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Steets, J.A., D.E. Wolf, J.R. Auld, and T.-L. Ashman (2007) The role of natural enemies in the expression and evolution of mixed mating in hermaphrodite plants and animals. Evolution 61:2043-2055 Although a large portion of plant and animal species exhibit intermediate levels of outcrossing, the factors that maintain this wealth of variation are not well understood. Natural enemies are one relatively understudied ecological factor that may influence the evolutionary stability of mixed mating. In this paper,we aim for a conceptual unification of the role of enemies in mating system expression and evolution in both hermaphroditic animals and plants. We review current theory and detail the potential effects of enemies on fundamental mating system parameters. In doing so, we identify situations in which consideration of enemies alters expectations about the stability of mixed mating. Generally,we find that inclusion of the enemy dimension may broaden conditions in which mixed mating systems are evolutionarily stable. Finally, we highlight avenues ripe for future theoretical and empirical work that will advance our understanding of enemies in the expression and evolution of mixed mating in their hosts/victims, including examination of feedback cycles between victims and enemies and quantification of mating system-related parameters in victim populations in the presence and absence of enemies.
Case, A.L., and T.-L. Ashman (2007) An experimental test of the effects of resource and sex ratio on maternal fitness and phenotypic selection in gynodioecious Fragaria virginiana. Evolution 61:1900-1911 Resources, sex ratio, and seed production by hermaphrodites covary among natural populations of many gynodioecious plant species, such that they are functionally #more dioecious# as resources become more limiting. Strong correlations among these three factors confound our understanding of their relative roles in maintaining polymorphic sexual systems. We manipulated resource availability and sex ratio and measured their effects on relative fertility and phenotypic selection through the maternal fitness of females and hermaphrodites of Fragaria virginiana. Tworesults were particularly surprising. First, hermaphrodites showed little variability in fecundity across resource treatments and showed strong positive and context-dependent selection for fruit set. This suggests that variation in hermaphrodite seed production along resource gradients in nature may result from adaptation rather than plasticity. Second, although females increased their fecundity with higher resources, their fertility was unaffected by sex ratio, which is predicted to mediate pollen limitation of females in natural populations where they are common. Selection on petal size of females was also weak, indicating aminimal effect of pollinator attraction on variation in the fertility of female plants. Hence, we found no mechanistic explanation for the complete absence of high-resource high female populations in nature. Despite strong selection for increased fruit set of hermaphrodites, both the strength of selection and its contribution to the maintenance of gynodioecy are severely reduced under conditions where females have high relative fecundity (i.e., low resources and high-female sex ratios). High relative fertility plus high female frequency means that the evolution of phenotypic traits in hermaphrodites (i.e., response to selection via seed function) should be manifested through females because most hermaphrodites will have female mothers. Fruit set was never under strong selection in females; hence, selection to increase fruit set hermaphrodites will be less effective in maintaining their fruiting ability in natural populations with low resources and high female frequency. In sum, both sex ratio and resource availability influence trait evolution indirectly#through their effects on relative fertility of the sexes and patterns of selection. Sex ratio did not impose strong pollen limitation on females but did directly moderate the outcome of natural selection by biasing the maternal sex of the next generation. This direct effect of sex ratio on the manifestation of natural selection is expected to have far greater impact on the evolution of traits, such as seed-producing ability in hermaphrodites and the maintenance of sexual polymorphisms in nature, compared to indirect effects of sex ratio on relative fertility of the sexes.
Steets, J.A., T.M. Knight, and T.-L. Ashman (2007) The interactive effects of herbivory and mixed mating for the population dynamics of Impatiens capensis. Am. Nat. 170:113-127 In this study, we examine the demographic consequences of mixed mating and explore the interactive effects of vegetative herbivory and mating system for population dynamics of Impatiens capensis, a species with an obligate mixed mating system (i.e., individuals produce both obligately selfing cleistogamous and facultatively outcrossing chasmogamous flowers). In two natural populations, we followed seeds derived from cleistogamous and chasmogamous flowers subject to different herbivory levels throughout their life cycle. Using a mating system-explicit projection matrix model, we found that mating system types differed in important vital rates. Cleistogamous individuals had higher rates of germination than did chasmogamous individuals, whereas chasmogamous individuals expressed a fecundity advantage over cleistogamous individuals. In addition, population growth was most sensitive to changes in vital rates of cleistogamous individuals, indicating the demographic importance of selfing for these populations. Herbivory also had demographic consequences; a 33%-49% reduction in herbivory caused the population growth rates to increase by 104%-132%, primarily because of effects on vital rates of selfed individuals. Our results not only uncover a novel consequence of mating system expression, that is, mating system influences population dynamics, but also shed light on the role of herbivores in maintaining mixed mating.
Ashman, T.-L., and L. Penet (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender dimorphic plant. Am. Nat. 169:595-608 Gender-dimorphic plants are often subject to sexdifferential enemy attack, but whether and how this contributes to trait evolution is unknown. To address this gap, we documented the spatiotemporal prevalence of sex-biased weevil damage in a gynodioecious strawberry. We then conducted path analysis to evaluate the direct and indirect pathways for weevils to affect female and male fertility and to mediate selection in two experimental gardens. Direct effects of weevils significantly reduced fertility and mediated selection on reproductive traits, even in the nonpreferred sex (females).Weevils significantly reduced floral display size in hermaphrodites in both gardens, and this translated into a substantial negative indirect effect on male fertility in the garden where the pathway to fertility via display was stronger. Thus, indirect effects of weevils can contribute to selection in hermaphrodites, which gain the majority of their fitness via male function. Our results also indicate that weevils often play a larger role than pollinators in shaping reproductive phenotype and thus raise the intriguing possibility that antagonists may be drivers of sexual dimorphism. Finally, our results support the view that mutualists, antagonists, and the abiotic environment should be considered when attempting to understand reproductive trait evolution in gender-dimorphic species.
Majetic, C.J., R.A. Raguso, S.J. Tonsor, and T.-L. Ashman (2007) Flower color-flower scent associations in polymorphic Hesperis matronalis (Brassicaceae). Phytochemistry 68:865-874 Floral scent emission rate and composition of purple and white flower color morphs of Hesperis matronalis (Brassicaceae) were determined for two populations and, for each, at two times of day using dynamic headspace collection and GC-MS. The floral volatile compounds identified for this species fell into two main categories, terpenoids and aromatics. Principal component analysis of 30 compounds demonstrated that both color morphs emitted more scent at dusk than at dawn. Color morphs varied in chemical composition of scent, but this differed between populations. The white morphs exhibited significant differences between populations, while the purple morphs did not. In the white morphs, one population contains color-scent associations that match expectations from classical pollination syndrome theory, where the flowers have aromatic scents, which are expected to maximize night-flying moth pollinator attraction; in the second population, white morphs were strongly associated with terpenoid compounds. The potential impact that pollinators, conserved biosynthetic pathways, and the genetics of small colonizing populations may have in determining population-specific associations between floral color and floral scent are discussed.
