancy often depends on specific environmental cues experienced by seeds after dispersal from the maternal plant. For example, seeds of many species commonly break dormancy only after being cooled for weeks or months at temperatures of 1°–5°C. Since these temperatures usually occur only during winter, seeds that require such stratification usually will not germinate until after the winter season (Bewley and Black, 1994
; Vleeshouwers, Bouwmeester, and Karssen, 1995
). Within a species or population, seeds can have different requirements for dormancy breakage and therefore may often vary in response to the same seasonal cues (reviewed in Baskin and Baskin, 1998
, Chapter 8). Geographic or ecotypic variation in seasonal dormancy has been observed in several species (e.g., Meyer, McArthur, and Jorgensen, 1989
; Meyer, 1992
; Kalisz and Wardle, 1994
). Understanding both the genetic basis and environmental determinants of such variation is important for understanding how seasonal dormancy may evolve.
Variation in seasonal dormancy may be strongly influenced by genes expressed in the maternal parent. Maternal control of germination can operate through the seed coat, endosperm, or maternal provisioning of resources and hormones (Dobrovolna and Cetl, 1966
; Goto, 1982
; Roach and Wulff, 1987
; Biere, 1991
; Platenkamp and Shaw, 1993
; Léon-Kloosterziel, Keijzer, and Koornneef, 1994; Lacey, Smith, and Case, 1997
; Baskin and Baskin, 1998
). The seed coat, composed of maternal tissue, mediates the environment that the embryo experiences (Schmitt, Niles, and Wulff, 1992
; Platenkamp and Shaw, 1993
; Donohue and Schmitt, 1998
). It imposes mechanical constraints to germination (Kugler, 1951
; Dobrovolna and Cetl, 1966
; Goto, 1982
; Biere, 1991
; Platenkamp and Shaw, 1993
; Léon-Kloosterzeil, Keijzer, and Koornneef, 1994) and can determine permeability (Baskin and Baskin, 1998
) and alter light environments experienced by the embryo (Botto, Sanchez, and Casal, 1995
). Thus, the evolution of seasonal dormancy may involve selection on genetic variation in germination responses to offspring environments among maternal parents, as well as among individual seeds (e.g., Donohue and Schmitt, 1998
).
The environment experienced by the maternal plant prior to seed dispersal may also strongly influence seasonal dormancy and germination timing. In particular, the photoperiod during seed maturation is a reliable indicator of season. Maternal photoperiod influences germination and dormancy in several species (Gutterman, 1992, 1993
; Baskin and Baskin, 1998
). For example, in the desert annual Ononis sicula, day-length variation caused changes in the development of the seed coat and its surface structure, modifying the permeability of the seed coat, fungal resistance of the seed coat, and seed longevity (Gutterman, 1992
). Through these morphological and physiological changes in maternal tissue, day length altered the timing of germination (see also Gutterman, 1972, 1978, 1993
; Gutterman and Evanari, 1972
; Pourrat and Jacques, 1978
). Such maternal environmental effects have been viewed as a form of potentially adaptive cross-generational phenotypic plasticity (Schmitt, Niles, and Wulff, 1992
; Schmitt, 1995
; Bernardo, 1996
; Donohue and Schmitt, 1998
; Mousseau and Fox, 1998
). The evolution of adaptive maternal effects requires selection to discriminate among maternal genotypes that differ in effects of the maternal environment on seasonal dormancy of progeny.
Thus, the evolution of seasonal dormancy can be viewed as the evolution of plasticity of seed traits to both the maternal and the progeny environment. For plastic dormancy and germination responses to evolve in response to natural selection, genetic variation for plasticity of germination traits to maternal and/or offspring environments must exist (e.g., Via and Lande, 1985
; Schlichting, 1986
; Van Tienderen, 1991
; Scheiner, 1993
). The expression of such variation and therefore the potential for response to selection may depend upon the environmental context. For example, expression of genetic variation in effects of parental photoperiod on dormancy breakage might differ between autumn and spring offspring environments or among sites differing in the length of the winter cold period experienced by seeds. Only a few studies have simultaneously examined genetic variation in germination responses to both maternal and offspring environments or tested for environment-specific expression of such variation (Schmitt, Niles, and Wulff, 1992
; Wulff, Caceres, and Schmitt, 1994
).
