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Reproductive Biology |
2Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland; 3Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014 Oulu, Finland
Received for publication May 7, 2002. Accepted for publication September 5, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: fruit set • Geraniaceae • Geranium sylvaticum • gynodioecy • pollen production • seed fitness • sex ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Gynodioecy most likely evolves when a female mutant invades and becomes established in a cosexual population (see for example Darwin, 1877
; Ross, 1970
, 1982
; Lloyd, 1975
, 1976
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1989
). A more controversial issue has been whether gynodioecy represents an intermediate stage in the evolutionary pathway to dioecy, as originally suggested by Darwin (1877)
. Lewis (1941)
proposed that gynodioecy and dioecy are independent breeding systems, a view supported by the fact that in several plant species gynodioecy seems to be a stable form of gender dimorphism (Gouyon and Couvet, 1988
).
The stability of gynodioecy depends in part on the sex determination mechanism (Ross, 1978
) that also affects female frequency. In gynodioecious species, gender can be determined by nuclear alleles or cytoplasmic male-sterility factors or by a combination of nuclear and cytoplasmic factors. The mode of sex determination determines the female fitness advantage required for the maintenance of females (Lewis, 1941
; Charlesworth and Charlesworth, 1978
). Females are required to produce only slightly more seeds than hermaphrodites to be maintained in a population if male sterility is determined by both cytoplasmic male-sterility factors and nuclear alleles restoring male fertility (e.g., Charlesworth and Charlesworth, 1981
). In general, stable gynodioecy has been connected to nuclear-cytoplasmic sex determination (Gouyon and Couvet, 1988
). In species with assumed or demonstrated nuclear-cytoplasmic gynodioecy, very variable and high female frequencies have been recorded (Ross, 1969
; Dommée, Assuoad, and Valdeyron, 1978
; del Castillo, 1993
; Williams, Kuchenreuther, and Drew, 2000
; Delph and Carroll, 2001
). Furthermore, high female frequencies have been observed in young and/or disturbed populations (Couvet, Bonnemaison, and Gouyon, 1986
), in which male-sterility mutations may emerge and increase in frequency until corresponding nuclear restorer alleles emerge (Dommée and Jacquard, 1985
; Couvet, Bonnemaison, and Gouyon, 1986
; Manicacci et al., 1996
). Correspondingly, female frequency has been observed to decline with population age, for example, in Thymus vulgaris, a species with cytoplasmic sex determination (Dommée and Jacquard, 1985
).
Regardless of the sex determination system, females will be maintained in a population only if their fitness is enhanced compared to hermaphrodites. One mechanism for females to outperform hermaphrodites is through increased seed production (e.g., Lloyd, 1975
, 1976
; Charlesworth and Charlesworth, 1978
). Because females do not produce pollen they have more resources available for other functions, such as seed production (Darwin, 1877
). Indeed, higher seed production of females has been found in several gynodioecious species, in which females have produced from 1.5 to over 2 times as many seeds as hermaphrodites (e.g., Kohn, 1988
; Ågren and Willson, 1991
; Sakai and Weller, 1991
; Atlan et al., 1992
; Sakai et al., 1997
). However, in a few species higher seed production of females has not been observed (Molina-Freaner and Jain, 1992
; del Castillo, 1993
; Williams and Fenster, 1998
), including our study species, Geranium sylvaticum (Vaarama and Jääskeläinen, 1967
). Another mechanism for females to outperform hermaphrodites is to produce high quality offspring. This may be achieved by relatively greater provisioning of individual seeds by females (Connor, 1965
; Koelewijn, 1996
; Gigord et al., 1998
) or by lower level of inbreeding depression in offspring produced by females (e.g., Mutikainen and Delph, 1998
, and references therein).
