How geitonogamous selfing affects sex allocation in hermaphrodite plants

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

ECOLOGICAL GENETICS OF GYNODIOECY IN SILENE VULGARIS: RELATIVE FITNESS OF FEMALES AND HERMAPHRODITES DURING THE COLONIZATION PROCESS

Recent theoretical models have addressed the influence of metapopulation dynamics on the fitness of females and hermaphrodites in gynodioecious plants. In particular, selection is thought to favor hermaphrodites during population establishment because that sex should be less prone to pollen limitation, especially if self-fertilization is possible. However, inbreeding depression could limit this advantage. In this experimental study of Silene vulgaris, a weedy gynodioecious plant, the fitness of females and hermaphrodites was estimated from seed production in both mixed-sex populations and for individuals isolated from these populations by 20, 40, 80, or 160 m. In mixed populations females display statistically significant greater per capita seed production owing to higher capsule production and higher rates of seed germination. The fitness of both sexes declines with increasing isolation, but at different rates, such that in the 160-m treatment hermaphrodites are by far the more fit sex. Allozyme studies suggest that this differential decline is because the selfing rate in hermaphrodites increases as a function of isolation, at least partially compensating for a decline in the availability of outcross pollen. Overall, the negative effects of pollen limitation on females far outweighs the negative effects of inbreeding depression following selfing in hermaphrodites. Thus, extinction/recolonization dynamics would appear to favor hermaphrodites as long as seed dispersal events exceed some critical distance.     

Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond

Comparisons of the causes and consequences of cross- and self-fertilization have dominated research on plant mating since Darwin's seminal work on plant reproduction. Here, I provide examples of these accomplishments, but also illustrate new approaches that emphasize the role of floral design and display in pollen dispersal and fitness gain through male function. Wide variation in outcrossing rate characterizes animal-pollinated plants. In species with large floral displays, part of the selfing component of mixed mating can arise from geitonogamy and be maladaptive because of strong inbreeding depression and pollen discounting. Floral strategies that separate the benefits of floral display from the mating costs associated with geitonogamy can resolve these conflicts by reducing lost mating opportunities through male function. The results from experiments with marker genes and floral manipulations provide evidence for the function of herkogamy and dichogamy in reducing self-pollination and promoting pollen dispersal. Evidence is also presented indicating that increased selfing resulting from changes to floral design, or geitonogamy in large clones, can act as a stimulus for the evolution of dioecy. The scope of future research on mating strategies needs to be broadened to include investigations of functional links among flowers, inflorescences and plant architecture within the framework of life-history evolution.     

Ploidy effects on the relationship between floral phenotype,reproductive investment,and fitness in an autogamous species complex

Premise

The relationships between reproductive investment, phenotype, and fitness have been broadly studied in cross-pollinated plants in contrast to selfing species, which are considered less interesting in this area because they are supposed to be a dead end in any evolutionary pathway. Still, selfing plants are unique systems to study these questions since the position of reproductive structures and traits related to flower size play an important role in female and male pollination success.

Methods

Erysimum incanum s.l. is a selfing species complex that has three levels of ploidy (diploids, tetraploids, and hexaploids) and traits that are typically associated with the selfing syndrome. Here, we used 1609 plants belonging to these three ploidies to characterize the floral phenotype and spatial configuration of reproductive structures, reproductive investment (pollen and ovule production), and plant fitness. Then, we used structural equation modelling to analyze the relationship between all these variables across ploidy levels.

Results

An increase in ploidy level leads to bigger flowers with anthers exserted farther and more pollen and ovules. In addition, hexaploid plants had higher absolute values for herkogamy, which is positively correlated with fitness. Ovule production significantly mediated the natural selection acting on different phenotypic traits and pollen production, a pattern that is maintained across ploidies.

Conclusions

The changes in floral phenotypes, reproductive investment, and fitness with ploidy level suggest that genome duplication can be a driver for transitions in reproductive strategy by modifying the investment in pollen and ovules and linking them with plant phenotype and fitness.     