Knight, T.M., J.A. Steets, and T.-L. Ashman (2006) A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. Am. J. Bot. 93:271-277 Our understanding of pollen limitation depends on a realistic view of its magnitude. Previous reviews of pollen supplementation experiments concluded that a majority of plant species suffers from pollen limitation and that its magnitude is high. Here, we perform a meta-analysis and find evidence that publication bias, experimental design, and the response variable chosen all influence the magnitude of pollen limitation. Fail-safe numbers indicate that publication bias exists for some measures of pollen limitation; significant results are more likely to be published and therefore available for review. Moreover, experiments conducted on only a fraction of a plant#s flowers and reproductive episodes report ;8-fold higher effect sizes than those on all flowers produced over the entire lifetime, likely because resource reallocation among flowers and across years contributes to estimates of pollen limitation. Studies measuring percentage fruit set report higher values of pollen limitation than those measuring other response variables, such as seeds per fruit, perhaps because many plant species will not produce fruits unless adequate pollen receipt occurs to fertilize most ovules. We offer suggestions for reducing the bias introduced by methodology in pollen supplementation experiments and discuss our results in the context of optimality theory.
Steets, J.A., R. Salla, and T.-L. Ashman (2006) Herbivory and competition interact to affect reproductive traits and mating system expression in Impatiens capensis. Am. Nat. 167:591-600 As a step toward understanding how community context shapes mating system evolution, we investigated the combined role of two plant antagonisms, vegetative herbivory and intraspecific competition, for reproduction and mating system expression (relative production of selfing, cleistogamous and facultatively outcrossing, chasmogamous flowers and fruits) of Impatiens capensis. In a survey of I. capensis populations, we found that vegetative herbivory and intraspecific competition were positively correlated. In a greenhouse experiment where leaf damage and plant density were manipulated, multispecies interactions had dramatic effects on reproductive and mating system traits. Despite having additive effects on growth, herbivory and competition had nonadditive effects for mating system expression, chasmogamous fruit production, flower number and size, and cleistogamous flower production. Our results demonstrate that competitive interactions influence the effect of herbivory (and vice versa) on fitness components and mating system, and thus antagonisms may have unforeseen consequences for mating system evolution, population genetic diversity, and persistence.
Steets, J.A., J.L. Hamrick, and T.-L. Ashman (2006) Consequences of vegetative herbivory for the maintenance of intermediate outcrossing in an annual plant. Ecology 87:2717-2727 Given the occurrence of mixed mating systems among plants, a general mechanism explaining the evolution and maintenance of this condition is needed. Although numerous theoretical models predict mixed mating to be evolutionarily stable, conditions favoring intermediate selfing are often stringent and have limited applicability. Here we investigated the role of vegetative herbivory, a ubiquitous biotic factor limiting plant reproduction, in the mating system expression of Impatiens capensis (Balsaminaceae), a species with an obligate mixed-mating system (individuals produce both selfing, cleistogamous, and facultatively outcrossing, chasmogamous flowers). Herbivory reduced proportional chasmogamous reproduction partially, but not entirely, through a reduction in plant size and the strength of this effect varied among replicates. Herbivory decreased geitonogamous selfing in chasmogamous flowers via several mechanisms including reduced chasmogamous flower display size and pollinator visitation rate and altered pollinator composition. Overall, herbivory caused a decrease in whole-plant outcrossing, indicating that the effects of herbivory on proportional chasmogamous reproduction, which favor selfing, outweigh the effects on chasmogamous outcrossing rate, which favor outcrossing. Not only do our findings unravel the mechanisms underlying herbivore-mediated changes in the mating system, but they also point to the role of natural enemies in contributing to the maintenance of a mixed mating system.
Ashman, T.-L. (2006) The evolution of separate sexes: A focus on the ecological context. Pp 419-465 in The Ecology and Evolution of Flowers, Harder, L.D., and S.C.H. Barrett, Ed. Oxford University Press, Oxford Sexual-system evolution has a long rich history of theoretical study, which has guided empirical explorations and the recent expansion of ideas concerning the role of ecological context in gender separation. In this chapter, I first provide a brief overview of theoretical understanding of a prominent sexual-system transition, namely, the gynodioecy pathway for the evolution of dioecy from hermaphroditism. I then review empirical support for several predictions based on theory and use these as a springboard to both highlight the strengths of existing theory and show how its limitations have helped reveal the importance of ecological context for the evolution of dioecy. I specifically review work that suggests that harsh environments mediate sexual-system evolution via sex-differential plasticity and sizedependent allocation, as well as consider less-studied mechanisms by which resource limitation can affect sexual-system evolution, including plant#pollinator interactions, mating system, and inbreeding depression. I then address the emerging role of enemies, and of multi-species interactions, in modifying fundamental parameters of gender models and thus selection for separate sexes. In doing so, I illustrate similarities and dissimilarities between underlying mechanisms and identify areas of interaction that demand empirical investigation. I conclude with a discussion of two unresolved issues: the stability of subdioecy and the dual role of pollinators in the evolution of separate sexes.
Delph, L.F., and T.-L. Ashman (2006) Trait selection in flowering plants: how does sexual selection contribute? Integr. Comp. Biol. 46:465-472 By highlighting and merging the frameworks of sexual selection envisioned by Arnold (1994) and Murphy (1998), we discuss how sexual selection can occur in plants even though individuals do not directly interact. We review studies on traits that influence pollen export and receipt in a variety of hermaphroditic and gynodioecious plants with the underlying premise that pollination dynamics influences mate acquisition. Most of the studies reviewed found that phenotypes that enhance pollen export are in harmony with those that enhance pollen receipt suggesting that in many cases pollinator visitation rates limit both male and female function. In contrast, fewer traits were under opposing selection; but when they were, the traits most often were associated with enhancing the specific aspects of a given sex function. Our review helps clarify and illustrate why sexual selection can be a component of trait evolution in hermaphrodite plants.
Ashman, T.-L., and C.J. Majetic (2006) Genetic constraints on floral evolution: A review and evaluation of patterns. Heredity 96:343-352 The characteristics of flowers influence most aspects of angiosperm reproduction, including the agents of pollination and patterns of mating. Thus, a clear view of the forces that mediate floral phenotypic evolution is central to understanding angiosperm diversity. Here, we inform on the capacity for floral phenotype to respond to selection by reviewing published data on heritabilities and genetic correlations for several classes of floral traits (primary sexual, attraction, mating system) in hermaphroditic plants. We find significant heritability for all floral traits but also variation among them, as well as a tendency for heritability to vary with mating system, but not life history. We additionally test predictions stemming from life history theory (eg, negative covariation between male-female traits and flower size-flower number), and ideas concerning the extent and pattern of genetic integration between flowers and leaves, and between the sexes of dioecious and gynodioecious species. We find mixed evidence for life history tradeoffs. We find strong support for floral integration and its relation with floral morphology (actinomorphy vs zygomorphy) and for a decoupling of floral and vegetative traits, but no evidence that modular integration varies with floral morphology. Lastly, we find mixed evidence for a relationship between the level of sexual dimorphism in attraction traits and the between-sex correlation in gender dimorphic plants.
