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Reproductive Biology |
2Unidad de Anatomía, Fisiología y Genética Forestal, Escuela Técnica Superior de Ingenieros de Montes, Universidad Politécnica de Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain; 3Department of Plant Sciences, University of Oxford, South Park Road, Oxford OX1 3RB UK
Received for publication July 18, 2002. Accepted for publication November 21, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: androdioecy • clonal reproduction • Dutch elm disease • riparian vegetation • seed abortion • sexual dimorphism • Ulmaceae • Ulmus minor
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and its evolutionary dynamics and maintenance have attracted much study, both empirically (reviewed in Webb, 1999
) and theoretically (reviewed in Charlesworth, 1999
). For example, maternally inherited male-sterility genes can rise in frequency in a population if the resulting females produce more seeds than their hermaphrodite counterparts (Lewis, 1941
; Lloyd, 1974
; Charlesworth and Ganders, 1979
; Frank, 1989
). For the spread of biparentally inherited male-sterility genes in fully outcrossing populations, females must produce at least twice the number of successful seeds as hermaphrodites; in partially selfing populations, the condition can be met more easily if the selfed progeny of hermaphrodites are less fit than outcrossed progeny, because females avoid self-fertilization (Lloyd, 1974
, 1975
; Ross and Weir, 1975
; Charlesworth and Charlesworth, 1978
; Ross, 1978
; Charlesworth, 1981
).
In comparison with male sterility, female sterility in hermaphroditic populations is exceedingly rare (Charlesworth, 1984
; Pannell, 2002a
). This rarity has been explained by theoretical models of androdioecy that show that males must always disperse more than twice as much successful pollen as hermaphrodites, regardless of the level of inbreeding. Indeed, self-fertilization by hermaphrodites makes the spread of female sterility more difficult because fewer ovules are available for males to fertilize (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
, 1981
; Charlesworth, 1984
). Although several cases of androdioecy have recently been described in both plants and animals, the clearest examples appear to have evolved as a result of the breakdown of dioecy (reviewed in Pannell, 2002a
), rather than from hermaphroditism.
Examples of the evolution of female sterility from hermaphroditism have come almost exclusively from the Oleaceae, where it has evolved several times independently (Wallander, 2001
). Within the family, a number of studies have addressed the dimorphism of the breeding system in Phillyrea angustifolia (Aronne and Wilcock, 1992
; Lepart and Dommée, 1992
; Traveset, 1994
; Pannell and Ojeda, 2000
; Vassiliadis et al., 2000
, 2002
). One hypothesis for the maintenance of female sterility implicates a trade-off between allocation to fruit production vs. survival, such that female-sterile individuals have more resources to allocate to tissue maintenance and carbohydrate storage than do hermaphrodites (Pannell and Ojeda, 2000
). A similar hypothesis has been suggested for the maintenance of female-sterile individuals in the Saxifragaceae. In the highly clonal arctic perennials Saxifraga cernua and S. foliolosa (Molau, 1992
; Molau and Prentice, 1992
), clonal propagation is significantly increased in plants that do not produce seeds (Molau, 1992
; but see Brochmann and Hapnes, 2001
). Nevertheless, there is still a good deal of uncertainty over the interpretation of female sterility in these long-lived species, and further research is necessary.
The possible role of trade-offs between sexual and asexual reproduction in the maintenance of female sterility with hermaphrodites generally deserves more attention, both from an empirical and a theoretical perspective. Theoretical analysis of models of sex allocation have tended to assume that a fixed quantity of resources is available for allocation to sexual reproduction and that the resources are divided optimally between male and female functions (e.g., Charnov, 1982
; but see Zhang and Jiang, 2002
). The assumption may be valid for annual species, but for long-lived plants, a hierarchy of allocation decisions may be critical, with the resources available for sexual reproduction trading off against allocation to other plant functions, such as growth, tissue maintenance, or survival. Unfortunately, there is still very little empirical data from species in which these processes might be important.