In this study, we investigated the effects of maternal and progeny environments on seed dormancy in the genetic model species Arabidopsis thaliana (Brassicaceae), a primarily selfing, weedy annual. Seasonal dormancy varies among known A. thaliana ecotypes, as well as among natural populations in North America (personal observation), Europe (Ratcliffe, 1965, 1976
; Effmertova, 1967
; Evans and Ratcliffe, 1972
), and worldwide (Nordberg and Bergelson, 1999
). Most populations in North America have been characterized as winter annuals that germinate only in autumn (Baskin and Baskin, 1983
; Nordberg and Bergelson, 1999
), whereas Rhode Island populations can germinate either in autumn or in spring (personal observation). Populations also differ in season of flowering, with Rhode Island populations flowering in both autumn and spring (personal observation), and southern populations (Baskin and Baskin, 1983
), flowering only in spring. As a consequence, seeds can be matured in different seasons and under different day lengths in some natural populations. In populations that experience harsh winter conditions then selection may favor maternal genotypes that produce seeds whose germination is enhanced by cold stratification when seeds are matured in a short-day photoperiod (autumn). A requirement for cold stratification in these seeds could prevent them from germinating too late in the autumn and could effectively postpone germination until after the winter cold. Conversely, seeds that matured under a long-day maternal photoperiod (spring) may have higher fitness if they do not have a requirement for cold stratification. A lack of a cold requirement would enable them to germinate early in the autumn. In populations where winter conditions are not severe the maternal photoperiod may still be an important predictor of offspring conditions but not of winter cold. Therefore, all plants are expected to germinate without stratification in autumn and flower under long days in spring, so selection is less likely to act upon variation in maternal photoperiod effects. The observed variation in seasonal dormancy and associated life-history characters among natural populations of A. thaliana provides a useful system for investigating the role of maternal effects on germination requirements in contributing to variation in and evolution of these important life-history characters. Arabidopsis thaliana's highly selfing nature relieves this system of the complex issue of maternal versus embryonic determination of dormancy, since the genotype of the maternal parent is generally equivalent to the genotype of the offspring.
We used F6 seeds of recombinant inbred lines derived from two natural populations, Cal-0 (Calver, UK) and Tac-0 (Tacoma, Washington, USA), differing in their cold requirement for germination. We allowed these seeds to mature on maternal plants under either long or short days and then determined the effect of cold stratification on germination. We addressed the following questions: (1) What is the effect of maternal photoperiod on the responsiveness of germination to stratification, that is, on the likelihood of fall vs. spring germination? (2) What is the effect of progeny stratification on the responsiveness of germination to maternal photoperiod, that is, can seasonal cues typical of fall or spring germination environments affect the expression of maternal photoperiod effects? (3) Is the germination response to maternal photoperiod and progeny stratification genetically variable in this sample? (4) How does maternal photoperiod influence the expression of genetic variation for germination requirements, and conversely, how does progeny cold treatment influence the expression of genetic variation for maternal photoperiod effects on germination?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Twelve replicates of these 40 families were grown in a short-day photoperiod and 12 replicates were grown in a long-day photoperiod, after which we collected their seeds (the F6) by family and photoperiod. The short-day maternal photoperiod consisted of 8 h of full-spectrum light in a compartment of a Conviron E-7 growth chamber (photosynthetic photon flux density or PPFD = 425 µmol·m–2·s–1). The long-day maternal photoperiod consisted of 8 h of full-spectrum light, followed by 8 h of low-fluence incandescent light (PPFD = 5 µmol·m–2·s–1). This treatment increased the perceived day length while maintaining daily PPFD at approximately the same level as in the short-day treatment (Lee and Amasino, 1995
). Plants in both treatments were maintained at 24°C.