Vamosi, J.C., T.M. Knight, J.A. Steets, S.J. Mazer, M. Burd, and T.-L. Ashman (2006) Pollination decays in biodiversity hotspots. Proc. Natl. Acad. Sci., USA 103:956-961 As pollinators decline globally, competition for their services is expected to intensify, and this antagonism may be most severe where the number of plant species is the greatest. Using meta-analysis and comparative phylogenetic analysis, we provide a global-scale test of whether reproduction becomes more limited by pollen receipt (pollen limitation) as the number of coexisting plant species increases. As predicted, we find a significant positive relationship between pollen limitation and species richness. In addition, this pattern is particularly strong for species that are obligately outcrossing and for trees relative to herbs or shrubs. We suggest that plants occurring in species-rich communities may be more prone to pollen limitation because of interspecific competition for pollinators. As a consequence, plants in biodiversity hotspots may have a higher risk of extinction and/or experience increased selection pressure to specialize on certain pollinators or diversify into different phenological niches. The combination of higher pollen limitation and habitat destruction represents a dual risk to tropical plant species that has not been previously identified.
Cole, D.H., and T.-L. Ashman (2005) Sexes show differential tolerance to spittlebug damage and consequences of damage for multi-species interactions. Am. J. Bot. 92:1708-1713 Antagonists can play a role in sexual system evolution if tolerance or resistance is sex-dependent. Our understanding of this role will be enhanced by consideration of the effects of antagonists on other plant-animal interactions. This study determined whether the sex morphs of a gynodioecious Fragaria virginiana differ in their susceptibility and response to damage by spittlebugs and whether damage altered pollinator attraction traits or interactions with other antagonists. Tolerance, but not resistance, to spittlebugs differed between the sexes. Generally, spittlebugs were more damaging to hermaphrodites than females, a finding in accord with the hypothesis that the pollen-bearing morph is less tolerant of source-damage than the pollen-sterile morph when damage is incurred during flowering. In both sex morphs, spittlebugs reduced inflorescence height, increased petal size, but did not affect the number of open flowers per day, suggesting that the net effect of damage may be to increase pollinator attraction. Spittlebug infestation modified interactions with other antagonists in a sex-dependent manner: spittlebugs reduced attack by bud-clipping weevils in hermaphrodites but increased infection by leaf fungi in females. The complex interactions between plant sex, antagonists, and pollinator attraction documented here emphasize the importance of considering sex-differential multi-species interactions in plant sexual evolution.
Ashman, T.-L. (2005) The limits on sexual dimorphism in vegetative traits in a gynodioecious plant. Am. Nat. 166:S5-16 Gynodioecious plants exhibit modest sexual dimorphism in vegetative and phenological traits, which stands in stark contrast to pronounced dimorphism in reproductive traits. I evaluate the roles of limited genetic variation, negative genetic covariation (within and between sex morphs), and lack of gender-differential selection in contributing to minimal sexual dimorphism for these traits in Fragaria virginiana. Major findings are as follows. First, selection was sometimes differential but rarely divergent between male and female fertility modes. Second, response to selection was constrained by low genetic variation and extensive genetic covariance. In fact, covariance between traits within sex morphs appears to represent a constraint on par with that of covariance between sex morphs. Third, these constraints combine with different modes of gamete transmission to produce very different gender-specific contributions to the mean phenotypes of the next generation. Finally, predicted responses to selection for several traits are concordant with the degree and direction of dimorphism in a closely related dioecious species. In sum, this work suggests that minimal sexual dimorphism in vegetative and phenological traits is due to similar directional selection via male and female fertility combined with the constraints of low genetic variation and extensive genetic covariance both within and between sex morphs.
Knight, T., J.A. Steets, J.C. Vamosi, S.J. Mazer, M. Burd, D.R. Campbell, M. Dudash, M.O. Johnston, R.J. Mitchell, and T.-L. Ashman (2005) Pollen limitation of plant reproduction: Pattern and Process. Annu. Rev. Ecol. Evol. S. 36:467-497 Quantifying the extent to which seed production is limited by the availability of pollen has been an area of intensive empirical study over the last few decades. While theory predicts that pollen augmentation should not increase seed production, a large number of empirical studies report significant and strong pollen limitation. Here, we use a variety of approaches to examine the correlates of pollen limitation in an effort to understand its occurrence and importance in plant evolutionary ecology. In particular, we examine the role of recent ecological perturbations in influencing pollen limitation, and discuss the relation between pollen limitation and plant traits. We find that the magnitude of pollen limitation observed in natural populations depends on both historical constraints and contemporary ecological factors.
Ashman, T.-L., D.H. Cole, M. Bradburn, B. Blaney, and R.A. Raguso (2005) Scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86:2099-2105 Most flowering plants rely on animal pollinators to transfer male gametes between individuals, and thus a significant problem for gender dimorphic plants is that pollinators often avoid female flowers. Here we show for the first time that one important reason pollinators shun female flowers is because they do not smell like males. We compared emission rates and floral scent composition in a gynodioecious wild strawberry (Fragaria virginiana) where females receive half as many visits by generalist pollinators as conspecific hermaphrodites. We used floral extracts to determine the source of sexually dimorphic odor and pollinator responses. Specifically, we used extracts of whole flowers and specific floral parts in choice tests to determine that pollinators preferred the scent of hermaphrodite flowers over those of females and that this discrimination was due primarily to the scent of hermaphrodite anthers. These data conclusively show that scent can be a major driver of pollinator behavior in gender dimorphic plants. Our results also indicate that scent is an important modulator of pollinator behavior even in a small flowered, weakly scented species visited by generalist pollinators, and not just peculiar to intensely scented, deceptive, or specialized pollination systems.
Ashman, T.-L., and E.A. King (2005) Are flower-visiting ants mutualists or antagonists? A study in a gynodioecious wild strawberry. Am. J. Bot. 92:891-895 Ants are common flower visitors. but their effects on plant reproductive fitness have not often been assessed. Flower-visiting ants were studied to determine whether they are antagonists or mutalists and whether they could influence floral or breeding system evolution in gynodioecious wild strawberry (Fragaria virginiana). Ant and flying pollinator (bees/flies) access to plants was manipulated, and visitation, fruit. and seed set were assessed. Ants visited flowers of hermaphrodites more often than those of females when bees and flies were excluded, but visited the sex morphs equally when they were present. Insect class did not influence fruit or seed set of hermaphrodites. In contrast. ants had both positive and negative effects on seed set in females. Females visited only by ants had 90% of the seed set of those visited only by bees/flies. and their seed set increased with ant visitation. The spatial pattern of seed set. however. suggests that ants may also damage pistils. Lastly. in contrast to bees and flies, ants failed to increase visitation with floral display size. Suggesting that ant presence at flowers Could reduce selection on this attractive trait. Findings suggest that when in high abundance. flower-visiting ants could affect breeding system and floral evolution in this gynodioecious plant.
Case, A.L., and T.-L. Ashman (2005) Sex-specific physiology and its implications for the cost of reproduction. Pp 126-154 in Reproductive Allocation in Plants, Reekie, E., and F. Bazzaz, Ed. Elsevier Science Press, London Ashman, T.-L., T.M. Knight, J.A. Steets, P. Amarasekare, M. Burd, D. Campbell, M. Dudash, M. Johnston, S.J. Mazer, R. Mitchell, M.T. Morgan, and W. Wilson (2004) Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences. Ecology 85:2408-2421 Determining whether seed production is pollen limited has been an area of intensive empirical study over the last two decades. Yet current evidence does not allow satisfactory assessment of the frequency, causes, or consequences of pollen limitation. Here, we critically evaluate existing theory and issues concerning pollen limitation. The main conclusion is that a change in approach is needed to determine whether pollen limitation reflects random fluctuations around a pollen/resource equilibrium (sensu Haig and Westoby 1988), an adaptation to stochastic pollination environments, or a chronic syndrome caused by an environmental perturbation. We formalize and extend Haig and Westoby's conceptual model and illustrate its use in guiding research on the evolutionary consequences of pollen limitation, i.e., whether plants evolve or have evolved to ameliorate pollen limitation. This synthesis also reveals that we are only beginning to understand when and how pollen limitation at the plant level translates into effects on plant population dynamics. We highlight the need for both theoretical and empirical approaches to gain a deeper understanding of the importance of life history characters, Allee effects, and environmental perturbations in population declines mediated by pollen limitation. Lastly, our synthesis identifies a critical need for research on potential effects of pollen limitation at the community and ecosystem levels.