In this paper, we document and discuss a new case of the evolution of female sterility from hermaphroditism that may be associated with a trade-off in allocation between asexual reproduction and fruit production. In Spanish populations of the wind-pollinated, long-lived field elm Ulmus minor, female sterility appears to be common, and, in the limited population sample available (discussed later), female sterility is at relatively high frequencies. A detailed histological account of the ontology of seed abortion in U. minor will be published elsewhere; essentially, abnormalities in endosperm and embryo development lead to abortion and resultant female sterility in flowers that appear to have full male function. Here we examine various aspects of the reproductive biology of U. minor over 2 yr for two Spanish populations with contrasting histories and population structures. In particular, we assess the distribution of phenotypic gender, as well as the capacity for self-fertilization and pollen fertilities of hermaphrodites and female-sterile individuals in: (1) a semi-natural population of U. minor, in which there is strong evidence for clonal growth and the frequency of female-sterile ramets is about 0.75, and (2) an experimental population in which the frequency of female-sterile individuals amongst 400 genets of diverse origin is about 0.25. Our observations suggest that female sterility in U. minor may be maintained because of their enhanced capacity for clonal growth relative to seed-bearing genotypes.
Sample replication among natural populations of U. minor has been limited in our study by the dramatic decline of Spanish populations through the effects of Dutch elm disease (Tainter and Baker, 1996
); indeed, the clonally propagating population investigated here is the only known large natural stand of U. minor remaining in Spain, although small stands and isolated individuals are still widely distributed. Nevertheless, important insights into the functional significance of female sterility in U. minor can be gained by comparing patterns of sex allocation in this population with those in the experimental population, which was established from a wide sample of genetically distinct individuals largely as a conservation response to the species' decline (Solla et al., 2000
). Because only one such comparison can be made, our study must be viewed as the formulation of a hypothesis rather than as a test. Studies of sex allocation in long-lived trees are rare, and this is the first such study in Ulmus minor. We hope it will encourage further analysis in other regions of the species' distribution.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In the study area in central Spain, flowering typically occurs in late February to early March, and fruit maturation takes approximately 45–50 d. Female sterility is common in Spanish populations and is manifest in several ways (see Results).
Study sites
Ulmus minor was sampled in one natural and one planted population in central Spain. The natural population comprises about 300 adult trees on the banks of the Manzanares River, situated at Rivas-Vaciamadrid, in the province of Madrid (henceforth Rivas; 40°20' N, 3°33' W). Although probably of natural origin, this population has been used by humans for coppicing and animal fodder, probably for centuries. Vegetative regeneration through resprouting is common. The population is only mildly affected by Dutch elm disease. The planted population was established as an elm clonal bank (CB) at Centro Nacional de Mejora Genética Forestal de Puerta de Hierro, close to Madrid (40°27' N, 3°46' W). The stand comprises more than 400 elms aged between 3 and 12 yr, of which approximately 70% are yet to flower. These were samples from seeds, grafts, and cuttings collected across Spain in order to represent the genetic diversity of the species in Spain.
Sampling and analysis
We calculated the mean number of ovules per flower on the basis of ovule counts in at least 10 flowers for each of eight different inflorescences in 40 different trees at CB and in 25 trees at Rivas (2002), as well as in at least 30 flowers for each of 40 trees at CB (2001). Gynoecium necrosis was evaluated in 2002 for 50 flowers per tree for 30 individuals at CB and for 25 individuals at Rivas within three phenological phases: phase III, in which anthers are well developed but with short staminal filaments; phase IV, in which staminal filaments have begun extending; and phase V, in which pollen is dispersed.
Fruit/flower and seed/flower ratios were recorded for at least 15 inflorescences in each of 40 trees in both 2001 and 2002 at CB (same marked individuals in both years) and for 71 individuals at Rivas in 2002 (reproductive studies were not possible at Rivas in 2001 because of the absence of flower production, probably from heavy frosts). Because of the height of trees at Rivas, measurements were taken for inflorescences in the lower limbs of the tree; 12 individuals were also sampled by a climber from the uppermost limbs to control for within-tree differences in gender expression. Similarly, at CB the seed production of taller trees (>3 m) was compared between upper and lower parts of the crown.
