Sexual differences in response to simulated herbivory in the gynodioecious herb <Emphasis Type="Italic">Geranium sylvaticum</Emphasis>

Several factors have been proposed to explain female maintenance in gynodioecious populations. In this study, we propose and test a novel hypothesis: greater tolerance to herbivory through more beneficial interactions with plant fungal mutualists might also help to explain female maintenance. Herbivory limits the amount of carbon and nutrients available for the plants and has been shown to affect mycorrhizal colonization. We hypothesized that simulated herbivory would decrease reproductive output, mycorrhizal colonization intensity, and the phosphorus content relatively more in hermaphrodites, so females would achieve higher advantage over hermaphrodites when under herbivory pressure. We tested it in the field using the gynodioecious plant Geranium sylvaticum. We found that simulated herbivory had a negative effect on the reproductive output in both sexes and that there was a similar reduction in fruit set, seed set, and total seed number in both sexes. Defoliation did not affect any fungal parameter measured, but decreased phosphorus content relatively more in females. The plants had a sex-specific relationship with mycorrhizae, but this was not related to herbivory. Thus, we conclude that females do not gain any specific advantage under defoliation from its symbionts at short-term even though it seems that the plants have sex-specific relationship with their mycorrhizal symbionts.     

Leaf damage and gender but not flower damage affect female fitness in Nemophila menziesii (Hydrophyllaceae)

Researchers can answer questions about the evolution or maintenance of separate sexes using dioecious plant systems. Because females in these species typically put more resources into reproductive effort than male plants, researchers have hypothesized that females may be less tolerant of the stresses found in marginal habitats. Herbivory can act as a biotic stressor that reduces resources in plants much like a marginal habitat can. Females may be limited by resources, and may thus be less tolerant to herbivory than males. Here, I explore the relationships between florivory, leaf herbivory, and gender in a gynodioecious, annual plant, Nemophila menziesii (Hydrophyllaceae, senso lato). I performed a crossed design experiment examining the main effects and interactions of plant gender, artificial leaf damage, and artificial flower damage on components of female plant fitness. Leaf damage decreased fruit set and females made significantly more fruit than hermaphrodites. However, contrary to theory, I found little evidence for a gender by damage interaction for either type of artificial herbivory. Based on these results, I propose more work exploring the effects of both source and sink damage in dioecious species to help elucidate where and when different sexual morphs are favored by natural selection.     

Dioecious species and arbuscular mycorrhizal symbioses: The case of Antennaria dioica

Sex-specific interactions with herbivores and pollinators have been observed in female and male plants of dioecious species. However, only a limited number of studies have revised sex-specific patterns in mycorrhizal symbiosis. To test whether female and male plants of Antennaria dioica differ in their relationship with arbuscular mycorrhizal (AM) fungi, we examined the temporal and spatial variation in AM fungi in female, male and non-reproductive A. dioica plants in three natural populations in Finland during flowering and after seed production. Our results are consistent with previous studies both under greenhouse and field conditions with the same species showing differences in AM colonization between the sexes linked with allocation to reproduction. Taken together, the results indicate that there is a sex-specific interaction between A. dioica and AM fungi. Overall, females have a greater investment in AM fungi, likely to enhance their uptake of soil nutrients and support the reproduction by seed.     

Attracting pollinators and avoiding herbivores: insects influence plant traits within and across years

Perennial plants interact with herbivores and pollinators across multiple growing seasons, and thus may respond to herbivores and pollinators both within and across years. Joint effects of herbivores and pollinators influence plant traits, but while some of the potential interactions among herbivory, pollination, plant size, and plant reproductive traits have been well studied, others are poorly understood. This is particularly true for perennial plants where effects of herbivores and pollinators may manifest across years. Here, we describe two experiments addressing the reciprocal interactions of plant traits with herbivore damage and pollination across 2 years using the perennial plant Chamerion angustifolium. We measured (1) plant responses to manipulation of damage and pollination in the year of treatment and the subsequent season, (2) damage and pollination responses to manipulation of plant size and flowering traits in the year of treatment, and (3) plant-mediated indirect interactions between herbivores and pollinators. We found that plant traits had little effect on damage and pollination, but damage and pollination affected plant traits in both the treatment year and the subsequent year. We found evidence of indirect effects between leaf herbivores and pollinators in both directions; indirect effects of pollinators on leaf herbivores have not been previously demonstrated. Our results indicate that pollen receipt results in shorter plants with fewer stems but does not change flower number, while leaf herbivory results in taller plants with fewer flowers. Together, herbivory and pollination may contribute to intermediate plant height and plants with fewer stems and flowers in our system.     

