Plant population dynamics, pollinator foraging, and the selection of self-fertilization

Many flowering plants rely on pollinators, self-fertilization, or both for reproduction. We model the consequences of these features for plant population dynamics and mating system evolution. Our mating systems-based population dynamics model includes an Allee effect. This often leads to an extinction threshold, defined as a density below which population densities decrease. Reliance on generalist pollinators who primarily visit higher density plant species increases the extinction threshold, whereas autonomous modes of selfing decrease and can eliminate the threshold. Generalist pollinators visiting higher density plant species coupled with autonomous selfing may introduce an effect where populations decreasing in density below the extinction threshold may nonetheless persist through selfing. The extinction threshold and selfing at low density result in populations where individuals adopting a single reproductive strategy exhibit mating systems that depend on population density. The ecological and evolutionary analyses provide a mechanism where prior selfing evolves even though inbreeding depression is greater than one-half. Simultaneous consideration of ecological and evolutionary dynamics confirms unusual features (e.g., evolution into extinction or abrupt increases in population density) implicit in our separate consideration of ecological and evolutionary scenarios. Our analysis has consequences for understanding pollen limitation, reproductive assurance, and the evolution of mating systems.     

Darwin's legacy: the forms,function and sexual diversity of flowers

Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwin''s insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwin''s seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwin''s efforts towards integration.     

Conservation implications of the reproductive ecology of Agalinis acuta (Scrophulariaceae)

Reproductive ecology of Agalinis acuta was investigated by examining potential for self-fertilization before and at anthesis, reproductive output from outcrossed vs. selfed matings, and effects of browsing, plant size, and conspecific plant density on seed and fruit production. These features of a plant species can provide indirect information pertinent to conservation such as patterns and maintenance of genetic diversity, risk associated with inbreeding depression, and changes in pollinator abundance or effectiveness. The species is self-compatible, with 97% of selfed flowers setting fruit; pollinators were not required for reproduction. However, seed set in self-pollinated fruits averaged 17-20% less than that in open-pollinated fruits. Geitonogamous and facilitated selfing are possible throughout anthesis and autonomous selfing is possible late in anthesis as corollas abscise. Delaying self-pollination until after outcrossing opportunities likely limits selfing rates and thus reduces risks associated with inbreeding but allows reproduction in absence of pollinators. Supplementing pollen on open-pollinated flowers yielded no additional seed set over controls. Neither early-season browsing of primary stems nor conspecific plant density had significant effects on number of fruits per plant, on fruit size, or on number of seeds from open-pollinated flowers. Currently, reproduction appears to be high (about 2400 seeds/plant), and future risks due to lack of genetic diversity are likely low.     

Reproductive compensation in the evolution of plant mating systems

Reproductive compensation, the replacement of dead embryos by potentially viable ones, is known to play a major role in the maintenance of deleterious mutations in mammalian populations. However, it has received little attention in plant evolution. Here we model the joint evolution of mating system and inbreeding depression with reproductive compensation. We used a dynamic model of inbreeding depression, allowing for partial purging of recessive lethal mutations by selfing. We showed that reproductive compensation tended to increase the mean number of lethals in a population, but favored self-fertilization by effectively decreasing early inbreeding depression. When compensation depended on the selfing rate, stable mixed mating systems can occur, with low to intermediate selfing rates. Experimental evidence of reproductive compensation is required to confirm its potential importance in the evolution of plant mating systems. We suggest experimental methods to detect reproductive compensation.     

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.     

A Measure of the Various Modes of Inbreeding in Kalmia latifolia

Inbreeding can occur in several ways. For a given species, analysingoverall inbreeding down to its component parts can be usefulin explaining how and why inbreeding is maintained in a population.Kalmia latifolia, a long-lived evergreen shrub, was chosen forthis study for two reasons: its unique floral morphology suggestedthat it was specially adapted to assure reproduction in thedelayed mode of self-fertilization, and previous studies hadsuggested that populations that were more limited by pollinatorsshowed higher rates of within-flower self-fertilization whenpollinators were excluded. Floral manipulations, controlledpollinations, and paternity analysis were performed to determinethe most common form of inbreeding within a flower, among flowersof one individual, or among related individuals. Although plantsare capable of setting seed within a flower, the overall rateof inbreeding was low. Among the modes of inbreeding withinone individual, a negligible selfing rate among emasculatedflowers suggests that selfing is more prevalent within a flowerthan among flowers on the same plant. In addition, as the multi-locusestimate of inbreeding was less than the single-locus estimate,inbreeding among related individuals also contributes to thenatural level of inbreeding. Copyright 2000 Annals of BotanyCompany Kalmia latifolia; mountain laurel; pollination; geitonogamy; autogamy; self-fertilization; inbreeding     