Phenotypic gender, in terms of prospective femaleness (Lloyd, 1980
), was estimated for each individual according to the formula Gi = gi / (gi + aiE), where gi is the average number of seeds per flower, ai is the average number of stamen-bearing flowers, and E = 
gi / ai relates the prospective contribution of the measured female to male reproductive units in the population.
The potential for self-fertilization and parthenocarpy was estimated in 2002 by isolating branches within paper bags for 60 individuals at CB and 25 individuals at Rivas. Pollen production was estimated in 2002 for seven female-sterile and seven hermaphrodite individuals at CB. Pollen mass per mature anther was estimated for each plant as the difference between the mean mass of the full anther and empty anther, using 50–100 anthers per tree. Flower production in branches with the same diameter was measured for four female-sterile individuals and four hermaphrodites at CB in 2002. Pollen viability was estimated in 2002 using the flurochromatic reaction (FCR) test (Heslop-Harrison and Heslop-Harrison, 1970
) on at least 100 pollen grains per tree for seven female-sterile individuals and nine hermaphrodites at CB. Pollen tube growth was observed in 2000 in flowers of four individuals pollinated with pollen from hermaphrodite trees, using fluorescence microscopy according to Martin (1959)
.
In 2001, three controlled pollinations were conducted on an individual that presented early gynoecial necrosis, using pollen from three different individuals. Pollination occurred before the gynoecial necrosis become generalized. Pollen tubes were observed in these crosses using fluorescence microscopy.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The production of flowers with single carpels and non-ovulated pistils was low in most of the trees examined (Fig. 5); 0.65 in 2001 and 0.68 in 2002 of the studied trees at CB had fewer than 10% of the flowers lacking ovules, while none of the trees sampled at Rivas in 2002 had more than 6% of their flowers lacking ovules. In those individuals in which non-ovulated gynoecia were frequent, this lack greatly decreased their seed production (Fig. 3). Although the extent of effect varied substantially between years in some individuals, (e.g., M-IN1 produced 0.80 ovules/flower in 2001 and 0.29 ovules/flower in 2002), there was a strong correlation in the number of ovules per flower across trees between years (Pearson r = 0.428, P = 0.021, n = 29), as well as between upper and lower branches (Pearson r = 0.931, P < 0.001, n = 20).
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In general, the causes of female sterility were varied (Fig. 3). In individuals expressing pre-zygotic female sterility (i.e., non-ovulated flowers and gynoecial necrosis), female-sterile flowers were more frequent in the lower branches than in the upper. In some individuals only the uppermost branches of the crown developed samaras.
Pollen production and parthenocarpy
There were no significant differences in flower production per branch between female-sterile individuals and cosexuals (Kruskal-Wallis test, P = 1.00). Similarly, we found no differences between the two gender classes in pollen viability (FCR test, ANOVA: F1,12 = 0.00, P = 0.99) or in pollen production per anther (F1,14 = 0.52, P = 0.48). However, the number of flowers per floral bud was slightly greater in female-sterile individuals than in hermaphrodites, both in CB (female-steriles, 20.91 ± 4.35 flowers per bud; hermaphrodites, 17.40 ± 4.60 flowers per bud; F1,18 = 5.72, P = 0.03) and in Rivas (female-steriles, 25.78 ± 2.37 flowers per bud; hermaphrodites, 20.32 ± 0.76 flowers per bud; F1,25 = 24.04, P = 0.00).
Observations of pollen germination on stigmas using fluorescence microscopy confirmed that pollen from hermaphroditic trees was functional. Self-fertilization was rare, suggesting self-incompatibility for U. minor (see also Mittempherger and La Porta, 1991
): in 32 of the 40 studied genotypes at CB in 2002, seed set after self-pollination was uniformly less than 0.01; in six other individuals, seed set was less than 0.05; only two individuals, both clones from the same locality, had higher levels of seed set after selfing, with values of 0.17 and 0.19. These low values contrasted strongly with the results of controlled crosses performed over several years in breeding trials at CB, where higher rates of full seed set have been routinely observed. For example, in the period 1999–2000 the percentage of full seed in controlled crosses in which cosexual individuals were used as female parental was 46.5 (López-Almansa, 2002
).
