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(American Journal of Botany. 1999;86:880-886.)
© 1999 Botanical Society of America, Inc.

Sex ratios and genetic variation in a functionally androdioecious species, Schizopepon bryoniaefolius (Cucurbitaceae)1

Junichi Akimoto 2 , Tatsundo Fukuhara 3 and Kihachiro Kikuzawa 2, 4

2Center for Ecological Research, Kyoto University, Kyoto 606-8502, Japan; and 3Faculty of Human and Environment Studies, Kyoto University, Kyoto 606-8501, Japan

Received for publication May 22, 1998. Accepted for publication October 19, 1998.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Androdioecy, coexistence of hermaphrodites and males, is an extremely rare breeding system in angiosperms. In the present study, Schizopepon bryoniaefolius (Cucurbitaceae) was confirmed to be functionally androdioecious based on observations of floral and pollen morphology and bagging experiments. Six out of the 11 studied populations consisted of only hermaphrodites, while the other five populations were androdioecious and the frequencies of males were consistently lower than those of hermaphrodites (5.5–28.3%). To understand the consequences of an androdioecious breeding system, genetic variation was estimated using four polymorphic allozyme loci. The degree of genetic differentiation among 11 populations was high (GST = 0.688). Inbreeding coefficients (FIS) for all loci significantly deviated from zero. In particular, the FIS values averaged across the polymorphic loci in hermaphrodite populations were close to unity, suggesting that hermaphrodites are predominantly selfing in the absence of males. A significant negative correlation was found between the frequencies of males and inbreeding coefficients, indicating that outcrossing rates depend on the population sex ratio.

Key Words: androdioecy • Cucurbitaceae • genetic differentiation • inbreeding coefficient • mating system • pollen morphology • Schizopepon bryoniaefolius • sex ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Androdioecy is a breeding system composed of both male and hermaphrodite individuals. It was early remarked that androdioecy is extremely rare or hardly exists (Darwin, 1877 ). Most of the plant species described as androdioecious in morphology have been revealed to be functionally dioecious (cryptic dioecy), that is, pollen of morphologically hermaphrodite flowers is sterile (Mayer and Charlesworth, 1991 ). For example, the pollen grains of apparent hermaphrodites lack cytoplasm in Decaspermum parviflorum (Kevan and Lack, 1985 ) or have no aperture in Saurauia veraguensis (Haber and Bawa, 1984 ) and Solanum spp. (Anderson and Symon, 1989 ).

Previous theoretical studies have attempted to explain the rarity of androdioecy in nature. Since male individuals in androdioecious species can contribute to the next generations only through pollen, a larger number of pollen grains of males must fertilize ovules to compensate for the lack of female reproductive success. The evolution of androdioecy requires at least twice as much pollen success of males as hermaphrodites, and high outcrossing rates and strong inbreeding depression make it easier for males to invade a hermaphrodite population (Lloyd, 1975 ; Charlesworth and Charlesworth, 1978 ; Charlesworth, 1984 ). The conditions for the establishment of androdioecy are difficult to satisfy if substantial self-fertilization occurs because mating opportunities for males are limited. Moreover, a computer simulation model of metapopulation dynamics indicated that a large proportion of seeds must be successfully dispersed to neighboring populations for the coexistence of males with hermaphrodites (Pannell, 1997a ).

Only two plant species, Datisca glomerata (Liston, Rieseberg, and Elias, 1990 ) and Mercurialis annua (Pannell, 1997b ), have been confirmed to be functionally androdioecious through the observation of pollen fertility in hermaphrodite plants. They have several common characteristics such as wind-pollination, relatively low male frequency in the populations, protogyny of hermaphrodite flowers, and larger pollen production in male plants than hermaphrodite ones. In D. glomerata, outcrossing rates, inbreeding depression, and male pollen production are sufficiently high to satisfy the theoretical conditions for the maintenance of androdioecy in the populations (Fritsch and Rieseberg, 1992 ; Rieseberg et al., 1993 ; Philbrick and Rieseberg, 1994 ). Mercurialis annua is a polyploid complex and androdioecy occurs only in hexaploid populations (Pannell, 1997b ). The compensation of male plants for the lack of female function, however, has not been understood in androdioecious breeding system except for the increase of pollen production relative to hermaphrodites. In contrast, it has been reported that females in gynodioecious species have the advantages of the avoidance of inbreeding depression by the obligate outcrossing (e.g., Shykoff, 1988 ; Maki, 1992 , 1993 ; Molina-Freaner and Jain, 1993 ; Sakai et al., 1997 ). Furthermore, little is known about genetic variation in androdioecious populations. In gynodioecious species, a few empirical studies have clarified the relationships between population sex ratio and mating systems (Sun and Ganders, 1986 ; Molina-Freaner and Jain, 1992 ; Tarayre and Thompson, 1997 ). Although the frequency of male plants in androdioecious populations may be related to levels of outcrossing in hermaphrodites, no study has paid attention to this relationship.