Seeds matured under these conditions were afterripened at room temperature for 
8 wk and then tested for germination as follows. Seeds from each family and maternal photoperiod were pooled across maternal replicates to ensure enough seeds for the experiment. Ten seeds from each combination of family and maternal photoperiod were placed on the surface of each of eight replicate petri dishes (50 x 9 mm) containing 5 mL of 0.5% agar dissolved in triple-distilled water. Four of the eight plates were given a cold and dark stratification treatment and four were not. This gave a total of 40 replicate seeds per family per photoperiod and stratification combination.
The plates that were subjected to the cold stratification treatment were sealed with plastic wrap, covered with aluminum foil (to ensure darkness), and placed at 4°C for 21 d. The number of seeds that had germinated in the dark was recorded for each plate immediately after removal from the dark stratification treatment. The plates were then divided equally between two Conviron E-7/2 growth chamber compartments (blocks) and were maintained at 24°C in a long-day photoperiod as described above. To minimize effects of potential environmental variation within chambers, the plates were randomly redistributed every 2 d. After 4 d, the number of germinants was recorded for each plate. Plates were then placed back into the growth chamber, and subsequent germinants were recorded after 10 d. Some seeds were obviously inviable as evidenced by severe fungal growth. Visual inspection of the remaining seeds (Baskin and Baskin, 1998
) provided estimates of seed viability. The total number of viable seeds was recorded for each plate.
The plates that were not stratified were immediately divided between the growth chamber compartments and were censused as described above. To test for viability, those seeds that had not germinated after 14 d were placed in the cold for 4 d to break dormancy and then placed back in the growth chambers and recensused 7 d later. Those that had still not germinated were visually inspected for viability.
For stratified plates, germination percentage was calculated for each replicate as the total number of germinants 14 d after removal from the 21 d cold, dark stratification treatment divided by the total number of viable seeds in each plate. Germination speed was calculated for each replicate as the number of germinants 4 d after removal from the stratification treatment divided by the number of germinants 14 d after removal from the stratification treatment. The percentage of seeds germinating in the dark was calculated as the number of seeds that had already germinated upon removal from the dark, cold stratification treatment divided by the total number of germinants 14 d after removal from the stratification treatment.
For unstratified plates, germination percentage was calculated for each replicate as the total number of germinants 14 d after sowing in petri plates divided by the total number of viable seeds in each plate. Germination speed was calculated for each replicate as the number of germinants 4 d after sowing in petri plates divided by the number of germinants after 14 d. All measurements of germination in all treatments were transformed to normality using the arcsine-square root transformation.
To test for effects of maternal genotype (i.e., family), maternal environment, progeny environment, and their interactions on germination percentage and germination speed, we used a four-way mixed-model ANOVA (SAS PROC GLM). Block, maternal photoperiod, and progeny stratification were fixed effects, and family was a random effect. The F tests for fixed effects were calculated from the expected mean squares with the mean square for block tested over error, maternal photoperiod and progeny stratification mean squares were tested over their two-way interactions with family, all two-way interaction mean squares were tested over the three-way interaction that was tested over error. Interactions with block were pooled with the error term (Newman, Bergelson, and Grafen, 1997
). Because we observed a significant three-way interaction between photoperiod, stratification, and family, we performed two separate three-way mixed-model ANOVAs, one with stratification and block as fixed main effects and family a random factor, within each maternal photoperiod treatment, and another with photoperiod and block as fixed main effects with family a random factor within each progeny stratification treatment. The effects of family and maternal photoperiod on the percentage of dark-germinating seeds were tested only for the stratified seeds in a mixed-model ANOVA, with block and photoperiod as fixed factors and family as a random factor. In all three of these analyses, the mean squares for block and family by treatment interaction were tested over error, while all family and treatment main effects mean squares were tested over the family by treatment interaction mean squares. Because some families performed poorly under some maternal photoperiods, there were only 26 families with seeds that had matured in both photoperiods. Seeds were collected from 27 families in the long-day photoperiod and 32 families in the short-day photoperiod. Therefore, only the 26 families common to both photoperiods were included in the four-way ANOVA and the three-way ANOVA performed within the two progeny stratification treatments. The three-way ANOVA performed within the long-day maternal photoperiod included 27 families, while the short-day ANOVA included 32 families.