Parthenocarpy (fruit development without ovule fertilization) was absent at Rivas and rare at CB in 2002, although two individuals produced parthenocarpic fruits in up to half the flowers. These fruits were generally smaller than those with developed embryos.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). However, the finding of a high incidence of female sterility in Spain would appear to be robust.
There is a general tendency in the Ulmaceae (sensu stricto, Song et al., 2001
) towards the production of female-sterile flowers, with species in three of its six genera described as andromonoecious (Tutin et al., 1964
; Letduzey, 1968
; Dottori, 1991
) and the remaining genera as generally polygamous (Hutchinson, 1967
). In Phyllostylon rhamnoides, an andromonoecius species, the flowers in the lower limbs of the trees present abortive gynoecia, whereas the flowers in the upper limbs are hermaphroditic (Dottori, 1991
), similar to the pattern we have observed in U. minor, where pre-zygotic female sterility is generally more frequent in the lower branches. Thus, gender characteristics appear to be phylogenetically conserved within the family. However, whereas andromonoecy described in these other species constitutes a monomorphic strategy (see Sakai and Weller, 1999
), the tendency towards separate sexes has reached an extreme in the bimodal distribution of gender displayed by U. minor. Similar between-species variation has been documented in the genus Solanum (Symon et al., 1979
). However, whereas in Solanum pollen-producing "hermaphrodite" morphs in cryptically dioecious populations are functionally female only (Anderson, 1979
; Anderson and Symon, 1989
; Knapp et al., 1998
), in U. minor the hermaphrodites disperse pollen capable of fertilizing ovules.
There were several different causes of reduced female fertility in U. minor. These have not been investigated in detail, but both genetic (pre- and post-zygotic) and ecological/environmental factors appear to contribute. Similarly, diverse mechanisms underlying the loss of sex have been documented in northern populations of the North American aquatic clonal plant Decodon verticillatus (Eckert et al., 1999
; Dorken and Eckert, 2001
), where low seed set was the result of the inability of pistils to support pollen tube growth. Although it seems possible that female fertility in U. minor may have been lost as a result of weak selection maintaining it, as suggested for D. verticillatus, female sterility in D. verticillatus generally affected all individuals in northern populations of the species' range, whereas in the populations of U. minor investigated here, female sterility gave rise to two broad gender classes, one of which included trees with high levels of fertility. This suggests that fertility in U. minor may be maintained by selection.
Evolutionary models have shown that female sterility is difficult to explain in a population of functional hermaphrodites (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1984
), a fact that is reflected in the exceptional rarity of androdioecy. These models emphasize that, in the absence of gender-specific viability differences, female-sterile individuals can only be maintained in a population if they sire more than twice as many successful offspring as do their hermaphroditic counterparts (reviewed in Pannell, 2002a
). In U. minor, we could identify no differences in the amount or viability of pollen produced in anthers of hermaphrodites vs. female-sterile individuals, and although floral buds have approximately 25% more flowers in female-sterile individuals than in cosexuals, it seems unlikely that female-sterile ramets produce twice the pollen that hermaphrodite ones do.
An important difference between the characteristics of U. minor and the assumptions made by current models concerns the nature of the individual. Theoretical analysis implicitly assumes genetically discrete individuals and makes predictions that depend on trade-offs between allocation to male function, female function, and viability or flowering intensity (Lloyd, 1975
; Charlesworth and Charlesworth, 1978
; Charlesworth, 1984
). In contrast, U. minor is a potentially clonal species that can spread vegetatively by sprouting from roots. We might expect sex allocation to depend also on a trade-off between allocation to sexual vs. asexual reproduction (Delph et al., 1993
; Westley, 1993
; Olejniczak, 2001
). Models for the maintenance of androdioecy do not consider the implications of clonality, but our observations suggest that, in the case of U. minor, these implications may be important. In a similar context, Leslie and Kline (1996
) argued for the importance of vegetative reproduction in the maintenance of a high proportion of female-sterile strains of a filamentous fungus.
