The evolution and maintenance of monoecy and dioecy in Sagittaria latifolia (Alismataceae)

Plant species rarely exhibit both monoecious and dioecious sexual systems. This limits opportunities to investigate the consequences of combined versus separate sex function on mating patterns and genetic variation and the analysis of factors responsible for the evolution and maintenance of the two sexual systems. Populations of the North American clonal aquatic Sagittaria latifolia are usually either monoecious or dioecious and often grow in close geographic proximity. We investigated mating patterns, genetic structure, and relationships between the two sexual systems using allozyme variation in populations from southern Ontario, Canada. As predicted, selfing rates in monoecious populations (n = 6, mean = 0.41) were significantly higher than in dioecious populations (n = 6, mean = 0.11). Moreover, marker-based estimates of inbreeding depression (delta) indicated strong selection against inbred offspring in both monoecious (mean delta = 0.83) and dioecious (mean delta = 0.84) populations. However, the difference in selfing rate between the sexual systems was not reflected in contrasting levels of genetic variation. Our surveys of 12 loci in 15 monoecious and 11 dioecious populations revealed no significant differences in the proportion of polymorphic loci (P), number of alleles per locus (A), or observed and expected heterozygosity (H(o) and H(e), respectively). Strong inbreeding depression favoring survival of outcrossed offspring may act to maintain similar levels of diversity between monoecious and dioecious populations. Despite geographical overlap between the two sexual systems in southern Ontario, a dendrogram of genetic relationships indicated two distinct clusters of populations largely corresponding to monoecious and dioecious populations. Reproductive isolation between monoecious and dioecious populations appears to be governed, in part, by observed differences in habitat and life history. We suggest that selfing and inbreeding depression in monoecious populations are important in the transition from monoecy to dioecy and that the maintenance of distinct sexual systems in S. latifolia is governed by interactions between ecology, life history, and mating.     

Chloroplast haplotype variation among monoecious and dioecious populations of Sagittaria latifolia (Alismataceae) in eastern North America

Aquatic plants commonly have extensive geographical distributions, implying few restrictions to dispersal. Here we investigate the postglacial history of an aquatic plant with contrasting sexual systems (monoecy and dioecy), which are predicted to affect dispersal ability. We examined the distribution of cpDNA haplotypes using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) among 76 populations (32 monoecious, 38 dioecious, two mixed and four undetermined populations) of Sagittaria latifolia sampled throughout eastern North America. We also use these data to investigate the polarity of the evolutionary transition between monoecy and dioecy. Using PCR-RFLP, we identified eight cpDNA haplotypes. All haplotypes were found in unglaciated areas of the species' range, clustered primarily in the southeastern United States, providing evidence that glacial refugia probably occurred in this area. Genetic diversity (hT) was more than six times greater among monoecious compared to dioecious populations. All seven of the haplotypes for which the sexual system could be determined were represented among monoecious populations. In contrast, only four haplotypes were detected in dioecious populations and 94% of individuals from dioecious populations possessed a single haplotype. Monoecious populations possessing this widespread haplotype were restricted to the southern portion of the range, indicating that dioecy probably originated in this region and then spread northwards. The distribution of cpDNA haplotypes in dioecious populations represents a subset of the variation found in monoecious populations, a pattern expected if dioecy has evolved from monoecy in S. latifolia.     