Genetic correlations across maternal photoperiods within each stratification treatment and across stratification treatments within each maternal photoperiod were calculated by the method of Fry (1992)
for unequal variances.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The effect of progeny stratification on the expression of maternal photoperiod effects
Stratification significantly influenced the effect of maternal photoperiod on germination percentage and speed (Table 1; Fig. 2). In stratified seeds, the short-day maternal photoperiod significantly increased mean germination percentage and speed (Table 4; Fig. 2). In contrast, in unstratified seeds, the short-day maternal photoperiod significantly decreased mean germination percentage, and there was no main effect of photoperiod on germination speed (Table 4; Fig. 2).
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The effect of maternal photoperiod on dark germination
Maternal short days significantly increased the mean percentage of stratified seeds germinating in the dark, simulating seed burial (Table 4; Fig. 3). However, the effect of maternal photoperiod on dark germination also differed significantly among families (Fig. 3; Table 4). Seed maturation under short days resulted in higher dark germination for some families, but lower dark germination for other families, relative to seeds matured under long days. For still other families, the maternal photoperiod had no effect on dark germination. However, a significant positive genetic correlation across maternal photoperiod environments indicated that the ranking of families in percentage of dark germination (that is, the propensity for germination of buried seeds) was relatively unaffected by the maternal photoperiod (rGE = 0.80; P < 0.001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Schlichting, 1986
; Van Tienderen, 1991
; Scheiner, 1993
) but may also contribute to within-population genetic variation for quantitative traits in general. Since the lines used in this experiment were recombinant inbreds from a cross between two natural populations that differed in seasonal dormancy, they will provide a useful tool for investigating the genetic basis of ecotypic differentiation of germination responses to seasonal cues.
The effect of maternal photoperiod on response to progeny stratification and seasonal timing of germination
In this study, maternal photoperiod influenced seed dormancy. In particular, seeds matured by parents under short days broke dormancy more readily when stratified, simulating spring conditions, but seeds matured under long days broke dormancy more readily on average when not stratified, simulating autumn conditions (Fig. 1). This observation is consistent with the natural history of A. thaliana. Most populations flower in the spring under long days, but some populations also have an autumn-flowering cohort. The photoperiod that maternal plants experience at the time of seed maturation may be a reliable predictor of progeny environmental conditions. Seeds matured under long days would be dispersed in late spring or early summer, toward the end of the growing season for Arabidopsis with the onset of hot weather in many regions. The observed maternal photoperiod effect would allow seeds matured under the longer days of spring to germinate in the autumn, without prolonged cold stratification. Those long-day seeds that did not germinate in the autumn and therefore do experience prolonged cold stratification may then enter a secondary dormancy, entering the seed bank, and may contribute to year to year variation among germinants. In populations with an autumn-flowering cohort, seeds would mature and disperse under short autumn days. A short-day maternal photoperiod would therefore predict imminent harsh winter conditions, which might prevent immediately germinating progeny from completing their life cycle. Induction of a stratification requirement for dormancy breakage by a short-day maternal photoperiod would allow autumn-matured progeny to overwinter safely as seeds and germinate under favorable conditions in spring. In such populations, maternal environmental effects on seasonal dormancy could thus result in two alternating generations per year.