Conditions that are ideal for the establishment of U. minor seedlings are likely to occur only rarely, usually following massive river floods that clear vegetation and produce a fertile muddy seed bed of alluvial deposits, as for U. davidiana var. japonica (Seiwa, 1997
) and other riparian species such as Populus nigra (Barsoum, 2001a
, b
) or Salix alba (Barsoum, 2001b
). It is possible that infrequent periodic floods would lead to a burst of successful sexual reproduction and the establishment of a new cohort of genets from seeds. Assuming that the gene(s) for female sterility are transmitted biparentally at nuclear loci, fewer than 50% of these seedlings would be expected to show female-sterile phenotypes, regardless of the frequency of female-sterile parents in the population. This fact suggests that the reproductive system of U. minor may exist in a dynamic equilibrium between periodic sexual reproduction following flooding and clonal proliferation during the intervening years when seedling establishment is not favored. Under the realistic assumption that flower production is proportional to biomass, at least in sexually mature individuals, the greater clonal spread of female-sterile genets would effectively increase their pollen production and siring success relative to that of hermaphrodites, contributing to their maintenance.
There are several reasons to believe that female-sterile individuals of U. minor may be maintained as a result of a trade-off between sexual and asexual reproduction. First, the great proliferation of female-sterility in the natural population we studied is difficult to account for using models that ignore clonal reproduction. Second, the spatial distribution of individuals was highly clumped with respect to gender, with the concentration of seed-producing trees around the margins of the population, suggesting local clonal proliferation. This clonality also appeared to be reflected in the reduced variation in floral traits in the natural population at Rivas. Finally, mature embryos of U. minor are rich in protein (J. C. López-Almansa, E. C. Yeung, and L. Gil, unpublished manuscript) and are thus probably expensive to produce, particularly considering that growth is likely to be more limited by nitrogen and phosphorous availability than by water, which is abundant in the riparian habitats occupied by this species. This situation, and the fact that samaras are photosynthetic, also suggests that carbon is unlikely to limit seed production. The substantial savings made through pre-zygotic sterility and seed abortion might thus lead to enhanced clonal proliferation of female-sterile genets (Westley, 1993
; Delph, 1999
). This hypothesis awaits testing through comparisons of clonal proliferation between hermaphrodic and female-sterile individuals.
Under the discussed scenario, should U. minor be regarded as androdioecious? Androdioecy strictly refers to a phenotypic gender polymorphism, with populations comprising two distinct classes of individual: female-sterile individuals or functional males; and hermaphroditic individuals, which transmit genes through both their male and female functions (Pannell, 2002b
). Our limited data would appear to meet these criteria. Hermaphrodites produce and disperse substantial quantities of viable, functional pollen, suggesting that they may contribute genes through both sexual functions and that they are therefore not likely to be functional females in cryptically dioecious populations (Mayer and Charlesworth, 1991
). Paternity analyses within populations are necessary to establish whether hermaphrodites do in fact sire seeds (Vassiliadis et al., 2002
). The largely consistent gender expression of individuals over 2 yr further argues against a reproductive system in which a single phenotypic class comprises individuals with labile gender. Moreover, four female-sterile individuals have been monitored for four consecutive years and never produced seeds (data not shown), although more samples are needed (cf. Jones and Gliddon, 1999
; Manicacci and Despres, 2001
). Nor are female-sterile individuals obviously just small individuals. Finally, the gender distribution in the two populations we have studied in detail is clearly bimodal, even though some members of the female-sterile class did produce a few seeds. Such gender inconstancy is common in plants (Lloyd and Bawa, 1984
), but the bimodality would suggest an underlying polymorphic strategy (cf. Thomson et al., 1989
). Muenchow (1998)
referred to a population of Sagittaria lancifolia subsp. lancifolia that displayed continuous yet bimodal variation in sex allocation as sub-androdioecious.