Resource Allocation and the Evolution of Self-Fertilization in Plants

This article develops a simple evolutionarily stable strategy (ESS) model of resource allocation in partially selfing plants, which incorporates reproductive and sex allocation into a single framework. The analysis shows that, if female fitness gain increases linearly with resource investment, total reproductive allocation is not affected by sex allocation, defined as the fraction of reproductive resources allocated to male function. All else being equal, the ESS total reproductive allocation increases with increasing selfing rate if the fitness of selfed progeny is more than half that of outcrossed progeny, while the ESS sex allocation is always a decreasing function of the selfing rate. Self-fertilization is much more common in annual than in perennial plants, and this association has been commonly interpreted in terms of an effect of life history on mating system. The model in this article shows that self-fertilization can itself cause the evolution of the annual habit. Incorporating the effects of pollen discounting may not have any influence on total reproductive allocation if female fitness gain is a linear function of resource investment, although the evolutionarily stable sex allocation is altered. Evolution of the selfing rate is found to be independent of reproductive and sex allocation under the mass-action assumption that self- and outcross pollen are deposited simultaneously on receptive stigmas and compete for access to ovules.     

Evolution of the Selfing Rate and Resource Allocation Models

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

Effects of floral display size on male and female reproductive success in Mimulus ringens

Background and Aims

The number of flowers blooming simultaneously on a plant may have profound consequences for reproductive success. Large floral displays often attract more pollinator visits, increasing outcross pollen receipt. However, pollinators frequently probe more flowers in sequence on large displays, potentially increasing self-pollination and reducing pollen export per flower. To better understand how floral display size influences male and female fitness, we manipulated display phenotypes and then used paternity analysis to quantify siring success and selfing rates.

Methods

To facilitate unambiguous assignment of paternity, we established four replicate (cloned) arrays of Mimulus ringens, each consisting of genets with unique combinations of homozygous marker genotypes. In each array, we trimmed displays to two, four, eight or 16 flowers. When fruits ripened, we counted the number of seeds per fruit and assigned paternity to 1935 progeny.

Key Results

Siring success per flower declined sharply with increasing display size, while female success per flower did not vary with display. The rate of self-fertilization increased for large floral displays, but siring losses due to geitonogamous pollen discounting were much greater than siring gains through increased self-fertilization. As display size increased, each additional seed sired through geitonogamous self-pollination was associated with a loss of 9·7 seeds sired through outcrossing.

Conclusions

Although total fitness increased with floral display size, the marginal return on each additional flower declined steadily as display size increased. Therefore, a plant could maximize fitness by producing small displays over a long flowering period, rather than large displays over a brief flowering period.     

The effects of floral display on pollinator visitation vary among populations ofPhacelia linearis (Hydrophyllaceae)

Summary Individual plants in gynodioecious populations ofPhacelia linearis (Hydrophyllaceae) vary in flower gender, flower size, and flower number. This paper reports the effects of variation in floral display on the visitation behaviour of this species' pollinators (mainly pollen-collecting solitary bees) in several natural and three experimental plant populations, and discusses the results in terms of the consequences for plant fitness. The working hypotheses were: (1) that because female plants do not produce pollen, pollen-collecting insects would visit hermaphrodite plants at a higher rate than female plants and would visit more flowers per hermaphrodite than per female; and (2) that pollinator arrival rate would increase with flower size and flower number, the two main components of visual display. These hypotheses were generally supported, but the effects of floral display on pollinator visitation varied substantially among plant populations. Hermaphrodites received significantly higher rates of pollinator arrivals and significantly higher rates of visits to flowers than did females in all experimental populations. Flower size affected arrival rate and flower visit rate positively in natural populations and in two of the three experimental populations. The flower size effect was significant only among female plants in one experimental population, and only among hermaphrodites in another. The effect of flower number on arrival rate was positive and highly significant in natural populations and in all experimental populations. In two out of three experimental populations, insects visited significantly more flowers per hermaphrodite than per female and visited more flowers on many-flowered plants than on few-flowered plants, but neither effect was detected in the third experimental population. Because seed production is not pollen-limited in this species, variation in pollinator visitation behaviour should mainly affect the male reproductive success of hermaphrodite plants. These findings suggest that pollinator-mediated natural selection for floral display inP. linearis varies in space and time.     