Sex determination and the evolution of dioecy from monoecy in Sagittaria latifolia (Alismataceae)

The role of mutations of small versus large effect in adaptive evolution is of considerable interest to evolutionary biologists. The major evolutionary pathways for the origin of dioecy in plants (the gynodioecy and monoecy-paradioecy pathways) are often distinguished by the number of mutations involved and the magnitude of their effects. Here, we investigate the genetic and environmental determinants of sex in Sagittaria latifolia, a species with both monoecious and dioecious populations, and evaluate evidence for the evolution of dioecy via gynodioecy or monoecy-paradioecy. We crossed plants of the two sexual systems to generate F1, F2 and backcross progeny, and grew clones from dioecious populations in low-and high-fertilizer conditions to examine sex inconstancy in females and males. Several lines of evidence implicate two-locus control of the sex phenotypes. In dioecious populations sex is determined by Mendelian segregation of alleles, with males heterozygous at both the male- and female-sterility loci. In monoecious populations, plants are homozygous for alleles dominant to male sterility in females and recessive to female sterility in males. Experimental manipulation of resources revealed sex inconstancy in males but not females. These results are consistent with predictions for the evolution of dioecy via gynodioecy, rather than the expected monoecy-paradioecy pathway, given the ancestral monoecious condition.     

Trade-offs between clonal and sexual reproduction in Sagittaria latifolia (Alismataceae) scale up to affect the fitness of entire clones

? Many plants combine sexual reproduction with vegetative propagation, but how trade-offs between these reproductive modes affect fitness is poorly understood. Although such trade-offs have been demonstrated at the level of individual shoots (ramets), there is little evidence that they scale up to affect genet fitness. For hermaphrodites, reproductive investment is further divided between female and male sexual functions. Female function should generally incur greater carbon costs than male function, which might involve greater nitrogen (N) costs. ? Using a common garden experiment with diclinous, clonal Sagittaria latifolia we manipulated investment in reproduction through female and male sex functions of 412 plants from monoecious and dioecious populations. ? We detected a 1?:?1 trade-off between biomass investment in female function and clonal reproduction. For male function, there was no apparent trade-off between clonal and sexual reproduction in terms of biomass investment. Instead, male function incurred a substantially higher N cost. ? Our results indicate that: trade-offs between investment in clonal propagation and sexual reproduction occur at the genet level in S.?latifolia; and sexual reproduction interferes with clonal expansion, with investment in female function limiting the quantity of clonal propagules produced, and investment in male function limiting the nutrient content of clonal propagules.     

Clonal genetic structure and diversity in populations of an aquatic plant with combined vs. separate sexes

Clonality is often implicated in models of the evolution of dioecy, but few studies have explicitly compared clonal structure between plant sexual systems, or between the sexes in dioecious populations. Here, we exploit the occurrence of monoecy and dioecy in clonal Sagittaria latifola (Alismataceae) to evaluate two main hypotheses: (i) clone sizes are smaller in monoecious than dioecious populations, because of constraints imposed on clone size by costs associated with geitonogamy; (ii) in dioecious populations, male clones are larger and flower more often than female clones because of sex‐differential reproductive costs. Differences in clone size and flowering could result in discordance between ramet‐ and genet‐based sex ratios. We used spatially explicit sampling to address these hypotheses in 10 monoecious and 11 dioecious populations of S. latifolia at the northern range limit in Eastern North America. In contrast to our predictions, monoecious clones were significantly larger than dioecious clones, probably due to their higher rates of vegetative growth and corm production, and in dioecious populations, there was no difference in clone size between females and males; ramet‐ and genet‐based sex ratios were therefore highly correlated. Genotypic diversity declined with latitude for both sexual systems, but monoecious populations exhibited lower genotypic richness. Differences in life history between the sexual systems of S. latifolia appear to be the most important determinants of clonal structure and diversity.     

Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae)

The flowers and inflorescences of animal-pollinated dioecious plants are generally small and inconspicuous in comparison with outcrossing cosexual species. The net benefits of an attractive floral display may be different for dioecious compared to cosexual populations because dioecious species experience a more severe reduction in pollen delivery when pollinators forage longer on fewer individuals. Here, we develop a model that predicts the decrease in pollen delivery in dioecious relative to cosexual populations from female-female, female-male and male-male visit sequences as the number of individuals visited varies. To evaluate the predictions of our model we conducted a common garden experiment with dioecious and monoecious (cosexual) arrays of the insect-pollinated herb Sagittaria latifolia. We find that, although increasing the advertisements of floral rewards (i.e. increasing floral display) attracts more pollinators to individuals, the probability that these pollinators subsequently deliver pollen to neighbouring plants depends on sexual system. Because the number of individual plants visited per foraging trip did not increase significantly with floral display, the relative pollination success of dioecious versus monoecious populations decreases with increased floral display. We propose that this could explain why dioecy is strongly correlated with reduced floral display among angiosperm species.     

