Male sterility, fitness gain curves and the evolution of gender specialization from distyly in Erythroxylum havanense

The evolution of dioecy from a monomorphic hermaphroditic condition requires two mutations, one producing females and one producing males. Conversely, a single mutation sterilizing one sexual function in one morph of distylous species would result in functional dioecy because such a mutation also affects the complementary function in the other morph. In this study, we tested these ideas with Erythroxylum havanense, a distylous species with morph-biased male sterility. Based on sex allocation theory we evaluated whether the invasion of thrum females is favoured over the maintenance of this morph cosexuals. Completely male sterile thrum plants obtained higher fitness returns than hermaphrodites or partial male sterile individuals of the same morph, thus favouring the invasion of female thrum plants. We concluded that because fruit production of pin individuals depends on the pollen produced by thrum plants, the invasion of thrum females would result on the evolution of functional dioecy.     

Evolution of habitat-dependent sex allocation in plants: superficially similar to, but intrinsically different from animals

Because pollen disperses and ovules do not, a basic difference in dispersal abilities of male and female gametes exists in plants. With an analytical model, we show that the combination of such sex-biased dispersal of gametes and variation of habitat quality results in two opposite selective forces acting on the evolution of sex allocation in plants: (i) a plant should overproduce pollen in good patches and overproduce ovules in poor patches in order to equilibrate secondary sex ratios of gametes after pollen dispersal; (ii) a plant should overproduce ovules in good patches and overproduce pollen in poor patches in order to increase the likelihood that its progeny establishes in good patches. Our theoretical results indicate that the evolution of habitat-dependent sex allocation should be favoured in plants, in a direction that depends on the relative dispersal ability of pollen and seeds. We also show that superficially similar predictions obtained for habitat-dependent evolutionarily stable sex allocation in animals actually result from a completely different balance between the two underlying evolutionary forces.     

ATTRACTIVE STRUCTURES AND THE STABILITY OF HERMAPHRODITIC SEX EXPRESSION IN FLOWERING PLANTS

Plant attributes serving both male and female sex functions are thought to favor hermaphroditic breeding systems over systems where sex expression is separated between individuals. Morphological features used by plants to attract biotic pollinators can be considered in this light, because such “attractive” structures are prerequisite for both pollen donation and receipt. A model involving allocation of a limiting resource between attractive structures benefiting both sex functions, structures benefiting male function only, and structures benefiting female function only, is constructed and analyzed using the evolutionary stable strategy (ESS) approach. Contrary to expectation, conditions resulting in large allocation to attractive structures tend to destabilize hermaphroditism, although the effect is slight. Substantial asymmetry in the benefits accruing to male and female fertility for a given investment in pollinator attraction produces more pronounced effects, reducing the parameter space in which hermaphroditism is expected. Results of this model are used to assess the importance of “accelerating gain” curves previously suggested for the evolution of dioecy in flowering plants. Accelerating gains associated with fruit production and dispersal represent female function only, and can be sufficient to initiate evolution toward dioecy. Accelerating gains associated with pollinator attraction may contribute to the evolution of separate sexes only if male function benefits from increased investment in attractive structures at a disproportionate rate compared to female function. Even in this instance, though, hermaphroditism may be evolutionarily stable.     

Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia

Stressful ecological conditions have been implicated in the evolution of separate sexes in plants. Gender dimorphic species are often found in drier habitats than their sexually monomorphic relatives, and gynodioecious populations appear closer to a dioecious state as resources, particularly water, become limiting. This pattern could result if dry conditions decrease the relative seed fitness of cosexual plants, allowing female plants to become established in monomorphic populations. We studied geographical variation in gender expression and biomass allocation among 12 monomorphic and dimorphic populations of Wurmbea dioica along a latitudinal precipitation gradient in southwestern Australia to provide insight into mechanisms by which aridity might favor transitions between sexual systems. Plants in monomorphic and dimorphic populations exhibited contrasting gender expression and patterns of biomass allocation in areas with different levels of precipitation. Among dimorphic populations, lower precipitation was associated with a higher frequency of female plants, and reduced allocation to female function by hermaphrodites during flowering. In contrast, stress conditions had no effect on female allocation at flowering in monomorphic populations. Across latitudes, unisexuals and cosexuals exhibited consistent differences in above ground traits, with cosexuals having larger leaves, taller stems and larger flowers. Although all plants were smaller under drier conditions, cosexuals decreased above ground allocation to vegetative and reproductive structures with decreasing latitude. In contrast, unisexuals increased allocation to reproduction in drier areas at the expense of below ground size. Aridity was associated with reduced flower size among all gender classes, but not with changes in flower number. These data do not support the hypothesis that resource limitation of female allocation in cosexual populations favors the establishment of gender dimorphism in W. dioica. Alternative hypotheses, involving higher selfing rates and enhanced survival of unisexuals relative to cosexuals under resource-limited conditions, are discussed as possible explanations for the origin of dioecy in W. dioica. This revised version was published online in August 2006 with corrections to the Cover Date.     

Sexual mass allocation in species with inflorescences as pollination units: a comparison between Arum italicum and Arisaema (Araceae)

Sex allocation models predict that cosexuality is stabilized by high allocation to attractive structures in pollen-limited species or by high allocation to shared structures that contribute to both genders. High investment in unilateral fixed costs favor the evolution of dioecy or gender change. With these predictions in mind, I studied sexual mass allocation at flowering in the monoecious Arum italicum (Araceae) and compared it with information available for its sex labile relative Arisaema dracontium. In A. italicum, 68% of biomass was allocated to structures believed to be involved in pollinator attraction and capture. This allocation pattern contrasts with that of Arisaema dracontium, in which 70% of biomass was allocated to scape, considered to be a unilateral fixed cost. The importance of attractive structures in A. italicum was further supported by a disproportionate increased allocation, in larger inflorescences, to the appendix (an attractive structure) compared to fertile flowers. In addition, an increase in inflorescence mass involved a disproportionate increase in mass allocation to male, rather than female, flowers. This pattern also contrasts with a size-related gender change from male to female in Arisaema species. These findings were consistent with sex allocation model predictions and shed light on the evolution of sex lability in Arisaema species.     

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.     

Size advantage for male function and size‐dependent sex allocation in Ambrosia artemisiifolia,a wind‐pollinated plant

In wind‐pollinated plants, male‐biased sex allocation is often positively associated with plant size and height. However, effects of size (biomass or reproductive investment) and height were not separated in most previous studies. Here, using experimental populations of monoecious plants, Ambrosia altemisiifolia, we examined (1) how male and female reproductive investments (MRI and FRI) change with biomass and height, (2) how MRI and height affect male reproductive success (MRS) and pollen dispersal, and (3) how height affects seed production. Pollen dispersal kernel and selection gradients on MRS were estimated by 2,102 seeds using six microsatellite markers. First, MRI increased with height, but FRI did not, suggesting that sex allocation is more male‐biased with increasing plant height. On the other hand, both MRI and FRI increased with biomass but often more greatly for FRI, and consequently, sex allocation was often female‐biased with biomass. Second, MRS increased with both height and MRI, the latter having the same or larger effect on MRS. Estimated pollen dispersal kernel was fat‐tailed, with the maximum distance between mates tending to increase with MRI but not with height. Third, the number of seeds did not increase with height. Those findings showed that the male‐biased sex allocation in taller plants of A. artemisiifolia is explained by a direct effect of height on MRS.     

Optimal sex allocation under pollen limitation

Most flowering plants are simultaneous hermaphrodites. Within species and even within local populations, sex allocation is usually highly plastic. Here, we link pollen sufficiency to the size of pollen-exchanging groups (i.e., pollen neighborhoods) and to pollen transfer efficiency, using an individual-based game-theoretic framework to determine the stable distribution of sex allocation that does not require the unrealistic assumption of infinitely large, panmictic populations. In the absence of selfing, we obtain the novel result that pollen limitation destabilizes hermaphroditism and favors separate sexes, whereas hermaphroditism remains stable without pollen limitation. With mixed mating, hermaphroditism is stable except when the fitness value of selfed offspring is less than half that of outcrossed offspring (i.e., strong inbreeding depression). In that case, the size of pollen neighborhoods, pollen transfer efficiencies, and the relative fitness of selfed offspring determine whether separate sexes or hermaphroditism is the stable outcome. The model thus predicts that separate sexes can derive from either of two ancestral states: obligate outcrossing under pollen limitation, or mixed mating (competing self-fertilization) under severe inbreeding depression. It also predicts conditions under which variance in sex-allocation among hermaphrodites within pollen exchanging groups along a gradient of pollen limitation can range from high (dioecy) to near zero (equal proportions of male and female investment).     

