Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions.

Reproductive traits are tightly linked to plant fitness and may therefore be mechanisms driving biological invasions, including the greater success of more phylogenetically novel introduced species in some systems. We present a phylogenetic comparative analysis of "Baker's law'', that introduced plants with the ability to reproduce autogamous or asexually may be better able to establish on introduction. We gathered data from both published and unpublished sources on pollen limitation of 141 species, including 26 introduced species and 115 native species. Our analysis compared differences in the proportion of autonomous autogamy, asexual reproduction, and pollen limitation among native, introduced noninvasive, and introduced invasive plant species, and included the phylogenetic novelty of the introduced species to the native species in that community. Introduced species were more likely to be autogamous than native species, consistent with Baker's law. On the other hand, introduced species were less likely to have the ability to reproduce asexually. Further, among species with no autonomous autogamy, pollen limitation was greater for introduced compared to native species. Such a result is consistent with the idea that plants entering a new continent receive lower quality or quantity of services from resident pollinators than species native to that continent. Finally, more phylogenetically novel invasive species had lower pollen limitation than less novel invasive species, potentially because they experience less competition for pollinators. This is the first evidence that enhanced pollination may be one mechanism driving the greater invasiveness of phylogenetically novel introduced species observed in some systems.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals.

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.

The interactive effects of herbivory and mixed mating for the population dynamics of Impatiens capensis.

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.

Herbivory and competition interact to affect reproductive traits and mating system expression in Impatiens capensis.

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.

Consequences of vegetative herbivory for maintenance of intermediate outcrossing in an annual plant.

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.

Genome size variation and evolution in allotetraploid Arabidopsis kamchatica and its parents, Arabidopsis lyrata and Arabidopsis halleri.

Polyploidization and subsequent changes in genome size are fundamental processes in evolution and diversification. Little is currently known about the extent of genome size variation within taxa and the evolutionary forces acting on this variation. Arabidopsis kamchatica has been reported to contain both diploid and tetraploid individuals. The aim of this study was to determine the genome size of A. kamchatica, whether there is variation in ploidy and/or genome size in A. kamchatica and to study how genome size has evolved. We used propidium iodide flow cytometry to measure 2C DNA content of 73 plants from 25 geographically diverse populations of the putative allotetraploid A. kamchatica and its parents, Arabidopsis lyrata and Arabidopsis halleri. All A. kamchatica plants appear to be tetraploids. The mean 2C DNA content of A. kamchatica was 1.034 pg (1011 Mbp), which is slightly smaller than the sum of its diploid parents (A. lyrata: 0.502 pg; A. halleri: 0.571 pg). Arabidopsis kamchatica appears to have lost ∼37.594 Mbp (3.6 %) of DNA from its 2C genome. Tetraploid A. lyrata from Germany and Austria appears to have lost ∼70.366 Mbp (7.2 %) of DNA from the 2C genome, possibly due to hybridization with A. arenosa, which has a smaller genome than A. lyrata. We did find genome size differences among A. kamchatica populations, which varied up to 7 %. Arabidopsis kamchatica ssp. kawasakiana from Japan appears to have a slightly larger genome than A. kamchatica ssp. kamchatica from North America, perhaps due to multiple allopolyploid origins or hybridization with A. halleri. However, the among-population coefficient of variation in 2C DNA content is lower in A. kamchatica than in other Arabidopsis taxa. Due to its close relationship to A. thaliana, A. kamchatica has the potential to be very useful in the study of polyploidy and genome evolution.

Heterogeneous selection on trichome production in Alaskan Arabidopsis kamchatica (Brassicaceae).

PREMISE OF THE STUDY: Environmental heterogeneity is thought to be one of the primary factors in the evolutionary maintenance of morphological variation. Here, we explore the role of environmental heterogeneity in the maintenance of variation in leaf hair (trichome) production in Arabidopsis kamchatica. • METHODS: We investigate abiotic correlates of trichome production in A. kamchatica via surveys of both herbarium specimens and wild populations. In addition, we examine patterns of phenotypic selection on trichome production among populations that differ in environmental characteristics. • KEY RESULTS: Trichome-producing herbarium specimens were more likely to occur at lower latitudes and in locations with lower mean annual precipitation and less annual variation in temperature than glabrous specimens. In surveys of wild populations, frequencies of trichome-producing plants were higher in drier habitats than in wetter environments. Using phenotypic selection analysis, we found divergent selection through female fitness (fruit production) on trichome number in populations that differ in environmental characteristics; there was selection for reduced trichome number in one population and selection for increased trichome number in another population. In a population containing both glabrous and trichome-producing plants, glabrous plants produced significantly more fruits than trichome-producing individuals, which indicates selection against the trichome morph. • CONCLUSIONS: Our results demonstrate that there is heterogeneity in selection among populations, which could be responsible for the maintenance of trichome variation in Alaskan populations of A. kamchatica.

Ovule number per flower in a world of unpredictable pollination.

The number of ovules per flower varies over several orders of magnitude among angiosperms. Here we consider evidence that stochastic uncertainty in pollen receipt and ovule fertilization has been a selective factor in the evolution of ovule number per flower. We hypothesize that stochastic variation in floral mating success creates an advantage to producing many ovules per flower because a plant will often gain more fitness from occasional abundant seed production in randomly successful flowers than it loses in resource commitment to less successful flowers. Greater statistical dispersion in pollination and fertilization among flowers increases the frequency of windfall success, which should increase the strength of selection for greater ovule number per flower. We therefore looked for evidence of a positive relationship between ovule number per flower and the statistical dispersion of pollen receipt or seed number per flower in a comparative analysis involving 187 angiosperm species. We found strong evidence of such a relationship. Our results support the hypothesis that unpredictable variation in mating success at the floral level has been a factor in the evolution of ovule packaging in angiosperms.

A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation.

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.

Pollination decays in biodiversity hotspots.

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.

Herbivory alters the expression of a mixed-mating system.

The direct and indirect effects of vegetative herbivory on the mating system of Impatiens capensis were analyzed through a survey of herbivory in natural I. capensis populations and manipulation of leaf damage in the field. Across 10 wild populations of I. capensis proportion of cleistogamous flowers had a significant positive exponential relationship with natural levels of herbivory. Similarly, experimental leaf damage increased the proportion of flowers and seeds that were cleistogamous. Leaf damage also reduced the biomass of cleistogamous progeny more severely relative to that of chasmogamous progeny. The cumulative effect of leaf damage was to increase plant reliance on fitness derived from cleistogamous progeny. Leaf damage indirectly affected mating system traits by reducing chasmogamous flower size, leading to a reduction in pollinator visitation. Under these experimental conditions, herbivory did not significantly reduce the number of simultaneously open flowers and potential for geitonogamy, nor did it result in significant changes in the composition of the pollinator fauna. These findings are among the first to demonstrate that herbivory has consequences for mating system and should be considered a factor shaping mating system evolution.