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(American Journal of Botany. 2003;90:949-953.)
© 2003 Botanical Society of America, Inc.

Brief Communications

Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae)1

Marie-Elise Morand-Prieur2, Christian Raquin, Jacqui A. Shykoff and Nathalie Frascaria-Lacoste

Laboratoire Ecologie, Systématique et Evolution (ESE), UMR CNRS-ENGREF 8079, Bâtiment 360, Université Paris-Sud, 91 405 Orsay Cedex, France

Received for publication October 10, 2002. Accepted for publication January 10, 2003.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Polygamy (including trioecy and subdioecy), the co-occurrence of males, hermaphrodites, and females in natural populations, is a rare and poorly studied breeding system expressed in Fraxinus excelsior L. (Oleaceae), a wind-pollinated tree. Here we investigate siring ability of pollen from male vs. hermaphrodite individuals to better understand this sex polymorphism. We conducted single-donor and two-donor pollination experiments and compared both fruit set and seed siring success, assessed with polymorphic microsatellite markers, of male and hermaphrodite individuals. Single pollen donor crosses allowed us to verify the male function of hermaphrodites. However, pollen from hermaphrodites was much less proficient than male pollen, with males siring 10 times as many fruits in single donor pollination treatments. This result was strengthened by the surprisingly low reproductive success of hermaphrodites in pollen competition conditions: of the 110 seedlings analyzed three were selfed and only one was sired by the hermaphrodite donor. The remaining 106 were sired by the male pollen donor. These results raise the question of the maintenance of male fertility in hermaphrodites in Fraxinus excelsior. Male function of hermaphrodites in this species now needs to be assessed under field conditions.

Key Words: androdioecy • Fraxinus excelsior • male reproductive success • microsatellites • Oleaceae • paternity assignment • pollen competition • polygamous mating system • trioecy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Breeding systems show great diversity in angiosperms but the co-occurrence of males, hermaphrodites, and females within the same population, identified by the general term "polygamy" (including trioecy and subdioecy), appears to be rare, representing 3.6% of species (Yampolsky and Yampolsky, 1922 ; Richards, 1997 ), and is poorly described.

Fraxinus excelsior L. (Oleaceae), a temperate tree species, has been variously described as polygamous, trioecious, or subdioecious (Binggeli and Power, 1999 ). The maintenance of diverse sexual forms in this species has not yet been studied. In particular, the relative male fertility of single sexed pure males vs. hermaphrodite individuals, though intensively investigated in other androdioecious species, remains unexplored in this one. Androdioecy, the rarest breeding system in angiosperms (Yampolsky and Yampolsky, 1922 ; Charlesworth, 1984 ), is defined by the co-occurrence of male and hermaphrodite individuals in natural populations. Only six plant species, three belonging to the Oleaceae family, are apparently functionally androdioecious, i.e., with male-fertile hermaphrodites coexisting with pure males (Liston et al., 1990 ; Lepart and Dommée, 1992 ; Pannell, 1997a ; Ishida and Hiura, 1998 ; Akimoto et al., 1999 ; Dommée et al., 1999 ; Vassiliadis et al., 2002 ). Moreover, maintenance of androdioecy requires a male fertility advantage of males over hermaphrodites. This male advantage was found for pollen production (Philbrick and Rieseberg, 1994 ; Pannell, 1997b ) and for fertilization ability in controlled crosses using single donor pollinations (Ishida and Hiura, 1998 ; Dommée et al., 1999 ; Vassiliadis et al., 2000 ). In natural populations however, male and hermaphrodite individuals may compete for seed siring (Pannell and Ojeda, 2000 ), and paternity analysis is needed to determine the effective male reproductive success of male vs. hermaphrodite individuals. Indeed in the androdioecious Phillyrea angustifolia pollen from hermaphrodites and males is equivalent in seed siring efficiency estimated by paternity analyses (Vassiliadis et al., 2002 ) although a male advantage is found under single donor conditions (Vassiliadis et al., 2000 ).

An important aspect of male success of pollen from male vs. hermaphrodite individuals could be seed siring ability in competition. To date no paternity analyses of different (i.e., male vs. hermaphrodite) pollen donors in controlled crosses have been reported in androdioecious species. More generally, although seed paternity is nonrandom when pollen from two or more pollen donors is applied to stigmas (see Marshall and Oliveras [2001] for a review of these studies), this has usually been related to pollen tube growth rate differences rather than phenotypic differences between the pollen donors (see for example; Björkman et al., 1995 ; Snow and Spira, 1996 ; Pasonen et al., 1999 ). On the other hand, in Caenorhabditis elegans, a well-studied androdioecious nematode, male sperm is superior to sperm of selfing hermaphrodites for fertilizing ova (Ward and Carrel, 1979 ; Hodgkin and Barnes, 1991 ; Singson et al., 1999 ), with a male advantage from two- to fourfold in offspring production (Hodgkin and Barnes, 1991 ).

