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Reproductive Biology |
Laboratoire d'Écologie, Systématique et Évolution, CNRS UPRESA 8079, Université de Paris-Sud (XI), Bâtiment 360, F-91405 Orsay Cedex, France
Received for publication July 26, 2002. Accepted for publication November 8, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: biparental inbreeding • correlations of outcrossed paternity • geitonogamy • gynomonoecy-gynodioecy • selfing
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Much interest has been given to the puzzling question of females' maintenance, modeled by Lewis (1941)
and Charlesworth and Charlesworth (1978)
and extensively studied in thyme (reviewed in Thompson et al., 1998
) and in an increasing number of species. Sex ratio within gynodioecious populations may vary greatly (from zero up to 95% of females) influencing plant reproductive success in several ways (Ashman and Diefenderfer, 2001
). Sex ratio, however, can also vary at the whole-plant level, and far less is known about variation within plants.
Many gynodioecious species include plants of intermediate phenotype bearing both pistillate and perfect flowers in varying proportions (hereafter referred to as mixed or gynomonoecious plants). These individuals have been considered too rare to be important for evolution of a gynodioecious mating system (Kaul, 1988
). Indeed, mixed individuals were often ignored or included in analyses as hermaphrodites, with the following exceptions (Philipp, 1980
; Shykoff, 1992
; Desfeux, 1996
; Koelewijn, 1996
; Koelewijn and van Damme, 1996
; Talavera et al., 1996
; Shykoff et al., 1997
; Andersson, 1999
; Maurice, 1999
; Widén and Widén, 1999
; Guitián and Medrano, 2000
; Collin et al., 2002
). However mixed individuals can outnumber females and thus represent an important but long-ignored arena of selection for nuclear and cytoplasmic genes involved in sex expression, particularly if gynomonoecious individuals are partially restored male steriles (Koelewijn, 1996
).
In the present study, we describe more precisely gynomonoecy-gynodioecy by estimating mating-system parameters for individual flowers on the three types of plants and linking the mating-system parameters to pollinator behavior and floral features, as suggested by Sun and Ganders (1988)
. To date, outcrossing rates for hermaphrodite individuals have been estimated in several gynodioecious species (listed in the Appendix on the American Journal of Botany Supplementary Data website at http://ajbsupp.botany.org/v90/) mainly to test whether females have an outcrossing advantage that could contribute to their maintenance in populations containing hermaphrodites (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1981
). Mean outcrossing rates vary greatly among species (Fig. 1) but also within species, depending on the population studied and/or year, as emphasized by Aide (1986)
for animal-pollinated plants. Hermaphrodites have a continuous distribution of outcrossing rates, with most species having a mixed mating system. Females are expected to be completely outcrossed, and values smaller than unity can be explained by biparental inbreeding (mating between relatives). Some exclusively hermaphroditic populations of gynodioecious species can have either very low (Chionographis japonica and Trifolium hirtum) or very high (Limnanthes douglasii) outcrossing rates; see Appendix (http://ajbsupp.botany.org/v90/).
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did not distinguish between male-sterile and male-fertile flowers on mixed plants. The presence of the two types of flowers on a single plant may influence plant fitness, because geitonogamy, which may generate inferior offspring through inbreeding depression (de Jong et al., 1993
), may occur for both pistillate and perfect flowers. Flower morphology (herkogamy) or phenology (protandry or protogyny) are usually sufficient to limit autogamy at the flower but not at the plant level when several flowers are open simultaneously (Pettersson, 1992
; Hidalgo and Ubera, 2001
). Geitonogamy should increase with the number of open flowers (Geber, 1985
; Klinkhamer and de Jong, 1993
; Harder and Barrett, 1995
), but could be influenced by floral sex ratio, the presence of pistillate flowers reducing self-pollen availability on mixed plants. Mixed plants would then be expected to be less selfed than pure hermaphrodites.