Steets, J.A., and T.-L. Ashman (2004) Herbivory alters the expression of a mixed-mating system. Am. J. Bot. 91:1046-1051 In this study we analyzed the mechanisms by which vegetative herbivory affects the mating system of Impatiens capensis. We conducted a survey of herbivory in natural I. capensis populations and performed a field experiment in which we manipulated leaf damage to understand the direct and indirect effects of herbivory on mating system. We found a significant exponential relationship between leaf damage and proportion of cleistogamous flowers among ten populations of I. capensis. Similarly, in the experimental manipulation, herbivory had its strongest effect on mating system by increasing the proportion of flowers and seeds that were cleistogamous. Herbivory also had transgenerational effects on mating system by causing a more severe reduction in the biomass of cleistogamous progeny relative to chasmogamous progeny. Accounting for both within-generation and transgenerational effects, the cumulative effect of leaf damage was to increase the plant reliance on fitness derived from cleistogamous progeny. Herbivory indirectly altered traits associated with mating system by reducing chasmogamous floral attraction leading to a reduction in pollinator visitation. Under the present set of experimental conditions, herbivory did not significantly reduce chasmogamous floral display size and potential for geitonogamy, nor did it result in significant changes in the composition of the pollinator fauna. Our findings are among the first to demonstrate that herbivory has consequences for mating system and should be considered a factor shaping mating system evolution.
Ashman, T.-L., D. Cole, and M. Bradburn (2004) Sex-differential resistance and tolerance to herbivory in a gynodioecious wild strawberry: Implications for floral and sexual system evolution. Ecology 85:2550-2559 We explore the effects of gender dimorphism on resistance (damage avoidance) and tolerance (growth and fitness compensation) to a flower bud clipping weevil in a gynodioecious wild strawberry. Using both natural populations and a common garden we document pervasive hermaphrodite-biased damage, and identify several floral traits associated with resistance. Lower flower number, lower pollen production per flower and earlier flowering date were associated with higher resistance. Because the sex morphs do not differ in flower number or flowering time, the presence of pollen is the main factor determining sex-differential resistance. We confirmed that simulated clipping was a good surrogate for weevil clipping, and used simulated clipping to assess sex morph- and sex function-specific tolerance. We found that females were less tolerant than hermaphrodites in terms of seed and fruit production, but the sex morphs were similarly unable to compensate fully in flower production. Hermaphrodites showed some ability to compensate in pollen/flower, but this was not large enough to offset flower losses, leading to net undercompensation for pollen/plant. We evaluated potential mechanisms for tolerance, and found that the number of reserve buds was the most consistent predictor of tolerance. Finally, we found that herbivory shifted sex expression of hermaphrodites towards greater femaleness via both plastic changes in allocation and direct effects of loss of male-functioning flowers. Our work indicates that the effects of herbivory on sexual system evolution can include sexual phenotype-biased herbivore damage, sex-dependent tolerance, as well as herbivory-induced changes in hermaphrodite sex allocation. In addition, this study suggests that pollen production is subject to selection via herbivores that opposes selection mediated by pollinators. Ashman, T.-L., and M.T. Morgan (2004) Explaining phenotypic selection on plant attractive characters: Male function, gender balance or ecological context? Proc. Roy. Soc. B Biol. Sci. 271:553-559 It is widely agreed that the flowers of hermaphrodite plants evolve in response to selection acting simultaneously through male and female sexual functions, but we know very little about the pattern of gender-specific selection. Here we review three current hypotheses for gender-specific selection by viewing them within a single phenotypic selection framework. We compile data from phenotypic selection and manipulative studies and evaluate the fit between empirical data and the hypotheses. In this preliminary analysis, we find that the neither the male function nor the gender balance hypotheses are well supported. However, the context dependence hypothesis is supported by the documented diversity of gender-specific selection and by evidence that selection through female fertility is significantly correlated with pollen limitation of seed production. Future studies contributing to our understanding of selection through male and female function in plants need to quantify and manipulate the ecological context for reproduction, as well as describe male and female fitness responses to fine scale trait manipulation.
Bernasconi, G., T.-L. Ashman, T.R. Birkhead, J.D.D. Bishop, U. Grossniklaus, E. Kubli, D.L. Marshall, B. Schmid, I. Skogsmyr, R.R. Snook, D. Taylor, I. Till-Bottraud, P.I. Ward, D. Zeh, and B. Hellriegel (2004) Evolutionary ecology of the prezygotic stage. Science 303:971-975 The life cycles of sexually reproducing animals and flowering plants begin with male and female gametes and their fusion to form a zygote. Selection at this earliest stage is crucial for offspring quality and raises similar evolutionary issues, yet zoology and botany use dissimilar approaches. There are striking parallels in the role of prezygotic competition for sexual selection on males, cryptic female choice, sexual conflict, and against selfish genetic elements and genetic incompatibility. In both groups, understanding the evolution of sex-specific and reproductive traits will require an appreciation of the effects of prezygotic competition on fitness.
Ashman, T.-L. (2004) Flower longevity. Pp 349-362 in Cell Death in Plants, Nooden, L.D., Ed. Elsevier Press, London Ashman, T.-L. (2003) Constraints on the evolution of males and sexual dimorphism: Field estimates of genetic architecture of reproductive traits in three populations of gynodioecious Fragaria virginiana. Evolution 57:2012-2025 To understand how genetic constraints may limit the evolution of males and sexual dimorphism in a gynodioecious species, I conducted a quantitative genetic experiment in a gynodioecious wild strawberry, Fragaria virginiana. I estimated and compared genetic parameters (narrow-sense heritabilities, between-trait and between-sex genetic correlations, as well as phenotypic and genetic variance-covariance matrices) in the two sex morphs from three populations grown in a common field garden. I measured pollen and ovule production per flower, petal size, fruit set, and flower number. My major findings are as follows. (1) The presence of a phenotypic trade-off between pollen production and fruit set in hermaphrodites reflects a negative genetic correlation in the narrow sense that is statistically significant when pooled across populations. (2) The main constraints on the evolution of males are low genetic variation for pollen per flower and strong positive correlations associated with ovule number (e.g., between pollen and ovules in hermaphrodites, and between ovules in hermaphrodites and females). (3) Traits with the lowest levels of sexual dimorphism (ovule number and flower number) have the highest between-sex genetic correlations suggesting that overlap in the expression of genes in the sex morphs constrains their independent evolution. (4) There are significant differences in G matrices between sex morphs but not among populations. However, evidence that male-female trait correlations in hermaphrodites were lower in populations with higher frequencies of females may indicate subtle changes in genetic architecture.
