How geitonogamous selfing affects sex allocation in hermaphrodite plants

Does the mode of self-pollination affect the evolutionarily stable allocation to male vs. female function? We distinguish the following scenarios. (1) An ‘autogamous’ species, in which selfing occurs within the flower prior to opening. The pollen used in selfing is a constant fraction of all pollen grains produced. (2) A species with ‘abiotic pollination’, in which selfing occurs when pollen dispersed in one flower lands on the stigma of a nearby flower on the same plant (geitonogamy). The selfing rate increases with male allocation but a higher selfing rate does not mean a reduced export of pollen. (3) An ‘animal-pollinated’ species with geitonogamous selfing. Here the selfing rate also increases with male allocation, but pollen export to other plants in the population is a decelerating function of the number of simultaneously open flowers. In all three models selfing selects for increased female allocation. For model 3 this contradicts the general opinion that geitonogamous selfing does not affect evolutionarily stable allocations. In all models, the parent benefits more from a female-biased allocation than any other individual in the population. In addition, in models 2 and 3, greater male allocation results in more local mate competition. In model 3 and in model 2 with low levels of inbreeding depression, hermaphroditism is evolutionarily stable. In model 2 with high inbreeding depression, the population converges to a fitness minimum for the relative allocation to male function. In this case the fitness set is bowed inwards, corresponding with accelerating fitness gain curves. If the selfing rate increases with plant size, this is a sufficient condition for size-dependent sex allocation (more allocation towards seeds in large plants) to evolve. We discuss our results in relation to size-dependent sex allocation in plants and in relation to the evolution of dioecy.     

The evolution of dioecy, heterodichogamy, and labile sex expression in Acer

The northern hemisphere tree genus Acer comprises 124 species, most of them monoecious, but 13 dioecious. The monoecious species flower dichogamously, duodichogamously (male, female, male), or in some species heterodichogamously (two morphs that each produce male and female flowers but at reciprocal times). Dioecious species cannot engage in these temporal strategies. Using a phylogeny for 66 species and subspecies obtained from 6600 nucleotides of chloroplast introns, spacers, and a protein-coding gene, we address the hypothesis (Pannell and Verdú, Evolution 60: 660-673. 2006) that dioecy evolved from heterodichogamy. This hypothesis was based on phylogenetic analyses (Gleiser and Verdú, New Phytol. 165: 633-640. 2005) that included 29-39 species of Acer coded for five sexual strategies (duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous trioecy, dichogamous subdioecy, and dioecy) treated as ordered states or as a single continuous variable. When reviewing the basis for these scorings, we found errors that together with the small taxon sample, cast doubt on the earlier inferences. Based on published studies, we coded 56 species of Acer for four sexual strategies, dioecy, monoecy with dichogamous or duodichogamous flowering, monoecy with heterodichogamous flowering, or labile sex expression, in which individuals reverse their sex allocation depending on environment-phenotype interactions. Using Bayesian character mapping, we infer an average of 15 transformations, a third of them involving changes from monoecy-cum-duodichogamy to dioecy; less frequent were changes from this strategy to heterodichogamy; dioecy rarely reverts to other sexual systems. Contra the earlier inferences, we found no switches between heterodichogamy and dioecy. Unexpectedly, most of the species with labile sex expression are grouped together, suggesting that phenotypic plasticity in Acer may be a heritable sexual strategy. Because of the complex flowering phenologies, however, a concern remains that monoecy in Acer might not always be distinguishable from labile sex expression, which needs to be addressed by long-term monitoring of monoecious trees. The 13 dioecious species occur in phylogenetically disparate clades that date back to the Late Eocene and Oligocene, judging from a fossil-calibrated relaxed molecular clock.     

Labile sex expression in plants

The range of environmental sex determination and sex changes throughout plant taxa from bryophytes and pteridophytes to spermatophytes is reviewed. Lability in sex expression occurs in many plant taxa but only in homosporous pteridophytes is labile sex the rule. Among angiosperms, labile sex appears to be more common among dioecious and monoecious plants than among hermaphrodites. However, hermaphrodites can control allocation to male and female functions by varying the relative emphasis on pollen and ovules. A majority of plants with labile sex expression are perennials, which indicates that flexibility in sex is more important for species with long life cycles. Environmental stress, caused by less-than-optimal light, nutrition, weather or water conditions, often favours maleness. The extreme lability in the sex expression of homosporous pteridophytes is suggested to be related primarily to the mating systems.     

