Effects of variation at the flower-colour A locus on mating system parameters in Ipomoea purpurea

Although alleles at both the W and A loci in the common morning glory, Ipomoea purpurea, produce similar white-flowered phenotypes, these alleles differ by over an order of magnitude in average frequency. In this initial attempt to determine the causes of this difference, we employed artificial arrays of plants to estimate mating system characteristics (total siring success, selfing rates and contribution to the outcross pollen pool) for the homozygous pigmented and white-flowered genotypes at the A locus. This experiment demonstrates that: (1) at both low and high frequencies, white-flowered plants were visited by pollinators at the same rate as plants with pigmented flowers; (2) at both frequencies, the a allele exhibited a greater total siring success (self and outcross pollen) than the A allele; (3) individuals of both genotypes contributed equally to the outcross pollen pool; and (4) aa plants may have a higher selfing rate than AA plants. Coupled with minimal inbreeding depression in I. purpurea, these observations indicate that the allele producing white flowers enjoys a transmission advantage that would tend to cause this allele to increase in frequency. This transmission advantage is very similar to that shown previously to be operating on the white-flowered allele at the W locus, although the specific causes of the advantage appear to differ between loci. The frequency difference between the two alleles is thus not likely to be due to differences in the effect of flower-colour variation on transmission. Rather, substantially greater deleterious pleiotropic effects associated with the white-flower a allele is likely to be the primary cause of the frequency difference.     

EVALUATING A SIMPLE APPROXIMATION TO MODELING THE JOINT EVOLUTION OF SELF‐FERTILIZATION AND INBREEDING DEPRESSION

A comprehensive understanding of plant mating system evolution requires detailed genetic models for both the mating system and inbreeding depression, which are often intractable. A simple approximation assuming that the mating system evolves by small infrequent mutational steps has been proposed. We examine its accuracy by comparing the evolutionarily stable selfing rates it predicts to those obtained from an explicit genetic model of the selfing rate, when inbreeding depression is caused by partly recessive deleterious mutations at many loci. Both models also include pollen limitation and pollen discounting. The approximation produces reasonably accurate predictions with a low or moderate genomic mutation rate to deleterious alleles, on the order of U = 0.02–0.2. However, for high mutation rates, the predictions of the full genetic model differ substantially from those of the approximation, especially with nearly recessive lethal alleles. This occurs because when a modifier allele affecting the selfing rate is rare, homozygous modifiers are produced mainly by selfing, which enhances the opportunity for purging nearly recessive lethals and increases the marginal fitness of the allele modifying the selfing rate. Our results confirm that explicit genetic models of selfing rate and inbreeding depression are required to understand mating system evolution.     

SELECTION ON A FLORAL COLOR POLYMORPHISM IN THE TALL MORNING GLORY (IPOMOEA PURPUREA): TRANSMISSION SUCCESS OF THE ALLELES THROUGH POLLEN

The W locus, a codominant locus influencing floral pigment intensity in the tall morning glory, Ipomoea purpurea, is polymorphic throughout the southeastern United States. Previous studies suggest that this polymorphism is actively maintained by balancing selection, and that increased selfing accompanied by lack of pollen discounting (“Fisher effect”) may act to protect the white allele when it is rare. Processes that act to protect the dark allele and thus stabilize the polymorphism in conjunction with the Fisher effect have not been previously detected. The goal of this study was to determine whether any of three such processes might operate in I. purpurea. Estimates of breeding system parameters in a large experimental population in which the white allele was in higher than normal frequency (0.5) provided little evidence that either dark- or light-flowered plants were more successful as pollen parents than white-flowered plants. In addition, no evidence was found for a transmission bias favoring the dark allele in the ovules produced by light heterozygotes. In contrast, a strong transmission bias favoring the dark allele in pollen of heterozygotes was observed. A simple model using parameter estimates derived from this and previous studies indicates that a balance between the Fisher effect and biased transmission in heterozygote pollen could account for many properties of the polymorphism.     

