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Ecology |
Department of Biology, Indiana University–Purdue University Indianapolis, 723 West Michigan Street, Indianapolis, Indiana 46202-5132 USA
Received for publication July 27, 2004. Accepted for publication February 2, 2005.
ABSTRACT
Sexual dimorphism in plants has been known for over two millennia. However, little is known about how male and female reproduction of dioecious species will respond to anthropogenic environmental perturbations. Using growth chambers, the effects of CO2 enrichment on male and female reproduction in Silene latifolia were examined and whether parental CO2 environment affected progeny germination and sex ratio. Reproduction of male and female S. latifolia was enhanced by a similar magnitude at elevated CO2. Over the growing season, males produced 16 times as many flowers as females did fruits per plant, but no difference in reproductive biomass between genders was observed at ambient or elevated CO2. Germination of seeds produced by plants grown at different CO2 concentrations was significantly different. Female seeds from higher CO2-grown plants tended to emerge earlier than those from ambient-CO2-grown plants, but emergence of male seeds was little affected. Overall, seeds from elevated-CO2-grown plants had 20% higher germination and were more female-biased than those from ambient-CO2-grown plants. Because of the enhanced reproduction and more female-biased progeny under elevated CO2, the population structure of this cosmopolitan weedy species will likely be altered in a future environment.
Key Words: Caryophyllaceae • dioecy • elevated CO2 • global change • progeny performance • reproduction • Silene latifolia
Dioecy in plants has been known to humans for more than two millennia. In the third century B.C., Theophrastus, in his Enquiry into Plants, described a ceremony in which a priest symbolically pollinated female trees of Phoenix dactylifera with male fronds to ensure good date crops for the year (Maheshwari, 1950
). As far back as in the first century B.C., farmers in China understood that male plants of Cannabis sativa produced pollen only and that most males in the field needed to be removed to achieve a higher yield of C. sativa seeds, an important food source (X. L. You, Zhejiang University, China, personal communication). In Qimin Yaoshu, also known as Chi Min Yao Shu, an agricultural encyclopedia published between 533 and 544 A.D., Jia provided detailed descriptions for identifying male and female C. sativa plants as well as seeds (You, 1994
). Since the 1877 publication of Charles Darwin's The Different Forms of Flowers on Plants of the Same Species, interest in understanding the fundamental biological processes of sexual and gender dimorphism in dioecious plant species has continued. It is now well documented that sexual and gender dimorphism is widespread in a variety of plant taxa and that male and female individuals of dioecious species differ morphologically, physiologically, as well as ecologically in their natural habitats under current environmental conditions (reviewed in Geber et al., 1999
).
Recent studies have shown differential physiological responses to global environmental changes, i.e., rising temperature and atmospheric CO2 concentration, in male and female individuals of dioecious species. For example, male Salix arctica plants had a significantly higher photosynthetic rate than females at elevated CO2, but only at a higher temperature (Jones et al., 1999
). Male saplings of Populus tremuloides had higher photosynthesis than females throughout the growing season, regardless of CO2 concentrations, but sexual difference in photosynthesis was greater at elevated than at ambient CO2 (Wang and Curtis, 2001
). Despite the common occurrence of dioecious plant species and the differential physiological responses to CO2 enrichment by male and female plants, little is known about how global environmental changes will affect the reproduction of male and female individuals of dioecious species and hence the fitness and population structure of the species. This study was intended to provide information on sex-specific reproductive responses to these environmental changes. More specifically, this study investigated how a doubling of atmospheric CO2 concentration would influence male and female reproduction of Silene latifolia Poiret, a widespread dioecious species. I hypothesized that CO2 enrichment would enhance male and female reproduction in S. latifolia because of the significantly higher photosynthetic rates observed in both males and females under CO2 enrichment (Wang and Griffin, 2003
). Additionally, I hypothesized that reproduction would increase more in females than in males because of developing fruits in females, which are strong sinks for photosynthates. Developing fruits in female plants of S. latifolia have been shown to increase photosynthetic rates, especially at elevated CO2 (Wang and Griffin, 2003
). Higher photosynthetic rates at elevated CO2 would therefore make females less resource constrained and result in greater reproduction than those at ambient CO2.