Schizopepon bryoniaefolius Maxim. (Cucurbitaceae) is morphologically androdioecious (Ohwi, 1953 ), but it remains unknown whether it is functionally androdioecious. This species frequently grows on the foot of mountains in Japan. In the present study, in order to establish functional androdioecy of S. bryoniaefolius, we first examined floral characters including pollen stainability and morphology and the composition of sexual morphs in natural populations. Second, allozyme variation was analyzed to estimate population genetic structure and heterozygote deficiency in the populations with various sex ratios. Finally, we tested the prediction, based on the relationship between population sex ratios and inbreeding coefficients, that levels of outcrossing in hermaphrodites increase with the frequency of male plants in the populations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant species
Schizopepon bryoniaefolius Maxim. (Cucurbitaceae) is a slender scandent annual distributed in East Asia (Japan, Korea, Sakhalin, and northeast China). It commonly inhabits the edge of deciduous forests in highlands such as mountain roadsides. Small, white flowers come out in August and the flowering duration lasts for ~1 mo. The existence of both morphologically hermaphrodite and male individuals has been noted (Ohwi, 1953 ). Hermaphrodite individuals produce solitary perfect flowers from leaf axils. Each hermaphrodite flower has three stamens, a short style with a three-lobed stigma, and a triangular hypogenous ovary. Ripe fruits burst open along the margin of three valves and disperse the seeds. The number of ovules per fruit is three, and up to three seeds are produced in a fruit. Male individuals conspicuously form racemose or paniculate inflorescences with many male flowers. Male flowers also have three stamens, but lack pistils completely.

Study sites and population sex ratios
At the flowering season, August and September in 1997, the numbers of male and hermaphrodite plants were surveyed in 11 populations of S. bryoniaefolius in Japan. The abbreviations and localities of the populations are shown in Table 1 and Fig. 1. Each population was defined as a series of continual patches along a roadside. Sexual morph, either hermaphrodite or male, was unambiguously determined in all individuals because S. bryoniaefolius is an annual and always produces flowers within one year of its life span. The numbers of all individuals of both sexual morphs in the populations were counted, and the frequencies of male plants were calculated for each population.


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  		Table 1. Locality, the number of male and hermaphrodite individuals, and the frequency of males in 11 populations of Schizopepon bryoniaefolius. Sample sizes for electrophoretic analysis are shown in parentheses.

 


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  		Fig. 1. The distribution of the 11 examined populations of Schizopepon bryoniaefolius in Japan.

 
Floral and pollen characters
In order to clarify whether S. bryoniaefolius is functionally androdioecious, the pollen fertility of both male and hermaphrodite flowers was inspected by cotton-blue stainability and morphology. Floral buds and flowers of both morphs were collected at the IWM population and stored in FAA (formalin:acetic acid:ethanol:water = 1:1:9:9 in volume). Pollen grains were picked up from indehiscent anthers and mounted with the solution of cotton-blue, ethanol, and glycerin to estimate the presence/absence of the cytosol in the grains. Pollen morphology was observed with a HITACHI S-3150 scanning electron microscope. The flower buds were dehydrated through ethanol series and critical-point dried. Then the anthers were mounted on stubs, dissected to uncover the pollen grains, and coated with gold. To examine both pollen fertility and self-compatibility of hermaphrodite flowers, 24 hermaphrodite plants were randomly chosen in the SRM population, and one preanthesis flower per plant was covered with a nylon mesh bag for the exclusion of pollinators.

Electrophoresis
Leaf materials of S. bryoniaefolius for electrophoresis were also collected from the same populations where sex ratio was examined. Within each population, ~50 hermaphrodite plants were sampled along a roadside. In androdioecious populations, as many male individuals as possible were collected because of the smaller number of males. The number of male and hermaphrodite individuals sampled for the electrophoretic analysis in each population is shown in Table 1.