Genetic variation in Ecballium elaterium (Cucurbitaceae): Breeding system and geographic distribution

Dioecy, the separation of sexes, has arisen independently many times in the course of angiosperm evolution. Avoidance of inbreeding is clearly involved in the evolution of dioecy, and as a consequence we predict that dioecious populations should maintain higher levels of genetic variation than closely related nondioecious populations. We tested that prediction by comparing allozymic variation in two closely related taxa, the monoecious and dioecious subspecies of the Mediterranean cucurbit, Ecballium elaterium. Thirteen polymorphic loci were screened for seeds sampled from 10 monoecious and 13 dioecious populations spanning the geographic ranges of the subspecies in Spain. The dioecious subspecies showed strikingly greater allelic diversity and heterozygosity than the monoecious subspecies. A hierarchical F-statistic analysis clearly demonstrated considerable genetic variation within populations for the dioecious populations, whereas for the monoecious populations almost all genetic variation resulted from differences among populations. The general pattern of homozygosity within monoecious populations suggests that they are highly inbred. In order to assess historical influences on current patterns of genetic variation, we conducted a genetic-distance analysis. The observed relationship between genetic distance and geographic distance between populations supports the hypothesis that the subspecies' current allopatric distributions on the Iberian Peninsula are the result of separate waves of colonization from the north (monoecious) and south (dioecious).     

Isolation and characterization of 11 microsatellite markers from Sagittaria latifolia (Alismataceae)

We developed 11 microsatellite loci for Sagittaria latifolia, an aquatic plant common to wetlands of North America. From an (AG)-enriched library, we identified 66 unique microsatellite sequences for which primers could be designed. Twenty-two loci reliably amplified a clear single band of expected size, and 11 loci were scoreable and polymorphic. For these 11 loci, we genotyped a monoecious and a dioecious population, yielding four to 14 alleles per locus. Three loci exhibited significant linkage disequilibrium leaving eight independent variable loci. Eight loci also amplified in four other Sagittaria species. These microsatellite loci will be useful to compare genetic structure among monoecious and dioecious populations of S. latifolia.     

The role of hybridization in the evolution of sexual system diversity in a clonal,aquatic plant

The stable coexistence within populations of females, males, and hermaphrodites (subdioecy) is enigmatic because theoretical models indicate that maintenance of this sexual system involves highly restricted conditions. Subdioecy is more commonly interpreted as a transitory stage along the gynodioecious pathway from hermaphroditism to dioecy. The widespread, North American, aquatic plant Sagittaria latifolia is largely composed of monoecious or dioecious populations; however, subdioecious populations with high frequencies of hermaphrodites (mean frequency = 0.50) characterize the northern range boundary of dioecy in eastern North America. We investigated two hypotheses for the origin of subdioecy in this region. Using polymorphic microsatellite loci, we evaluated whether subdioecy arises through selection on standing genetic variation for male sex inconstancy in dioecious populations, or results from hybridization between monoecious and dioecious populations. We found evidence for both pathways to subdioecy, although hybridization was the more common mechanism, with genetic evidence of admixture in nine of 14 subdioecious populations examined. Hybridization has also played a role in the origin of androdioecious populations in S. latifolia, a mechanism not often considered in the evolution of this rare sexual system. Our study demonstrates how hybridization has the potential to play a role in the diversification of plant sexual systems.     