When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans

In gynodioecious plant species with nuclear‐cytoplasmic sex determination, females and hermaphrodites plants can coexist whenever female have higher seed fitness than hermaphrodites. Although the effect of self fertilization on seed fitness in hermaphrodites has been considered theoretically, this effect is far from intuitive, because it can either increase the relative seed fitness of the females (if it leads hermaphrodites to produce inbred, low quality offspring) or decrease it (if it provides reproductive assurance to hermaphrodites). Hence, empirical investigation is needed to document whether relative seed fitness varies with whether pollen is or is not limiting to seed production. In the current study, we measured fruit set and seed production in both females and hermaphrodites and the selfing rate in hermaphrodites in two experimental patches that differed in sex ratios in the gynodioecious plant Silene nutans. We found an impact of plant gender, patch, and their interaction, with females suffering from stronger pollen limitation when locally frequent. In the most pollen‐limited situation, the selfing rate of hermaphrodites increased and provided hermaphrodites with a type of reproductive assurance that is not available to females. By integrating both the beneficial (reproductive assurance) and costly effects (through inbreeding depression) of self‐pollination, we showed that whether females did or did not exhibit higher seed fitness depended on the degree of pollen limitation on seed production.     

Size-dependent pollen:ovule ratios and the allometry of floral sex allocation in Clarkia (Onagraceae) taxa with contrasting mating systems

Multiple field populations of two pairs of diploid sister taxa with contrasting mating systems in the genus Clarkia (Onagraceae) were surveyed to test predictions concerning the effects of resource status, estimated as plant size, on pollen and ovule production and on the pollen:ovule (P:O) ratio of flowers. Most theoretical models of size-dependent sex allocation predict that, in outcrossing populations, larger plants should allocate more resources to female function. Lower P:O ratios in larger plants compared to smaller plants have been interpreted as supporting this prediction. In contrast, we predicted that P:O ratio should not vary with plant size in predominantly selfing plants, in which each flower contributes to reproductive success equally through male and female function. We found that, in all four taxa, both ovule and pollen production per flower usually increased significantly with plant size and that the shape of this relationship was decelerating. However, ovule production either decelerated more rapidly than or at the same rate as pollen production with plant size. Consequently,the P:O ratio increased or had no relationship with plant size. This relationship was population-specific (not taxon-specific) and independent of the mating system. Possible explanations for the increasing maleness with plant size are discussed.     

Genotypic variation for reproductive characters,and the influence of pollen-ovule ratio on selfing rate in rape seed (Brassica napus)

The variance component for genotypic effects and covariable plant vigor were estimated for pollen production, number of ovules, the weight of the flower without anther sacs and pistil, and the gender of the whole plant, in the rape seed variety Topas. There was a significant effect of the genotype for all measured characters. We did not find any trade-off between the male and female functions. Small plants were relatively more male-biased than large plants. The weight of the flower without anther sacs or pistil was positively correlated with pollen production. The selfing rates of the lines were positively correlated with the pollen-ovule ratio, suggesting that the selfing rate of individual plants is positively correlated with pollen-ovule ratio, thus supporting the “mass-action” model. It is proposed that the observed increase in the population selfing rate during the flowering season for some species, including rape seed, can be caused by an overall decrease in male investment.     

Floral dimorphism, pollination, and self-fertilization in gynodioecious GERANIUM RICHARDSONII (Geraniaceae)