Differences in female reproductive success between female and hermaphrodite individuals in the subdioecious shrub Eurya japonica (Theaceae)

Subdioecy is thought to occupy a transitional position in the gynodioecy–dioecy pathway, explaining one of the evolutionary routes from hermaphroditism to dioecy. Quantifying any female reproductive advantage of females versus hermaphrodites is fundamental to examining the spectrum between subdioecy and dioecy; however, this is challenging, as multiple interacting factors, such as pollen limitation and resource availability, affect plant reproduction. We compared the female reproductive success of females and hermaphrodites via a field experiment in which we hand‐pollinated individuals of the subdioecious shrub Eurya japonica of similar size growing under similar light conditions. Effects of pollen limitation and seed quality were also evaluated through comparing the results of hand‐ and natural‐pollination treatments and performing additional laboratory and greenhouse experiments. Overall, females had higher fruit set and produced heavier fruit and more seeds than hermaphrodites, and these results were more pronounced for hand‐pollinated than for natural‐pollinated plants of both sexes. We also found that seeds naturally produced by females had a higher mean germination rate. These results indicate that females had a pronounced advantage in female reproductive success under conditions of no pollen limitation. The sexual difference in the degree of pollen limitation suggests a pollinator‐mediated interaction, whereas the higher female reproductive success of females even under natural conditions implies that E. japonica is a good model species for elucidating the later stages of the gynodioecy–dioecy pathway.     

Pollination intensity influences sex ratios in dioecious Rumex nivalis, a wind-pollinated plant

Determining the mechanisms governing sex-ratio variation in dioecious organisms represents a central problem in evolutionary biology. It has been proposed that in plants with sex chromosomes competition between pollen tubes of female- versus male-determining microgametophytes (certation) causes female-biased primary sex ratios. Experimental support for this hypothesis is limited and recent workers have cast doubt on whether pollen-tube competition can modify sex ratios in dioecious plants. Here we investigate the influence of variation in pollination intensity on sex ratios in Rumex nivalis, a wind-pollinated alpine herb with strongly female-biased sex ratios. In a garden experiment, we experimentally manipulated pollination intensity using three concentric rings of female recipient plants at different distances from a central group of male pollen donors. This design enabled us to test the hypothesis that increasing pollen load size, by intensifying gametophyte competition, promotes female-biased sex ratios in R. nivalis. We detected a significant decline in pollen load at successive distance classes with concomitant reductions in seed set. Sex ratios of progeny were always female biased, but plants at the closest distance to male donors exhibited significantly greater female bias than more distant plants. The amount of female bias was positively correlated with the seed set of inflorescences. Hand pollination of stigmas resulted in approximately 100-fold higher stigmatic pollen loads than wind-pollinated stigmas and produced exceptionally female-biased progenies (female frequency = 0.96). Our results are the first to demonstrate a functional relation between stigmatic pollen capture, seed set, and sex ratio and suggest that certation can contribute towards female-biased sex ratios in dioecious plants.     

Floral biology and pollination mechanisms of four Mexico-endemic Fuchsia species with contrasting reproductive systems