It is difficult to evaluate the actual relative importance of sexual or vegetative reproduction under natural conditions. The natural environment of U. minor probably included not only its current location in the narrow riparian strip at Rivas (and was common more widely before the spread of Dutch elm disease), but also the adjacent meadows, which were cleared for agriculture. Prior to flood mitigation management through dam and canal construction, more frequent large-scale flooding over these meadows might have allowed more frequent establishment of elm seedlings, leading to a different balance between clonal and sexual reproduction than probably occurs in less disturbed sites.
In conclusion, our study of U. minor has revealed a pattern of widespread female sterility maintained in clonally propagating populations that also contain female-fertile hermaphrodites. We hypothesize that low levels of seed production may be maintained through a trade-off in allocation between sexual and clonal reproduction; this hypothesis needs to be tested through comparisons of clonal growth of seed-producing vs. female-sterile individuals. Data on mating patterns and paternity analysis would also be valuable. Unfortunately, answering these questions poses major practical challenges in a long-lived clonal tree. In the case of U. minor, the practical difficulties are compounded by the demise of its natural populations by the effects of Dutch elm disease. With the current unprecedented decline of biodiversity in general, whatever its ultimate causes, it is sobering to consider the extent to which our ability to study important and interesting evolutionary processes will increasingly be compromised in similar ways.
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FOOTNOTES |
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4 Present address: Universidad Católica de Ávila, C/ Canteros s/n, 05005 Ávila, Spain
5 Author for reprint requests (lgil{at}montes.upm.es
)
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LITERATURE CITED |
|---|
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Anderson G. J. D. E. Symon 1989 Functional dioecy and andromonoecy in Solanum. Evolution 43: 204-219[CrossRef][ISI]
Aronne G. C. C. Wilcock 1992 Breeding system of Phillyrea latifolia L. and Phillyrea angustifolia L.: evidence for androdioecy. Giornale Botanico Italiano 126: 263.
Barsoum N. 2001a Regeneration: requirements and promotion measures. In F. Lefèvre, N. Barsoum, B. Heinze, D. Kajba, P. Rotach, S. M. G. de Vries, and J. Turok [eds.], EUFORGEN Technical Bulletin: In situ conservation of Populus nigra, 16–24. International Plant Genetic Resources Institute, Rome, Italy
Barsoum N. 2001b Relative contribution of sexual and asexual regeneration strategies in Populus nigra and Salix alba during the first years of establishment on a braided gravel bed river. Evolutionary Ecology 15(4): 255-279[CrossRef][ISI]
Brochmann C. A. Hapnes 2001 Reproductive strategies in some arctic Saxifraga (Saxifragaceae), with emphasis on the narrow endemic S. svalbardensis and its parental species. Botanical Journal of the Linnean Society 137: 31-49[CrossRef]
Charlesworth D. 1981 A further study of the problem of the maintenance of females in gynodioecious species. Heredity 46: 27-39
Charlesworth D. 1984 Androdioecy and the evolution of dioecy. Biological Journal of the Linnean Society 23: 333-348
Charlesworth D. 1999 Theories of the evolution of dioecy. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 33–60. Springer-Verlag, Heidelberg, Germany
Charlesworth D. B. Charlesworth 1978 A model for the evolution of dioecy and gynodioecy. American Naturalist 112: 975-997[CrossRef][ISI]
Charlesworth D. B. Charlesworth 1981 Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society 15: 57-74