Dioecy,more than monoecy,affects plant spatial genetic structure: the case study of Ficus

In this analysis, we attempt to understand how monoecy and dioecy drive spatial genetic structure (SGS) in plant populations. For this purpose, plants of the genus Ficus were used as a comparative model due to their particular characteristics, including high species diversity, variation in life histories, and sexual systems. One of the main issues we assessed is whether dioecious fig tree populations are more spatially genetically structured than monoecious populations. Using the Sp statistic, which allows for quantitative comparisons among different studies, we compared the extent of SGS between monoecious and dioecious Ficus species. To broaden our conclusions we used published data on an additional 27 monoecious and dioecious plant species. Furthermore, genetic diversity analyses were performed for two monoecious Ficus species using 12 microsatellite markers in order to strengthen our conclusions about SGS. Our results show that dioecy, more than monoecy, significantly contributes to SGS in plant populations. On average, the estimate of Sp was six times higher for dioecious Ficus species than monoecious Ficus species and it was two times higher in dioecious than monoecious plant species. Considering these results, we emphasize that the long‐distance pollen dispersal mechanism in monoecious Ficus species seems to be the dominant factor in determining weak spatial genetic structure, high levels of genetic diversity, and lack of inbreeding. Although Ficus constitute a model species to study SGS, a more general comparison encompassing a wider range of plants is required in order to better understand how sexual systems affect genetic structure.     

Patterns of plant sexual systems in subtropical evergreen broad-leaved forests in Ailao Mountains,SW China

Aims Sexual systems influence many components of the ecology and evolution of plant populations and have rarely been documented in subtropical evergreen broad-leaved forests (SEBLF). Here we report frequency distribution and ecological correlates of plant sexual systems in SEBLF at Ailao Mountains, and compare our results with that of tropical and cool temperate forests.Methods We examine the sexual systems of 703 species of woody angiosperms belonging to 103 families and 296 genera based on a comprehensive survey of SEBLF at Ailao Mountains Natural Reserve. Information of plant sexual systems and ecological traits were mainly based on published literatures and specimens as well as our field observations. The associations between plant sexual system and ecological traits were assessed with chi-square tests.Important findings Among these species, 60.2% were hermaphroditic, 15.8% were monoecious and 24.0% were dioecious. The percentage of dioecious sexual system among tree species (22.2%) in SEBLF was comparable to those of tropical tree floras, but much higher than those of temperate forests at North America. The percentage of monoecious sexual system among tree species (30.1%) in SEBLF was higher than that of tropical tree floras, but much lower than those of temperate forests at North America. Monoecy was significantly associated with the tree growth form and was relatively common in temperate genera. Dioecy was significantly associated with fleshy fruits and monoecy was significantly associated with dry fruit type in SEBLF. The high percentage of diclinous sexual systems (monoecy and dioecy) in SEBLF may be associated with the origin of the flora and the prevalence of relatively small inconspicuous flowers of the forests in the Oriental Region.     

Sexual Systems and Ecological Correlates in an Azonal Tropical Forests, SW China

Unlike the seriate lowland rain forests in SE Asia, the tropical vegetation of Xishuangbanna (SW China) has developed in habitats with comparatively lower temperatures and precipitation. Consequently, although most of the families and genera of the flora are components of tropical ecosystems, many have reached their distribution limits in latitude. Selection pressures on sexual systems in these environments may be different from that experienced in lowland tropical regions. Here, we examine the sexual systems of 685 species of flowering plants belonging to 109 families and 356 genera based on 42 plots with a total area of 15.4 ha and compare our results with surveys of sexual systems from other tropical ecosystems. Among these species, 60.6 percent were hermaphroditic, 14.3 percent were monoecious, and 25.1 percent were dioecious. The percentage of dioecious sexual system among tree species (26.1%) was similar or higher than that of other tropical tree floras. Monoecy was significantly associated with the tree growth form and was relatively common in seasonal forest vegetation. Sexual systems involving unisexual flowers (dicliny) are particularly well represented in the tropical forests of Xishuangbanna accounting for 39.4 percent of all species surveyed. This pattern may be associated with the prevalence of relatively small inconspicuous flowers in the tropical forests of SE Asia and their correlation with diclinous sexual systems generally.     