Samples were ground in a cold Tris-HCl extraction buffer, and the supernatant was used for electrophoresis. Vertical polyacrylamide gel electrophoresis (PAGE) was conducted following the method as described by Shiraishi (1988) . Four enzyme systems, which showed polymorphic and interpretable banding patterns in preliminary studies, were chosen and assayed: aspartate aminotransferase (AAT), diaphorase (DIA), shikimate dehydrogenase (SkDH), and [NADP] malate dehydrogenase (ME).

Data analysis
Allele frequencies at four polymorphic loci were calculated for each population. The gene diversity within a population (H), which is equal to expected heterozygosity, was calculated for each population. The levels of genetic differentiation among populations were estimated using coefficient of gene differentiation (GST) which is defined as the proportion of interpopulation genetic diversity to total genetic diversity (Nei, 1987 ). Standard errors for each locus were estimated using jackknife procedures across populations (Sokal and Rohlf, 1995 ; Weir, 1996 ).

In addition, the inbreeding coefficient (FIS) was calculated for six populations (HNE, HRY, IWM, KMT, MYK, and SRM) because there was no polymorphic locus in the other five populations. This statistic represents the deficiency of heterozygosity expected from random mating, and therefore is positively correlated with levels of selfing in plants (Ritland and Ganders, 1987 ; Holtsford and Ellstrand, 1989 ). Standard errors of inbreeding coefficients could not be estimated because the number of polymorphic loci in each population was not sufficient to perform the jackknife method over loci. The deviations of FIS from zero over all loci for each population were tested by chi-square values, {chi}2 = NFIS2(a - 1), where N is the number of individuals and a is the number of alleles at each locus (Li and Horvitz, 1953 ). Inbreeding coefficients of hermaphrodites and males were calculated separately for the androdioecious populations in which at least ten males were sampled. Wilcoxon's signed-ranks test (Sokal and Rohlf, 1995 ) was used to see whether there is a significant effect of sex on FIS. The relationship between the frequencies of male plants and the mean inbreeding coefficients (FIS) was analyzed by Kendall's rank correlation test (Sokal and Rohlf, 1995 ). Since male individuals were sampled in excess of population sex ratio in this study, inbreeding coefficients may be overestimated or underestimated if substantial differences in the coefficients between the two sexes occur. To evaluate the relationship exactly, inbreeding coefficients were adjusted for each of the populations by weighting the contribution of each sex morph according to its proportion in the population.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Floral biology
The morphological differences of floral traits between hermaphrodites and males were obvious. Hermaphrodite flowers have three stamens and a pistil, while male flowers have only three stamens and lack a pistil (Figs. 2–4). Anthers and stigma in hermaphrodite flowers are very close to each other (Fig. 3). Of 24 bagged hermaphrodite flowers, 16 samples were collected and eight set fruits with fully developed seeds.



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  		Figs. 2–6. Scanning electron micrographs of floral and pollen morphology in Schizopepon bryoniaefolius. 2. Hermaphrodite flower. Two petals and three sepals are removed. Scale bar = 1 mm. 3. Detail of stamens and stigma of hermaphrodite flower. Scale bar = 1 mm. 4. Male flower. Scale bar = 1 mm. 5. Pollen grain of hermaphrodite flower. Scale bar = 20 µm. 6. Pollen grain of male flower. Scale bar = 20 µm.

 
Pollen fertility and morphology
Most pollen grains in both male and hermaphrodite flowers were stained in cotton-blue solution, indicating that they are filled with cytosolic substance. In pollen morphology, no apparent difference could be found between the two sexual morphs. The pollen grains of both morphs were tricolporate, spherical in shape, ~25 µm in diameter, and had coarsely reticulate surface (Figs. 5–6).

Population sex ratio
The number of plants of each sexual morph and male frequency of S. bryoniaefolius are summarized in Table 1. Six out of the 11 populations completely lacked male individuals, while the frequencies of male plants varied among the five androdioecious populations ranging from 5.5 to 28.3%. The sex ratios of males to hermaphrodites in all populations showed a significant deviation from the 1:1 ratio (chi-square test; P < 0.001). The sex ratio did not depend on geography or population size (Table 1, Fig. 1).