The effect of progeny stratification on the expression of maternal photoperiod effects
The observation that expression of maternal photoperiod effects depended upon stratification suggests that the impact of these maternal effects may depend upon the seasonal environment experienced by the offspring. The effect of maternal photoperiod on germination percentage of seeds that had experienced cold, simulating spring germinating conditions, was in the opposite direction of the maternal photoperiod effect for those seeds that did not receive cold (Fig. 2). A main effect of maternal photoperiod on germination speed was detected only in stratified seeds. Other studies have also shown that the effect of the maternal environment on the phenotypic expression of progeny characters may depend on the progeny environment (Alexander and Wulff, 1985
; Miao, Bazzaz, and Primack, 1991a, b
; Schmitt, Niles, and Wulff, 1992
; Platenkamp and Shaw, 1993
; Lacey, 1996). Because A. thaliana seeds matured under short days were more likely to germinate following stratification while long-day seeds germinated more readily without stratification, maternal photoperiod may influence the season of germination, and therefore, the expression of maternal effects on germination. This is an important point for species like A. thaliana that are rapidly expanding their range. In some geographic locations seasonal differences in photoperiod may not necessarily be followed by drastically different temperature conditions, although other factors may vary. An invasive genotype that is plastic to maternal photoperiod may show no selective advantage or even a disadvantage if optimal germination conditions in the new location are different.
These interacting influences of maternal photoperiod and progeny stratification on germination may be important determinants of the variation in seasonal dormancy and other life-history traits that are well documented among geographically distinct populations of this species (Nordberg and Bergelson, 1999
). The mechanism of "summer annual" vs. "winter annual" life histories in A. thaliana, however, is controversial (Nordberg and Bergelson, 1999
). It is thought that these contrasting life histories are functions of both dormancy behavior and vernalization requirements for flowering (Napp-Zinn, 1976
; Nordberg and Bergelson, 1999
). Our results suggest that maternal photoperiod effects may also contribute to such variation. Because seeds are matured in both spring and autumn in some populations of A. thaliana, timing of germination and the photoperiod under which seeds are matured can vary in natural populations. This study suggests that the timing of seed maturation can influence the season of germination. If season of germination, in turn, influences the timing of reproduction and seed maturation, then variation in phenology may result. For example, some autumn germinants may flower in late autumn and mature their seeds under short days. Unlike their parents, these seeds are very likely to germinate in the spring rather than the autumn because of their increased requirement for stratification, leading to variation between generations in season of germination. Likewise, most plants that flower in the autumn are likely to be from seeds matured under long days, since seeds matured under short days will have flowered in the spring. This leads to variation in flowering time as well. In this manner, maternal effects on germination may contribute to ecologically important variation in life history and phenology.
Genetic variation for maternal photoperiod effects
The potential contribution of environmental maternal effects to life history variation does not exclude the potential importance of genetic variation for the same traits. For maternal photoperiod effects and seasonal dormancy to evolve, genetic variation must exist within natural populations (Schmitt, Niles, and Wulff, 1992
; Donohue and Schmitt, 1998
). We found strong evidence for such variation within our sample, which was derived from two natural populations. However, the expression of genetic variation for seasonal dormancy depended upon the maternal photoperiod, and conversely, the expression of genetic variation for the maternal effect depended on stratification. Similarly, Schmitt, Niles, and Wulff (1992)
found that the expression of genetic variation for germination responses of Plantago lanceolata to maternal light environment depended on the offspring's light environment. Thus, the genetic potential for evolutionary response to natural selection on maternal effects and/or seasonal dormancy will depend upon the seasonal environment. Moreover, the relative frequency of genotypes in a germinating cohort, and their relative position in the emergence hierarchy, may differ between spring and fall generations and be influenced by the maternal photoperiod.
Geographic variation in germination behavior has been documented in many species (e.g., Cruden, 1974
; Van der Vegte, 1978
; Hacker et al., 1984
; Hacker and Ratcliff, 1989
; Meyer and Monsen, 1991
; Meyer, Allen, and Beckstead, 1997
). Germination timing is an important contributor to life-history variation in other species with variation in seasonal dormancy. For example, in Campanula americana, germination timing strongly influences timing of reproduction and consequently the annual vs. biennial strategy (Kalisz and Wardle, 1994
; Wardle, 1998
). Our results suggest that maternal environmental effects, such as photoperiod effects, may contribute to such variation in dormancy in A. thaliana. Explicit investigations of parental effects on dormancy may reveal mechanisms for the maintenance of variation in dormancy and corresponding life-history characters within (Effmertova, 1967
; Masuda and Washitani, 1990
; Baskin and Baskin, 1998
) and among natural populations.