Another objective of this study was to examine the effects of growth CO2 concentrations of parent plants on progeny performance as measured in seed germination. Parental CO2 concentration can affect offspring performance in hermaphroditic herbaceous species primarily through its effect on resource allocation and on elemental stoichiometry in the seeds (Huxman et al., 1998
, 2001
), I hypothesized that growth CO2 concentrations of male and female S. latifolia parents would affect germination of the seeds they produced. The third objective of this study was to determine the effects of elevated CO2 on progeny sex ratio in S. latifolia. Sex ratio in this common dioecious species has been extensively studied since Correns' classic experiment with the genus Silene nearly a century ago (Correns, 1917
). Silene latifolia populations have been observed to be mildly but ubiquitously female biased (reviewed in Taylor, 1996
), but studies have also found that the degree of female bias varies from one maternal family to another and in some families sex ratio is even male-biased (Carroll and Mulcahy, 1993
; Lyons et al., 1994
; Taylor, 1994
). No information, however, is available on the effects of elevated CO2 on sex ratio in S. latifolia. Results from this study will provide insights into whether parental CO2 environment will affect progeny sex ratio and allow us to predict how the population structure of this weedy species may be altered in a future environment.
MATERIALS AND METHODS
Study species
Silene latifolia is a short-lived perennial herb of Eurasian origin that has been naturalized in North America (Voss, 1985
). The sex of S. latifolia is determined by heteromorphic X/Y sex chromosomes with XY being male and XX being female (Westergaard, 1958
; Parker, 1990
; Ye et al., 1991
). Silene latifolia has become a model system for studying sexual dimorphism (Meagher, 1992
, 1994
; Delph and Meagher, 1995
) and sex-determination mechanisms (Grant et al., 1994a
, b
; Hardenack et al., 1994
) and is likely the most extensively studied dioecious species. Silene latifolia was chosen in this study for examining responses of male and female reproduction to elevated CO2 because it is easy to grow and both male and female individuals produce many flowers. Seeds of S. latifolia for this study were collected from different fruiting females in a natural population near the University of Michigan Biological Station (UMBS) at Pellston, Michigan, USA.
Growth conditions
The experiment was conducted in two controlled environmental growth chambers (Model E-15, Conviron, Winnipeg, Manitoba, Canada) at Indiana University–Purdue University Indianapolis (IUPUI), Indiana, USA. The CO2 concentration was targeted at 365 µmol · mol–1 (averaged 386 ± 0.3 µmol · mol–1 over the season. Mean ± 1 SE) for the ambient CO2 treatment and at 730 µmol · mol–1 (averaged 696 ± 0.5 µmol · mol–1 over the season) for the elevated CO2 treatment 24 h · d–1 for the duration of the experiment. The average air temperature in the chambers was 27.9°/20.0°C for the ambient CO2 chamber and 27.8°/20.0°C for the elevated CO2 chamber with a target temperature of 28.0°/20.0°C (day/night) for both treatments. Measured photosynthetic photon flux density was approximately 600 µmol · m–2 · s–1 at leaf surface during the 18-h photoperiod (0900–0300 hours). Relative humidity in the chambers was 59.9% for the ambient CO2 chamber and 60.2% for the elevated CO2 chamber, close to the target of 60.0%. Soil was watered to field capacity daily with deionized water throughout the experiment and nutrients were supplemented by adding Osmocote Plus (15-11-13, Scotts-Sierra Horticultural Products, Marysville, Ohio, USA) after seedling transplanting. All pots in the chambers were rotated weekly between the chambers and CO2 concentrations changed accordingly.