Genetic variation among and within population
Allele frequencies at four polymorphic loci in 11 populations of S. bryoniaefolius are given in Table 2. Of the 11 surveyed populations, four hermaphrodite populations (SGD, NKK, KWK, and KYM) and one androdioecious population (MNK) were monomorphic for all loci and therefore the gene diversity within a population (h) was zero (Table 2). As a result, the hermaphrodite populations tended to have less genetic variation than the androdioecious ones. The gene diversity in the two hermaphrodite populations (SRM, HRY) where polymorphic loci were observed, however, was as large as that in androdioecious ones (Table 2). The mean GST for 11 populations was 0.688 (Table 3).


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  		Table 2. Allele frequencies and gene diversity within a population (h) at four polymorphic loci in 11 populations of Schizopepon bryoniaefolius.

 

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  		Table 3. Total gene diversity (HT), gene diversity within population (HS), and coefficient of genetic differentiation (GST) for four loci in the populations of Schizopepon bryoniaefolius. Standard errors are shown in parentheses.

 
Inbreeding coefficients (FIS) for polymorphic loci in each population are shown in Table 4. For all polymorphic loci, inbreeding coefficients were significantly different from zero. The mean FIS values ranged from 0.386 to 0.978. Inbreeding coefficients in the three androdioecious populations were remarkably different between the two sexes (Wilcoxon's signed-ranks test; z = -2.366, P = 0.018). The FIS values of males were close to zero except for one locus in KMT, while hermaphrodites showed significant heterozygote deficiencies for all loci (Table 5). A significant negative correlation was found between the frequencies of male plants and inbreeding coefficients (Kendall's rank correlation test; {tau} = -0.966, P = 0.0065) (Fig. 7).


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  		Table 4. Inbreeding coefficients (FIS) in the six populations of Schizopepon bryoniaefolius with polymorphic loci.

 

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  		Table 5. Inbreeding coefficients (FIS) of male and hermaphrodite plants in three androdioecious populations of Schizopepon bryoniaefolius.

 


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  		Fig. 7. Relationship between the frequencies of males and the mean inbreeding coefficients (FIS) in six populations of Schizopepon bryoniaefolius. Each FIS value is adjusted on the basis of sex ratio in natural populations (Kendall rank correlation; {tau} = -0.966, P = 0.0065).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Functional androdioecy of Schizopepon bryoniaefolius
Both male and hermaphrodite flowers of S. bryoniaefolius produced stainable pollen grains with apertures, suggesting that both sexes have fertile pollen grains. Pollinator exclusion tests showed that hermaphrodite plants are self-compatible and autogamous, indicating that hermaphrodites have both male and female function. Moreover, six out of the 11 populations were composed of only hermaphrodite plants. These results provided the conclusive evidence that S. bryoniaefolius is functionally androdioecious.

The frequencies of hermaphrodites and males in all populations deviated from the 1:1 ratio that is commonly observed in cryptic dioecy (Charlesworth, 1984 ). In particular, the absence of males in several populations suggests that male plants are not indispensable for the establishment or sexual reproduction in populations. In all androdioecious populations, the frequencies of males were consistently lower (up to 28.3%) than those of hermaphrodites. This result is consistent with the frequencies of males in other functionally androdioecious species. In Datisca glomerata, males occur at a frequency of < 25% (Liston, Rieseberg, and Elias, 1990 ), and less than ~30% in Mercurialis annua (Pannell, 1997c ).

Hermaphrodites of S. bryoniaefolius have perfect flowers, although most species of Cucurbitaceae are either monoecious or dioecious. Of the other seven species in Schizopepon, one is monoecious and six are dioecious (Lu and Zhang, 1986 ). The monoecious species, S. monoicus, has one or two female flowers and numerous male ones on the same inflorescence, while the dioecious species have racemose or paniculate inflorescences in males and solitary ones in females. The evolutionary processes from dioecy require only the addition of stamens to pistillate flowers, whereas the evolution from monoecious species requires not only this change but also the separation of the two sex morphs into different plants. These suggest that the androdioecious breeding system in S. bryoniaefolius was derived from dioecious species. Two other androdioecious species were reported to be derived from dioecious ones on the ground that all relatives within the genus are dioecious (Liston, Rieseberg, and Elias, 1990 ; Pannell, 1997b ). The derivation of D. glomerata from a dioecious ancestor was also supported by a phylogenic reconstruction of Datiscaceae based on restriction site mapping of polymerase chain reaction amplified chloroplast DNA fragments (Rieseberg, Hanson, and Philbrick, 1992 ).