Geographic variation in seasonal life histories is also likely to be strongly influenced by genetic variation in maternal effects and seasonal dormancy. We detected substantial genetic variation for maternal photoperiod effects and seasonal dormancy in recombinant inbred lines from a cross between natural ecotypes with different seasonal dormancy strategies. Since we did not observe segregation of the Tac-0 parental phenotype in any line, our results suggest genetic differentiation of the parental ecotypes at several loci. We plan to conduct quantitative trait loci (QTL) mapping of later generations of the Cal x Tac families to elucidate the genetic basis of the observed differentiation between the parental populations in seasonal dormancy behavior.
In conclusion, seasonal dormancy in A. thaliana results from interactions between environments experienced in two generations. Maternal environmental effects on germination were strong, but they depended on the progeny environment. Moreover, the expression of genetic variation for the maternal effect depended on the progeny environment. The evolution of maternal effects in general, and seasonal dormancy in particular, will therefore depend on the nature of selection in both maternal and progeny environments, as well as the expression of genetic variation in each of those environments (Donohue and Schmitt, 1998
). Thus, a multigenerational perspective may be necessary in order to understand the origin and maintenance of the life-history variation observed in natural populations of A. thaliana.
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FOOTNOTES |
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2 Current address: Temple University School of Medicine, Philadelphia, Pennsylvania 19140 USA.
3 Author for reprint requests (Lisa_Dorn{at}brown.edu
).
4 Current address: T. H. Morgan School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506 USA.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Baskin C. C. J. M. Baskin 1998 Seeds: ecology, biogeography and evolution of dormancy and germination. Academic Press, San Diego, California, USA
Baskin J. M. C. C. Baskin 1983 Seasonal changes in the germination responses of buried seeds of Arabidopsis thaliana and ecological interpretation. Botanical Gazette 144: 540-543[CrossRef]
Bernardo J. 1996 Maternal effects in animal ecology. American Zoologist 36: 83-105
Bewley J. D. M. Black 1994 Dormancy and the control of germination. In Seeds: physiology of development and germination, 2nd ed. Plenum, New York, New York, USA
Biere A. 1991 Parental effects in Lynchis flos-cucli. I: seed size, germination and seedling performance in a controlled environment. Journal of Evolutionary Biology 3: 447-465[ISI]
Botto J. R. Sanchez J. Casal 1995 Role of phytochrome B in the induction of seed germination by light in Arabidopsis thaliana. Journal of Plant Physiology 146: 307-312[ISI]
Cruden R. W. 1974 The adaptive nature of seed germination in Nemophila menziesii. Aggr. Ecology 55: 1295-1305
Dobrovolna J. I. Cetl 1966 An increase of germination of dormant seeds by pricking. Arabidopsis Information Service 3: 33
Donohue K. J. Schmitt 1998 Maternal environmental effects in plants: adaptive plasticity?. In T. A. Mousseau and C. W. Fox [eds.], Maternal effects as adaptations. Oxford University Press, New York, New York, USA
Effmertova E. 1967 The behaviour of "summer annual", "mixed", and "winter annual" natural populations as compared with early and late races in field conditions. Arabidopsis Information Service 4
Evans J. D. Ratcliffe 1972 Variation in "after-ripening" of seeds of Arabidopsis thaliana and its ecological significance. Arabidopsis Information Service 9: 3-5