Experiment on reproduction
One hundred and twenty plastic pots (0.4-L volume) were used for seed germination. Two seeds were sowed in each pot filled with Premier Pro-Mix (Premier Horticulture, Quebec, Quebec, Canada) on 13 December 2002. Sixty pots were placed in the ambient CO2 chamber and another 60 in the elevated CO2 chamber immediately after seed planting. Approximately 90% of seed germination occurred 1 wk after sowing. Each pot was thinned to one plant 2 wk after sowing. Of the 60 seedlings at each CO2 level, 40 were selected to be transplanted into 3.8-L pots filled with the same growth medium supplemented with Osmocote Plus on 6 January 2003. Seedlings for transplanting were selected to ensure evenness in height and vigor. Each chamber then contained 40 pots with one seedling each. The sexes of the plants were unknown at this stage and could not be determined until plants started flowering 1 wk after transplanting. There were 27 males and 13 females in the ambient CO2 chamber and 22 males and 18 females in the elevated CO2 chamber. On 6 February, some pots were randomly selected for removal so that each chamber contained 10 male and 10 female plants. The unpollinated female flowers from the removed pots were harvested for examining mass of female flowers. Male flowers were collected daily from each male plant. All female flowers were hand-pollinated daily with male flowers for the first 3 d of blooming. Aborted female flowers were collected from the chamber floors, and it was therefore not possible to match the aborted female flower with the female plant. Fruits were collected from plants at maturation but before dehiscence. Seeds were separated from capsules and stored at room temperature. Male flowers and emptied fruit capsules were oven dried at 70°C for 72 h before weighing. All plants were harvested on 27 May 2003, when most leaves had wilted.
Experiment on seed germination and sex ratio
After completion of the first experiment, a second one was conducted to examine germination and sex ratio of progeny from plants grown at different levels of CO2. Twelve 8.4-L pots were filled with Pro-Mix (Premier Horticulture) growth medium and wetted thoroughly by immersion in plastic trays filled with water. Six pots were moved to the ambient CO2 chamber and another six to the elevated CO2 chamber. Soil surface was leveled to ensure uniformity of sowing depth before 40 seeds were spread evenly on each pot and covered with 1 mm of soil to keep the seeds moistened at all times. Seeds from ambient- and elevated-CO2-grown plants were sowed in pots in the ambient and elevated CO2 chambers, respectively. The pots were checked daily for germination, and each emergence was labeled so its sex could be determined later. Three weeks after the first emergence, seedlings were transplanted into 3.8-L pots with their labels for a density of six plants per pot before being moved to the greenhouse to avoid overcrowding in the chambers. Plant sex was identified when plants started flowering.
To determine the sex ratio of S. latifolia seeds collected from its natural habitat at UMBS, a greenhouse experiment was conducted in the IUPUI Department of Biology greenhouse concurrently with the first chamber experiment. Forty seeds were sowed in each of 16 pots (8.4-L volume filled with Pro-Mix). Because of the high plant density in the pots after emergence, plant sex was determined as soon as possible, sometimes by manually opening flower buds. After sex determination, plants were removed from the pots to reduce plant density. At the completion of this experiment, an additional greenhouse experiment also using seeds collected from UMBS was conducted to increase sample size. The 80 plants from the first growth chamber experiment were also included in calculating sex ratio of seeds from its natural habitat at UMBS.
Statistical analysis
For comparison between sexes at either ambient or elevated CO2, the experimental unit was each individual plant. It is therefore valid to use inferential statistics to test for sex effects within each CO2 concentration. In order to use statistics for comparing CO2 treatments, CO2 concentrations in the two chambers were alternated and all pots rotated weekly. All pots were randomized within the chambers at each rotation. The little variation in environmental conditions between the chambers further validates the use of inferential statistics for the results. Chi-square tests were used for sex ratio comparisons within a CO2 concentration and two-tailed t tests were performed for comparisons of reproductive parameters between genders and between CO2 treatments.