The evolution of self-fertilization in perennials

Abstract Many plants are perennials, but studies of self-fertilization do not usually include features of perennial life histories. We therefore develop models that include selfing, a simple form of perenniality, adult inbreeding depression, and an adult survivorship cost to seed production. Our analysis shows that inbreeding depression in adults diminishes the genetic transmission advantage associated with selfing, especially in long-lived perennials that experience inbreeding depression over many seasons. Perennials also pay a cost when selfing increases total seed set at the expense of future survivorship and reproduction. Such life-history considerations shed new light on the generalization that annuals self-fertilize more than perennials. Past research suggested reproductive assurance as an explanation for this association, but common modes of selfing offer equal reproductive assurance to annuals and perennials. Instead, perennials may avoid selfing because of adult inbreeding depression and the cost to future survivorship and reproduction.     

Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations

The fact that selfing increases seed set (reproductive assurance) has often been put forward as an important selective force for the evolution of selfing. However, the role of reproductive assurance in hermaphroditic populations is far from being clear because of a lack of theoretical work. Here, I propose a theoretical model that analyzes self-fertilization in the presence of reproductive assurance. Because reproductive assurance directly influences the per capita growth rate, I developed an explicit demographic model for partial selfers in the presence of reproductive assurance, specifically when outcrossing is limited by the possibility of pollen transfer (Allee effect). Mating system parameters are derived as a function of the underlying demographical parameters. The functional link between population demography and mating system parameters (reproductive assurance, selfing rate) can be characterized. The demographic model permits the analysis of the evolution of self-fertilization in stable populations when reproductive assurance occurs. The model reveals some counterintuitive results such as the fact that increasing the fraction of selfed ovules can, in certain circumstances, increase the fraction of outcrossed ovules. Moreover, I demonstrate that reproductive assurance per se cannot account for the evolution of stable mixed selfing rates. Also, the model reveals that the extinction of outcrossing populations depends on small changes in population density (ecological perturbations), while the transition from outcrossing to selfing can, in certain cases, lead the population to extinction (evolutionary suicide). More generally, this paper highlights the fact that self-fertilization affects both the dynamics of individuals and the dynamics of selfing genes in hermaphroditic populations.     

Lower selfing rate at higher altitudes in the alpine plant Eritrichium nanum (Boraginaceae)

A general hypothesis on mating patterns in alpine plants states that self-fertilization should increase with increasing altitude as a result of pollinator limitation at higher altitudes. However, realized selfing rates under natural conditions, as based on genetic progeny analysis, have not yet been determined for any alpine species across altitude. We therefore assessed the realized selfing rates in about 100 open-pollinated families of the high-alpine cushion plant Eritrichium nanum, sampled along an altitudinal gradient in the Swiss Alps, by using progeny analysis based on six microsatellites. In marked contrast to the general hypothesis, realized selfing rates in E. nanum significantly decreased with increasing altitude, and only progenies from low altitudes were predominantly selfed. However, the higher selfing rates of individuals at lower altitudes could have been caused by unfavorable weather conditions during early growing season when low-elevation plants flowered. In summary, our results on selfing rates in an alpine plant across altitude as well as the results of other studies using experimental hand-pollinations and/or population genetic methods generally do not support the expectation of higher selfing rates at higher altitudes. We therefore ask for further critical examination of realized mating systems in alpine plants.     

Allee effect and self-fertilization in hermaphrodites: reproductive assurance in a structured metapopulation

Reproductive assurance through selfing during colonization events or when population densities are low has often been put forward as a mechanism selecting for the evolution of self-fertilization. Such arguments emphasize on the role of both local demography and metapopulation processes. We developed a model for the evolution of self-fertilization in a structured metapopulation in which local densities are not steady because of population growth. Reproduction by selfing is density-independent (reproductive assurance) but selfed seeds endure inbreeding depression, whereas reproduction by outcrossing is density-dependent (Allee effect). First, we derived an analytical criterion for metapopulation viability as a function of the selfing rate and metapopulation parameters. We show that outcrossers can develop a viable metapopulation when they produce a high amount of dispersal seeds that counterbalances their incapacity to found new populations from low densities. Second, the model shows there is a positive feedback between demography and outcrossing rates, leading to either complete outcrossing or selfing. Specifically, we illustrate that inbreeding depression can paradoxically favor the evolution of selfing because of its negative effect on density. Also, complete outcrossing can be selected despite pollen limitation, although it does not provide a full seed set. This model underlines the influence of the mating system both on demography and gene dynamics in a metapopulation context.     

Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans

Sexual reproduction occurs in two fundamentally different ways: by outcrossing, in which two distinct partners contribute nuclei, or by self-fertilization (selfing), in which both nuclei are derived from the same individual. Selfing is common in flowering plants, fungi, and some animal taxa. We investigated the genetic basis of selfing in the homothallic fungus Aspergillus nidulans. We demonstrate that alpha and high-mobility group domain mating-type (MAT) genes, found in outcrossing species, are both present in the genome of A. nidulans and that their expression is required for normal sexual development and ascospore production. Balanced overexpression of MAT genes suppressed vegetative growth and stimulated sexual differentiation under conditions unfavorable for sex. Sexual reproduction was correlated with significantly increased expression of MAT genes and key genes of a pheromone-response MAP-kinase signaling pathway involved in heterothallic outcrossing. Mutation of a component MAP-kinase mpkB gene resulted in sterility. These results indicate that selfing in A. nidulans involves activation of the same mating pathways characteristic of sex in outcrossing species, i.e., self-fertilization does not bypass requirements for outcrossing sex but instead requires activation of these pathways within a single individual. However, unlike heterothallic species, aspects of pheromone signaling appeared to be independent of MAT control.     

Evolutionary analysis of a key floral trait in aquilegia canadensis (ranunculaceae): genetic variation in herkogamy and its effect on the mating system

The mating system of flowering plant populations evolves through selection on genetically based phenotypic variation in floral traits. The physical separation of anthers and stigmas within flowers (herkogamy) is expected to be an important target of selection to limit self-fertilization. We investigated the pattern of phenotypic and genetic variation in herkogamy and its effect of self-fertilization in a broad sample of natural populations of Aquilegia canadensis, a species that is highly selfing despite strong inbreeding depression. Within natural populations, plants exhibit substantial phenotypic variation in herkogamy caused primarily by variation in pistil length rather than stamen length. Compared to other floral traits, herkogamy is much more variable and a greater proportion of variation is distributed among rather than within individuals. We tested for a genetic component of this marked phenotypic variation by growing naturally pollinated seed families from five populations in a common greenhouse environment. For three populations, we detected a significant variation in herkogamy among families, and a positive regression between parental herkogamy measured in the field and progeny herkogamy in the greenhouse, suggesting that there is often genetic variation in herkogamy within natural populations. We estimated levels of self-fertilization for groups of flowers that differed in herkogamy and show that, as expected, herkogamy was associated with reduced selfing in 13 of 19 populations. In six of these populations, we performed floral emasculations to show that this decrease in selfing is due to decreased autogamy (within-flower selfing), the mode of selfing that herkogamy should most directly influence. Taken together, these results suggest that increased herkogamy should be selected to reduce the production of low-quality selfed seed. The combination of high selfing and substantial genetic variation for herkogamy in A. canadensis is enigmatic, and reconciling this observation will require a more integrated analysis of how herkogamy influences not only self-fertilization, but also patterns of outcross pollen import and export.     

RESPONSE TO SELECTION IN PARTIALLY SELF-FERTILIZING POPULATIONS. I. SELECTION ON A SINGLE TRAIT

Self-fertilization is a common form of reproduction in plants and it has important implications for quantitative trait evolution. Here, I present a model of selection on quantitative traits that can accommodate any level of self-fertilization. The “structured linear model” (SLM) predicts the evolution of the mean phenotype as a function of three distinct quantities: the mean additive genetic value, the directional dominance, and the mean inbreeding coefficient. Stochastic simulations of truncation selection demonstrate the accuracy of the SLM in predicting changes in the mean and variance of a quantitative trait over the full range of selfing rates. They also illustrate how complex interactions between selection and mating system determine the population distribution of inbreeding coefficients and also the amount of linkage disequilibrium. Changes in the genetic variance due to linkage disequilibria, which are commonly referred to as the “Bulmer effect,” are greatly magnified by selfing. This complicates the relationship between selfing rate and response to selection. Like the random mating theory, the parameters of the SLM can be estimated from phenotypic data.     

