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.     

Perspective: Evolution of flower color in the desert annual Linanthus parryae: Wright revisited

Linanthus parryae, a diminutive desert annual with white or blue flowers, has been the focus of a long-standing debate among evolutionary biologists. At issue is whether the flower color polymorphism in this species is the product of random genetic drift, as Sewall Wright argued, or of natural selection, as proposed by Carl Epling and his colleagues. Our long-term studies of three polymorphic populations in the Mojave Desert demonstrate that flower color is subject to selection that varies in both time and space in its direction and magnitude. For all sites taken together, blue-flowered plants produced more seeds than white-flowered plants in years of relatively low seed production, whereas white-flowered plants had higher fitness in years of high seed production. Evidence of selection on flower color was found in two of the three study sites. Differences in fitness between the color morphs were sometimes large, with selection coefficients as high as 0.60 in some years. Our longest period of observations was at Pearblossom site 1, where plants reached appreciable densities in seven of the 11 years of study. Here we found significant differences in the seed production of the color morphs in six years, with three years of blue advantage and three years of white advantage. For all sites taken together, total spring precipitation (March and April) was positively correlated with both absolute and relative seed production of the color morphs. At Pearblossom site 1, blue-flowered plants typically had a fitness advantage in years of low spring precipitation, whereas white-flowered plants had a fitness advantage in years of high spring precipitation. This temporal variation in selection may contribute to the maintenance of the flower-color polymorphism at Pearblossom site 1, whereas gene flow from neighboring populations is proposed as the principal factor maintaining the polymorphism at the other study sites. We found no significant differences between the color morphs in pollinator visitation rate or in their carbon isotope ratio, a measure of water-use efficiency. Although the mechanism of selection remains elusive, our results refute Wright's conclusion that the flower color polymorphism in L. parryae is an example of isolation by distance, a key component of his shifting balance theory of evolution.     

The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization

Background

The field of plant mating-system evolution has long been interested in understanding why selfing evolves from outcrossing. Many possible mechanisms drive this evolutionary trend, but most research has focused upon the transmission advantage of selfing and its ability to provide reproductive assurance when cross-pollination is uncertain. We discuss the shared conceptual framework of these ideas and their empirical support that is emerging from tests of their predictions over the last 25 years.

Scope

These two hypotheses are derived from the same strategic framework. The transmission advantage hypothesis involves purely gene-level selection, with reproductive assurance involving an added component of individual-level selection. Support for both of these ideas has been garnered from population-genetic tests of their predictions. Studies in natural populations often show that selfing increases seed production, but it is not clear if this benefit is sufficient to favour the evolution of selfing, and the ecological agents limiting outcross pollen are often not identified. Pollen discounting appears to be highly variable and important in systems where selfing involves multiple floral adaptations, yet seed discounting has rarely been investigated. Although reproductive assurance appears likely as a leading factor facilitating the evolution of selfing, studies must account for both seed and pollen discounting to adequately test this hypothesis.

Conclusions

The transmission advantage and reproductive assurance ideas describe components of gene transmission that favour selfing. Future work should move beyond their dichotomous presentation and focus upon understanding whether selection through pollen, seed or both explains the spread of selfing-rate modifiers in plant populations.     

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.     

THE EVOLUTION OF ASSORTATIVE MATING AND SELFING WITH IN- AND OUTBREEDING DEPRESSION

The effect of inbreeding and outbreeding depression on the evolution of assortment are often considered separately. For instance, inbreeding depression is usually thought to shape selfing rates whereas outbreeding depression is commonly thought to affect the evolution of assortative mating. In this article, we consider the evolution of assortment in a context of local adaptation and we show that it is a typical situation in which both effects act simultaneously to shape the degree of selfing or assortative mating. More specifically, we show that selection on a modifier of mating can be partitioned into three distinct effects: a transmission advantage, an association to heterozygosity (proportional to inbreeding depression), and an association to beneficial alleles (proportional to outbreeding depression), so that random mating may evolve even with strong local adaptation. In addition, we show that it is necessary to carefully delimit the conditions for polymorphism at local adaptation locus to study the evolution of assortment. In particular, the range of parameters most favorable to the maintenance of polymorphism corresponds to situations favoring less assortment.     

How much better are females? The occurrence of female advantage,its proximal causes and its variation within and among gynodioecious species

Background

Gynodioecy is a reproductive system of interest for evolutionary biologists, as it poses the question of how females can be maintained while competing with hermaphrodites that possess both male and female functions. One necessary condition for the maintenance of this polymorphism is the occurrence of a female advantage, i.e. a better seed production or quality by females compared with hermaphrodites. Theoretically, its magnitude can be low when sterility mutations are cytoplasmic, while a 2-fold advantage is needed in the case of nuclear sterility. Such a difference is often thought to be due to reduced inbreeding depression in obligatory outcrossed females. Finally, variation in sex ratio and female advantage occur among populations of some gynodioecious species, though the prevalence of such variation is unknown.

Scope

By reviewing and analysing the data published on 48 gynodioecious species, we examined three important issues about female advantage. (1) Are reduced selfing and inbreeding depression likely to be the major cause of female advantage? (2) What is the magnitude of female advantage and does it fit theoretical predictions? (3) Does the occurrence or the magnitude of female advantage vary among populations within species and why?