RESULTS
When grown in controlled environments, female S. latifolia plants had a tendency to flower earlier than males regardless of CO2 concentration (Table 1). However, only plants grown at elevated CO2 showed a significant gender difference in age at first reproduction, with females flowering 1.6 d earlier than males on average. Male plants grown at elevated CO2 produced significantly more flowers per plant than those at ambient CO2 (Fig. 1A). By the time of harvesting, elevated-CO2-grown males had produced 6743 flowers per plant compared to 5268 flowers per plant for males grown at ambient CO2. On average, one female plant produced 320 fruits at ambient CO2 and 422 fruits at elevated CO2 (Table 1). Male plants therefore produced approximately 16 times as many flowers as females did fruits per plant, regardless of their growing environments. Aborted female flowers accounted for approximately 10% of the total female flowers and were not included in calculating the final flower numbers, because they were collected only after they had fallen to the chamber floors and as a result could not be attributed to a specific female plant. Male flowers produced early in the season were significantly larger than flowers produced later in the season at both ambient and elevated CO2 (Fig. 1B). For example, the average mass of the first flowers was 0.015 g for ambient-CO2- and 0.017 g for elevated-CO2-grown males. One month after flowering, the average mass of male flowers dropped to 63% and 54% of the initial mass for males in ambient and elevated CO2, respectively. By the end of the growing season, male flowers weighed only 46% and 36%, respectively, of the initial flowers for males in ambient and elevated CO2. Individual flower mass and the overall pattern of change in average flower mass (i.e., a precipitous decline during the first 2 wk of flowering followed by a more gradual decline toward the end of the season), however, did not differ significantly between CO2 treatments. Cumulatively, males produced 44.0 g flowers at ambient CO2 and 52.5 g flowers at elevated CO2, an enhancement of 19% at elevated CO2 (Fig. 1C).
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Progeny from plants in both ambient and elevated CO2 started emerging 4 d after sowing (Fig. 2). For seeds from females grown at ambient CO2, 55% of emergence occurred within 6 d of sowing (Fig. 2A), while for seeds from plants in elevated CO2, 67% of the emergence occurred during the same period (Fig. 2B). Eight days after sowing, however, there was no difference in germination between the CO2 treatments with 85% and 86% of germination completed for seeds from females in ambient and elevated CO2, respectively. The average emergence time was 5.9 ± 0.16 and 5.7 ± 0.14 d for seeds from ambient- and CO2-grown plants, respectively. Cumulatively, 87% of the seeds from elevated-CO2-grown plants germinated, compared to only 67% of seeds from ambient-CO2-grown plants.
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Reproduction of S. latifolia plants as affected by CO2 concentration
Under controlled environments, female S. latifolia plants started flowering 31 d after planting, 1.6 d earlier than did males, regardless of CO2 concentrations. The results are in general agreement with those from an earlier greenhouse experiment showing that female S. latifolia plants flowered 33 d after planting and males flowered 1.7 d later in low nutrient soils, although no difference in flowering age between genders was observed in high nutrient soils (Purrington, 1993
). Results from these indoor experiments, however, were in contrast with those from a field experiment by Purrington and Schmitt (1998)
, who found that males and females flowered 323 and 329 d after planting, respectively, in a natural habitat of S. latifolia in Rhode Island, USA. Among the many differences in growing conditions between the controlled environments and the natural habitat, the most likely factor that caused such a large difference in emergence time was light environment. The field-grown plants remained in vegetative stage for almost 11 mo after emergence, presumably due to the late sowing in the field experiment. Seeds were sowed in early July and emergence did not occur until early September in the field (Purrington and Schmitt, 1998
). By then the day length at the latitude of the field site was less than 13.5 h, which was too short for this long-day species to bolt at the ambient temperature. Plants therefore did not flower until May of the following year (Purrington and Schmitt, 1998
), when day length was longer than the critical day length for S. latifolia. In this study, day length was maintained at 18 h from the beginning and newly emerged seedlings were immediately exposed to long days. As a result, plants flowered only a month after sowing. In its natural habitats in the midwestern United States, S. latifolia seeds typically emerge in late April, and flowering starts in June and continues into October. Its reproductive phenology is similar in southern Canada, where plants do not start flowering until after being exposed to long days in June (McNeill, 1977
).