TRANSMISSION ADVANTAGE FAVORS SELFING ALLELE IN EXPERIMENTAL POPULATIONS OF SELF‐INCOMPATIBLE WITHERINGIA SOLANACEA (SOLANACEAE)

The evolution of self‐fertilization is one of the most commonly traversed transitions in flowering plants, with profound implications for population genetic structure and evolutionary potential. We investigated factors influencing this transition using Witheringia solanacea, a predominantly self‐incompatible (SI) species within which self‐compatible (SC) genotypes have been identified. We showed that self‐compatibility in this species segregates with variation at the S‐locus as inherited by plants in F1 and F2 generations. To examine reproductive assurance and the transmission advantage of selfing, we placed SC and SI genotypes in genetically replicated gardens and monitored male and female reproductive success, as well as selfing rates of SC plants. Self‐compatibility did not lead to increased fruit or seed set, even under conditions of pollinator scarcity, and the realized selfing rate of SC plants was less than 10%. SC plants had higher fruit abortion rates, consistent with previous evidence showing strong inbreeding depression at the embryonic stage. Although the selfing allele did not provide reproductive assurance under observed conditions, it also did not cause pollen discounting, so the transmission advantage of selfing should promote its spread. Given observed numbers of S‐alleles and selfing rates, self‐compatibility should spread even under conditions of exceedingly high initial inbreeding depression.     

Frequency-dependent pollen discounting contributes to maintenance of a mixed mating system in the common morning glory Ipomoea purpurea

Pollen discounting, a reduction in outcross success associated with increased selfing, was evaluated in the common morning glory Ipomoea purpurea. A field experiment was conducted to estimate selfing rates and outcross success using small arrays of plants with large or small anther-stigma distance (ASD). To evaluate the effect of genotypic composition on the mating-system parameters, arrays were composed of five different frequencies of small- and large-ASD genotypes. While the selfing rates of genotypes with small ASD were consistently higher than genotypes with large ASD regardless of the genotypic frequency, outcross success was negatively frequency dependent. The genotype that was at lower frequency in the array had higher outcrossing success in three out of the four array types with unequal frequencies. This advantage-when-rare phenomenon can contribute to preventing the fixation of either extreme ASD-morph and maintaining a mixed mating system in I. purpurea.     

POLLEN DISCOUNTING AND THE SPREAD OF A SELFING VARIANT IN TRISTYLOUS EICHHORNIA PANICULATA: EVIDENCE FROM EXPERIMENTAL POPULATIONS

Floral traits that increase self-fertilization are expected to spread unless countered by the effects of inbreeding depression, pollen discounting (reduced outcross pollen success by individuals with increased rates of self-fertilization), or both. Few studies have attempted to measure pollen discounting because to do so requires estimating the male outcrossing success of plants that differ in selfing rate. In natural populations of tristylous Eichhornia paniculata, selfing variants of the mid-styled morph are usually absent from populations containing all three style morphs but often predominate in nontrimorphic populations. We used experimental garden populations of genetically marked plants to investigate whether the effects of population morph structure on relative gamete transmission by unmodified (M) and selfing variants (M‘) of the mid-styled morph could explain their observed distribution. Transmission through ovules and self and outcross pollen by plants of the M and M’ morphs were compared under trimorphic, dimorphic (S morph absent), and monomorphic (L and S morphs absent) population structures. Neither population structure nor floral morphology affected female reproductive success, but both had strong effects on the relative transmission of male gametes. The frequency of self-fertilization in the M' morph was consistently higher than that of the M morph under all morph structures, and the frequency of self-fertilization by both morphs increased as morph diversity of experimental populations declined. In trimorphic populations, total transmission by the M and M' morphs did not differ. The small, nonsignificant increase in selfing by the M' relative to the M morph was balanced by decreased outcross siring success, particularly on the S morph. In populations lacking the S morph, male gamete transmission by the M' morph was approximately 1.5 times greater than that by the M morph because of both increased selfing and increased success through outcross pollen donation. Therefore, gamete transmission strongly favored the M' morph only in the absence of the S morph, a result consistent with the distribution of the M' morph in nature. This study indicates that floral traits that alter the selfing rate can have large and context-dependent influences on outcross pollen donation.     

The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation

We model the evolution of plant mating systems under the joint effects of pollen discounting and pollen limitation, using a dynamic model of inbreeding depression, allowing for partial purging of recessive lethal mutations by selfing. Stable mixed mating systems occur for a wide range of parameter values with pollen discounting alone. However, when typical levels of pollen limitation are combined with pollen discounting, stable selfing rates are always high but less than 1 (0.9相似文献   

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.     