In this paper we investigate the gynomonoecious-gynodioecious mating system of the self-compatible rock pink Dianthus sylvestris Wulf. (Caryophyllaceae). Mixed individuals are common in this species (Shykoff et al., 1997
; A. Erhardt, University of Basel, personal communication) and several flowers are often open per plant, allowing for geitonogamy. As in many other gynodioecious species (Delph, 1996
; Shykoff et al., 2003
), pistillate flowers of D. sylvestris are smaller than the protandrous perfect ones (Collin et al., 2002
). Estimates of the mean outcrossing rates and correlations of outcrossed paternity were estimated from electrophoretic data on progeny arrays. These parameters were estimated at both plant and flower levels, allowing comparisons between pistillate and perfect flowers on both pure-sexed (i.e., females and hermaphrodites) and mixed plants. We ask the following questions: (1) How do mixed individuals behave in comparison with pure-sexed plants? (2) Are pistillate and perfect flowers on mixed plants different from each other and from those on pure-sexed plants? (3) Does flower size dimorphism influence outcrossing rates and correlations of outcrossed paternity? We discuss the observed patterns in light of pollinator behavior and consider the role of mixed plants and their importance in the evolution of gynodioecy, testing whether their progeny might be less inbred than those of hermaphrodite plants.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Seeds harvested from these open-pollinated plants were stored in paper bags at room temperature and germinated in January 2000 on 1% water agar (protocol in Collin et al., 2002
). Thirty-six maternal parents were chosen and 8–15 seedlings from a single fruit from each of 13 females and 13 hermaphrodites and from two fruits, one pistillate and one perfect, from 10 mixed plants were grown.
Electrophoresis
Electrophoretic analyses were performed on extracts from tender young leaves from the middle of seedling rosettes aged 6–12 wk. About 100–120 mg of fresh material was crushed in 1.5-mL Eppendorfs with 100 µL of extraction buffer and Fontainebleau sand before centrifuging (10 min at 7900 x g). The supernatant was then absorbed onto Whatman no. 3 filter paper wicks that were inserted into 13% horizontal starch gels (with 3% sucrose). Amino acids were resolved on histidine pH 6.5 buffer systems run for 18 h at 2 W per gel. Allozyme variation was assayed for various enzyme systems, and three of them appeared to be easy to interpret and polymorphic: phosphoglucose-isomerase (Pgi, EC 5.3.1.9), phosphoglucomutase (Pgm, EC 2.7.5.1) and 6-phosphogluconate-dehydrogenase (6-Pgd, EC 1.1.1.4.3). All extraction, gel, and staining procedures were modified either from Wendel and Weeden (1990)
or Pasteur et al. (1987)
.
Estimation of outcrossing rates
Five loci were scored and genotypic data were obtained for 696 plants from the 46 families. Outcrossing rates were determined using Ritland and Jain's (1981)
multilocus maximum likelihood estimation program (MLTR 1994 version 1.1, accessible at http://genetics.forestry.ubc.ca/ritland/programs.html; Ritland, 1990
). Standard deviations were determined based on 1500 bootstrap analyses; maternal genotypes were estimated as part of the maximum likelihood procedure. Two kinds of analyses were performed: population estimates allowed us to calculate overall multilocus (tm) and mean single locus (ts) outcrossing rates, bootstraps using families as units of observation. Family estimates gave outcrossing rates per family, bootstraps using individual offspring as units of observation. Unfortunately several families gave unrealistic outcrossing estimates higher than unity, as can occur in families with multiple heterozygous parents (Ritland, 1990
; MLTR manual). These values could thus not be used for detailed examination of outcrossing rates of individual flowers, precluding comparisons using individual progenies. The correlations of outcrossed paternity (rp), i.e., the probability that two individuals drawn at random from the same progeny array are full-sibs, were also estimated.
We estimated plant level outcrossing rates of mixed plants using equal representation of pistillate and perfect flowers. However gynomonoecious plants seldom bear a one-to-one floral sex ratio. The proportion of pistillate flowers generally follows a U-shaped distribution with most plants bearing a majority of perfect flowers (e.g., in Silene italica, Maurice, 1999
). In D. sylvestris, of 28 mixed plants for which total flower production was recorded in an experimental garden, 20 (71.4%) bore fewer than 40% pistillate flowers. For the field population, 15 of 25 (60%) bore fewer than 40% pistillate flowers. Therefore our outcrossing estimates for gynomonoecious plants will be biased if the two floral genders have different outcrossing rates.