Different arbuscular mycorrhizal interactions in male and female plants of wild Carica papaya L.

The different resource demands on male and female plants of dioecious species can lead to secondary sexual dimorphisms. Male and female plants might also interact differently with antagonists and mutualists. We used a repeated measures natural experiment in five subpopulations to investigate secondary sexual dimorphism in Carica papaya including interactions with arbuscular mycorrhizal fungi. Male and female plants did not differ in size or growth rate, but male plants flowered earlier than female plants. We observed different patterns of root colonization by arbuscular mycorrhizal fungi in male and female plants of C. papaya. These differences between the sexes preceded the flowering of most female plants. Female plants were sensitive to changes in soil fertility and adjusted the extent of their root colonization by arbuscular mycorrhizal fungi accordingly. Overall, the different resource demands on male and female plants seem to modulate the interactions of C. papaya with arbuscular mycorrhizal fungi.     

Resource allocation in an annual herb: Effects of light,mycorrhizal fungi,and defoliation

Concurrent interactions and the availability of resources (e.g., light) affect the cost/benefit balance during mutualistic and antagonistic interactions, as well as plant resource allocation patterns. Mycorrhizal interactions and herbivory concur in most plants, where mycorrhizae can enhance the uptake of soil nutrients by plants as well as consuming a large fraction of the plant's carbon, and defoliation usually reduces light interception and photosynthesis, thereby causing direct losses to the hosts of mycorrhizal fungi. Both types of interactions affect the carbon budget of their host plants and thus we predict that the relative costs of herbivory and mycorrhizal colonization will increase when photosynthesis is reduced, for instance in light limited environments. We conducted a greenhouse experiment using Datura stramonium to investigate the effects of defoliation and mycorrhizal inoculation on the resource allocation patterns in two different light environments. Defoliated plants overcompensated in terms of leaf mass in both light environments, but total seed mass per fruit was negatively affected by defoliation in both light environments. Mycorrhizal inoculation had a positive effect on vegetative growth and the leaf nitrogen content, but defoliation negates the benefit of mycorrhizal interactions in terms of the leaf nitrogen content. In general, D. stramonium compensated for the relative costs of concurrent mycorrhizal interactions and defoliation; plants that lacked both interactions exhibited the same performance as plants with both types of interactions.     

Genetic constraints on floral evolution: a review and evaluation of patterns

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.     

Interactions between aboveground herbivores and the mycorrhizal mutualists of plants

Plant growth, reproduction and survival can be affected both by mycorrhizal fungi and aboveground herbivores, but few studies have examined the interactive effects of these factors on plants. Most of the available data suggest that severe herbivory reduces root colonization by vesicular-arbuscular and ectomycorrhizal fungi. However, the reverse interaction has also been documented - mycorrhizal fungi deter herbivores and interact with fungal endophytes to influence herbivory. Although consistent patterns and mechanistic explanations are yet to emerge, it is likely that aboveground herbivore-mycorrhiza interactions have important implications for plant populations and communities.     

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

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

Sex-specific responses to mycorrhiza in a dioecious species

In most studies about dioecious plants, the role of arbuscular mycorrhizae (AM) and the potential sex-specific differences between the plant hosts have been overlooked. Because plant sexes frequently differ in drought tolerance and AM fungal colonization provides higher resistance to drought, we investigated whether the relation of mycorrhizal fungi with either male or female Antennaria dioica plants differs using a factorial experiment. We hypothesized that because AM usually increase growth rate and male plants usually grow larger than females, males should gain more benefit from the mycorrhizal symbiosis in terms of mineral nutrition and water supply. Because of higher demands of carbohydrates (C) in males, we expected males to allocate less C resources to the mycorrhizal fungus so that the associated fungi should benefit less of the association with males. In contrast to our initial hypothesis, the male plants, although faster growing under drought, did not gain more symbiosis-mediated benefits than did the females, and both sexes seemed to provide resources equally to their fungal symbiont. Therefore, we conclude that the two plant sexual morphs provide equal amounts of C to their fungal root symbionts and that they can gain specific benefits from the symbiosis, which, however, depend on soil water availability.     

Sex-specific variation in the interaction between Distichlis spicata (Poaceae) and mycorrhizal fungi

Associations between mycorrhizal fungi and plants can influence intraspecific competition and shape plant population structure. While variation in plant genotypes is known to affect mycorrhizal colonization in crop systems, little is known about how genotypes affect colonization in natural plant populations or how plant sex might influence colonization with mycorrhizal fungi in plant species with dimorphic sexual systems. In this study, we analyzed mycorrhizal colonization in males and females of the wetland dioecious grass Distichlis spicata, which has spatially segregated sexes. Our results suggest that D. spicata males and females interact with mycorrhizal fungi differently. We discuss the implications for the role of this sex-specific symbiotic interaction in the maintenance of the within-population sex ratio bias of D. spicata.     