Charlesworth D. F. R. Ganders 1979 The population genetics of gynodioecy with cytoplasmic-genic male-sterility. Heredity 43: 213-218[ISI]
Charnov E. L. 1982 The theory of sex allocation. Princeton University Press, Princeton, New Jersey, USA
Delph D. F. 1999 Sexual dimorphism in life history. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 149–173. Springer-Verlag, Heidelberg, Germany
Delph D. F. Y. Lu L. D. Jayne 1993 Patterns of resource-allocation in a dioecious Carex (Cyperaceae). American Journal of Botany 80: 607-615[CrossRef][ISI]
Dorken M. E. C. G. Eckert 2001 Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). Journal of Ecology 89: 339-350[CrossRef]
Dottori N. 1991 Anatomía reproductiva en Ulmaceae s.l.: 3. Esporangios, esporogénesis y gametogénesis de Phyllostylon rhamnoides y Celtis tala. Kurtziana 21: 81-110
Eckert C. G. M. E. Dorken S. A. Mitchell 1999 Loss of sex in clonal populations of a flowering plant, Decodon verticillatus (Lythraceae). Evolution 53: 1079-1092[CrossRef][ISI]
Frank S. A. 1989 The evolutionary dynamics of cytoplasmic male sterility. American Naturalist 133: 345-376[CrossRef][ISI]
Heslop-Harrison J. Y. Heslop-Harrison 1970 Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate. Stain Technology 45: 115-120[ISI][Medline]
Hutchinson J. 1967 The genera of flowering plants. Oxford University Press, Oxford, UK
Jones B. C. Gliddon 1999 Reproductive biology and genetic structure in Lloydia serotina. Plant Ecology 141: 151-161[CrossRef][ISI]
Kaul M. L. H. 1988 Male sterility in higher plants. Springer-Verlag, Berlin, Germany
Knapp S. V. Persson S. Blackmore 1998 Pollen morphology and functional dioecy in Solanum (Solanaceae). Plant Systematics and Evolution 210: 113-139[CrossRef][ISI]
Lepart J. B. Dommée 1992 Is Phillyrea angustifolia L. (Oleaceae) an androdioecious species?. Botanical Journal of the Linnean Society 108: 375-387
Leslie J. F. K. K. Klein 1996 Female fertility and mating type effects on effective population size and evolution in filamentous fungi. Genetics 144: 557-567[Abstract]
Letduzey R. 1968 Ulmacées. In A. Aubréville [ed.], Flore du Cameroun, vol. 8, 3–65. Muséum National d'Histoire Naturelle, Paris, France
Lewis D. 1941 Male sterility in natural populations of hermaphrodite plants. New Phytologist 40: 56-63[CrossRef]
Lloyd D. G. 1974 Theoretical sex ratios of dioecious and gynodioecious angiosperms. Heredity 32: 11-34[ISI]
Lloyd D. G. 1975 The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45: 325-339[CrossRef][ISI]
Lloyd D. G. 1980 Sexual strategies in plants. III. A quantitative method for describing the gender of plants. New Zealand Journal of Botany 18: 103-108
Lloyd D. G. K. S. Bawa 1984 Modification of the gender of seed plants in varying conditions. Evolutionary Biology 17: 255-336[ISI]
López-Almansa J. C. 2002 Biología de la reproducción en Ulmus minor Mill. y sus híbridos en España. Ph.D. thesis, Universidad Politécnica de Madrid, Madrid, Spain
Manicacci D. L. Despres 2001 Male and hermaphrodite flowers in the alpine lily Lloydia serotina. Canadian Journal of Botany 79: 1107-1114[CrossRef]
Martin F. W. 1959 Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 125-128[ISI][Medline]
Mayer S. S. D. Charlesworth 1991 Cryptic dioecy in flowering plants. Trends in Ecology and Evolution 6: 320-325
Mittempherger L. M. La Porta 1991 Hybridization studies in the Eurasian species of elm (Ulmus spp). Silvae Genetica 40: 237-243
Molau U. 1992 On the occurrence of sexual reproduction in Saxifraga cernua and Saxifraga foliolosa (Saxifragaceae). Nordic Journal of Botany 12: 197-203[ISI]
Molau U. H. C. Prentice 1992 eproductive system and population structure in three arctic Saxifraga spp. Journal of Ecology 80: 149-161[CrossRef]