COMPARATIVE ANALYSES OF SEX‐RATIO VARIATION IN DIOECIOUS FLOWERING PLANTS

Dioecious plant species commonly exhibit deviations from the equilibrium expectation of 1:1 sex ratio, but the mechanisms governing this variation are poorly understood. Here, we use comparative analyses of 243 species, representing 123 genera and 61 families to investigate ecological and genetic correlates of variation in the operational (flowering) sex ratio. After controlling for phylogenetic nonindependence, we examined the influence of growth form, clonality, fleshy fruits, pollen and seed dispersal vector, and the possession of sex chromosomes on sex‐ratio variation. Male‐biased flowering sex ratios were twice as common as female‐biased ratios. Male bias was associated with long‐lived growth forms (e.g., trees) and biotic seed dispersal and fleshy fruits, whereas female bias was associated with clonality, especially for herbaceous species, and abiotic pollen dispersal. Female bias occurred in species with sex chromosomes and there was some evidence for a greater degree of bias in those with heteromorphic sex chromosomes. Although the role of interactions among these correlates require further study, our results indicate that sex‐based differences in costs of reproduction, pollen and seed dispersal mechanisms and sex chromosomes can each play important roles in affecting flowering sex ratios in dioecious plants.     

Size-dependent ESS sex allocation in wind-pollinated cosexual plants: fecundity vs. stature effects

To theoretically investigate the single and compound effects of relative fecundity and relative stature of plants on size-dependent sex allocation (SDS) in wind-pollinated cosexual species, we developed a game model and analysed ESS sex allocation of large and small plants having totally or partially different reproductive resources and different pollen and seed dispersal areas in a population. We found that e.g. when both sized plants have large pollen dispersal areas relative to their seed dispersal areas, which plants are male-biased is largely determined by relative fecundity (t) and relative size of seed dispersal area (k) of the large plants to the small plants: If t >k, large plants tend to be more male-biased even if relative size of pollen dispersal area of large to small plants (l) is smaller than k. If t相似文献   

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.     

Incidence of dioecy in relation to growth form,pollination and dispersal

Summary Recent theories predict the evolution of dioecy among higher plants, in association with certain pollination and fruit dispersal traits. However, reported associations of dioecy with pollination, dispersal and growth form traits have not distinguished the effects of each trait separately, controlling for the others. Because these traits are associated among themselves, existing analyses may involve spurious or indirect correlations. This paper reports the incidence of dioecy in a subarctic and an arctic flora, and analyzes the occurrence of dioecy among vascular plants classified jointly by growth form, floral (pollination) syndrome, and fruit (dispersal) syndrome. Dioecism is no more frequent in the arctic flora as a whole, but its incidence increases northward among woody plants. This increase is associated with an increase in the proportion of woody species having small, inconspicuous flowers, and not with the syndrome of fleshy or animal dispersed fruits. Within the floras of Alaska, California, and the Northeastern US, dioecy is markedly more frequent among woody plants and among plants having small, inconspicuous flowers, and that is the only strong statistical association of dioecy for the species of these floras. When genera and families are analyzed similarly, dioecy is also associated significantly with dispersal syndrome. Thus, among angiosperms, evidence currently does not support either an uniquely strong or exclusive association of dioecy with dispersal traits, as it does for gymnosperms (Givnish 1980). It is extremely desirable to analyze the occurrence of dioecy among taxa classified jointly by all relevant ecological traits, rather than analyzing marginal distributions.     