Fenner M. 1985 Dormancy. In G. M. Dunnet and C. H. Gimingham [eds.], Seed ecology. Chapman and Hall, London, UK
Fry J. D. 1992 The mixed-model analysis of variance applied to quantitative genetics: biological meaning of the parameters. Evolution 46: 540-550[CrossRef][ISI]
Goto N. 1982 The relationship between characteristics of seed coat and dark-germination by gibberellins. Arabidopsis Information Service 19: 29-38
Gutterman Y. 1972 Delayed seed dispersal and rapid germination as survival mechanisms of the desert plant Blepharis persica (Burm.) Kuntze. Oecologia 17: 145-149
———. 1978 Seed coat permeability as a function of photoperiodical treatments of the mother plants during seed maturation in the desert annual plant: Trigonella arabica, del. Journal of Arid Environments 1: 141-144
———. 1992 Maternal effects on seeds during development. In M. Fenner [eds.], Seeds: the ecology of regeneration in plant communities. Redwood Press, Melksham, UK
———. 1993 Seed germination in desert plants. Springer, Berlin, Germany
———, and M. Evanari 1972 The influence of day length on seed coat colour, an index of water permeability, of the desert annual Ononis sicula Guss. Journal of Ecology 60: 713-719[CrossRef][ISI]
Hacker J. B. M. H. Andrew J. G. McIvor J. J. Mott 1984 Evaluation in contrasting climates of dormancy characteristics of seed of Digitaria milanjiana. Journal of Applied Ecology 21: 961-969[CrossRef][ISI]
———, and D. Ratcliff 1989 Seed dormancy and factors controlling dormancy breakdown in buffalo grass accessions from contrasting provenances. Journal of Applied Ecology 26: 201-212
Kalisz S. G. M. Wardle 1994 Life history variation in Campanula americana (Campanulaceae): population differentiation. American Journal of Botany 81: 521-527[CrossRef][ISI]
Kelly C. A. 1992 Spatial and temporal variation in selection on correlated life-history traits and plant size in Chamaecrista fasciculata. Evolution 46: 1658-1673[CrossRef][ISI]
Kugler I. 1951 Untersuchungen uber das Keimverhalten einiger Rassan van Arabidopsis thaliana (L.) Heynh. beitrag zur Atiologie der Blutenbildung. Beiträge zur Biologie der Pflanzen 28: 173-210
Lacey E. P. 1996 Parental effects in Plantago lanceolata L. I.: a growth chamber experiment to examine pre- and postzygotic temperature effects. Evolution 50: 865-878[CrossRef][ISI]
———, S. Smith A. L. Case 1997 Parental effects on seed mass: seed coat but not embryo/endosperm effect. American Journal of Botany 84: 1617-1620[Abstract]
Lee I. R. M. Amasino 1995 Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiology 108: 157-162[Abstract]
Leon-Kloosterziel K. M. C. J. Keijzer M. Koornneef 1994 A seed shape mutant of Arabidopsis that is affected in integument development. Plant Cell 6: 385-392[Abstract]
Masuda M. I. Washitani 1990 A comparative ecology of the seasonal schedules for ‘reproduction by seeds' in a moist, tall grassland community. Functional Ecology 4: 169-182[CrossRef][ISI]
———, and ———. 1992 Differentiation of spring emerging and autumn emerging ecotypes in Galium spurium L. var. echinospermon. Oecologia 89: 42-46[CrossRef][ISI]
Meyer S. E. 1992 Habitat correlated variation in firecracker penstemon (Penstemon eatonii Gray: Scrophulariaceae) seed germination response. Bulletin of the Torrey Botanical Club 119: 268-279[CrossRef][ISI]
———, P. S. Allen J. Beckstead 1997 Seed germination regulation in Bromus tectorum (Poaceae) and its ecological significance. Oikos 78: 475-785[CrossRef][ISI]
———, E. D. McArthur G. L. Jorgensen 1989 Variation in germination response to temperature in rubber rabbitbrush (Chrysothamnus nauseosus: Asteraceae) and its ecological implications. American Journal of Botany 76: 981-991[CrossRef][ISI]
———, andS. B. Monsen 1991 Habitat-correlated variation in mountain big sagebrush (Artemisia tridentata ssp. vaseyana) seed germination patterns. Ecology 72: 739-742[CrossRef][ISI]