The selective maintenance of gynodioecy depends on the relative fitness of the male-sterile (female) and hermaphroditic morphs. Females may compensate for their loss of male fitness by reallocating resources from male function (pollen production and pollinator attraction) to female function (seeds and fruits), thus increasing seed production. Females may also benefit from their inability to self-fertilize if selfing and inbreeding depression reduce seed quality in hermaphrodites. We investigated how differences in floral resource allocation (flower size) between female and hermaphroditic plants affect two measures of female reproductive success, pollinator visitation and pollen receipt, in gynodioecious populations of Geranium richardsonii in Colorado. Using emasculation treatments in natural populations, we further examined whether selfing by autogamy and geitonogamy comprises a significant proportion of pollen receipt by hermaphrodites. Flowers of female plants are significantly smaller than those of hermaphrodites. The reduction in allocation to pollinator-attracting structures (petals) is correlated with a significant reduction in pollinator visitation to female flowers in artificial arrays. The reduction in attractiveness is further manifested in significantly less pollen being deposited on the stigmas of female flowers in natural populations. Autogamy is rare in these protandrous flowers, and geitonogamy accounts for most of the difference in pollen receipt between hermaphrodites and females. Female success at receiving pollen was negatively frequency dependent on the relative frequency of females in populations. Thus, two of the prerequisites for the maintenance of females in gynodioecious populations, differences in resource allocation between floral morphs and high selfing rates in hermaphrodites, occur in G. richardsonii.     

Selection caused by self-fertilization I. Four measures of self-fertilization and their effects on fitness

The standard models of selfing in seed plants consider only the ovules, which are assumed to have a constant selfing rate. It has recently become clear, however, that hermaphrodite or monoecious populations frequently show sexual asymmetry (nonconstant pollen:ovule fertilities among individuals). Such asymmetry usually results in pollen selfing rates which differ from those for the ovules and are frequency-dependent even for constant ovule selfing rates. A recent study of selfing rates for all gametes of an individual is extended here to include four selfing rates (for ovules, pollen, all gametes, and zygotes), and simple mathematical relationships linking the four rates are obtained. Unlike earlier models of selfing, it is not assumed that the ovule selfing rate is constant, but instead that this rate, like all the others, is determined by the mobility of the pollen, which in turn is determined by the floral biology and ecology. It is found that all four selfing rates are usually frequency-dependent. The selfing rate for all gametes (the combined selfing rate) is usually intermediate between those for the ovules and pollen, and the zygotic rate is usually the smallest of the four. The exceptions to the above statements occur for relatively extreme situations, such as complete selfing for pollen or ovules, no selfing, or sexual symmetry. Three modes of selfing are considered: prior (PS), competing (CS), and delayed (DS) self-fertilization. It is shown that if there are at least two types with different selfing rates in the population, then the ranking of their selfing rates may depend upon the frequencies of the types (for the combined and the zygotic rates), may be frequency-independent (ovule rate), or may be dependent or independent, according to the mode of selfing (pollen rate). The effects of the various influences on the amount of selfing are by no means negligible. Thus a numerical study shows pollen selfing rates for one type which vary from 0.09 to 0.96, according to its frequency. Another numerical result shows a change in combined selfing rate from 0.13 to 0.86, depending solely on the mode of selfing. Results for Scots Pine show that an ovule selfing rate of 0.5 was accompanied by a combined rate of 0.143.The population selfing rate is not the same as the mean of individual selfing rates, and can only be obtained if female fitnesses as well as ovule selfing rates are known for each type.Previous models of selfing have failed to distinguish between the effects of increased selfing and increased pollen fertility, with the result that increased selfing always resulted in greater fitness. In the present models the two effects are distinguishable, and it is found that increased selfing may result in increased or decreased fitness, depending also on population density and on a form of pollen density. Thus the old dogma that in the absence of viability and fertility selection increased selfing always results in increased fitness is finally refuted, and the importance of the influence of ecological parameters on selfing and fitness is emphasized, since population density and pollen density influence the selfing rates.     