Tactics for male reproductive success in plants: contrasting insights of sex allocation theory and pollen presentation theory

The basic tenet of sex allocation theory is that an organism'sreproductive success, through either male or female function,can be represented as a sex-specific, monotonic, increasingfunction of the organism's investment of resources in that function.The shapes of these curves determine what patterns of resourceallocation can be evolutionarily stable. Although SA theoryhas stimulated creative thinking about plant sexual tactics,quantifying the shapes of male and female gain curves has provenso difficult that other approaches must be considered. I contrastsex allocation theory to a different, emerging viewpoint, pollenpresentation theory (PPT), which attempts to address variationin reproductive success by measuring and modeling the quantitativefates of pollen grains. Models suggest that RS through malefunction depends heavily on the packaging and gradual dispensingof pollen to pollinators, even with the amount of investmentheld constant. Many plants do deploy pollen gradually, throughmorphological and "behavioral" mechanisms that range from obviousto subtle. They may thereby influence many aspects of the evolutionof sexual modes in plants, including transitions between dioecyand cosexuality. After reviewing the main implications of themodels, I discuss recent work aimed at testing some key assumptionsand predictions by functional and comparative studies in thegenus Penstemon. Species of Penstemon conform to PPT predictionsthat bee-adapted flowers will restrict per-visit pollen availabilitymore than hummingbird-adapted flowers.     

Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism

One evolutionary pathway from plants with combined male and female functions (hermaphroditism) to those with separate sexes (dioecy) involves females coexisting with hermaphrodites (gynodioecy). The research presented here explores sex allocation in Fragaria virginiana (a gynodioecious wild strawberry), within the context of theory on the gynodioecy–dioecy transition. By growing clonally replicated plants in the greenhouse and surveying six populations in situ, I evaluated the effects of plant size, genotype, sexual identity, population of origin and female frequency on sex allocation. I found significant positive effects of plant size on most sex allocation traits studied. In addition to strong sex-specific allocation patterns, I found significant broad-sense heritabilities for all traits, suggesting that plants could respond to selection. Moreover, there was a negative genetic correlation between pollen production and fruit set per flower within hermaphrodites, lending support to a basic assumption of sex allocation theory. On the other hand, several sex allocation traits, namely pollen and ovules per flower in hermaphrodites, were positively genetically correlated, suggesting that they may act to constrain the evolution of sexual dimorphism. Populations differed in the frequency of females, and females were more prevalent on sites with lower soil moisture and where hermaphrodites were least likely to produce fruit, suggesting that females’ seed fitness relative to that of hermaphrodites may be strongly environment-dependent in this species.     

Animal dispersal dynamics promoting dioecy over hermaphroditism

Because of the separation of sexual function to male and female individuals, dioecious species have fewer pollen and seed bearers and thus experience disadvantages due to increased aggregation of reproductive function. Because of this disadvantage, models predict that dioecious females must have substantially more than twice the fecundity of hermaphrodites, yet empirical data suggest that female fecundity advantages are commonly much lower. Here, we incorporate animal foraging dynamics--and the heightened dispersal of seeds that may accompany increases in fecundity of dioecious females--into a spatially explicit mathematical model. We focus on the competition for germination sites with varying seed production, seed dispersal ability, and mortality, and we find that preferential foraging on dioecious females reduces the stringent fecundity requirements of dioecy to values in accordance with empirical estimates. This finding contributes to our understanding of the correlation between dioecy and fleshy fruits and highlights the importance of mutualist dispersers to dioecious species.     

Seed sex ratio in dioecious plants depends on relative dispersal of pollen and seeds: an example using a chessboard simulation model