Transposable element number in mixed mating populations

Theoretical population genetic studies of transposable elements focus almost exclusively on random mating species, whereas many plants reproduce through partial or substantial self-fertilization. Here I develop computer simulation and analytic approximations of simplified element dynamics (transposition balanced by selective elimination) in partially self-fertilizing populations, using Ty1-copia elements for biological inspiration. Under the most plausible models and parameter values, element numbers decrease with self-fertilization when element insertions are deleterious, but may increase when ectopic exchange regulates element number. Conclusions for models of ectopic exchange depend in part on parameters for which little firm empirical evidence is available. Small changes in selfing rate can lead to abrupt changes in element number when homozygous and heterozygous elements have markedly different fitness effects. Equilibrium element numbers can be sensitive to population size, especially at high selfing rates. Elements are frequently lost in small highly selfing populations under the deleterious insertion model. In contrast, small highly selfing populations can accumulate very large numbers of elements under ectopic exchange. Empirical data on element number and localization in plants with different mating systems suggests that deleterious insertion, rather than ectopic exchange, may regulate element number. Limitations to available empirical data, especially the lack of comparison between closely related species differing in mating system, mean that this conclusion is tentative.     

EXPERIMENTAL EVIDENCE FOR FREQUENCY DEPENDENT SELF-FERTILIZATION IN THE GYNODIOECIOUS PLANT, SILENE VULGARIS

After over a half century of empirical and theoretical research regarding the evolution and maintenance of gynodioecy in plants, unexplored factors influencing the relative fitnesses of females and hermaphrodites remain. Theoretical studies suggest that hermaphrodite self-fertilization (selfing) rate influences the maintenance of gynodioecy and we hypothesized that population sex ratio may influence hermaphrodite selfing rate. An experimental test for frequency-dependent self-fertilization was conducted using replicated populations constructed with different sex ratios of the gynodioecious plant Silene vulgaris . We found that hermaphrodite selfing increased with decreased hermaphrodite frequency, whereas evidence for increased inbreeding depression was equivocal. We argue that incorporation of context dependent inbreeding into future models of the evolution of gynodioecy is likely to yield novel insights into sex ratio evolution.     

Why is cleistogamy a selected reproductive strategy in Impatiens capensis (Balsaminaceae)?

Cleistogamy (self-fertilization in closed flowers) differs from chasmogamy (open-pollinated fertilization) mainly in sustaining selfing. Why numerous species develop both of the reproductive modes on the same individuals has long puzzled biologists. In a novel hypothesis presented here, I propose that cleistogamy could be a means by which inbred lines are created and maintained in natural populations; these lines would continuously experience self-improvement via natural selection and via crosses among lines at the chasmogamous flowers to benefit the populations. Supporting evidence for the hypothesis was found in Impatiens capensis where cleistogamous ovules were fertilized proportionately less (56%) than chasmogamous ovules (67%) in natural populations, but crosses among cleistogamous progeny in the greenhouse led to a nearly 10% increase of fertilized chasmogamous ovules. I established a novel fitness model specific to the cleistogamous species to further examine how various aspects of the mating system affect plant performance. A low inbreeding depression (0.07) was consequently found for the surveyed natural populations of I. capensis , suggesting that the individual-level percentage of cleistogamy and the population-level selfing rate may have evolved in the direction of reducing the overall inbreeding depression. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 543–553.     