INBREEDING DEPRESSION IN ANDRODIOECIOUS POPULATIONS OF DATISCA GLOMERATA (DATISCACEAE)

Several workers have suggested that the rarity of androdioecy (the presence of males and hermaphrodites in a breeding population) in nature is due to the large fitness gain required by male plants in order to be maintained by selection. As part of an ongoing investigation of this hypothesis, we tested the effects of selfing on fitness in functionally androdioecious populations of Datisca glomerata. We compared progeny from self-fertilizations, cross-fertilizations with pollen from male plants only, cross-fertilizations with pollen from hermaphrodite plants only, and open-pollinated flowers for several measures of progeny fitness including seed weight, germination rate, and seedling weight. Significant inbreeding depression was observed for androdioecious populations of D. glomerata for both seed and seedling weights. However, no significant differences were observed across treatments for seed germination percentages. The observation of significant levels of inbreeding depression in this study, combined with prior evidence of threefold greater pollen production by males, may at least partially account for the large fitness increase required by males to be maintained by selection.     

Pollen discounting and the evolution of selfing in Arenaria uniflora (caryophyllaceae)

Although most models of mating system evolution assign a central role to the male transmission advantage of selfing genotypes, empirical data on the male fitness consequences of increased self-pollination are still uncommon. Here, I use measures of pollen import and export by focal plants in genotyped arrays to investigate the effects of floral morphology and pollination environment on self and outcross male function. Plants from an autogamous population of Arenaria uniflora (Caryophyllaceae) exhibit complete pollen discounting relative to closely related outcrossers, as do morphologically intermediate F1 hybrids between the two populations. However, the low cumulative male fitness of hybrids probably results from reduced pollen number or competitive ability, rather than a nonlinear relationship with floral morphology. When surrounded by selfers, plants from the outcrosser population self-fertilize at nearly the same rate as selfers (>80%), but have much lower self male fitness due to reduced fruit set. Because outcross siring success is also extremely low (<8%) in this treatment, these mate-limited outcrossers are at male fitness disadvantage to both pseudocleistogamous selfers and nonlimited outcrossers. The relative male fitness of plants with different mating systems appears dependent on the ecological context, as well as on morphological trade-offs.     

Functional pleiotropy and mating system evolution in plants: frequency-independent mating

Mutations that alter the morphology of floral displays (e.g., flower size) or plant development can change multiple functions simultaneously, such as pollen export and selfing rate. Given the effect of these various traits on fitness, pleiotropy may alter the evolution of both mating systems and floral displays, two characters with high diversity among angiosperms. The influence of viability selection on mating system evolution has not been studied theoretically. We model plant mating system evolution when a single locus simultaneously affects the selfing rate, pollen export, and viability. We assume frequency-independent mating, so our model characterizes prior selfing. Pleiotropy between increased viability and selfing rate reduces opportunities for the evolution of pure outcrossing, can favor complete selfing despite high inbreeding depression, and notably, can cause the evolution of mixed mating despite very high inbreeding depression. These results highlight the importance of pleiotropy for mating system evolution and suggest that selection by nonpollinating agents may help explain mixed mating, particularly in species with very high inbreeding depression.     

Pollination ecology and inbreeding depression control individual flowering phenologies and mixed mating

We analyze evolution of individual flowering phenologies by combining an ecological model of pollinator behavior with a genetic model of inbreeding depression for plant viability. The flowering phenology of a plant genotype determines its expected daily floral display which, together with pollinator behavior, governs the population rate of geitonogamous selfing (fertilization among flowers on the same plant). Pollinators select plant phenologies in two ways: they are more likely to visit plants displaying more flowers per day, and they influence geitonogamous selfing and consequent inbreeding depression via their abundance, foraging behavior, and pollen carry‐over among flowers on a plant. Our model predicts two types of equilibria at stable intermediate selfing rates for a wide range of pollinator behaviors and pollen transfer parameters. Edge equilibria occur at maximal or minimal selfing rates and are constrained by pollinators. Internal equilibria occur between edge equilibria and are determined by a trade‐off between pollinator attraction to large floral displays and avoidance of inbreeding depression due to selfing. We conclude that unavoidable geitonogamous selfing generated by pollinator behavior can contribute to the common occurrence of stable mixed mating in plants.     