The aim of the present study was to give some insights into the polygamous breeding system of Fraxinus excelsior under controlled conditions. Several single-donor and two-donor crosses were performed. We analyzed fruit set and also assigned paternity using microsatellite markers to (1) estimate potential male fertility of hermaphrodites, (2) compare male reproductive success of males and hermaphrodites in single-donor pollinations, and (3) assess seed siring success of males and hermaphrodites in pollen competition conditions.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study species
Common ash (Fraxinus excelsior L., Oleaceae) is a deciduous forest tree with wind-pollinated flowers and wind-dispersed fruits, distributed throughout Europe and Asia Minor (Wardle, 1961 ). Sexual types present a continuum from pure male to pure female individuals, with a range of hermaphrodites in between (Wardle, 1961 ; Picard, 1982 ; Binggeli and Power, 1999 ; Wallander, 2001 ). A single individual can have varying proportions of more than one sort of flowers (staminate plus perfect or pistillate plus perfect) (Binggeli and Power, 1999 ; Wallander, 2001 ). Perfect flowers consist of one pistil and two stamens attached to the base of the ovary (Binggeli and Power, 1999 ; Wallander, 2001 ). Flowers have neither calyx nor corolla and are tightly clumped in inflorescences borne on lateral buds. Flowering occurs in the north of France in March–April and usually lasts 3–4 wk within a given population. Perfect flowers are protogynous, although anther dehiscence occurs while the stigma is still receptive. The ovary contains four ovules, and fruits are generally one-seeded winged samaras.

Controlled crosses
Six Fraxinus excelsior individuals (four hermaphrodite trees and two males) located on the Orsay University campus were used as parents in the controlled crosses. No pure female trees were present, so the hermaphrodites H1, H2, H3, and H4 were used as maternal trees. Two of these (H1 and H2) were pure hermaphrodites, bearing only perfect flowers, and these were also chosen as hermaphrodite pollen donors. Two pure males (M1 and M2), bearing only staminate flowers, were chosen as the male pollen donors. Hermaphrodite trees were tested for self-compatibility in several years by bagging inflorescences before bud opening. Though early development of fruits was normal, immature samaras all abscissed and fell, suggesting self-incompatibility (see Morand et al., 2002 ).

In March 1999, flowering branches of pollen donors were cut for pollen collection. These branches were put into water in the laboratory and stored at room temperature until flowering. Pollen was harvested either on sheets of aluminum foil (pollen donors M1 and H1) or in maize pollen-collecting bags (donors M2 and H2). Pollen germination rate was determined for all four individuals by counting 2 x 100 pollen grains incubated for 6 h at 24°C on pollen growth medium containing 1.27 mmol/L Ca(NO3)2, 1.62 mmol/L H3BO3, 0.2 mmol/L KH2PO4, 0.05 mmol/L K2HPO4, and 351 mmol/L sucrose (Mulcahy and Mulcahy, 1983 ) and solidified with 5 g/L Phytagel (Sigma Aldrich, Saint Quentin Fallavier, France) before autoclaving. Pollen germination was similar between individuals with the same pollen collection method but differed between the following collection methods: aluminum foil in vitro pollen germination rate of 0.43 ± 0.02 (mean ± 1 SD; N = 4); maize pollen bags in vitro pollen germination rate of 0.16 ± 0.05 (N = 4). The number of inflorescences from which we collected pollen was equivalent from one tree to another.

Three pollination treatments were performed by bagging inflorescences before bud opening and brushing pollen over the open stigmas as soon as they appeared and 1 wk later: (1) pollination with pollen from one hermaphrodite tree (H1 or H2), (2) pollination with pollen from one male tree (M1 or M2), (3) pollination with a mass for mass mixture of pollen from one male tree and one hermaphrodite tree (pollen competition treatment). For this last treatment, we mixed pollen with equivalent in vitro germination rates, giving two different pollen mixtures: (M2 + H2) and (M1 + H1). A total of 25 controlled crosses on one pair of inflorescences each were carried out, using each of the four mother trees for all three treatments (Table 1). Because the flowers are small, the number of flowers per inflorescence could not be counted for each pollination; however, within a pollen recipient tree, the number of flowers per inflorescence is comparable. One to three controlled crosses was performed per pollination combination (donor[s]) and recipient) (Table 1). Finally, as the four mother trees were hermaphrodite, autonomous selfing was possible since the numerous tiny hermaphrodite flowers could not be emasculated. However, no self-pollen was manually added. Bags were removed 3 wk after the first pollination treatment and fruits were collected and counted in mid-August. Seedlings for molecular analysis were obtained as described in Raquin et al. (2002) , with a slight modification of the H10 culture medium (containing 28 mmol/L sucrose instead of 14 mmol/L sucrose and 14 mmol/L maltose).