Families were grouped in order to compare estimates between different plant types (female, mixed, and hermaphrodite) and flower sexes (pistillate and perfect); two-tailed t tests with critical level adjusted by the Bonferroni method (Rice, 1989
) were used to compare mean values per group. Because pistillate and perfect flowers on mixed plants are not independent and outcrossing values per family were not available, a paired t test could not be performed and some pseudo-replication remains for the analysis considering flower sex.
Because outcrossing rates were determined from established 6- to 12-wk-old rosettes, some selfed progeny may have been eliminated by early-acting inbreeding depression, so that true selfing values were underestimated (Maki, 1993
; Sakai et al., 1997
). Husband and Schemske (1996)
, in their review of the inbreeding depression literature, found that many outcrossing species express inbreeding depression early in the life cycle. However, we detected no significant differences between parental sexes for seed set, seed germination, and seedling mortality (data in Table 1; Collin et al., 2002
), so we conclude that this source of bias was negligible.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Indeed, population outcrossing estimates from analyses using all loci or with only three polymorphic loci did not differ (data not shown). However, we decided to retain all five loci for all estimations since fewer family outcrossing estimates were superior to one when Pgi2 and 6-Pgd were included.
Outcrossing rates
The overall outcrossing rate was quite high, tm = 0.885 ± 0.032 (multilocus estimation ± SD), for this population of Dianthus sylvestris. Estimations by flower sex revealed that pistillate flowers (born on female and mixed plants combined) were not completely outcross pollinated (tm = 0.935 ± 0.051; t test of difference from unity, t = 6.11, N = 23, P < 0.001), while perfect flowers' progeny were significantly more selfed (tm = 0.834 ± 0.047; t test, t = 9.38, N = 46, P < 0.001). The overall increase in outcrossing rate because of flower male sterility was 10.1%.
Mixed plants had outcrossing rates that were intermediate but not significantly different from the hermaphrodites (Table 2; t test, t = 2.4, N = 23, P = 0.0257, critical P value of 0.0167 after Bonferroni correction). The progeny of female plants were completely outcrossed on average (Table 2; t test of difference from unity, t = 0.41, N = 13, P > 0.5) and significantly different from mixed plants (t test, t = 5.34, N = 23, P < 0.001, critical P value as before). Pistillate flowers on mixed plants had the lowest proportion of outcrossed progeny but did not significantly differ in outcrossing rate from perfect flowers on hermaphrodite plants (Table 2; t test, t = 0.27, N = 23, P > 0.5). Perfect flowers on mixed plants had outcrossing rates intermediate between those of pistillate (t test, t = 3.55, N = 23, P < 0.002, critical value as before) and perfect flowers (t test, t = 5.45, N = 23, P < 0.001, critical value as before) on female and hermaphrodite plants, respectively. Figure 2a shows that, with the exception of pistillate flowers from mixed plants (FM), flower categories of larger mean size had higher mean selfing rates than those of smaller mean size.
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Correlations of outcrossed paternity
In this study more than one pollen donor fertilized single flowers, with a mean of 61.5 ± 19.9% of outcrossed full-sibs within families. If we consider the progeny of the three types of plants, the percentage of outcrossed full-sibs was lower for female plants (46.0 ± 24.3%) than for hermaphrodite and mixed plants (62.8 ± 20.8%, t test, t = 4.89, N = 26, P < 0.001; and 67.2 ± 18.9%, t test, t = 5.98, N = 23, P < 0.001, respectively), which did not significantly differ (t test, t = 1.36, N = 23, P > 0.1). Figure 2b shows a positive relationship between the correlation of outcrossed paternity (rp) and mean flower size for three categories of flowers (pistillate flowers from female plants and perfect flowers from both hermaphrodite and mixed plants). However, as for outcrossing rates, pistillate flowers from mixed plants did not follow that trend, with a value not different from unity (t test, t = 0.47, N = 10, P > 0.5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Kohn and Biardi, 1995
). Further analyses are required to quantify pollen and seed dispersion and the occurrence of mating between relatives in this species.
The gynomonoecious-gynodioecious breeding system
We had expected that mixed plants, because of the presence of pistillate flowers, should exhibit reduced selfing at the plant level. We did not find this advantageous reduced selfing of gynomonoecy because the mean selfing rate of flowers on these mixed plants was as high as that of the hermaphrodites. However, analyses at the plant level were not sufficient to reveal all insights into gynomonoecy-gynodioecy. Analyses performed at the flower level showed that the four flower categories behaved in very different ways, making it important to consider pistillate and perfect flowers on mixed plants separately. Indeed, as perfect flowers revealed lower selfing rates than did pistillate ones within mixed plants, the mean selfing rate for these plants may have been overestimated, considering that mixed plants frequently bear more perfect than pistillate flowers whereas our estimations were based on an equal representation of each flower sex.