Ashley, M.V., J. Wilk, S.M.N. Stynan, K.J. Craft, K.L. Jones, K.A. Geldman, K.S. Lewers, and T.-L. Ashman (2003) High variability and disomic segregation of microsatellites in the octaploid Fragaria virginiana Mill. (Rosaceae). Theor. Appl. Genet. 107:1201-1207 The objectives of the present study were to develop microsatellite markers for the wild strawberry, Fragaria virginiana, to evaluate segregation patterns of microsatellite alleles in this octoploid species, and assess genetic variability at microsatellite loci in a wild population. A genomic library was screened for microsatellite repeats and several PCR primers were designed and tested. We also tested the use of heterologous primers and found that F. virginiana primers amplified products in cultivated strawberry, Fragaria ananassa Duch. and Fragaria chiloensis. Similarly, microsatellite loci developed from cultivated strawberry also successfully amplified F. virginiana loci. We investigated four microsatellite loci in detail, three developed from F. virginiana and one from cultivated strawberry. A survey of 100 individuals from a population of F. virginiana in Pennsylvania demonstrated high heterozygosities (He or gene diversity ranged from 0.80 to 0.88 per locus) and allelic diversity (12-17 alleles per locus), but individual plants had no more than two alleles per locus. Segregation patterns in parents and progeny of two controlled crosses at these four loci were consistent with disomic Mendelian inheritance. Together these findings suggest that the genome of F. virginiana is "highly diploidized" and at least a subset of microsatellite loci can be treated as codominant, diploid markers. Significant heterozygote deficiencies were found at three of the four loci for hermaphroditic individuals but for only one locus among females in this gynodioecious species.
Morgan, M.T., and T.-L. Ashman (2003) Quantitative character evolution under complicated sexual systems, illustrated in gynodioecious Fragaria virginiana. Am. Nat. 162:257-264 Many taxa, especially plants, are famous for their diverse and complicated sexual systems. This diversity presents an obstacle to application of otherwise standard methods in evolutionary analysis. One example involves the quantitative genetics (Lande 1976, 1979; Lande and Arnold 1983) of phenotypic evolution. Standard methods of quantitative genetic analysis have been extended to and applied in separate sexed (Lande 1980; Meagher 1992, 1994; Ferguson and Fairbairn 2000) and hermaphroditic (Morgan 1992, 1994; Morgan and Schoen 1997) species, but quantitative genetic methods have not been developed to address other mating systems such as andro- and gynodioecy; andro-, gyno-, and monoecy; or heterostyly. In this note, we develop Gaussian quantitative genetic approximations to describe how selection shapes traits expressed in females and hermaphrodites of a gynodioecious species where sex is under simple nuclear gene control. We then illustrate the approach through analysis of selection acting on petal size in Fragaria virginiana. Results of the empirical analysis suggest diverse ways in which sexual systems influence the evolution of quantitative characters. Finally, we give examples of how concepts used here (i.e., the inheritance of sex determination, fertility-weighted sex morph ratio, and sex morph-specific and gender-specific phenotypic selection) can be applied to phenotypic evolution in other complicated sexual systems.
Ashman, T.-L. (2002) Quantitative genetics of reproductive traits in sexually dimorphic Fragaria virginiana: Preliminary analyses. Pp 25-28 in Strawberry Research to 2001, Hokanson, S.C., and A.R. Jamieson, Ed. ASHS Press, Alexandria, VA Kalla, S.B., and T.-L. Ashman (2002) The effects of pollen competition on progeny vigor in Fragaria virginiana (Rosaceae) depend on progeny growth environment. Int. J. Plant Sci. 163:335-340 Competition among pollen grains to fertilize ovules is expected to lead to increased vigor of the resulting progeny. Tests of this "pollen competition hypothesis," however, have been equivocal and this may, in part, be due to the levels of pollen competition (pollen load sizes) and/or progeny growth environment chosen. Our study of Fragaria virginiana controlled for these variables by identifying seeds produced under low and high pollen loads from an empirically derived pollen load-seed set response curve. We assessed fitness of seeds at germination under uniform conditions, but fitness of progeny at juvenile and adult life stages under two different resource levels in the greenhouse. We hypothesized that the effect of pollen load size on progeny vigor would be stronger when progeny were grown under low resources than when grown under high resources. We found that the effect of pollen load size was negligible at germination, but was significant in later life when assessed under two resource levels. The direction of the pollen-load effect, however, depended on the progeny growth environment. Under low resources progeny from high pollen loads grew faster, attained greater biomass, and had a higher probability of flowering than progeny from low pollen loads, while the reverse was true under high resource availability. These results indicate that the effects of pollen competition on juvenile and adult characters depend on progeny growth environment
Ashman, T.-L. (2002) The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83:1175-1184 Evolutionary biologists have repeatedly argued that environmental factors have influenced the evolution of dioecy (males and females) from hermaphroditism in plants. While many researchers have focused on the role of pollinators and abiotic factors, far fewer have considered the enemy component of the environment. In this paper, I explore how herbivory may impact the evolution of dioecy from hermaphroditism through gynodioecy. This synthesis shows that the widespread occurrence of male-biased enemy attack in sexually dimorphic species is likely to have significant consequences for both the first and second steps in the evolution of dioecy through gynodioecy. I identify several ways that herbivory can influence sexual system evolution, review the handful of studies that have explored them, and highlight exciting new avenues for research. From this review and synthesis, I conclude that consideration of enemies will provide a fresh dimension to our understanding of plant sexual systems.
Ashman, T.-L., J. Pacyna, C. Diefenderfer, and T. Leftwich (2001) Size-dependent sex allocation in a gynodioecious wild strawberry: The effects of sex morph and inflorescence architecture. Int. J. Plant Sci. 162:327-334 Some models of sex allocation predict that if male fitness gains decelerate faster than female fitness gains with increasing size, then plants should increase allocation to female function with increasing plant size. We tested this prediction in a gynodioecious (females and hermaphrodites) wild strawberry by manipulating plant size in clonally replicated genotypes, by hand-pollinating with pollen from unrelated donors, and by measuring sex allocation response at two levels: among flowers and within flowers. These methods avoided potential confounding factors that can occur in studies of size-based allocation under natural conditions, such as genotype-based variation in size, and size-based variation in pollen limitation or self-pollination. They also allow us to determine if inflorescence architecture represented a constraint on the response to plant size. We found that a 75% increase in the vegetative size of hermaphrodites resulted in 78% more flowers, 91% more fruits, 10% more pollen per flower, and 16% more ovules per flower. These responses to plant size represent a significant modification of phenotypic gender at the within-flower level (pollen : ovule ratio) but not at the among-flower level (fruit : flower ratio). We also found that while female plants enhanced flower and fruit allocation with plant size to the same degree as hermaphrodites, they increased ovule number per flower to a greater degree. Sex differential effects of plant size such as those just described could influence breeding system evolution if they alter the relative seed fertility of the sex morphs. We also found that inflorescence architecture modified the response to plant size. Specifically, the effect of plant size on ovule number was strongest in basal positions and was absent at the most distal position. This, combined with a trend in the opposite direction for pollen production, resulted in position-dependent pollen : ovule ratios. Small plants had higher pollen : ovule ratios than large plants at the primary (basal) position, equivalent ratios at intermediate positions, and lower ratios at the quaternary (distal) position. We suggest that this architectural variation in response to plant size may result from structural limitations or physiological trade-offs within the inflorescence.