Muenchow G. E. 1998 Subandrodioecy and male fitness in Sagittaria lancifolia subsp. lancifolia (Alismataceae). American Journal of Botany 85: 513-520[Abstract]
Olejniczak P. 2001 Evolutionarily stable allocation to vegetative and sexual reproduction in plants. Oikos 95: 156-160[CrossRef][ISI]
Pannell J. R. 2002a The evolution and maintenance of androdioecy. Annual Review of Ecology and Systematics 33: 397-425
Pannell J. R. 2002b What is functional androdioecy?. Functional Ecology 16: 862-865[CrossRef][ISI]
Pannell J. R. F. Ojeda 2000 Patterns of flowering and sex-ratio variation in the Mediterranean shrub Phillyrea angustifolia (Oleaceae): implications for the maintenance of males with hermaphrodites. Ecology Letters 3: 495-502[CrossRef][ISI]
Ross M. D. 1978 The evolution of gynodioecy and subdioecy. Evolution 32: 174-188[CrossRef][ISI]
Ross M. D. B. S. Weir 1975 Maintenance of male sterility in plant populations III. Mixed selfing and random mating. Heredity 35: 21-29[ISI]
Sakai A. K. S. G. Weller 1999 Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 1–31. Springer-Verlag, Heidelberg, Germany
Seiwa K. 1997 Variable regeneration behaviour of Ulmus davidiana var. japonica in response to disturbance regime for risk spreading. Seed Science Research 7: 195-207[ISI]
Solla A. M. Burón S. Iglesias L. Gil 2000 Spanish program for the conservation and breeding of elms against DED. In C. P. Dunn [ed.], The elms: breeding, conservation, and disease management, 295–303. Kluwer Academic, Dordrecht, The Netherlands
Song B. H. X. Q. Wang F. Z. Li D. Y. Hong 2001 Further evidence for paraphyly of the Celtidaceae from the chloroplast gene matK. Plant Systematic and Evolution 228: 107-115[CrossRef]
Symon D. E. R. N. Lester A. D. Skelding 1979 Sex forms in Solanum (Solanaceae) and the role of pollen-collecting insects. In J. G. Hawkes [ed.], The biology and taxonomy of the Solanaceae, 385–397. Academic Press, New York, New York, USA
Tainter F. H. F. A. Baker 1996 Principles of forest pathology. John Wiley and Sons, New York, New York, USA
Thomson J. D. K. R. Shivanna J. Kenrick R. B. Know 1989 Sex expression, breeding system, and pollen biology of Ricinocarpos pinifolius: a case of androdioecy?. American Journal of Botany 76: 1048-1059[CrossRef][ISI]
Traveset A. 1994 Reproductive biology of Phillyrea angustifolia L. (Oleaceae) and effect of galling-insects on its reproductive output. Botanical Journal of the Linnean Society 114: 153-166[CrossRef]
Tutin T. G. V. H. Heywood N. A. Burges D. H. Valentine S. M. Walters D. A. Webb 1964 Flora Europaea. Cambridge University Press, Cambridge, UK
Vassiliadis C. J. Lepart P. Saumitou-Laprade P. Vernet 2000 Self-incompatibility and male fertilization success in Phillyrea angustifolia (Oleaceae). International Journal of Plant Sciences 161: 393-402[CrossRef][ISI][Medline]
Vassiliadis C. Saumitou-Laprade J. Lepart F. Viard 2002 High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia. Evolution 56: 1362-1373[CrossRef][ISI][Medline]
Wallander E. 2001 Evolution of wind pollination in Fraxinus (Oleaceae): an ecophylogenetic approach. Ph.D. thesis, Göteborg University, Göteborg, Sweden
Webb C. J. 1999 Empirical studies: evolution and maintenance of dimorphic breeding systems. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 61–95. Springer-Verlag, Heidelberg, Germany
Westley L. C. 1993 The effect of inflorescence bud removal on tuber production in Helianthus tuberosus L. (Asteraceae). Ecology 74: 2136-2144[CrossRef][ISI]
Zhang D. Y. X. H. Jiang 2002 Size-dependent resource allocation and sex allocation in herbaceous perennial plants. Journal of Evolutionary Biology 15: 74-83[CrossRef][ISI]
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