Pre-dispersal seed predation in gynodioecious Geranium sylvaticum is not affected by plant gender or flowering phenology

Sex-specific interactions with antagonists may explain female maintenance in gynodioecious populations if seeds produced by hermaphroditic plants are preferred over seeds produced by female plants. Among antagonistic interactions, pre-dispersal seed predators have received relatively little attention even though they may exert sex-specific selective pressures on the evolution of floral and flowering traits. In this work, I investigate temporal variation in seed predation in gynodioecious Geranium sylvaticum, where in addition to female and hermaphrodite individuals, plants with an intermediate sexual expression are also present in most populations. Specifically, I examined whether seed predation is linked to flowering phenology, plant gender, and sexual dimorphism in floral and seed traits over the flowering season using an experimental field population. Within the population, I selected female, intermediate, and hermaphrodite plants with different timing of flowering onset (early, mid, or late), and collected seeds across the fruiting period. Seeds were weighed and examined for seed predator damage. The results show that the three genders experienced similar levels of seed predation attack regardless of their flowering phenology, and that overall seed predation was not related to changes in seed production or seed mass. These results suggest that sexual dimorphism in seed predation cannot be responsible for female maintenance in this species.     

The Evolution and Consequences of Sex-Specific Reproductive Variance

Natural selection favors alleles that increase the number of offspring produced by their carriers. But in a world that is inherently uncertain within generations, selection also favors alleles that reduce the variance in the number of offspring produced. If previous studies have established this principle, they have largely ignored fundamental aspects of sexual reproduction and therefore how selection on sex-specific reproductive variance operates. To study the evolution and consequences of sex-specific reproductive variance, we present a population-genetic model of phenotypic evolution in a dioecious population that incorporates previously neglected components of reproductive variance. First, we derive the probability of fixation for mutations that affect male and/or female reproductive phenotypes under sex-specific selection. We find that even in the simplest scenarios, the direction of selection is altered when reproductive variance is taken into account. In particular, previously unaccounted for covariances between the reproductive outputs of different individuals are expected to play a significant role in determining the direction of selection. Then, the probability of fixation is used to develop a stochastic model of joint male and female phenotypic evolution. We find that sex-specific reproductive variance can be responsible for changes in the course of long-term evolution. Finally, the model is applied to an example of parental-care evolution. Overall, our model allows for the evolutionary analysis of social traits in finite and dioecious populations, where interactions can occur within and between sexes under a realistic scenario of reproduction.     

Grazing tolerance and mycorrhizal colonization: Effects of resource manipulation and plant size in biennial Gentianella campestris

As herbivory usually leads to loss of photosynthesizing biomass, its consequences for plants are often negative. However, in favorable conditions, effects of herbivory on plants may be neutral or even beneficial. According to the compensatory continuum hypothesis plants can tolerate herbivory best in resource-rich conditions. Besides herbivory, also primarily positive biotic interactions like mycorrhizal symbiosis, bear carbon costs. Tritrophic plant–fungus–herbivore interaction further complicates plant's cost-benefit balance, because herbivory of the host plant is expected to cause decline in mycorrhizal colonization under high availability of soil nutrients when benefits of symbiosis decline in relation to costs. To gain insight into above interactions we tested the effects of plant size and resource manipulation (simulated herbivory and fertilization) on both above-ground performance and on root fungal colonization of the biennial Gentianella campestris.Clipping caused allocation shift from height growth to branches in all groups except in large and fertilized plants. For large plants nutrient addition may have come too late, as the number of meristems was most likely determined already before the fertilization. Clipping decreased the amount of DSE (dark septate endophytic) fungi which generally are not considered to be mycorrhizal. The effect of clipping on total fungal colonization and colonization by arbuscular mycorrhizal (AM) fungal coils were found to depend on host size and resource level. Dissimilar mycorrhizal response to simulated herbivory in small vs. large plants could be due to more intensive light competition in case of small plants. Carbon limited small plants may not be able to maintain high mycorrhizal colonization, whereas large clipped plants allocate extra resources to roots and mycorrhizal fungi at the expense of above-ground parts. Our results suggest that herbivory may increase carbon limitation that leads re-growing shoots and fungal symbionts to function as competing sinks for the limited carbon reserves.     