Two principles are important for the optimal sex ratio strategy of plants. (1) Sib mating. Because seed dispersal is restricted, sib mating may occur which selects for a female bias in the seed sex ratio. (2) Local resource competition (LRC). If a plant produces pollen its nuclear genes are dispersed in two steps: first through the pollen and then, if the pollen is successful in fertilizing an ovule on another plant, through the seed. If the plant produces an ovule, its genes are dispersed only through the seed. By making pollen instead of ovules the offspring of a single plant is then spread out over a wider area. This reduces the chance that genetically related individuals are close together and need to compete for the same resource. The effect is the strongest if pollen is dispersed over a much wider area than seeds. Less LRC for paternally vs. maternally derived offspring selects for a male bias in sex allocation. We study the above‐mentioned opposite effects in dioecious plants (with separate male and female individuals), with maternal control over the sex ratio (fraction males) in the seeds. In a two‐dimensional spatial model female‐biased sex ratios are found when both pollen and seed dispersal are severely restricted. If pollen disperses over a wider area than seeds, which is probably the common situation in plants, the seed sex ratio becomes male‐biased. If pollen and seeds are both dispersed over a wide area, the sex ratio approaches 0.5. Our results do not change if the offspring of brother–sister matings are less fit because of inbreeding depression.     

Testing hypotheses for excess flower production and low fruit-to-flower ratios in a pollinating seed-consuming mutualism

Pollinator attraction, pollen limitation, resource limitation, pollen donation and selective fruit abortion have all been proposed as processes explaining why hermaphroditic plants commonly produce many more flowers than mature fruit. We conducted a series of experiments in Arizona to investigate low fruit-to-flower ratios in senita cacti, which rely exclusively on pollinating seed-consumers. Selective abortion of fruit based on seed predators is of particular interest in this case because plants relying on pollinating seed-consumers are predicted to have such a mechanism to minimize seed loss. Pollinator attraction and pollen dispersal increased with flower number, but fruit set did not, refuting the hypothesis that excess flowers increase fruit set by attracting more pollinators. Fruit set of natural- and hand-pollinated flowers were not different, supporting the resource, rather than pollen, limitation hypothesis. Senita did abort fruit, but not selectively based on pollen quantity, pollen donors, or seed predators. Collectively, these results are consistent with sex allocation theory in that resource allocation to excess flower production can increase pollen dispersal and the male fitness function of flowers, but consequently results in reduced resources available for fruit set. Inconsistent with sex allocation theory, however, fruit production and the female fitness function of flowers may actually increase with flower production. This is because excess flower production lowers pollinator-to-flower ratios and results in fruit abortion, both of which limit the abundance and hence oviposition rates, of pre-dispersal seed predators.     

A hypothesis for the evolution of androdioecy: the joint influence of reproductive assurance and local mate competition in a metapopulation

In a subdivided population with recurrent local extinction and re-colonisation, competition amongst related pollen or sperm to fertilise ovules or eggs (‘local mate competition’) is expected to select for female-biased sex allocation. Population turnover should also select against unisexuality in favour of self-fertile cosexuality, because males and females are unable to establish new populations on their own (‘Baker's Law’). Here I argue that androdioecy, a rare breeding system in which males co-occur with hermaphrodites, may evolve in a metapopulation under the joint action of local mate competition and Baker's Law if rates of self-fertilisation decrease with increasing population size. The hypothesis makes several predictions regarding patterns of life-history and sex allocation that are borne out by recent observations of androdioecious species in several unrelated lineages of plants and animals. This revised version was published online in July 2006 with corrections to the Cover Date.     

Pollen profile,spatial structure,and access to sex in asexual hermaphrodites

Classical cost‐of‐sex models predict the rapid fixation of asexual reproduction. Coexistence of sexuals and asexuals is common among hermaphrodite plants, however, providing asexuals with access to sex via their male function; some of the sexually reproduced progeny they sire will be asexual. The ability of asexuals to sire progeny is often hindered by the production of poor quality pollen. Using cellular automata, it is shown that decreases in pollen quality in asexuals can greatly increase the period of coexistence of sexuals and asexuals and, consequently, the cumulative contribution of sex to asex. Extensive periods of coexistence are only likely, however, if pollen and seed are dispersed locally, in which case coexistence over thousands of generations can be achieved. It is argued that, with local dispersal, the negative relationship between pollen quality and the period of coexistence of sex and asex will result in patterns of geographic parthenogenesis in which asexuals that coexist with sexuals will exhibit a poor male function, whereas asexuals with a very efficient male function will occur in exclusively asexual populations. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 954–966.     

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.