Selfing rates of pearl millet (Pennisetum typhoides Stapf and Hubb.) under natural conditions

The selfing rate of pearl millet (Pennisetum typhoides Stapf and Hubb.) has been determined under natural conditions. This species is said to be allogamous. Nine test plants homozygous for a particular allele on the alcohol dehydrogenase: ADH A locus (A₁A₁) were sown 2.5 m one from each other interspersed among 300 plants homozygous for the same locus (A₂A₂); these nine plants served as indicators of selfing. In the 20 spikes produced by these a test plants, the selfing rates varied between 2.2% and 21.7%. Selfmg rates were not significantly different within spikes of the same plant, except for one individual. There was no significant correlation between the rate of selfing and the density of the pollen shadow (estimated from the number of spikes producing pollen during the female phase of test plants) or variation in protogyny.     

FIXATION PROBABILITIES OF SELFING RATE MODIFIERS IN SIMULATIONS WITH SEVERAL DELETERIOUS ALLELES WITH LINKAGE

The fixation rates of selfing rate modifiers were found by stochastic simulation in an infinite site model, including effects of several deleterious alleles with variable effects, which were randomly distributed in the genome without assuming any pollen discounting. Previous results on the evolution of selfing obtained by more precise methods were in this study further validated, and it was concluded that the effect of genetic associations on the evolution of mating systems is small except in the case of full pollen discounting. Furthermore, attention was given to the uneven distribution of the genetic load in the population, and the accompanying large among-genome variation in fixation rates. This among-genome variation will be of significance for the evolution of mating systems.     

Coevolution of self-fertilization and inbreeding depression. II. Symmetric overdominance in viability

We describe the evolutionary dynamics of a modifier of selfing coevolving with a locus subject to symmetric overdominance in viability under general levels of reduction in pollination success as a consequence of self-fertilization (pollen discounting). Simple models of the evolution of breeding systems that represent inbreeding depression as a constant parameter do not admit the possibility of stable mixed mating systems involving both inbreeding and random mating. Contrary to this expectation, we find that coevolution between a modifier of selfing and a single overdominant locus situated anywhere in the genome can generate evolutionarily attracting mixed mating systems. Two forms of association between the modifier locus and the viability locus promote the evolution of outcrossing. The favored heterozygous genotype at the viability locus develops positive associations with modifier alleles that enhance outcrossing and with the heterozygous genotype at the modifier locus. Associations between outcrossing and high viability evolve immediately upon the introduction of a rare modifier allele, even in the absence of linkage.     

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.     

Selfing rates in natural populations of Echium vulgare: a combined empirical and model approach

1. We quantified geitonogamous selfing in Echium vulgare , a self-compatible, bumble-bee pollinated plant. A maximum estimate of selfing was determined using a paternity analysis with RAPDs. In the first experiment, bumble-bees visited a sequence of virgin flowers. The percentage selfing increased rapidly from 12% in the first flower visited, up to 50% in the 15th flower visited in the sequence. In the second experiment, when bees visited plants in a natural population, the average selfing of plants increased with the number of open flowers from 0% to maximally 33%.
2. The results obtained in both experiments are consistently lower than predicted by our model on pollen dynamics ( Rademaker, de Jong & Klinkhamer 1997 ). We modified the model on pollen dynamics to link it more to the field situation with observations on flower stage, flower opening and bumble-bee preference, so that the bumble-bees encounter a variable number of pollen grains per flower. We also adjusted the parameters. If less pollen adheres to the bee (25% instead of 50%) after removal from the anthers, or if bees arrive at a plant with more pollen grains (6000 instead of 4448), the predictions of the model in regard to selfing could be improved but were still high compared with the observed selfing rates measured with RAPDs.
3. We suggest that the model is consistent with pollen dynamics in the field. However, post-pollination processes like selective abortion could play a role in E. vulgare .     