Mating systems and population genetic differentiation
The absence of genetic variation within a population was more frequent in hermaphrodite populations than in androdioecious ones, although the gene diversity in two other hermaphrodite populations (SRM, HRY) was large. This suggests that hermaphrodite populations have passed through more severe genetic drift and/or founder effects than androdioecious ones.

Overall 11 populations of Schizopepon bryoniaefolius showed a high degree of genetic differentiation, and the GST value (0.688) was higher than the average of 78 selfing species (GST = 0.51) reviewed by Hamrick and Godt (1990) . Wright (1951) demonstrated that even a small amount of gene flow among populations could be enough to impede genetic population differentiation. The large GST value of this species represents not only stochastic genetic drift accompanied by fluctuation of population size but also restricted gene flow among populations. As a result, it is unlikely that female sterile genes spread extensively over adjacent populations.

Inbreeding coefficients for all loci deviated significantly from those expected under random mating. In particular, the large FIS values in hermaphrodite populations suggest that hermaphrodites of S. bryoniaefolius are primarily selfing. Self-compatibility and proximity between anthers and stigma in hermaphrodite flowers likely promote self-fertilization within a flower. The FIS value of S. bryoniaefolius is as large as that of Datisca glomerata (FIS = 0.617), which was estimated from a small population (Liston, Rieseberg, and Elias, 1989 ). These results suggest that selfing is predominant in S. bryoniaefolius, which may contradict the model requirement that a high level of outcrossing is preferable for the evolution of androdioecy (Lloyd, 1975 ; Charlesworth and Charlesworth, 1978 ). The predictions of the models are based on the assumption that outcrossing rates of the hermaphrodites do not depend on the male frequency of the population, which clearly contradicts with the present results (Table 5, Fig. 7). According to recent thought, the occurrence of self- and cross-fertilization involves various factors such as pollinator activity and timing of pollen reception (Lloyd and Schoen, 1992 ). The model would be modified by incorporating the parameters based on these ecological factors. Furthermore, whether the condition for the evolution of androdioecy in previous models is satisfied depends on the magnitude of inbreeding depression and pollen production of males relative to hermaphrodites. We did not examine these parameters in the present study. Further studies, including the evaluation of these parameters, are ongoing to understand the maintenance of males in S. bryoniaefolius.

The maintenance of male plants in an androdioecious breeding system
In the androdioecious populations, the FIS values of male plants were nearly zero, while hermaphrodites showed a significant heterozygote deficiency. This contrasting result is likely to reflect the association of parental mating and sex, i.e., male offspring are generated through the cross between male and hermaphrodite parents. Since female sterility of male plants can be controlled only by nuclear genes due to maternal inheritance of cytoplasmic genes in angiosperms (Charlesworth and Charlesworth, 1978 ), it is plausible that maleness in Schizopepon bryoniaefolius is determined by nuclear genes. Recently, the mechanisms of sex determination in androdioecious plants were elucidated by reciprocal crossing experiments. Males appear to be determined by double recessive homozygotes at two loci in Datisca glomerata (Wolf, Rieseberg, and Spencer, 1997 ) and by dominant alleles at several loci in Mercurialis annua (Durand and Durand, 1991 ; Pannell, 1997d ).

A significant negative correlation between the frequencies of males and inbreeding coefficients may provide an important clue to understand the contribution to the next generations through male individuals in an androdioecious breeding system. This result suggests that pollen dispersed from male flowers can successfully fertilize ovules of hermaphrodites in proportion to the frequency of males in androdioecious populations. Since paniculate male inflorescences comprise ~10–20 flowers and are much more conspicuous than solitary hermaphrodite ones, male plants are expected to produce a larger amount of pollen and attract more pollinators than hermaphrodites. We are currently collecting the data on floral traits and pollinator attraction. The preference of pollinators for male flowers may be a major factor increasing levels of outcrossing, which plays an important role in the maintenance of males in S. bryoniaefolius.


   FOOTNOTES
 
1 The authors thank M. Maki, H. Shibaike, K. Ishida, and H. Kudoh for critical comments on the manuscript, and E. Kinoshita, S. Fujii, M. Tateno, M. Maki, and K. Inoue for information on localities of the study plant. Back

4 Corresponding author (e-mail: kikuzawa@ecology.kyoto-u.ac.jp). Junichi Akimoto (1973–1998) died in a traffic accident on 24 September 1998, during his trip to investigate Schizopepon. Back


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 ABSTRACT
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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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