Miao S. L. F. A. Bazzaz R. B. Primack 1991a Effects of maternal nutrient pulse on reproduction of two colonizing Plantago species. Ecology 72: 586-596[CrossRef][ISI]
———, ———, and ———. 1991b Persistence of maternal nutrient effects in Plantago major: the third generation. Ecology 72: 1634-1642[CrossRef][ISI]
Mousseau T. A. C. W. Fox [eds.] 1998 Maternal effects as adaptations. Oxford University Press, Oxford, UK
Napp-Zinn K. 1976 Population genetical and gene geographical aspects of germination and flowering in Arabidopsis thaliana. Arabidopsis Information Service 13
Newman J. A. J. Bergelson A. Grafen 1997 Blocking factors and hypothesis testing in ecology: is your statistics text wrong?. Ecology 78: 1312-1320[ISI]
Nordberg M. J. Bergelson 1999 The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 86: 470-475
Platenkamp G. A. J. R. G. Shaw 1993 Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47: 540-555[CrossRef][ISI]
Pourrat Y. R. Jacques 1978 The influence of photoperiodic conditions received by the mother plant on morphological and physiological characteristics of Chenopodium polyspermum L. seeds. Plant Science Letters 4: 273-279
Ratcliffe D. 1965 The geographical and ecological distribution of Arabidopsis and comments on physiological variation. Arabidopsis Information Service 1 (Supplement)
———. 1976 Germination characteristics and their inter- and intra-population variability in Arabidopsis. Arabidopsis Information Service 13: 34-45
Roach D. A. R. D. Wulff 1987 Maternal effects in plants. Annual Review of Ecology and Systematics 18: 209-235
Scheiner S. M. 1993 Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35-68[CrossRef][ISI]
Schlichting C. D. 1986 The evolution of phenotypic plasticity in plants. Annual Review of Ecology and Systematics 17: 667-693[CrossRef][ISI]
Schmitt J. 1995 Genotype-environment interaction, parental effects, and the evolution of plant reproductive traits. In P. Hoch and A. Stephenson [eds.], Experimental and molecular approaches to plant biosystematics. Missouri Botanical Gardens, St. Louis, Missouri, USA
———, J. Niles R. D. Wulff 1992 Norms of reaction of seeds traits to maternal environments in Plantago lanceolata. American Naturalist 139: 451-466[CrossRef][ISI]
Silvertown J. 1988 The demographic and evolutionary consequences of seed dormancy. In A. J. Davy, M. J. Hutchings, and A. R. Watkinson [eds.], Plant population ecology. Blackwell Scientific Publications, Oxford, UK
Van der Schaar W. C. Alonso-Blanco K. M. Leon-Kloostrziel R. C. Jansen J. W. Van Ooijen M. Koornneef 1997 QTL analysis of seed dormancy in Arabidopsis using recombinant inbred lines and MQM mapping. Heredity 79: 190-200
Van der Vegte F. W. 1978 Population differentiation and germination ecology in Stellaria media (L.) Vill. Oecologia 37: 231-245[CrossRef][ISI]
Van Tienderen P. H. 1991 Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45: 1317-1331[CrossRef][ISI]
Via S. R. Gomulkiewicz G. De Jong S. M. Scheiner C. D. Schlichting P. H. Van Tienderen 1995 Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10: 212-217[CrossRef]
———, and R. Lande 1985 Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505-522[CrossRef][ISI]
Vleeshouwers L. M. H. J. Bouwmeester C. M. Karssen 1995 Redefining seed dormancy: an attempt to integrate physiology and ecology. Journal of Ecology 83: 1031-1037[CrossRef]
Wardle G. M. 1998 A graph theory approach to demographic loop analysis. Ecology 79: 2539-2549[ISI]
Wulff R. D. C. Caceres J. Schmitt 1994 Seed and seedling responses to maternal and offspring environments in Plantago lanceolata. Functional Ecology 8: 763-769[CrossRef][ISI]
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