Loss of gametophytic self-incompatibility with evolution of inbreeding depression

Gametophytic self-incompatibility (SI) in plants is a widespread mechanism preventing self-fertilization and the ensuing inbreeding depression, but it often evolves to self-compatibility. We analyze genetic mechanisms for the breakdown of gametophytic SI, incorporating a dynamic model for the evolution of inbreeding depression allowing for partial purging of nearly recessive lethal mutations by selfing, and accounting for pollen limitation and sheltered load linked to the S-locus. We consider two mechanisms for the breakdown of gametophytic SI: a nonfunctional S-allele and an unlinked modifier locus that inactivates the S-locus. We show that, under a wide range of conditions, self-compatible alleles can invade a self-incompatible population. Conditions for invasion are always less stringent for a nonfunctional S-allele than for a modifier locus. The spread of self-compatible genotypes is favored by extremely high or low selfing rates, a small number of S-alleles, and pollen limitation. Observed parameter values suggest that the maintenance of gametophytic SI is caused by a combination of high inbreeding depression in self-incompatible populations coupled with intermediate selfing rates of the self-compatible genotypes and sheltered load linked to the S-locus.     

THE ROLE OF INBREEDING DEPRESSION IN MAINTAINING THE MIXED MATING SYSTEM OF THE COMMON MORNING GLORY,IPOMOEA PURPUREA

Theoretical studies show that, although inbreeding depression (ID) will counterbalance the transmission advantage of selfing, it can only maintain a mixed mating system in plants when at least one of the following two conditions is met: (1) there is a positive association between selfing rates and the level of ID; and (2) ID is greater than 0.5 for the female component of fitness, while the average ID for male and female fitness is less than 0.5. This study tests whether these two conditions hold in the common morning glory, Ipomoea purpurea, which has a mixed mating system with 30% self-fertilization. Inbreeding depression was found in all but one fitness component measured in two groups of plants with distinct anther-stigma distances (ASD), a character that influences selfing rates. However, when examined separately, a negative association was found between selfing rates and ID; plants with large ASD (low-selfing-rate genotypes) tended to have higher ID than ones with small ASD (high-selfing-rate genotypes). Furthermore, the overall lifetime ID for male (12.5%) and female (24%) components of fitness, averaged across two ASD groups, were lower than what is necessary for ID to maintain an evolutionarily stable mixed mating system. Therefore, although inbreeding depression contributes to balancing the transmission advantage of selfing, it is not likely to be the primary mechanism maintaining the mixed mating system of I. purpurea. The contribution of other mechanisms is discussed.     

The reproductive assurance benefit of selfing: importance of flower size and population size

Autonomous selfing can provide reproductive assurance (RA) for flowering plants that are unattractive to pollinators or in environments that are pollen limited. Pollen limitation may result from the breakdown of once-continuous habitat into smaller, more isolated patches (habitat fragmentation) if fragmentation negatively impacts pollinator populations. Here we quantify the levels of pollen limitation and RA among large and small populations of Collinsia parviflora, a wildflower with inter-population variation in flower size. We found that none of the populations were pollen limited, as pollen-supplemented and intact flowers did not differ in seed production. There was a significant effect of flower size on RA; intact flowers (can self) produced significantly more seeds than emasculated flowers (require pollen delivery) in small-flowered plants but not large-flowered plants. Population size nested within flower size did not significantly affect RA, but there was a large difference between our two replicate populations for large-flowered, small populations and small-flowered, large populations that appears related to a more variable pollination environment under these conditions. In fact, levels of RA were strongly negatively correlated with rates of pollinator visitation, whereby infrequent visitation by pollinators yielded high levels of RA via autonomous selfing, but there was no benefit of autonomous selfing when visitation rates were high. These results suggest that autonomous selfing may be adaptive in fragmented habitats or other ecological circumstances that affect pollinator visitation rates.     

Differential siring success of Pgi genotypes in Clarkia Unguiculata (Onagraceae)

Competition among pollen grains for the fertilization of ovules can play an important role in determining the male and female reproductive success of flowering plants. To examine the influence of pollen-donor genotype on male reproductive success, hand-pollinations were conducted on Clarkia unguiculata and the siring success of pollen-donor plants was compared between donors homozygous for different allelomorphs of the allozyme PGI (phosphoglucoisomerase). Donors homozygous for the B allele sired more seeds than C-allele donors. Single-donor crosses indicated that C-donor-sired seeds are aborted more often than are B-donor-sired seeds, suggesting that the B-allele donor's advantage in mixed pollinations was a result of differential abortion. A negative relationship between pollen load and the siring success of B-allele donors implies that pollen from B-allele donors has reduced performance relative to C-allele donors when pollen loads are high. These data demonstrate consistent differences in siring success between individuals homozygous for different alleles at a single locus and suggest that variation at the Pgi locus may be maintained by a post-pollination trade-off.     