Aims The evolution of the outstanding variation of reproductive systems in angiosperms has been considered an important driver of lineage diversification. Closely related hermaphroditic and dioecious species with biotic pollination provide the opportunity to study and compare traits related to pollinator attraction and their consequences on reproductive components. A higher predictability of pollination syndromes is expected in dioecious species, which are dependent on pollinators, than in self-compatible hermaphroditic taxa. Dioecious species may suffer pollen limitation depending on the quality of floral rewards and the kind and abundance of pollinators, whereas no pollen limitation is expected in hermaphroditic species with autonomous self-pollination. Additionally, in the absence of pollen limitation, more or better seeds are expected in dioecious species, according to the sexual specialization hypothesis.Methods In natural populations of the hermaphroditic Fuchsia fulgens and Fuchsia arborescens and dioecious Fuchsia parviflora and Fuchsia obconica, all endemic to Mexico, we first described flower phenology, flower production and longevity and nectar volume and concentration. Then, we evaluated the correspondence between floral visitors and pollination syndromes. In hermaphrodite plants, we determined the level of herkogamy and the potential for autonomous self-pollination. Finally, we evaluated the effect of pollen limitation on fruit set and seed number and assessed seed germination for all species.Important findings In contrast to our prediction, dioecious species did not show a higher correspondence between pollination syndromes and floral visitors than did hermaphrodites; however, male flowers exhibited a higher correspondence than female flowers. No pollen limitation was detected in dioecious species, for which visitation rate did not differ between male and female flowers. The hermaphroditic F. fulgens showed pollen limitation for seed number, despite the presence of autonomous selfing. Fruit set from autonomous pollination was higher in F. arborescens, which showed a lower level of herkogamy compared with F. fulgens. Finally, dioecious species produced fewer but heavier seeds compared with hermaphrodite species. Although Fuchsia is classified as an outcrossing genus, both hermaphroditic species showed autonomous self-pollination. The heavier but lower number of seeds per fruit in dioecious species may be related to the more efficient resource allocation expected from sexual specialization. This could play an important role in the evolution of dioecy; however, a comparative phylogenetic approach is required to confirm this hypothesis.     

Floral sex ratios, disease and seed set in dioecious Silene dioica

1 In the dioecious, perennial herb Silene dioica , the density of pollen donors in a population is determined by overall plant density, the sex ratio and the proportion of plants infected with the anther-smut fungus Microbotryum violaceum , which results in permanent sterility of both male and female plants.
2 Pollinators ( Bombus spp.) were found to prefer male flowers and to avoid diseased flowers. This may result in an overall lower visitation frequency and increased risk for pollen limitation in populations with a low density of males or a high incidence of disease.
3 Compared with open-pollinated flowers, hand pollination resulted in a significant increase in the number of seeds produced per fruit in populations with an experimentally reduced proportion of males (25% and 50% male flowers) but not in a naturally male-dominated population (75% male flowers). Seed production per plant was increased by hand pollination only in the most female-dominated population. Because the floral sex ratio is often male-biased, resources rather than pollen availability are likely to set the upper limit for total seed production per individual in most healthy populations of S. dioica.
4 There was a negative relationship between seed set and incidence of disease across 22 populations in both years of a field study. However, there was no consistent difference between the responses of highly diseased populations (incidence 30–56%) and populations with a low disease incidence (incidence 0–8%) to hand pollination.
5 In a greenhouse experiment with cloned hand-pollinated females, the presence of spores on healthy flowers was found to reduce seed set significantly. In highly diseased populations, therefore, the frequent deposition of spores by flower visitors onto remaining healthy plants may decrease seed production below the potential level determined by resources or pollen availability.     

Environmental conditions affect sex expression in monoecious, but not in male and female plants of Urtica dioica

Urtica dioica is a sub-dioecious plant species, i.e. males and females coexist with monoecious individuals. Under standard conditions, seed sex ratio (SSR, fraction of males) was found to vary significantly among seed samples collected from female plants originating from the same population (0.05–0.76). As a first step, we investigated the extent to which SSR and sex expression of male, female, and monoecious individuals is influenced by external factors. We performed experiments to analyse: (1) whether the environment of a parental plant affects the sex ratio (SR) of its offspring, (2) whether SSR can be affected by environmental conditions before flowering, and (3) whether sex expression of male, female and monoecious plants that have already flowered can be modified by environmental conditions or by application of phyto-hormones. Within the range of our experimental design, SSR was not influenced by external factors, and gender in male and female plants was stable. However, sex expression in monoecious plants was found to be labile: flower sex ratio (FSR, fraction of male flowers) differed considerably between clones from the same individual within treatments, and increased toward 100% maleness under benign conditions. These results provide strong evidence that monoecious individuals are inconstant males, which alter FSR according to environmental circumstances. In contrast, we consider sex expression in male and female individuals to be solely genetically based. The observed variation in SSR between maternal parents cannot be explained by sex-by-environment interactions.     