Ashman, T.-L., and C. Diefenderfer (2001) Sex ratio represents a unique context for selection on attractive traits: consequences for the evolution of sexual dimorphism. Am. Nat. 157:334-347 We explored the idea that sex ratio represents a unique context for selection on attractive traits by manipulating sex ratio and pollinator abundance in experimental populations of a gender dimorphic wild strawberry, Fragaria virginiana. We found that increasing the frequency of functional males (the pollen-bearing morph) increased the frequency of pollen-collecting syrphid flies in the pollinator assemblage, decreased pollinator visitation to less preferred morph (females), and decreased the degree of pollen-limitation of females. Moreover, sex ratio influenced the strength of selection on petal size through female fitness, but did not alter the strength of selection through male fitness components, suggesting that sex ratio can alter the gender-bias of selection on an attractive trait. This study of context-dependent selection has important implications for the evolution of sexual dimorphism in attractive traits. First, it suggests that only certain conditions generate male-biased selection, and thus could lead to selection-driven male-biased petal size dimorphism. And second, it suggests that flexible pollinator foraging may be an important mechanism by which sex ratio influences selection on attractive traits. Third, it implies that variation in sex ratio could limit the evolution of sexual dimorphism, and/or could maintain genetic variation in attractive traits.
Ashman, T.-L., S. Shivitz, and J. Swetz (2000) Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana. Oikos 90:347-356 Pollinators of gender dimorphic (e.g. gynodioecious or dioecious) species often show a preference for hermaphrodite or male flowers over conspecific females, and such pollinator selectivity can have implications for the evolution of sexual dimorphism. However, because the sex morphs differ in several floral features, it is not readily apparent which specific traits generate differential pollinator service. In this study, we sought to understand the basis of pollinator preferences for hermaphrodites to females of gynodioecious Fragaria virginiana. We extend a previous study that revealed that lack of pollen-filled anthers and shorter petals were not solely responsible for small bee and fly discrimination against females, by investigating the roles of other morphological features, reward characters, and floral context in bringing about pollinator discrimination. Using floral manipulations we revealed that small bees preferentially visit flowers with wide petals, more nectar, intact stamens, as well as flowers located in hermaphrodite-dominated patches. Specifically, bees were able to remotely detect nectar presence. In addition, bees were attracted to both the anther sac and the filament regions of the stamen, indicating that not only anthers, but also filaments may function as visual or olfactory cues to pollen reward. Furthermore, pollinator preference for flowers in hermaphrodite-dominated patches serves to intensify their discrimination against female flowers which occur predominantly in female-dominated patches. For the most part, preferences of flies mirrored those of the bees with the exception that flies also showed a significant preference for flowers held high over those held closer to the ground. These results indicate that a suite of character differences contributes to pollinators' preferences for hermaphrodite to female flowers. Furthermore, they suggest pollinators could mediate selection on both floral morphology and reward in this species.
Ashman, T.-L. (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81:2577-2591 Pollinator selectivity is thought to influence the evolution of separate sexes in plants because of its potential to limit plant reproductive success. Selective visitation could also constrain or promote the phenotypic divergence of the sexes. In this study I explored the causes and consequences of selectivity by generalist pollinators of a gynodioecious wild strawberry (Fragaria virginiana), and thus provide insight into potential pollinator-mediated selection for dioecy and sexual dimorphism. I found that flowers of F. virginiana show pronounced sexual dimorphism in petal length, stamen length, nectar and pollen production, and that this results in dramatic and consistent levels of sex-differential visitation by ants, bees and flies. I performed manipulations of hermaphrodite flowers to understand the basis of selectivity and found that much of bee and fly preference for hermaphrodite flowers derived from their strong preference for longer petals, but also from a more subtle preference for pollen-filled anthers. These studies also revealed that other traits contribute to the observed discrimination against females. A stronger relationship existed between bee visitation and pollen receipt in females, than between bee visitation and pollen removal from hermaphrodites. An analysis of natural variation in petal and stamen length confirmed the central role of petal length, and also showed a lack of an effect of vestigial stamen length in pollination success of females. It also revealed a significant effect of stamen length, but not of petal length, on pollen removal. The data suggests that pollinator selectivity may affect the evolution of floral sexual dimorphism, both by exerting selection that could lead to the maintenance of stamens in females, and by exerting selection to increase petal length in females. However, the response of sexual dimorphism to pollinator-mediated selection will depend on the level of genetic integration of these (and other) floral traits, both within and between, the sex morphs.
Ashman, T.-L., and M.S. Hitchens (2000) Dissecting the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana. Am. J. Bot. 87:197-204 In this study we dissect the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana. We separated out the effects of resource competition during flowering from those of inflorescence architecture, as well as identified the effects of sex morph and genotype. We found position-based variation in petal length, ovule, pollen, and flower number to be influenced more by architecture than by our resource manipulations during flowering. We also found both genotype- and sex-specific intra-inflorescence patterns. Furthermore, our data indicate that the sex morph-specific intra-inflorescence patterns result from architectural modifications of the basic pattern. In fact, sex-differential intra-inflorescence patterns suggest that fitness through male and female function may be maximized by different resource distribution patterns within the inflorescence and may have been modified by past selection. Specifically, females invested heavily in ovules at positions where fruit set was most likely (primary and secondary), at the expense of flower number and allocation per flower at more distal positions. Whereas functional males invested minimally in ovules at all flower positions and produced the most abundantly flowered inflorescences, hermaphrodites, on the other hand, showed intermediate patterns, implying a compromise between sex functions. We suggest that consideration of intra-inflorescence allocation and inflorescence architecture may reveal the mechanism underlying sexual dimorphism in flower allocation and number.
Ashman, T.-L. (1999) Quantitative genetics of floral traits in a gynodioecious wild strawberry Fragaria virginiana: implications for the independent evolution of female and hermaphrodites floral phenotypes. Heredity 83:733-741 The independent evolution of floral phenotype is an important part of the process of gender specialization during the evolution of dioecy from hermaphroditism. However, we have little information on the genetic variation of floral traits in species with separate genders. Gynodioecious species (co-occurrence of females and hermaphrodites) have a breeding system intermediate between hermaphroditism and complete separation of the sexes (dioecy) and thus can provide insight into the genetic architecture underlying floral phenotype with respect to both primary (stamens and carpels) and secondary (petals) sexual traits. I used a nested breeding design to examine the potential for response to selection on floral traits and to examine whether this response would be similar in the two sex morphs of gynodioecious Fragaria virginiana. There was significant genetic variation underlying all floral traits, although narrow-sense heritabilities (ranging from -0.25 to 0.44) were, in most cases, much lower than broad-sense ones (ranging from 0.28 to 1.53). Moreover, the sex morphs differed significantly in their heritabilities for shared traits, such as stamen length, and showed a tendency towards differing significantly in others, like carpel number and petal length. In addition, correlations between the sex morphs for these traits (ranging from 0.41 to 0.58) were significantly greater than 0, but less than 1. These results indicate that greater sexual dimorphism could evolve in this population of F. virginiana, even if selection on these traits is not divergent. However, strong developmental integration of floral traits (e.g. stamen length and petal length) and high levels of nonadditive genetic variance may represent barriers to the evolution of complete sexual dimorphism.