Theoretically, the relative seed fitness of females is expected to correlate positively with female frequency (Lewis, 1941
; Lloyd, 1976
; Charlesworth, 1981
). Thus, sex ratio variation among populations may be explained by any ecological or genetic factors that affect the relative seed fitness of the two gender morphs. Negative correlations between the relative seed fitness of hermaphrodites and female frequency or between fruit set of hermaphrodites and female frequency have been observed in a few studies (Delph, 1990
; Barrett, 1992
; Wolfe and Shmida, 1997
; Ashman, 1999
; Delph and Carroll, 2001
). An increase in female frequency may in turn select for increased male function in hermaphrodites and the functional gender of hermaphrodites may become more male biased (e.g., Charlesworth and Charlesworth, 1978
). Furthermore, if hermaphrodites are more plastic in their seed production, they may be less likely to produce fruit on stressful sites (Delph, 1990
; Ashman, 1999
). Thus, the relative seed fitness of hermaphrodites may be environment dependent. Consequently, stressful environmental conditions are sometimes found to be associated with high female frequency (Delph, 1990
; Puterbaugh, Wied, and Galen, 1997
).
In this study we examined sex ratios and relative seed fitness of females and hermaphrodites in natural populations of Geranium sylvaticum in Finland. In the 1960s Vaarama and Jääskeläinen (1967)
found that most of the Finnish populations of G. sylvaticum are gynodioecious with female frequency varying from 1.8 to 22.2%. They also found that hermaphroditic plants produced slightly more seeds and the seeds were significantly larger than the seeds of female plants, whereas seed germination success did not differ between females and hermaphrodites. Thus, G. sylvaticum has been widely cited as an example of a gynodioecious species in which females do not produce more seeds than hermaphrodites (e.g., van Damme and van Delden, 1984
; Ågren and Willson, 1991
). In a study of a related gynodioecious species, Geranium maculatum, Ågren and Willson (1991)
found that female frequency varied from 0.5 to 24.3% and that females produced 1.6 times more seeds than hermaphrodites. Assuming equivalent seed quality, in G. maculatum the higher seed production of females thus clearly contributes to the maintenance of females (Ågren and Willson, 1991
).
By comparing the present sex ratios of Geranium sylvaticum to those observed by Vaarama and Jääskeläinen (1967)
we were able to assess the stability of the gynodioecious breeding system in this species. We addressed the following specific questions: (1) What is the level of sex ratio variation in Finnish populations of Geranium sylvaticum and has it changed in the last 35 yr? (2) Is population size (as an indicator of population age) negatively correlated with female frequency? (3) Is latitude positively correlated with female frequency, i.e., are females more frequent in populations located in more stressful sites? (4) Do females and hermaphrodites differ in the number of seeds produced? (5) Do females produce higher quality offspring in terms of seed size, seed germination, or juvenile survival? (6) Is relative seed fitness of hermaphrodites negatively correlated with female frequency? (7) Is there variation in pollen production and pollen viability among populations and is pollen production of hermaphrodites relative to their seed production correlated with female frequency?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). One individual consists of one to several ramets; we determined individuals as all the ramets belonging to a single rhizome. Most populations of G. sylvaticum are gynodioecious (Vaarama and Jääskeläinen, 1967
) with female frequency varying from 1.8 to 22.2%. Geranium sylvaticum starts flowering in the beginning of June in southern Finland and in July in northern Finland. The flower color varies from deep purple to white. There are five pistils and ten anthers, arranged in two whorls of five, in each protandrous flower. The pistils and anthers are functional and their size is not reduced in the perfect flowers of hermaphroditic plants. In addition to females with pistillate flowers without anthers there also are plants with reduced nonfunctional anthers; these plants were classified as females. Plants with 1–9 functional anthers we classified as intermediate plants. The flowers are pollinated by bumble bees, syrphid flies, and other dipterans. Butterfly larvae and beetles are also found in the flowers as herbivores.
The fruit of G. sylvaticum is a schizocarp with five locules. There are two ovules on axial placentas in each of the locules, i.e., each flower bears ten ovules. We did not observe any variation in ovule number among individuals or between the genders (E. Asikainen and P. Mutikainen, unpublished data). Usually only five or fewer seeds develop in each fruit. The seeds mature in about 3 wk after pollination. Just before the fruit matures, it changes from green to brown, and finally the awns separate from the central axis to disperse the seeds.