The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae)

Collinsia verna, blue-eyed Mary, has floral attributes of an outcrossing species, yet most flowers readily self-pollinate under greenhouse conditions. Here we describe the mechanism of self-pollination in C. verna via changes in relative positions of the stigma and anthers and late timing of receptivity, resulting in delayed selfing. Each flower contains four anthers that dehisce sequentially over ∼1 wk. Pollen that is not collected by pollinators accumulates in the keel petal and retains high viability (>80% pollen germination) up to the time of corolla abscission. The stigmatic surface does not become receptive until after the third anther dehisces. This overlap in the sexual phases is concurrent with a change in herkogamy during floral development. In most flowers (70%), the stigma has moved to the front of the keel and is positioned near the anthers when the third anther dehisces. Under field conditions, fruiting success of plants within pollinator exclosures was ∼75% of the fruiting success in open-pollinated plants (33% fruiting success via autogamy vs. 44% fruiting success, respectively). Collinsia verna plants in pollinator exclosures exhibit variation in autogamy rates within natural populations (range 0–80%). In addition, only half of naturally pollinated, receptive flowers examined had pollen tubes growing in their styles. In contrast, shortly after corolla abscission, nearly all flowers examined (96%) had pollen tubes in their styles. Thus we find that in C. verna, autogamy occurs late in floral development, which has the potential to provide substantial reproductive assurance, and that individuals vary in their ability to set fruit through this mechanism. We suggest that delayed selfing mechanisms may be overlooked in other species and that variable pollinator availability may play a significant role in the maintenance of mixed mating in species with delayed selfing, such as C. verna.     

Trade-offs between male and female reproduction associated with allozyme variation in phosphoglucoisomerase in an annual plant (Clarkia unguiculata: Onagraceae)

The genotype of an individual for allozymes such as phosphoglucoisomerase (Pgi) is often not neutral with regard to fitness. Studies of several taxa have found consistent fitness differences among Pgi genotypes expressing different allozymes. We conducted a greenhouse experiment with Clarkia unguiculata to determine whether allelic variation at the Pgi-C1 locus may affect components of male and female function. We found significant differences in siring success between pollen donors homozygous for different Pgi alleles. When a mixture of pollen was applied to stigmas under conditions of gametophytic competition (more pollen deposited on stigmas than there are ovules available to fertilize), donors homozygous for the C allele of Pgi sired more seeds per fruit than B-allele donors. Differences between genotypes with respect to female fertility per fruit contrasted with the male advantage associated with the C allele. Recipients homozygous for the C allele produced fruits with more aborted seeds and fewer viable seeds than recipients homozygous for the B allele. These results suggest that allelic variation at a single locus may have opposing effects on male and female reproductive success in C. unguiculata, and that trade-offs between the two types of reproductive success could contribute to the maintenance of variation at the Pgi-C1 locus.     

GAMETOPHYTIC SELF-FERTILIZATION IN HOMOSPOROUS PLANTS: DEVELOPMENT,EVALUATION, AND APPLICATION OF A STATISTICAL METHOD FOR EVALUATING ITS IMPORTANCE

The methods described here make it possible to use data on sporophytic genotype frequencies to estimate the frequency of gametophytic self-fertilization in populations of homosporous plants. Bootstrap bias reduction is effective in reducing or eliminating the bias of the maximum likelihood estimate of the gametophytic selfing rate. The bias-corrected percentile method provides the most reliable confidence intervals for allele frequencies. The percentile method gives the most reliable confidence intervals for the gametophytic selfing rate when selfing is common. The maximum likelihood intervals, the percentile intervals, the bias-corrected percentile intervals, and the bootstrap t intervals are all overly conservative in their construction of confidence intervals for the gametophytic selfing rate when self-fertilization is rare. Application of the recommended methods indicates that gametophytic self-fertilization is quite rare in two sexually reproducing populations of Pellaea andromedifolia studied by Gastony and Gottlieb (1985).