Male S. latifolia plants grown at elevated CO2 had a 67% higher photosynthetic rate averaged over the season and as a result had 56% greater biomass accumulation than those grown at ambient CO2 at the end of the growing season (Wang and Griffin, 2003
). Higher photosynthesis and vegetative growth generally translate into greater reproductive growth in long-day plants, which was indeed observed in this study. Males grown at elevated CO2 produced 19% more flower mass than those grown at ambient CO2 over the growing season. To achieve greater flower mass, males could have produced larger flowers with little change in flower numbers or they could have produced a larger number of flowers with little change in individual flower mass, i.e., a resource trade-off between flower size and flower number (Eckhart, 1999
). The present results demonstrated that elevated-CO2-grown males used the second strategy to accumulate greater flower mass. Male plants at elevated CO2 produced 28% more flowers than those at ambient CO2, but individual flower mass remained unchanged. For the same reproductive biomass, increasing the number of flowers will likely be more effective than producing larger, but fewer flowers for pollen grains to reach female flowers in this mostly insect-pollinated species, because a larger number of flowers increases the chance of having at least some flowers visited by the pollinators. Over the season, however, male plants produced increasingly smaller flowers, most likely due to lower photosynthetic rates and therefore increasing resource constraints in older male S. latifolia plants (Wang and Griffin, 2003
).
Growth at elevated CO2 increased fruit number in female S. latifolia plants by 32%, similar in magnitude to the increase of male flowers in response to CO2 enrichment (28%). However, like individual male flowers, individual fruit mass or seed mass was little affected by CO2 concentration. These results demonstrate that S. latifolia plants, both male and female, allocate their resources to producing more reproductive units than to producing larger but fewer units. This reproduction pattern remains unchanged for plants grown at elevated CO2, when resource limitation was less stringent as a result of the higher photosynthesis in higher CO2-grown females (Wang and Griffin, 2003
). Despite the much heavier female than male flowers, no significant difference in reproductive investments between males and females was observed, due primarily to the 16 times more male flowers than fruits produced per plant. In a greenhouse study, Laporte and Delph (1996)
also found males produced approximately 16 times as many flowers as did pollinated females. Females have been found to allocate more to reproduction than males both absolutely and proportionately in some earlier experiments (Gross and Soule, 1981
; Gehring and Linhart, 1993
; Delph and Meagher, 1995
; Laporte and Delph, 1996
), in contrast to results from a recent study (Wang and Griffin, 2003
) and this study, which showed similar proportionate allocations between males and females. The disagreement was most likely caused by different growth conditions of the plants in various experiments and by the relatively small sample size (N = 10) for males and females in the present study. For example, difference in male and female reproductive investment was not statistically significant despite 15% more investments by the females (P = 0.2305). Results from the present study also refuted my original hypothesis that elevated CO2 would increase reproduction more in females than in males.
Progeny germination and sex ratio
Male and female seeds were differentially affected in their germination by the growth CO2 concentrations of parent plants. While the germination patterns for male seeds from ambient- and elevated-CO2-grown plants were similar, the patterns for female seeds were significantly different, i.e., elevated-CO2-grown female seeds emerged earlier compared to ambient-CO2-grown ones. One reason for such a difference was a higher mortality of female seeds from ambient-CO2-grown plants. While this cause could not be ruled out in this study, it does not seem plausible because of the nearly identical sex ratios in seeds and adults observed in this species (Taylor, 1996
). Another possible reason for the different germination patterns of female seeds at different CO2 concentrations was a higher mortality of early female seedlings. This was unlikely because there was no observed difference in mortality of seedlings between ambient- and elevated-CO2-grown seeds or between males and females at either CO2 level. No seedling mortality was found in the period between emergence and reproductive maturity.
Although sex in S. latifolia is determined by chromosomes (Westergaard, 1958
; Ye et al., 1991
), the mechanism for the commonly observed deviation from a 1 : 1 sex ratio is still being debated. Correns (1928)
postulated that different growing speed of pollen tubes containing X and Y chromosomes was the main reason for female bias in S. latifolia. While some experiments support Correns' hypothesis (Taylor et al., 1999
), some others do not corroborate the pollen competition theory. For example, female bias was observed even when there was limited pollen (Mulcahy, 1967
) and in natural habitats where pollen limitation is likely (Alexander, 1987
). On the other hand, progeny were found to be male-biased when there was intense pollen competition but female-biased when pollen competition was less intense (Lassere et al., 1996
). Shaw and Mohler (1953)
hypothesized that the more sex ratio deviates from equality, the greater the selective advantage conferred upon the minority sex. This hypothesis is valid only to the extent that a lower sex ratio would result in female competition for pollen in S. latifolia. This seems an unlikely scenario in this study considering the copious number of male flowers and the multiple hand-pollination of the same female flowers over a period of 3 d. Pollen tube competition, therefore, could not be the only factor determining sex ratio in S. latifolia.