Ashman, T.-L. (1999) Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. J. Evol. Biol. 12:648-661 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 hermaphrodites' may be strongly environment-dependent in this species.
Ashman, T.-L. (1998) Is relative pollen production or removal a good predictor of relative male fitness? An experimental exploration with a wild strawberry (Fragaria virginiana, Rosaceae). Am. J. Bot. 85:1166-1171 Understanding plant reproduction requires knowledge of genetic contributions through pollen and seeds. Since direct genetic assessments of fitness through pollen are often intractable, reproductive ecologists use components of male fitness such as pollen production and pollen removal as surrogates for paternity. However, we know little of the strength of the relationship between these components and actual paternity. Here, I report on a study undertaken to examine the relationship of pollen production and removal with paternity in Fragaria virginiana, a wild strawberry. A morphological marker was used to track paternity in experimental arrays exposed to native pollinators. Relative pollen production proved to be a poor predictor of relative paternity in most arrays, and over all arrays there was no significant correlation between relative paternity and relative pollen production. In contrast, relative pollen removed correlated significantly and positively with proportion of seeds sired, suggesting that a plant's contribution to the pool of removed pollen is a good predictor of its male reproductive success. Deviations from expected paternity based on relative pollen removal suggest a systematic overestimation of the siring success of plants with low pollen removal. And, in at least one specific case, low pollen removal may be explained by delayed anther dehiscence, which could lower the effectiveness of the removed pollen.
Ashman, T.-L., and D.J. Schoen (1997) The cost of floral longevity in Clarkia tembloriensis: an experimental investigation. Evol. Ecol. 11:289-300 The hypothesis that flower maintenance requires resources that would be used to support other plant functions (i.e., a cost of floral maintenance) was tested by experimentally manipulating floral longevity. Plants of Clarkia tembloriensis, a species with pollination-induced flower senescence, received either early or late pollinations (long and short longevities, respectively). We examined the effect of this manipulation on (1) per-flower allocation to nectar production and (2) flower, fruit and seed production per plant under two levels of resource availability. The direct costs of floral longevity measured in terms of nectar sugar were high: flowers that were maintained 35% longer invested proportionately more in nectar sugar (30%). At the whole-plant level, a cost of floral longevity was manifested as reduced seed production, but the magnitude of this cost varied with resource level. While plants with longer-lived flowers showed a 12% reduction in seed production, those that experienced reduced resource levels via partial defoliation, showed a decrement in seed production that was almost three times larger (34%). These differences were not brought about by changes in the number of flowers and fruits, but by significant alterations in their sizes. A model that expresses the cost of flower maintenance as a trade-off between floral longevity and seed production shows that an optimal flower longevity is determined by both the rate of fitness accrual and the cost of floral maintenance.
Ashman, T.-L., and D.J. Schoen (1996) Floral longevity: fitness consequences and resource costs. Pp 112-139 in Floral Biology, Barrett, S.C.H, and D.G. Lloyd, Ed. Chapman and Hall, New York Schoen, D.J., and T.-L. Ashman (1995) The evolution of floral longevity: Resource allocation to maintenance versus construction of repeated parts in modular organisms. Evolution 49:131-139 The component parts of modular organisms often show interspecific variation in their longevity. In plants, the flower is an example of such a structure. Models are developed in this paper to predict optimal floral longevity (the optimal length of time that flowers should remain open and functional) under a variety of conditions. A tradeoff involving allocation of resources to floral construction versus floral maintenance is assumed. The main model variables are the rate at which pollen and seed fitness accrue over time (fitness-accrual rates) and the daily cost of maintaining an existing flower relative to the cost of constructing a new one (floral maintenance cost). Long-lived flowers are selected when fitness-accrual rates and floral maintenance costs are low, whereas short-lived flowers are selected when fitness-accrual rates and floral maintenance costs are high. Dichogamy favors longer-lived flowers relative to homogamy, whereas nonindependence among flowers in their attractiveness to pollinators (attraction to flower clusters) selects for shorter-lived flowers. Reduction in floral maintenance costs later on in the flower's life favors longer-lived flowers. Observations on the dissemination and receipt of pollen in individual flowers over time, together with measurements of corolla respiration and nectar sugar production rate are required to test the model quantitatively. The parameters important to the evolution of optimal floral longevity (i.e., maintenance and construction costs, and fitness-accrual rates) may be general features of evolution of optimal longevities of other repeated structures.
Ashman, T.-L. (1994) Reproductive allocation in hermaphrodite and female plants of Sidalcea oregana ssp. spicata (Malvaceae) using 4 currencies. Am. J. Bot. 81:433-438 Reproductive allocation was investigated in female and hermaphrodite plants of gynodioecious Sidalcea oregana ssp. spicata. Total reproductive investment and partitioning of that investment was documented at the level of whole plants in terms of four ecologically relevant currencies: biomass, nitrogen, phosphorus, and potassium. Nutrient augmentations in the field confirmed that nutrients were limiting plant vegetative growth and propensity to flower; thus the use of these nutrients as currency was appropriate. Once the effects of plant size were removed, the sex morphs allocated similar total amounts of biomass, nitrogen, phosphorus, and potassium to reproduction, but partitioned those differentially. For any given individual size, females allocated larger proportions of their reproductive resource budgets to seeds. Hermaphrodites' reproductive investment in pollen and flowers was allocated at the expense of allocation to seeds. These data are relevant to the evolution of gynodioecy from hermaphroditism and support the hypothesis that females reallocate resources not spent on pollen to seeds.
Ashman, T.-L., and D.J. Schoen (1994) How long should flowers live? Nature 371:788-791 Floral longevity, the length of time a flower remains open and functional, varies among plant species. Flowers of some species live less than one day (morning glory), whereas others live for several weeks (orchids). By viewing floral longevity as a resource allocation strategy, we now incorporate the study of its evolution into the well developed theoretical framework provided by evolutionarily stable strategy models that address variation in life history. Flowers must remain open to contribute to plant fitness through ovule fertilization and pollen dissemination, when they require resources for respiratory maintenance and pollinator attraction. Accordingly, floral senescence should occur when the expected fitness gain per unit of floral maintenance investment diminishes to the point where it becomes more profitable to construct a new flower than to maintain an existing one. Our experimental evidence supports floral longevity as an adaptation that balances rates of pollen receipt and removal against the cost of floral maintenance.
Ashman, T.-L. (1994) A dynamic perspective on the cost of reproduction in plants. Am. Nat. 144:300-316 The physiological cost of reproduction was investigated in a perennial plant species, Sidalcea oregana ssp. spicata. Two different classes of estimates of current reproductive investment were compared, with the goal of identifying the most powerful predictor of future reproductive effort. ''Static'' estimates, those typically used to measure current reproductive investment (i.e., biomass or nutrients allocated to reproduction), neglect the physiological processes that influence actual reproductive expenditure. Conversely, ''dynamic'' estimates that incorporate reproductive photosynthesis or respiration, nectar production, or reproductive nutrient resorption offer a more accurate assessment of current reproductive investment. I assessed the potential for nutrient resorption from senescing reproductive structures to mitigate the cost of reproduction. Significant proportions of nitrogen and phosphorus were resorbed from floral structures, but structures differed in resorption potential and efficiency. Moreover, dynamic estimates of nutrient investment were better predictors of future reproductive effort than were static estimates. Dynamic estimates appear to be closer indicators of realized physiological cost of reproduction. By taking a dynamic perspective of reproductive investment, we may be better equipped to address the potential for evolutionary change in life history and sex allocation in plants.