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  		Table 1. Numbers of Fraxinus excelsior fruits (Fruit) and seeds (Seed) obtained for each pollination. Number of viable embryos (Embryos) obtained after rehydration following Raquin et al. (2002) is also given. N is the number of seedlings analyzed with the microsatellite markers. Paternity M, Paternity H, and Selfed are, respectively, the number of seedlings assigned to the male pollen donor, the number of seedlings assigned to the hermaphrodite pollen donor, and the number of selfed seedlings

 
Microsatellite analysis
A total of 146 seedlings were analyzed with microsatellite markers to check paternity. Table 1 summarizes the distribution of seedlings over the various pollination treatments. All seven viable seedlings resulting from pollination with a hermaphrodite pollen donor were analyzed to verify whether they were sired by the putative donor or resulted from pollen contamination. A sample of seedlings from the male pollen donor treatment was analyzed and for the pollen competition treatment, a sample of offspring from each pollinated branch was genotyped.

Leaves of parent trees and young seedlings were collected and frozen at –80°C in the laboratory before DNA extraction. Total DNA was extracted either from 100 mg of material using the DNeasy Plant Mini Kit (Qiagen, Courtaboeuf, France) or from 50 mg of material using the DNeasy 96 Plant Kit (Qiagen). Among the microsatellite markers isolated on Fraxinus excelsior by Brachet et al. (1999) and Lefort et al. (1999) , six loci were used: M2–30, FEMSATL 4, 11, 12, 16, and 19. The 20 µL of polymerase chain reaction (PCR) mixture contained 15 ng of template DNA for the parents and 30 ng for the seedlings, 90 µmol/L of dNTP, 0.375 µmol/L of each primer, 1.5 µL of 10x buffer, and 0.375 units of Taq polymerase (Q-Biogene, Illkirch, France). For the locus FEMSATL 12, 0.375 mmol/L of MgCl2 was also added. Amplification reactions were carried out as described in Brachet et al. (1999) and Lefort et al. (1999) . The PCR products were separated by electrophoresis in 6% polyacrylamide gels and visualized by silver staining according to Streiff and Lefort (1997) .

Statistical analyses
A mixed partially nested ANOVA model using JMP 5.0 software (SAS, 1995 ) was used to test the effect of pollen donor identity (nested within pollination treatment), recipient identity (nested within pollination treatment), and pollination treatment (three levels: male, hermaphrodite, pollen mixture) on fruit set.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Male fertilities of hermaphrodites and males
The molecular analysis of 143 of the 146 seedlings revealed no paternity inconsistent with the genotype of the experimental pollen donor, and the other three seedlings had genotypes consistent with selfing, giving no evidence for pollen contamination. Hermaphrodites were thus capable of siring seed, although their male fertility was lower than that of males (see below) and we found the first evidence to our knowledge for partial self-compatibility of Fraxinus excelsior hermaphrodites.

No significant differences were observed between pollen donors (nested within pollination treatment; F3,10 = 0.24, P = 0.87) or between hermaphrodite recipients (nested within pollination treatment; F9,10 = 0.82, P = 0.61), so we carried out a simplified ANOVA that detected a significant effect of pollination treatment on fruit set per pollinated branch (Welch unequal variance; F2,11 = 14.44, P = 0.0008). Multiple comparisons separated hermaphrodite donors from the other two pollination treatments, with male pollen donors siring 10 times more fruits than hermaphrodites (Fig. 1).



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  		Fig. 1. Mean number of fruit per cross (+1 SD) after different pollination treatments on four hermaphrodite recipients (see Table 1 ). x H, pollination using pollen from hermaphrodite donors; x M, pollination using pollen from male donors; x (M + H), pollination using a pollen mixture from one hermaphrodite donor and one male donor. Means associated with the same lowercase letter were not significantly different (nonparametric multiple comparisons, P < 0.05)

 
Male and hermaphrodite seed siring success in pollen competition
Of the 107 outcrossed seedlings analyzed, 106 were sired by the male and only one by the hermaphrodite pollen donor (Fig. 2). In our controlled conditions of pollen competition, the two Fraxinus excelsior males generally excluded the two hermaphrodite pollen donors from siring seed.