Selection caused by self-fertilization

The generally held view that increased self-fertilization should be advantageous in the absence of counteracting selective forces reducing viability or fertility is reexamined. It is pointed out that the models on which this view is based all imply a gain in male (pollen) fertility with increased selfing. Hence, the postulated advantage may equally well be due to increased fertility, a fact which reopens the discussion on the selective significance of differential selfing. A new model for differential self-fertilization is presented which avoids built-in fertility selection by explicitly considering pollen available for self- and for cross-pollination. Plant types are distinguished with respect to their amounts r_i of pollen available for self-pollination, and these types are assumed to be identical with respect to their pollen and ovule fertilities. Moreover, the efficiency of cross-pollination is allowed to depend, for example, on population density, thus giving rise to a parameter b called “crossing potential”, while the efficiency of self-pollination is described by a parameter a called “selfing potential”. These parameters may be conceived of as ecological parameters. Increasing r_i produces a simultaneous increase in each of the four measures of self-fertilization (introduced in Part I of the present series) irrespective of the values of the ecological parameters. It is then shown that increased selfing can be both advantageous and disadvantageous in terms of fitness, dependig on the ecological parameters as well as on the mode of self-fertilization (i.e. where selfing occurs before or after outcrossing). The main result is, roughly, that for both selfing modes high crossing and low selfing potential favour increased cross-fertilization, while the reverse favours increased self-fertilization. However, the regions for a and b in which this holds true differ substantially for the two selfing modes. In the complements of these regions strange conditions for the evolution of increased selfing or outcrossing, respectively, exist. The significance of these results for explaining experimental observations is discussed.     

The mixed mating system of the sea palm kelp Postelsia palmaeformis: few costs to selfing

Naturally isolated populations have conflicting selection pressures for successful reproduction and inbreeding avoidance. These species with limited seasonal reproductive opportunities may use selfing as a means of reproductive assurance. We quantified the frequency of selfing and the fitness consequences for inbred versus outcrossed progeny of an annual kelp, the sea palm (Postelsia palmaeformis). Using experimentally established populations and microsatellite markers to assess the extent of selfing in progeny from six founding parents, we found the frequency of selfing was higher than expected in every population, and few fitness costs were detected in selfed offspring. Despite a decline in heterozygosity of 30 per cent in the first generation of selfing, self-fertilization did not affect individual size or reproduction, and correlated only with a marginally significant decline in survival. Our results suggest both that purging of deleterious recessive alleles may have already occurred and that selfing may be key to reproductive assurance in this species with limited dispersal. Postelsia has an alteration of a free-living diploid and haploid stage, where the haploid stage may provide increased efficiency for purging the genetic load. This life history is shared by many seaweeds and may thus be an important component of mating system evolution in the sea.     

Prior selfing and the selfing syndrome in animals: an experimental approach in the freshwater snail Biomphalaria pfeifferi.

Inbreeding species of hermaphroditic animals practising copulation have been characterized by few copulations, no waiting time (the time that an isolated individual waits for a partner before initiating reproduction compared with paired individuals) and limited inbreeding (self-fertilization) depression. This syndrome, which has never been fully studied before in any species, is analysed here in the highly selfing freshwater snail Biomphalaria pfeifferi. We conducted an experiment under laboratory conditions over two generations (G1 and G2) using snails sampled from two populations (100 individuals per population). G1 individuals were either isolated or paired once a week (potentially allowing for crosses), and monitored during 29 weeks for growth, fecundity and survival. Very few copulations were observed in paired snails, and there was a positive correlation in copulatory activity (e.g. number of copulations) between the male and female sexual roles. The waiting time was either null or negative, meaning that isolated individuals initiated reproduction before paired ones. G2 offspring did not differ in hatching rate and survival (to 28 days) between treatments, but offspring from paired individuals grew faster than those from isolated individuals. On the whole, the self-fertilization depression was extremely low in both populations. Another important result is that paired G1 individuals began laying (selfed) eggs several weeks prior to initiating copulation: this is the first characterization of prior selfing (selfing initiated prior to any outcrossing) in a hermaphroditic animal. A significant population effect was observed on most traits studied. Our results are discussed with regard to the maintenance of low outcrossing rates in highly inbreeding species.     

INBREEDING DEPRESSION UNDER JOINT SELFING,OUTCROSSING, AND ASEXUALITY

Partial asexual reproduction was introduced into a model of inbreeding depression due to nearly recessive lethal mutations in a partially selfing population. The frequencies of asexuality, selfing, and outcrossing were either constant or occurred in cycles of a single sexual generation followed by one or more asexual generations. We found that increasing the degree of asexuality generally increases the inbreeding depression maintained in an equilibrium population with a given selfing rate. This is due to the increase in the number of mutations relative to sexual generations during which selfing-induced purging of mutations may take place. For very high genomic mutation rates, sufficient to produce a threshold rate of self-fertilization for purging recessive lethal mutations, asexuality can have the opposite effect, decreasing equilibrium inbreeding depression, because of an increase in the efficiency of selection against mutations in heterozygotes with asexuality.