Phenotypic divergence and inter-specific trait correlation in a plant-pollinator/seed predator mutualism

Plant-pollinator interactions have been suggested as key drivers of morphological divergence and speciation of the involved taxa. These interactions can also promote sexual dimorphism in both the plant and pollinator, particularly if the pollinator is also a seed-eater and/or exerts different selection pressures on male and female plants. Here we tested the hypotheses that plant-pollinator interactions can be reflected in trait variation and sexual dimorphism in both organisms within and across populations. Across nine European populations, we examined intraspecific variation and sexual dimorphism in phenotypic traits potentially involved in the plant–insect interaction of the dioecious white campion Silene latifolia (Caryophyllaceae) and its specialist pollinator Hadena bicruris (Noctuidae). This interaction is expected to entail sex-specific selective pressures, as female moths lay eggs on female plants and the larvae predate on the seeds during their development. We compared divergence in phenotypic traits among populations and between sexes within populations, examined correlations between plant and pollinator traits, and between phenotypic distances and genetic distances among co-occurring populations for both plants and insects. We found key differences in phenotypic traits across populations of both the plant and moth, though only in the moth were these differences correlated with geographic distances. We also found evidence for sexual dimorphism in the plant but not in the pollinator. Evolution of floral sexual dimorphism in S. latifolia most likely results from the joint contribution of different selective forces, including biotic interactions with H. bicruris moths.     

Herbivores do not discriminate between leaves of female and hermaphrodite individuals of gynodioecious Daphne laureola (Thymelaeaceae)

The outcome of plant-animal interactions in dioecious plant species frequently depends on the gender of the plant individuals. It has even been proposed that these interactions could mediate the evolution of plant reproductive systems from hermaphroditism to dioecy. Gynodioecy is the most frequent intermediate stage in this evolutionary process, however, little is known about the relevance of gender dimorphism in plant-animal relationships others than pollination for gynodioecious species. In this study herbivores (Noctuid larvae) were used as subjective referees to detect differences between leaves of female and hermaphrodite Daphne laureola individuals. Larvae collected in the field were allowed to choose between leaves of female and hermaphrodite individuals at both flowering and fruiting period. There was no preference for either of the genders suggesting that the absence of male reproductive function in D. laureola shrubs does not cause dissimilarities in leaf characteristics that can affect herbivores.     

Pollination by fungus gnats in four species of the genus Mitella (Saxifragaceae)

The first example of pollination by fungus gnats in the eudicots is reported. The genus Mitella (Saxifragales) is characteristically produces minute, inconspicuous, mostly dull-coloured flowers with linear, sometimes pinnately branched, petals. To understand the function of these characteristic flowers, we studied the pollination biology of four Mitella species with different floral traits and different sexual expression: dioecious M. acerina , gynodioecious M. furusei var. subramosa , and hermaphroditic M. stylosa var. makinoi and M. integripetala. Flower-bagging experiments showed that wind pollination did not occur in the dioecious and gynodioecious species. Two years of observations of flower visitors at six study sites in Japan revealed that the principal pollinators of all four Mitella were specific species of fungus gnats (Mycetophilidae), which landed on the flowers with their long spiny legs settling on the petals. Characteristically, numerous pollen grains were attached to the fungus gnats in specific locations on the body. Although, on average, 1.3–2.6 fungus gnats visited each inflorescence per day, the fruit set of both bisexual and female flowers exceeded 63%. These results suggest that fungus gnats are highly efficient pollinators of Mitella spp., and that Mitella flowers are morphologically adapted to pollination by fungus gnats.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 449–460.     

The transition to gender dimorphism on an evolutionary background of self-incompatibility: an example from Lycium (Solanaceae)

Populations of three North American species of Lycium (Solanaceae) are morphologically gynodioecious and consist of male-sterile (i.e., female) and hermaphroditic plants. Marked individuals were consistent in sexual expression across years and male sterility was present throughout much of the species' ranges. Controlled pollinations reveal that L. californicum, L. exsertum, and L. fremontii are functionally dioecious. Fruit production in females ranged from 36 to 63%, whereas hermaphrodites functioned essentially as males. Though hermaphrodites were mostly male, investigation of pollen tube growth reveals that hermaphrodites of all dimorphic species were self-compatible. Self-fertilization and consequent inbreeding depression are commonly invoked as important selective forces promoting the invasion of male-sterile mutants into cosexual populations. A corollary prediction of these models is that gender dimorphism evolves from self-compatible ancestors. However, fruit production, seed production, and pollen tube number following outcross pollination were significantly higher than following self-pollination for three diploid, cosexual species that are closely related to the dimorphic species. The data presented here on incompatibility systems are consistent with the hypothesis that polyploidy disrupted the self-incompatibility system in the gynodioecious species leading to the evolution of gender dimorphism.