Study populations and sex ratios
To examine the level of natural variation in sex ratios we determined the sex ratios of 23 G. sylvaticum populations in southwestern, central, and northern Finland in summer 2000 (Fig. 1). Population sizes varied from 221 to 1464 flowering individuals (Table 1). All flowering plants in each population were checked for their gender (except in population P9 where about half of the individuals were checked). We examined three or more flowers on each plant. Each population was checked only once, when most of the plants of the population were in flower. If a plant had no open flowers at that time, we opened a few flower buds to find out the gender. Plants were classified as hermaphrodites, females, and intermediate plants. To examine the significance of heterogeneity in sex ratios among populations we performed a heterogeneity G test by hand (Sokal and Rohlf, 1981
). To test for the stability of gynodioecy in G. sylvaticum, we compared the sex ratios of populations surveyed both in this study and by Vaarama and Jääskeläinen in 1960s. Because the previous study presents the sex ratio data within regions in Finland, we pooled our data on five populations that are located in the Turku region. Three of these populations were the same as those studied by Vaarama and Jääskeläinen (1967
; P17–19). It is highly likely that the two other populations (P8 and P20) were also included in the study of Vaarama and Jääskeläinen (1967)
. Using the pooled data, we compared the sex ratios of 1960s and 2000 with a 
2 test.
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). After the stratification we moved the seeds to a greenhouse (20°C). We checked the seeds for germination every second day for 6 mo and followed seedling survival for 6 mo after germination.
In 2001 we measured seed production of the permanently marked plants as in 2000. Unfortunately, we lost three populations because of human activities. These three lost populations were replaced by two new ones (Fig. 1; Table 1; populations P12, P13). Because we followed the same plants for two years, we analyzed the data on flower number, seeds per flower, and seed mass with repeated measures ANOVA using year as the within factor. Population was used as a random factor and gender as a fixed factor, and the error terms were determined according to Zar (1996)
. To fulfill the assumptions of ANOVA, the number of flowers per plant was lognormally transformed. Data on germination and survival of seedlings were not normally distributed with homogenous variances even after transformations. Therefore, we used ANOVA with ranked values to examine the differences in germination and survival between genders and among populations (Zar, 1996
). In 2001 we also counted the number of fruits produced and calculated fruit set by dividing the number of fruits by the number of flowers produced by the plant. Fruit set was analyzed with two-way ANOVA with plant sex as a fixed factor and population as a random factor.
To examine the factors that affect female frequency in a population we calculated Spearman's nonparametric correlation coefficients between female frequency and population size and between female frequency and the distance from the most southern population. Further, we calculated the seed fitness of hermaphrodites relative to that of females by dividing the mean number of seeds per flower produced by hermaphrodites by the mean number of seeds per flower produced by females for each population. We then calculated Spearman's correlation coefficients between female frequency and the relative seed fitness of hermaphrodites for both study years.
Pollen production
In 2001 we also measured pollen production of the hermaphrodites in 10 populations. Early in the season mesh bags were placed around five flower buds on each of 20 plants in each of the 10 populations. When the flowers had opened and the pollen was mature we collected three flowers on each plant; in population P11 only two flowers per plant were collected due to low flower production. The collected flowers were transported to the laboratory in plastic tubes. We placed one drop of methylene blue on a microscope slide, cut two inner whorl anthers from each flower, and rolled the anthers in the drop to release the pollen. We then covered the drop with an object glass. Two days later we counted the total number of pollen grains and the percentage of viable pollen grains under a light microscope. These data were analyzed using one-way ANOVA with population as a random factor. The percentage of viable pollen grains was arcsine transformed.