植物性别决定的研究进展

通过回顾近年来以多种植物为材料进行的性染色体观察,性别决定基因及调控方式的研究,对植物性别决定的机制进行了初步探讨,从而可以看出不同植物具有不同的性别决定机制：对于有性染色体的植物而言,目前已经从Y染色体上分离和鉴定了许多与雄性发育紧密相关的基因;部分性别决定基因和调控序列已利用构建减法文库,诱导突变体等方法从一些植物中获得。此外,还有研究表明,DNA脱甲基化,以及某些激素(如赤霉素、乙烯、Ace)都对植物的性别决定有重要作用。     

Effects of inbred/outbred crosses on progeny sex ratio in Silene latifolia (Caryophyllaceae)

Sex ratio polymorphism has been extensively studied in Silene latifolia, but it is neither known whether inbreeding (which is likely to occur under field conditions) affects it, nor which of the proposed mechanisms (Y degeneration, X-linked drive) is more important. Both mechanisms predict reduced pollen performance. In this study, females were crossed with pollen from related and unrelated males in single-donor and two-donor crosses, and the sex ratio of offspring (n = 866, 60 crosses), sons'in vitro pollen germination and sex ratios in parental families were scored. Flowers receiving only unrelated pollen produced a significant excess of sons. Sex ratios were not significantly correlated between generations. Sons'in vitro pollen germination was significantly negatively correlated with the 'sex-ratio phenotype' of maternal grandfathers, but not of fathers. This generation leap may be consistent with X-linked determinants because Y-linked determinants alone cannot explain it (grandfathers, fathers and sons share the same Y chromosome). Further work is required, but inbreeding and limited dispersal may lead to local accumulation of biasing factors, a process potentially countered by conditional shifts to produce more sons in pure outbred crosses.     

Simulated herbivory enhances leaky sex expression in the dioecious herb Mercurialis annua

Background and AimsPlant reproductive traits are widely understood to be responsive to the selective pressures exerted by pollinators, but there is also increasing evidence for an important role for antagonists such as herbivores in shaping these traits. Many dioecious species show leaky sex expression, with males and females occasionally producing flowers of the opposite sex. Here, we asked to what extent leakiness in sex expression in Mercurialis annua (Euphorbiaceae) might also be plastically responsive to simulated herbivory. This is important because enhanced leakiness in dioecious populations could lead to a shift in both the mating system and in the conditions for transitions between combined and separate sexes.MethodsWe examined the effect of simulated herbivory on the sexual expression of males and females of M. annua in two experiments in which different levels of simulated herbivory led to enhanced leakiness in both sexes.Key ResultsWe showed that leaky sex expression in both males and females of the wind-pollinated dioecious herb M. annua is enhanced in response to simulated herbivory, increasing the probability for and the degree of leakiness in both sexes. We also found that leakiness was greater in larger females but not in larger males.ConclusionsWe discuss hypotheses for a possible functional link between herbivory and leaky sex expression, and consider what simulated herbivory-induced leakiness might imply for the evolutionary ecology of plant reproductive systems, especially the breakdown of dioecy and the evolution of hermaphroditism.     

Dioecy and the evolution of sex ratios in ants

Split sex ratios, when some colonies produce only male and others only female reproductives, is a common feature of social insects, especially ants. The most widely accepted explanation for split sex ratios was proposed by Boomsma and Grafen, and is driven by conflicts of interest among colonies that vary in relatedness. The predictions of the Boomsma–Grafen model have been confirmed in many cases, but contradicted in several others. We adapt a model for the evolution of dioecy in plants to make predictions about the evolution of split sex ratios in social insects. Reproductive specialization results from the instability of the evolutionarily stable strategy (ESS) sex ratio, and is independent of variation in relatedness. We test predictions of the model with data from a long-term study of harvester ants, and show that it correctly predicts the intermediate sex ratios we observe in our study species. The dioecy model provides a comprehensive framework for sex allocation that is based on the pay-offs to the colony via production of males and females, and is independent of the genetic variation among colonies. However, in populations where the conditions for the Boomsma–Grafen model hold, kin selection will still lead to an association between sex ratio and relatedness.     

Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis

Sex allocation theory predicts that reproducing individuals will increase their fitness by facultatively adjusting their relative investment towards the rarer sex in response to population shifts in operational sex ratio (OSR). The evolution of facultative manipulation of sex ratio depends on the ability of the parents to track the conditions favouring skewed sex allocation and on the mechanism controlling sex allocation. In animals, which have well-developed sensorial mechanisms, facultative adjustment of sex ratios has been demonstrated on many occasions. In this paper, we show that plants have mechanisms that allow them to evaluate the population OSR. We simulated three different conditions of population OSR by manipulating the amount of pollen received by the female flowers of a monoecious herb, and examined the effect of this treatment on the allocation to male vs. female flowers. A shortage of pollen on the stigmas resulted in a more male-skewed sex allocation, whereas plants that experienced a relatively pollen rich environment tended to produce a more female-skewed sex allocation pattern. Our results for Begonia gracilis demonstrate that the individuals of this species are able to respond to the levels of pollination intensity experienced by their female flowers and adjust their patterns of sex allocation in accordance to the expectations of sex allocation theory.     

Impact of plant flowering phenology on the cost/benefit balance in a nursery pollination mutualism,with honest males and cheating females

This study documents the flowering phenology and its potential consequences on a nursery pollination mutualism between a dioecious plant, in which honest male plants, but not cheating females, allow the specific pollinator to reproduce within inflorescences. Very few pollinators were found to emerge during plant anthesis, leading to a low (if any) potential benefit through pollen dispersal. This opens the question why male plants do not also cheat their pollinators. Female plants flowered late in the season, when many males had just achieved their own anthesis, which increased the efficiency of pollen transfer. Finally, some late‐flowering males reached their anthesis simultaneously with females, which open the possibility for pollinator to choose between honest males and cheating females. Nevertheless, female plants were found to produce fruits, even though fruit production was limited by pollen (and pollinator) supply, meaning that cheating was not entirely retaliated by the mutualistic partner.     

Evolutionary stability of sex chromosomes in snakes

Amniote vertebrates possess various mechanisms of sex determination, but their variability is not equally distributed. The large evolutionary stability of sex chromosomes in viviparous mammals and birds was believed to be connected with their endothermy. However, some ectotherm lineages seem to be comparably conserved in sex determination, but previously there was a lack of molecular evidence to confirm this. Here, we document a stability of sex chromosomes in advanced snakes based on the testing of Z-specificity of genes using quantitative PCR (qPCR) across 37 snake species (our qPCR technique is suitable for molecular sexing in potentially all advanced snakes). We discovered that at least part of sex chromosomes is homologous across all families of caenophidian snakes (Acrochordidae, Xenodermatidae, Pareatidae, Viperidae, Homalopsidae, Colubridae, Elapidae and Lamprophiidae). The emergence of differentiated sex chromosomes can be dated back to about 60 Ma and preceded the extensive diversification of advanced snakes, the group with more than 3000 species. The Z-specific genes of caenophidian snakes are (pseudo)autosomal in the members of the snake families Pythonidae, Xenopeltidae, Boidae, Erycidae and Sanziniidae, as well as in outgroups with differentiated sex chromosomes such as monitor lizards, iguanas and chameleons. Along with iguanas, advanced snakes are therefore another example of ectothermic amniotes with a long-term stability of sex chromosomes comparable with endotherms.     

Evolution of the Selfing Rate and Resource Allocation Models

Abstract First, evolutionary theories of selfing of terrestrial plants are reviewed briefly. The evolution of the selfing rate is controlled mainly by (1) the benefit of enhanced genetic relatedness to seeds and (2) the cost of lowered fitness of selfed offspring (inbreeding depression), being modified by (3) fertility assurance under pollen limitation, (4) reduced performance as pollen donor, (5) reduced expenditure to male function, and (6) lowered genetic recombination. Models of the joint evolution of selfing and inbreeding depression predict either strong outcrossing or predominant selfing. Although wind-pollinated plants fit the prediction, some animal-pollinated species have intermediate selfing rates, refuting the theory.
Second, three resource allocation models are analyzed, in which an individual plant optimally allocates limited resources to outcrossed seeds, selfed seeds, and to energy reserves for the next year. The first model explains how the number of outcrossed and selfed offspring change with plant size when they differ in dispersal distance. The second model predicts that, in a disturbed habitat, the plant is likely to be annual and to produce both selfed and outcrossed seeds; in contrast, in a stable habitat, the plant tends to be perennial and to abort selfed seeds selectively. Hand pollination may increase seed production for perennials but not for annuals. The third model explains the observed difference between animal and wind pollinated plants in the out-crossing rate pattern by the difference in the way pollen acquisition increases with investment.