Ashman, T.-L., L.F. Galloway, and M.L. Stanton (1993) Apparent vs. effective mating in an experimental population of Raphanus sativus. Oecologia 6:102-107 Effective mating in plant populations need not occur during periods of peak pollinator activity and flowering. We measured seasonal and diurnal patterns of pollinator activity, pollen and ovule availability, and seed production in an experimental population of Raphanus sativus to infer the times of reproductively effective mating. On a seasonal scale, we found that most ''effective matings'', those resulting in mature seeds, occurred very early in the season, well before the peak of flowering and pollinator activity. At a finer scale, diurnal schedules of flower opening, stigma saturation with pollen, and pollen removal indicated that most effective matings occurred before noon, even though pollinator activity increased later in the day. These patterns may be most common in populations that are not pollen limited, but other ecological factors (e.g. seed predation, resource depletion) could weaken the correspondence between pollination and effective mating. Stanton, M.L., T.-L. Ashman, L.F. Galloway, and H.J. Young (1992) Estimates of male fitness in natural populations. Pp 62-90 in Ecology and Evolution of Plant Reproduction: New Approaches, Wyatt, R., Ed. Chapman and Hall, New York Ashman, T.-L., and I. Baker (1992) Variation in floral sex allocation with time of season and currency. Ecology 73:1237-1243 Sex allocation patterns and nutrient investments in floral components were investigated in hermaphroditic morphs of Sidalcea oregana ssp. spicata utilizing a micro-technique for the determination of nitrogen and phosphorus content. A plant's investment in flowers and individual floral components decreased from early to late in the season. The primary sexual structures (gynoecium and pollen) showed less severe seasonal declines in nitrogen and phosphorus allocation than did the sepals and petals. Phenotypic gender remained relatively constant throughout the season. Sepals, gynoecium tissue, and pollen had significantly higher concentrations of nitrogen and phosphorus than did the androecium and petals. Pollen had the highest requirement for phosphorus. These results suggest that the sex functions could be limited by different nutrients. Proportional allocation to floral structures varied with time of season and currency used. A seasonal decrease in the proportion of biomass in the sepals was accompanied by an increase in the proportional allocation to each of the reproductive structures. Selection may favor preserving a minimum level of allocation to the primary sexual structures if gamete (or zygote) fitness is influenced by resource availability during production and/or maturation.
Ashman, T.-L. (1992) Indirect costs of seed production within and between seasons in a gynodioecious species. Oecologia 92:266-272 Dimorphic species, especially those with unisexual and hermaphroditic individuals, provide an opportunity to study the dynamics of resource allocation to reproductive function. In this study, I investigated the effects of manipulating seed production on reproductive allocation within a season and between seasons in females and hermaphrodites of gynodioecious Sidalcea oregana ssp. spicata. Plants were either hand-pollinated to ensure maximum seed set (seed plants), or prohibited from pollination and seed set (no-seed plants). These treatments were effective; seed plants produced an average of 120 seeds whereas no-seed plants produced no seeds. Within a season, seed plants and no-seed plants produced similar numbers of flowers, but seed plants significantly reduced the amount of biomass allocated to each flower compared to no-seed plants. The sexual morphs differed in per-flower allocation; hermaphrodites allocated significantly more biomass to most floral structures (except to ovules) relative to females. Nonetheless, the sexual morphs exhibited similar proportional reductions in flower size in response to seed production. When allocation to floral display was characterized by petal length, the sexual morphs responded differently during the season; hermaphrodites, in both seed treatments, maintained larger petals over the season while females greatly reduced theirs. This could be interpreted as adaptive if pollen removal is positively related to petal size. In the season following the manipulations of seed production, plants which produced seeds in 1989 had reduced allocation to inflorescences (and flowers) in 1990 compared to plants which did not produce seeds in 1989. A similar trend was not detected for vegetative growth between seasons. The sexual morphs did not differ significantly in their between season responses to the seed treatment. Ashman, T.-L. (1992) The relative importance of inbreeding and maternal sex in determining progeny fitness in Sidalcea oregana ssp. spicata, a gynodioecious plant. Evolution 46:1862-1874 Gynodioecious plant populations contain both hermaphrodite and female individuals. For females to be maintained they must compensate for their loss of reproductive fitness through pollen. Females may achieve compensation by producing more and/or higher quality seeds than hermaphrodites. In this study, I investigated the independent and interactive effects of maternal sexual identity and inbreeding level on fitness of the progeny of hermaphrodites and females of Sidalcea oregana ssp.spicata. Seeds produced by selfing hermaphrodites and by outcrossing or sib-crossing hermaphrodites and females, were planted in the field and greenhouse. Maternal-sex effects were substantial at the juvenile stages of the life cycle; seeds of females germinated in higher proportions and produced seedlings that grew significantly faster. Inbreeding effects were manifested primarily at the adult stage of the life cycle. Outcrossed plants were significantly larger and produced more flowers per plant than sib-crossed and selfed plants growing in the greenhouse. Progeny of hermaphrodites and females appeared to respond similarly to sib-matings. The maternal-sex effects observed in Sidalcea may have been related to cytoplasmically inherited factors and could be a driving force in the maintenance of females. Inbreeding depression could play a role in determining the fitness of both sex morphs, if females experience biparental inbreeding in the field. Frequent inbreeding of hermaphrodites may not be necessary to explain the maintenance of gynodioecy in this species.
Ashman, T.-L., and M.L. Stanton (1991) Seasonal variation in pollination dynamics of the sexually dimorphic species, Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72:993-1003 We explored the combined effects of seasonal variation in both pollinator assemblage and availability of pollen donors on pollination in a gynodioecious species, Sidalcea oregana ssp. spicata (Malvaceae). Hermaphrodites produced flowers with significantly larger petals but maintained fewer open flowers per inflorescence than females. Flowers of hermaphrodites produced 50% more nectar sugar in the 24 h after anthesis than the flowers of females. Nectar sugar production was also significantly and positively correlated with petal length. Pollinator visitation rates were influenced more by differences in petal length than by differences in flower number per inflorescence. Consequently, hermaphrodites experienced higher visitation rates on a per-flower basis. Female flowers tended to receive pollen at a lower rate than hermaphrodites, but remained in the receptive female-phase longer than hermaphrodites. On average, the length of the period of flower receptivitiy declined as pollen deposition rate increased. These opposing processes resulted in the sex morphs receiving equivalent levels of pollination. Seasonal variation in the rate of pollen reception was more strongly influenced by the efficiency of the available pollinator pool than by rates of visitation. Dramatic seasonal shifts in the composition of the pollinator assemblage and pollen availability were correlated with increased pollination intensity as the season progressed. Not only were more pollen grains received, but they arrived in a shorter period of time and the number of potential pollen donors (hermaphrodites) increased. These findings suggest that pollen competition in both sex morphs may be more intense late in the season.
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