The genetics of sex determination in stinging nettle (<Emphasis Type="Italic">Urtica dioica</Emphasis>)

Urtica dioica (“stinging nettle”) includes both dioecious and monoecious forms. In most sexually dimorphic angiosperm species, the genetic mechanisms of sex determination are completely unknown. The few species that include both monoecious and dioecious forms provide an unusual opportunity to examine the genetic mechanisms that underlie the separation of sexual functions, through crossing experiments and analysis of progeny segregation. Our focus is on the genetic mechanisms distinguishing monoecious and dioecious forms of U. dioica. A complicated picture of sex determination in this species has resulted from crosses between dioecious and monoecious subspecies, as well as between dioecious and monoecious forms of the same subspecies. Most significant is evidence for a maternal influence on sex determination and for the possibility of gynodioecy as an intermediate stage in the evolutionary pathway to dioecy. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Reproductive biology in a tropical shrubland of Venezuelan Guayana

Plant sexual systems were evaluated in a tropical shrubland community of Venezuelan Guayana. Of 89 plant species, 73.0% were hermaphrodite, 12.4% monoecious, 10.1 % submonoecious, and 4.5 % dioecious. Temporal variation of sexual expression showed that hermaphrodite species were mostly adichogamous and monoecious, submonoecious species dichogamous (protandrous andprotogynous). Herkogamy was an important mechanism promoting cross-pollination. Of 38 hermaphrodite species, 39.5 % were herkogamous. Plant sexual systems were not associated with life form. Most species were pollinated mostly by large and medium-size bees. Pollinator specificity and pollen load transportation, were higher for monoecious species than for hermaphrodite, submonoecious and dioecious ones. Both pollinator specificity and pollen transportation were not significantly different among representatives of the latter three sexual systems. Plant sexual systems were significantly associated with dispersal syndromes; dioecious species had bird-dispersal syndromes, the other sexual systems mostly anemochory, epizoochory and endozoochory; but many hermaphrodites were anemochorous.     

Genetic correlations with floral display lead to sexual dimorphism in the cost of reproduction

In dioecious plants, females typically invest more biomass in reproduction than males and consequently experience stronger life-history trade-offs. Sexual dimorphism in life history runs counter to this pattern in Silene latifolia: females acquire less carbon and invest more biomass in reproduction, but males pay a higher cost of reproduction. The species is sexually dimorphic for many traits, especially flower number, with males producing many, small flowers compared to females. We tested whether the cost of reproduction is higher in males because flower number, which we presume to be under sexual selection in males, is genetically correlated with traits that would affect life-history trade-offs. We performed artificial selection to reduce the sexual dimorphism in flower size and looked at correlated responses in ecophysiological traits. We found significant correlated responses in total vegetative mass, leaf mass, leaf thickness, and measures of CO(2) exchange. Individuals in the many-and-small-flowered selection lines did not grow as large or invest as much biomass in leaves, and their leaves exhibited an up-regulated physiology that shortened leaf life span. Our results are consistent with the hypothesis that genetic correlations between floral display and ecophysiological traits lead to a higher cost of reproduction for males.     