We tested whether hermaphrodites allocate relatively more resources to male function in populations with high female frequency. We calculated the pollen production of hermaphrodites relative to their seed production by dividing the number of pollen grains per flower by the number of seeds produced per flower and then calculated the mean value for each population in 2001. We then calculated Spearman's correlation coefficient between female frequency and relative pollen production of hermaphrodites. All statistical analyses were performed with SPSS statistical software (Norusis, 1990
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 7.614, df = 1, P = 0.997). There was no significant correlation between female frequency and population size that we used as an indicator of population age (Spearman's r = –0.18, P = 0.402, N = 23). Female frequency and the distance of the population from the most southern population correlated marginally significantly (Spearman's r = 0.41, P = 0.051, N = 23). Intermediate plants (i.e., plants with less than 10 functional anthers) were found in 11 of the 23 populations at very low frequencies (0–1%), except in population P19 where the frequency of intermediate plants was 42%.
Seed production
Hermaphrodites produced marginally significantly more flowers than females (Fig. 2A; Table 2). On average, fruit set of females was 1.4 times higher in 2001 than the fruit set of hermaphrodites (F1,7 = 14.76, P = 0.006; Fig. 2B). There also was significant variation in fruit set among populations (F7,250 = 7.713, P < 0.0001; Fig. 2B). Females and hermaphrodites differed in the number of seeds produced per flower (Table 2). Females produced 1.2 times more seeds per flower than hermaphrodites in 2000 and 1.7 times more seeds per flower in 2001 (Fig. 2C). In addition, interaction between sex and population was significant for the number of seeds produced per flower (Table 2). This was caused by unequal differences between the sexes among populations (Fig. 2C) and by the higher number of seeds produced per flower by hermaphrodites compared to females in two of the populations (Fig. 2C; P2, P8). Moreover, we found significant differences among the populations in the number of flowers, number of seeds per flower, and seed mass (Fig. 2; Table 2).
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Offspring quality
Overall, the germination rate was low, with a mean of 17.8% (±1.4; 1 SE) in females and a mean of 14.6% (±1.1) in hermaphrodites. There were significant differences among populations in germination, but no statistically significant differences between the genders (Table 3). We found no significant differences between genders (females, 92.0 ± 1.6; hermaphrodites, 93.6% ± 1.3) or among populations in survival during the first 6 mo after germination (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and those of our study show that the female frequency varies from 0 to <30%. Furthermore, our test with those populations that were surveyed in both studies suggests that the sex ratios have not changed significantly. The constancy of the sex ratios in time and constancy of the variation in sex ratio among populations suggest that gynodioecy in G. sylvaticum is stable, although within a particular population the proportion of females may slightly vary over time within a certain range. The observed constancy of the upper limit of female frequency (
30%) suggests that genetic and/or ecological factors set an upper limit to the frequency of females. In a previous study on Plantago lanceolata de Haan et al. (1997)
observed significant changes in sex ratios over a time scale of 10–12 yr. They suggested that sex ratio variation in P. lanceolata is created by continuous change in the composition of the sex morphs within the populations. Similarly, our study populations may be of different age and thus their sex ratios have not reached equilibrium, which may explain the observed variation in sex ratio among populations. Alternatively, the relative fitness of the gender morphs changes continuously within a population, which then generates sex ratio variation. However, it was not possible to exclude the importance of environmental factors in determining female frequency in P. lanceolata (de Haan et al., 1997
), as seems to be the case also in G. sylvaticum (this study).
A different equilibrium sex ratio could be optimal in each gynodioecious population because of environmentally dependent fitness (de Haan et al., 1997
). For example, relative fitness of hermaphrodites has commonly been observed to decrease in stressful environments (Delph, 1990
; Puterbaugh, Wied, and Galen, 1997
; Wolfe and Shmida, 1997
; Ashman, 1999
). We found a marginally significant correlation between female frequency and distance of the population from the most southern population. Hence, female frequency tends to be higher in the northern populations, which presumably is due to harsher environmental conditions. Another factor affecting female frequency is the age of the population (Dommée and Jacquard, 1985
; Couvet, Bonnemaison, and Gouyon, 1986
). Since the age and size of a plant population are often correlated (Watkinson, 1997
), we tested the correlation between female frequency and population size but found no significant correlation between these traits. This suggests that there is no link between female frequency and population age, which may indicate that female frequency is not solely determined by the genetic factors involved in sex determination.