The commonly observed female-biased sex ratio in this species has been hypothesized to be caused simply by males having higher juvenile mortality in natural populations (Carroll and Mulcahy, 1993
; Gehring and Linhart, 1993
). Results from this experiment, however, do not support the differential mortality hypothesis, because no seedling mortality was observed throughout the experiment. This is consistent with the work of Lyons et al. (1994)
, who found no seedling or plant mortality in their experiment. Another possible cause of apparent female bias is lower germination of male seeds (Lyons et al., 1994
). A recent study using PCR technique, however, cast doubt on this hypothesis. Sex ratios in developing and mature seeds were found to be nearly identical to sex ratios in the adults of four S. latifolia families, demonstrating clearly that sex ratio bias in those families of S. latifolia originated among male gametes, either during gametogenesis or pollen tube growth (Taylor, 1996
). The finding of no seedling mortality in this experiment and in Lyons et al. (1994)
indicates that multiple mechanisms may be responsible for sex ratio deviation in S. latifolia.
It has been suggested that genetic sex determination in a dioecious plant species might be flexible to some extent (Frick and Cavers, 1989
) and species may "choose" between male and female offspring based on environmental cues (Lloyd and Bawa, 1984
). As a matter of fact, it has been postulated that S. latifolia could maintain an optimal sex ratio for maximal seed production (Mulcahy, 1967
). The optimal sex ratio ought to be different under different conditions, e.g., lower and higher concentrations of CO2. This could partly explain why sex ratio tended to be more female-biased in seeds from females grown at elevated CO2. A more female-biased sex ratio in a higher CO2 environment, where resources are less constrained, would increase seed production and therefore its fitness. Other growth conditions favorable for plant growth, or a combination of these favorable conditions, could have a similar effect on sex ratio. Different sex ratios in plants grown from seeds collected from natural habitats differing in site fertility render additional support to this argument. Seeds collected from Michigan, USA, for this study did not deviate from a 1 : 1 sex ratio with 46% being female, but seeds collected from Colorado, USA, for a greenhouse experiment were significantly female-biased with 72% individuals being female (Gehring and Linhart, 1993
). The habitats where seeds were collected for these two experiments differ in nutrients and soil moisture, as the Michigan habitat is sandy and low in resource availability while the Colorado habitat is a riparian forest (Gehring and Linhart, 1993
), which is generally high in resources, such as soil nutrients and water availability. In addition to the genotypic variations in sex ratios among various maternal families, differences in resource availability between these sites might also have contributed to the different sex ratios.
In summary, CO2 enrichment greatly increased male and female reproduction in S. latifolia, primarily by increasing flower number instead of flower size. The substantially greater number of flowers produced by males offset the much heavier female flowers and fruits and hence no significant difference in reproductive biomass between the genders was observed at either ambient or elevated CO2. Growth of parent plants at elevated CO2, however, had significant effects on progeny performance, e.g., a 20% higher seed germination and more pronounced female-bias. The synergistic effects of a greater number of seeds produced per female plant, a higher seed germination, and more female-biased seeds in the higher CO2 environment will likely make S. latifolia, a cosmopolitan weedy species, even more widespread in the future, as atmospheric CO2 concentration continues to increase as a result of accelerated anthropogenic activities.
FOOTNOTES
The author thanks Drs. Patricia Clark, Lynda Delph, Colin Purrington, Ann Sakai, and two anonymous reviewers for constructive comments on an earlier draft of this manuscript. The author also expresses gratitude to Thi Huyen Huynh for her many contributions to this study and to Mica Kleber, Sarah Heath, Sarah Richards, Steve Cassady, and Hayden Johnson for their technical support during various phases of this experiment. This research was financially supported by the School of Science, Indiana University–Purdue University Indianapolis. 
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2 = 2.56, P > 0.05). For progeny of plants grown in the chambers, N = 209 for males and N = 233 for females at ambient CO2 (