Perfect flowers from mixed plants showed less selfing than those from hermaphrodites. Pistillate flowers on these mixed plants had the highest selfing rates. This result shows that autogamous self-pollination is not important in this species, because with much autogamous selfing all perfect flowers should show similar rates of selfing and pistillate flowers should not. Indeed, perfect flowers are protandrous, so selfing is likely to result from geitonogamy, as in Geranium richardsonii (Williams et al., 2000
). We suggest that floral size dimorphism contributes to this pattern (Fig. 2a). Perfect flowers are larger than pistillate ones, and large flowers are known to be more attractive to pollinators (Bell, 1985
; Eckhart, 1992a
). Furthermore, they provide more nectar rewards than pistillate flowers (Eckhart, 1999
; Ponomarev and Dem'Yanova [1975] cited in Uno, 1982
; Talavera et al., 1996
; Shykoff et al., 1997
; Ashman et al., 2000
), although females may accumulate nectar if they are poorly visited (Delph and Lively, 1992
; Eckhart, 1992a
, b
). Thus, pollinators are expected to first visit these larger perfect flowers, as observed by Müller (quoted by Darwin, 1877
), who hypothesized that more conspicuous perfect flowers in gynodioecious species are visited first, ensuring pollination of less showy pistillate ones. Perfect flowers on mixed plants should, in consequence, generally receive outcrossed pollen. Pollinators finding abundant nectar in first-visited perfect flowers should remain longer in the patch (Hodges, 1995
). Subsequently, they should thus visit the smaller, less rewarding pistillate flowers, which would then receive geitonogamous pollination. Higher selfing rates for flowers visited later in the pollinator visitation sequence similarly occurs in simultaneously flowering perfect flowers of hermaphrodite species (Harder and Barrett, 1995
).
Thus, we suggest that pollinator response to floral size dimorphism could explain why perfect flowers on mixed plants were on average more outcrossed than those on hermaphrodite plants. However, flower size was not found to influence outcrossing rates in the hermaphroditic species Lupinus nanus (Horovitz and Harding, 1972
) or G. achilleifolia (Schoen, 1982
) or in several species of gynodioecious Bidens (Sun and Ganders, 1988
). Thus important questions remain open on the role of flower size, plant size, and flower sex ratio in outcrossing rates, particularly in size-dimorphic species (Valdeyron et al., 1977
). Experiments are planned to test the effect of these plant features on family outcrossing rates in this species.
Most flowers of D. sylvestris received pollen from more than one donor except pistillate flowers from mixed plants. Dianthus sylvestris is mainly pollinated by two species of Lepidoptera, the diurnal Macroglossum stellatarum L. (Lepidoptera: Sphingidae) and the nocturnal Hadena compta Schiff. (Lepidoptera: Noctuidae). Low carryover is characteristic of pollination by Lepidoptera that present only small amounts of pollen on their coiled probosces (Wiklund et al., 1979
), so several pollinator visits may contribute to pollination (Pettersson, 1991
), which would lead to multiple paternity of seeds from single fruits. Outcrossed seeds from pistillate flowers on mixed plants, however, appeared to be sired by a single pollen donor, suggesting overall fewer visits to these flowers. Seed set does not differ between pistillate flowers from mixed and female plants, however (Collin et al., 2002
), so a single visit appears to deliver enough pollen to completely fertilize these flowers, particularly if the pollinator has just visited perfect flowers on the same plant.