Seed and pollen production
According to the previous results of Vaarama and Jääskeläinen (1967)
hermaphroditic plants produced more and larger seeds than females in Geranium sylvaticum. We found a significant difference in seed production in both study years between females and hermaphrodites. Contrary to the results from the 1960s, females produced 1.2 times more seeds per flower in 2000 and 1.7 times more seeds per flower in 2001. Moreover, fruit set of females was 1.4 times higher than fruit set of hermaphrodites in 2001. Thus, G. sylvaticum should no longer be cited as an example of a species in which females do not produce more seeds than hermaphrodites. Our results also highlight the temporal variation in the relative seed fitness of the two gender morphs. The higher seed production of females observed here only partly explains the maintenance of females since relative seed fitness varied considerably between the two study years and among the study populations. For example, considerably higher seed fitness of hermaphrodites was found in three populations in 2000 (P2, P5, P8) and in one population in 2001 (P12). Female frequency in these populations varied from 4.6 to 16.1%. This yearly variation indicates that several environmental and ecological factors with significant yearly variation, such as weather, pollinator abundance, or herbivory, affect the seed fitness and that these factors may affect the sex morphs in a different fashion. Since the number of seeds produced per fruit did not differ between genders (E. Asikainen and P. Mutikainen, upublished data) and the number of flowers was marginally significantly higher in hermaphrodites, the difference in seed fitness between females and hermaphrodites is mainly due to the lower fruit set of hermaphrodites. A similar result was found in a previous study of Silene acaulis by Delph and Carroll (2001)
.
If females do not produce sufficiently more seeds their maintenance in a population may be explained by production of higher quality seeds (Lewis, 1941
; Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1981
). We found no differences between females and hermaphrodites in seed mass, while, for example, in Eritrichum aretioides the seeds of females were heavier than those of hermaphrodites (Puterbaugh, Wied, and Galen, 1997
). Moreover, as the results of Vaarama and Jääskeläinen (1967)
previously suggested, there were no differences between the sexes in seed germination and juvenile survival.
In a few previously studied gynodioecious species the relative seed fitness of females satisfies the condition of Lewis' (1941)
model for the maintenance of females. For example, in Thymus vulgaris and Schiedea adamantis females produced two times as many seeds per fruit as hermaphrodites (Atlan et al., 1992
; Sakai et al., 1997
). However, in several cases the relative seed fitness of females falls between one and two (Kohn, 1988
; Maki, 1993
). In addition, in some species no difference in seed production has been found between females and hermaphrodites (del Castillo, 1993
; Puterbaugh, Wied, and Galen, 1997
). At about the same female frequencies (0.5 to 24.3%) as observed in G. sylvaticum in the present study, 1.6 times higher seed production of females per plant has been observed in G. maculatum (Ågren and Willson, 1991
). Thus, the relative seed fitness of females observed here for G. sylvaticum is similar to that observed for other gynodioecious species in general and for other Geranium species.
Differences in flower size have been observed in many gynodioecious species; hermaphrodites usually have larger flowers than females (Darwin, 1877
; Lloyd and Webb, 1977
; Delph, 1996
; Ashman, 1999
). Correspondingly, in G. sylvaticum the petals of hermaphrodites are 1.6 times larger than those of females (E. Asikainen and P. Mutikainen, unpublished data). Thus, hermaphrodites may produce larger and extra flowers to attract pollinators and to produce pollen. This should increase the relative fitness of hermaphrodites in terms of probability of pollination and pollen production. However, significantly higher proportion of flowers turned into fruits in females. Overall, both the number of seeds produced per flower (mean 1.0) and fruit set (mean 0.50) were remarkably low in G. sylvaticum, which indicates that reproductive output is constrained by factors other than the ovule number. We are currently examining the effects of two factors commonly suggested as explanations for low fruit set, i.e., resource and pollen limitation (e.g., Schemske, 1980
; Bierzychudek, 1981
; Cohen and Dukas, 1990
).