The evolution of males: support for predictions from sex allocation theory using mating arrays of sagittaria latifolia (alismataceae)

Investment in male function should often yield diminishing fitness returns, subjecting the evolution of male phenotypes to substantial constraints. In plants, the subdivision of male function via the gradual presentation of pollen might minimize these constraints by preventing the saturation of receptive stigmas. Here, we report on an investigation of (1) patterns of investment in male function by plants in hermaphroditic (monoecious) and dioecious populations of Sagittaria latifolia, and (2) patterns of siring success by males versus hermaphrodites in experimental mating arrays. We show that in natural populations, males from dioecious populations had greater investment in male function than hermaphrodites in monoecious populations. However, as a proportion of total flower production, males presented substantially fewer flowers at once than hermaphrodites. In comparison with hermaphrodites, therefore, males prolonged the period over which they presented pollen. In mating arrays comprised of females, males, and hermaphrodites, siring success by males increased linearly with flower production. This finding is consistent with the existence of a linear gain curve for male function in S. latifolia and supports the idea that the gradual deployment of male function enables plants to avoid diminishing returns on the investment in male function.     

Sex expression in EgyptianThymelaea hirsuta (Thymelaeaceae) populations

The sex expression inThymelaea hirsuta was assessed in five habitats in the western Mediterranean desert of Egypt. The survey over two main flowering periods indicated that the sexual expression of this plant is complex and labile. Beside the dioecious male and female states, five monoecious states were detected. The dioecious states are more abundant and less labile. There is a clear shift from monoecious towards dioecious states and in general favour of males from the first (late autumn) to the second (late winter) flowering period. These results are discussed in view of the adaptive theories and evolution.     

Hybridization, polyploidy, and evolutionary transitions between monoecy and dioecy in Bryonia (Cucurbitaceae)

Correns's 1903 (Berichte der Deutschen Botanischen Gesellschaft 21: 133-147) crosses between a monoecious and a dioecious species of Bryonia revealed the simple Mendelian inheritance of dioecy and provided the first instance of an XY sex determination system in any organism. Bryonia ranges from the Canary Islands to Central Asia and comprises seven dioecious and three monoecious species; its closest relative, Ecballium elaterium, has dioecious and monoecious populations. We used chloroplast (cp) and nuclear (nr) gene phylogenies to infer sexual system evolution in Bryonia. We also tested for associations between sexual system and ploidy level, based on published and original chromosome counts. Conflicts between cp and nr topologies imply that the dioecious hexaploid B. cretica arose from hybridization(s), probably involving the dioecious diploids B. dioica, B. syriaca, and/or B. multiflora. A tetraploid dioecious endemic on Corsica and Sardinia probably originated from B. dioica via autopolyploidy. While the cp phylogeny resolves few species relationships, the nr tree implies at least two evolutionary changes in sexual system. There is no correlation between sexual system and ploidy level. Molecular clocks suggest that the deepest divergence, between a species on the Canary Islands and the ancestor of all remaining species, occurred ca. 10 million years ago.     

Population dynamics of species with gynogenetic sibling species

Models are formulated for the population dynamics of a monoecious or dioecious species with an all-female parthenogenetic sibling species which is also gynogenetic. Continuous, deterministic reproduction and mortality, a stationary age distribution, random mating, and limited sexual competence for all individuals are posited. It is also supposed that in the dioecious case males do not distinguish between true and gynogenetic females. Similarly, hermaphrodites do not differentiate hermaphrodites and gynogens. The model implies that extinction is highly likely in the dioecious situation, but much less so in the monoecious one. Empirical evidence is reviewed and related to the assumptions and conclusions.     

Fitness and sexual response to population density in Daphnia pulex

1. The switch between asexual and sexual reproduction is an important fitness component in cyclically parthenogenetic populations as it is the key to persistence in unstable habitats and because it influences population genetic characteristics such as linkage disequilibrium and population genetic structure.
2. Genetic variation for sexual and asexual reproductive rate ( R _C) was examined, under varying population density, in Daphnia pulex sampled from a rockpool system and two other distinct European localities.
3. Density affected the switch to sexual behaviour, as found in other studies and reduced R _c. Production of males was not correlated with sexual reproduction, promoting outcrossing.
4. Genetic variation was found for the response to density, both within and between populations. There was substantial variation within the rockpools despite their demographic instability, indicating rapid recovery of life-history variation or maintenance during bottlenecks.