The role of gynomonoecious individuals
In gynodioecious species, female individuals must have a reproductive advantage to be maintained in populations with hermaphrodites, either through higher outcrossing rates or resource economy (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1981
). However pistillate flowers face some disadvantages. These flowers may be discriminated against by pollinators because of their small size (Delph, 1996
; Delph et al., 1996
) and rarity (Levin, 1972
). Uno (1982)
hypothesized that pistillate flowers mimic perfect ones in order to be pollinated, and pollinators prefer hermaphroditic flowers in Fragaria virginiana (Ashman et al., 2000
). Furthermore, females are dependent on the presence and frequency of hermaphrodites for pollen (McCauley and Taylor, 1997
; McCauley and Brock, 1998
; Graff, 1999
). Female plants that present some perfect flowers may have higher reproductive success because attractiveness may be enhanced if the mixed plants present a showier structure for pollinators (Hessing, 1988
; Bertin and Kerwin, 1998
). Second, pistillate flowers on mixed plants may benefit from local pollen availability.
Desfeux (1996)
proposed that gynomonoecy represents a bet-hedging strategy (Philippi and Seger, 1989
). Mixed individuals benefit from reallocation of resources saved on small pistillate flowers (Atlan et al., 1992
) and/or lower selfing rates, while simultaneously ensuring against pollen limitation by producing some perfect pollen-bearing flowers. Whether pistillate flowers on mixed plants really experience enhanced pollen availability within these plant needs to be tested in this species, because reproductive limitation by pollen is rarely found in females of gynodioecious species (reviewed in Burd, 1994
) and depends on local population sex ratios (Widén and Widén, 1990
; Widén, 1992
; Desfeux, 1996
; McCauley and Brock, 1998
; Graff, 1999
). In addition we found no clear outcrossing advantage for mixed plants as a whole, when considering the average outcrossing rates between pistillate and perfect flowers. However the mean outcrossing rate we calculated for these plants may have been underestimated because it does not take into account the majority of perfect flowers usually found on mixed plants, so an outcrossing advantage of mixed plants could exist. To conclude, no clear advantage was found yet, at the whole-plant level, for mixed plants compared to pure-sexed plants. On the contrary, the association of pistillate and perfect flowers on mixed plants seems to be a disadvantage, leading to weaker males than the hermaphrodites because they produce less pollen and probably weaker females because pollen and floral features are costly and pistillate flowers receive abundant geitonogamous pollination.
However, we have found an unexpected result by analyzing at the flower level, suggesting a novel advantage to mixed plants. The presence of female flowers on mixed individuals significantly increased the outcrossing rates for the perfect flowers, though high outcrossing rates were not found for the pistillate flowers where this was expected, possibly because pollinators visit large perfect flowers first. Mixed plants usually bore fewer pistillate than perfect flowers. Thus, even a minority of female flowers on the mixed plants significantly reduced the selfing rate by the perfect flowers. Indeed, this result implies a whole-plant reduction in selfing rate if fruits were either sampled exhaustively or at random, but this outcrossing advantage is enjoyed by the perfect flowers not the pistillate flowers, where it would generally be expected. In the presence of inbreeding depression, this significantly reduced selfing rate in the majority of flowers on mixed plants could enhance their whole-plant reproductive success. More detailed studies are underway to investigate the effect of varying sex ratio on the outcrossing rates of pistillate and perfect flowers on mixed individuals.
If there is nucleo-cytoplasmic sex determination in this species, as has been demonstrated for another Caryophyllaceae (Charlesworth and Laporte, 1998
), gynomonoecious plants may be partially restored male steriles (Koelewijn, 1996
) or heteroplasmic individuals bearing a mixture of male-sterile and male fertile cytoplasms (Andersson, 1999
). Under the former hypothesis of partially restored male steriles (Koelewijn, 1996
), production of higher quality seeds by perfect flowers on mixed individuals could contribute to the representation of male-sterile cytoplasms in the population. Pollen export from such plants, and thereby the dissemination of nuclear genes with poor restoration ability, however, may be impeded by geitonogamous loss to stigmas of pistillate flowers. This process could increase the frequency of females in gynomonoecious-gynodioecious populations. On the other hand, if perfect flowers on mixed individuals bear male-fertile cytoplasms, better offspring from these flowers should reduce the representation of male-sterile cytoplasms in the population as a whole, and local seed dispersal should produce patches of hermaphroditic plants. More detailed studies of pollen export by mixed plants as well as a more thorough understanding of the inheritance of sex and the genetic basis of partial male sterility will be necessary to understand the role that these mixed individuals can play in the evolutionary dynamics of male sterility.
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FOOTNOTES |
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2 Author for correspondence (carine.collin{at}ese.u-psud.fr
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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