HOW SELFING,INBREEDING DEPRESSION,AND POLLEN LIMITATION IMPACT NUCLEAR‐CYTOPLASMIC GYNODIOECY: A MODEL

Gynodioecy, the co‐occurrence of females and hermaphrodites, is often due to conflicting interactions between cytoplasmic male sterility genes and nuclear restorers. Although gynodioecy often occurs in self‐compatible species, the effect of self‐pollination, inbreeding depression, and pollen limitation acting differently on females and hermaphrodites remains poorly known in the case of nuclear‐cytoplasmic gynodioecy (NCG). In this study, we model NCG in an infinite population and we study the effect of selfing rate, inbreeding depression, and pollen limitation on the maintenance of gynodioecy and on sex ratios at equilibrium. We found that selfing and inbreeding depression have a strong impact, which depends on whether restorer cost acts on male or female fitness. When cost affects male fitness, the strength of cost has no effect, whereas selfing and inbreeding depression only impact gynodioecy by modifying the value of the female advantage. When cost affects female fitness, selfing facilitates NCG and reduces the role of strength of the cost, even when no inbreeding depression occurs, whereas inbreeding depression globally restricts the maintenance of the polymorphism. Finally, we found that pollen limitation could additionally strongly modify the dynamic of gynodioecy. We discuss our findings in the light of empirical data available in gynodioecious species.     

The effect of protandry on siring success in Chamerion angustifolium (Onagraceae) with different inflorescence sizes

Abstract Protandry, a form of temporal separation of gender within hermaphroditic flowers, may reduce the magnitude of pollen lost to selfing (pollen discounting) and also serve to enhance pollen export and outcross siring success. Because pollen discounting is strongest when selfing occurs between flowers on the same plant, the advantage of protandry may be greatest in plants with large floral displays. We tested this hypothesis with enclosed, artificial populations of Chamerion angustifolium (Onagraceae) by experimentally manipulating protandry (producing uniformly adichogamous or mixed protandrous and adichogamous populations) and inflorescence size (two-, six-, or 10-flowered inflorescences) and measuring pollinator visitation, seed set, female outcrossing rate, and outcross siring success. Bees spent more time foraging on and visited more flowers of larger inflorescences than small. Female outcrossing rates did not vary among inflorescence size treatments. However, seed set per fruit decreased with increasing inflorescence size, likely as a result of increased abortion of selfed embryos, perhaps obscuring the magnitude of geitonogamous selfing. Protandrous plants had a marginally higher female outcrossing rate than adichogamous plants, but similar seed set. More importantly, protandrous plants had, on average, a twofold siring advantage relative to adichogamous plants. However, this siring advantage did not increase linearly with inflorescence size, suggesting that protandry acts to enhance siring success, but not exclusively by reducing between-flower interference.     

Inbreeding in Mimulus guttatus Reduces Visitation by Bumble Bee Pollinators

Inbreeding in plants typically reduces individual fitness but may also alter ecological interactions. This study examined the effect of inbreeding in the mixed-mating annual Mimulus guttatus on visitation by pollinators (Bombus impatiens) in greenhouse experiments. Previous studies of M. guttatus have shown that inbreeding reduced corolla size, flower number, and pollen quantity and quality. Using controlled crosses, we produced inbred and outbred families from three different M. guttatus populations. We recorded the plant genotypes that bees visited and the number of flowers probed per visit. In our first experiment, bees were 31% more likely to visit outbred plants than those selfed for one generation and 43% more likely to visit outbred plants than those selfed for two generations. Inbreeding had only a small effect on the number of flowers probed once bees arrived at a genotype. These differences were explained partially by differences in mean floral display and mean flower size, but even when these variables were controlled statistically, the effect of inbreeding remained large and significant. In a second experiment we quantified pollen viability from inbred and self plants. Bees were 37–54% more likely to visit outbred plants, depending on the population, even when controlling for floral display size. Pollen viability proved to be as important as floral display in predicting pollinator visitation in one population, but the overall explanatory power of a multiple regression model was weak. Our data suggested that bees use cues in addition to display size, flower size, and pollen reward quality in their discrimination of inbred plants. Discrimination against inbred plants could have effects on plant fitness and thereby reinforce selection for outcrossing. Inbreeding in plant populations could also reduce resource quality for pollinators, potentially resulting in negative effects on pollinator populations.