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  		Fig. 2. An example of a 6% polyacrylamide gel after silver staining at the microsatellite locus M2-30. Mo, the hermaphrodite recipient tree H3; M, the male pollen donor M1; H, the hermaphrodite pollen donor H1; lanes 1–21, the progeny obtained with this mixture pollen treatment (M1 + H1). Allelic sizes are given in base pairs. As no allele is shared between the three heterozygote parents at locus M2-30, paternity could be unambiguously attributed to the male pollen donor for each seedling

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
We found that (1) hermaphrodites are male-fertile and partially self-compatible, (2) in single donor pollinations, male pollen donors have a greater seed siring success than hermaphrodites, and (3) in pollen competition conditions, male donors almost always exclude hermaphrodites from ovule fertilization.

The two pure hermaphrodites used in our controlled crosses both successfully sired seed. However, the very low fruit set and the few viable embryos obtained from these single-donor pollinations suggest far lower pollen fertility of hermaphrodites than males. Indeed, we found a 10-fold male fertility advantage for male pollen donors over hermaphrodites that was further accentuated under pollen competition conditions, where males sired almost all analyzed seeds. Male advantage in fertilization success, but not of this magnitude, is known in other androdioecious species (Ishida and Hiura, 1998 ; Dommée et al., 1999 ; Vassiliadis et al., 2000 ).

Low fertilization success of hermaphrodites could result either from a poor male function of this sex phenotype or from genetic incompatibility between the few individuals tested, since it is possible that the few hermaphrodite donors and recipients shared common incompatibility alleles. These two points remain to be elucidated, for example by examining pollen tube growth in two-donor pollinations to assess pollen quality of both sexual forms and by performing additional crosses between genetically distant individuals.

The three selfed offspring found in the pollen competition treatment suggest that Fraxinus excelsior is partially self-compatible despite general failure of fruit production following selfing (Morand et al., 2002 ). Although we can now assert that common ash seems partially self-compatible under certain pollination regimes, selfing rates in natural populations remain to be assessed.

In natural conditions where several pollen donors compete for ovule fertilization, male reproductive success of hermaphrodites may be very low in Fraxinus excelsior. In Phillyrea angustifolia, however, where the relative male fertilities of males and hermaphrodites were assessed in single-donor pollinations and in a natural population, single donor fertilization success did not predict relative siring success of males vs. hermaphrodites (Vassiliadis et al., 2000 , 2002 ). These results emphasize the importance of assessing relative male reproductive success of hermaphrodites under natural conditions. Thus, the next step in our study of the functional mating system of Fraxinus excelsior will be to perform a paternity analysis in a natural population using the available microsatellite markers.

If the very high advantage in fertility of males over hermaphrodites is verified in natural populations of common ash, the maintenance of a male function in hermaphrodite individuals becomes a puzzle with two types of explanation. First, hermaphrodites may be functionally male fertile, but able to reproduce only in the absence of competing males, for example in populations composed of only hermaphrodites and females. This might be the case in newly colonized forest gaps or open habitats, if the numerous seeds of females comprise most of the seed rain. Although to date the genetic basis of sex determination in this species is unknown, there appears to be a strong genetic component as individuals of the same clone have similar sex phenotype (M.-E. Morand-Prieur and C. Raquin, personal observation). If female or hermaphrodite progenies are more likely to segregate female and hermaphrodite offspring than male ones, newly founded populations may contain few or no males. Secondly, pollen production and the relics of male fertility may represent a stage in the transition from hermaphroditism towards dioecy in this species. In fact, the low male fertility of hermaphrodites can be considered as a female-biased functional gender, as defined in Lloyd (1980) .

In conclusion, in Fraxinus excelsior, male individuals have higher fertilization success than do hermaphrodites both alone and in competition. The question of the maintenance of male function in hermaphrodites needs further investigation and requires paternity analysis under field conditions. The resolution of this question will help to define more precisely the mating system of this species (polygamy in the strict sense, trioecy, or subdioecy) and allow us to better understand it from an evolutionary point of view.


   FOOTNOTES
 
1 The authors thank P. Bertolino, O. Cudelou and O. Jonot for laboratory work. The first author acknowledges an FCPR grant from the French Ministry of Agriculture (FMA). The ENGREF institution from the FMA provided financial support. Back

2 Author for reprint requests (marie-elise.morand{at}ese.u-psud.fr ) Back


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TOP
 ABSTRACT
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 MATERIALS AND METHODS
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 DISCUSSION
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