Relative fitness and female frequency
It has been suggested that the selective processes that determine the sex ratios in gynodioecious populations are frequency dependent (Lloyd, 1975
; McCauley and Taylor, 1997
; McCauley and Brock, 1998
). In G. sylvaticum variation in female frequency was negatively correlated with the seed fitness of hermaphrodites relative to that of females, indicating frequency dependency. This result concurs with theory (Lloyd, 1976
) and is similar to the results of several previous studies on other gynodioecious species (Delph, 1990
; Barrett, 1992
; Wolfe and Shmida, 1997
; Ashman, 1999
; Delph and Carroll, 2001
). In addition to the genetic sex determining factors, sex ratio variation and relative fitness of the sex morphs in gynodioecious species are affected by ecological factors that can be frequency dependent by nature. For example, hermaphrodites of self-compatible species may suffer less from pollen limitation that increases with increasing female frequency (Fleming et al., 1994
; Maurice and Fleming, 1995
; McCauley and Taylor, 1997
; McCauley and Brock, 1998
). Furthermore, the rates of self-fertilization of hermaphrodites may vary in relation to female frequency since the number of hermaphrodites producing pollen for outcrossing decreases with increasing female frequency. Consequently, inbreeding depression may be higher in populations with high female frequency (Lloyd, 1975
), which may in turn affect the relative fitness of the sex morphs. Without exact knowledge on the sex determination system we cannot rigorously estimate the relative effects of genetic and ecological factors on the variation of sex ratio and relative fitness. On the other hand, a correlation between population age and female frequency has been thought to indicate that sex ratio variation is highly dependent on the genetics of sex determination (Dommee and Jacquard, 1985
; Couvet, Bonnemaison, and Gouyon, 1986
; Manicacci et al., 1996
). Since we did not find such a correlation between female frequency and population size (used here as an indicator of population age), our results might suggest that ecological factors cause a significant part of the variation in relative fitness of hermaphrodites and, consequently, in sex ratios of the populations.
Even if there were significant differences among populations in the amount of pollen grains produced per flower, relative pollen production of hermaphrodites was not positively correlated with female frequency. Thus, hermaphrodites do not respond to increasing female frequency by increasing their allocation to male function at the expense of female function. Similarly to our results, female frequency did not correlate with pollen production in Fragaria virginiana (Ashman, 1999
).
The maintenance of gynodioecy in Geranium sylvaticum
Stable gynodioecy is generally connected to a sex determination mechanism in which both nuclear and cytoplasmic factors determine the gender (Gouyon and Couvet, 1988
). Species with nuclear-cytoplasmic sex determination have high and highly variable female frequencies. Variable female frequencies have also been recorded in Geranium sylvaticum (Vaarama and Jääskeläinen, 1967
; this study). Thus, the sex determination system may partly explain the maintenance of females in gynodioecious G. sylvaticum populations. If sex determination is nuclear cytoplasmic, the higher seed production of females may be sufficient to explain the maintenance of females with the observed frequencies. On the other hand, the relative seed fitness of hermaphrodites was negatively correlated to female frequency that also was higher in northern populations. Given also the observed yearly variation in relative seed fitness, our results highlight the importance of environmental factors for the maintenance of females in G. sylvaticum. To determine the relative roles of genetic and environmental factors in the maintenance of gynodioecy in this species we need more data on the mode of gender inheritance, selfing rate of hermaphrodites, and amount of inbreeding depression, as well as on ecological factors that contribute to the relative seed fitness of the gender morphs.
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FOOTNOTES |
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4 Author for reprint requests (eija.asikainen{at}utu.fi
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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