Conclusions

It was found that a female advantage occurred in 40 species, with a magnitude comprised between 1 and 2 in the majority of cases. In many species, reduced selfing may not be a necessary cause of this advantage. Finally, female advantage varied among populations in some species, but both positive and negative correlations were found with female frequency. The role of reduced selfing in females for the evolution of gynodioecy, as well as the various processes that affect sex ratios and female advantage in populations are discussed.     

Epistasis,inbreeding depression,and the evolution of self-fertilization

Inbreeding depression resulting from partially recessive deleterious alleles is thought to be the main genetic factor preventing self-fertilizing mutants from spreading in outcrossing hermaphroditic populations. However, deleterious alleles may also generate an advantage to selfers in terms of more efficient purging, while the effects of epistasis among those alleles on inbreeding depression and mating system evolution remain little explored. In this article, we use a general model of selection to disentangle the effects of different forms of epistasis (additive-by-additive, additive-by-dominance, and dominance-by-dominance) on inbreeding depression and on the strength of selection for selfing. Models with fixed epistasis across loci, and models of stabilizing selection acting on quantitative traits (generating distributions of epistasis) are considered as special cases. Besides its effects on inbreeding depression, epistasis may increase the purging advantage associated with selfing (when it is negative on average), while the variance in epistasis favors selfing through the generation of linkage disequilibria that increase mean fitness. Approximations for the strengths of these effects are derived, and compared with individual-based simulation results.     

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   

植物交配系统的进化、资源分配对策与遗传多样性

影响植物自交率进化的选择力量主要体现在两个方面：当外来花粉量不足时,自交可以提高植物的结实率,即雌性适合度（繁殖保障）;而如果进行自交的花粉比异交花粉更易获得使胚珠受精的机会,那么自交也可以提高植物的雄性适合度（自动选择优势）。但是,鉴别什么时候是繁殖保障、什么时候是自动选择优势导致了自交的进化却是极其困难的。花粉贴现降低了自交植物通过异交花粉途径获得的适合度,即减弱了自动选择优势,而近交衰退既减少了自动选择优势也减少了繁殖保障给自交者带来的利益。具有不同交配系统的植物种群将具有不同的资源分配对策。理论研究已经说明,自交率增加将减少植物对雄性功能的资源分配比例,但将使繁殖分配加大,而且在一定条件下交配系统的改变甚至可以导致植物生活史发生剧烈变化,即从多年生变为一年生。文献中支持自交减少植物雄性投入的证据有很多,但是对繁殖分配与自交率的关系目前还没有系统的研究。资源分配理论可以解释植物繁育系统的多样性,尤其是能够说明为什么大多数植物都是雌雄同体的。自交对植物种群遗传结构的影响是减少种群内的遗传变异,增加种群间的遗传分化。长期以来人们一直猜测,自交者可能会丢掉一些长期进化的潜能,目前这个假说得到了一些支持。     

An explicit model for the inbreeding load in the evolutionary analysis of selfing

I present analytical predictions for the equilibrium inbreeding load expected in a population under mutation, selection, and a regular mating system for any population size and for any magnitude and recessivity of the deleterious effects. Using this prediction, I deduce the relative fitness of mutant alleles with small effect on selfing to explore the situations where selfing or outcrossing are expected to evolve. The results obtained are in agreement with previous literature, showing that natural selection is expected to lead to stable equilibria where populations show either complete outcrossing or complete selfing, and that selfing is promoted by large deleterious mutation rates. I find that the evolution of selfing is favored by a large recessivity of deleterious effects, while the magnitude of homozygous deleterious effects only becomes relevant in relatively small populations. This result contradicts the standard assumption that purging in large populations will only promote selfing when homozygous deleterious effects are large, and implies that previously published results obtained assuming lethal mutations in large populations can be extrapolated to nonlethal alleles of similar recessivity. This conclusion and the general approach used in this analysis can be useful in the study of the evolution of mating systems.     

Individual Variation in Inbreeding Depression: The Roles of Inbreeding History and Mutation

We use mutation-selection recursion models to evaluate the relative contributions of mutation and inbreeding history to variation among individuals in inbreeding depression and the ability of experiments to detect associations between individual inbreeding depression and mating system genotypes within populations. Poisson mutation to deleterious additive or recessive alleles generally produces far more variation among individuals in inbreeding depression than variation in history of inbreeding, regardless of selfing rate. Moreover, variation in inbreeding depression can be higher in a completely outcrossing or selfing population than in a mixed-mating population. In an initially random mating population, the spread of a dominant selfing modifier with no pleiotropic effects on male outcross success causes a measurable increase in inbreeding depression variation if its selfing rate is large and inbreeding depression is caused by recessive lethals. This increase is observable during a short period as the modifier spreads rapidly to fixation. If the modifier alters selfing rate only slightly, it fails to spread or causes no measurable increase in inbreeding depression variance. These results suggest that genetic associations between mating loci and inbreeding depression loci could be difficult to demonstrate within populations and observable only transiently during rapid evolution to a substantially new selfing rate.     

Arctic mustard flower color polymorphism controlled by petal-specific downregulation at the threshold of the anthocyanin biosynthetic pathway

Intra- and interspecific variation in flower color is a hallmark of angiosperm diversity. The evolutionary forces underlying the variety of flower colors can be nearly as diverse as the colors themselves. In addition to pollinator preferences, non-pollinator agents of selection can have a major influence on the evolution of flower color polymorphisms, especially when the pigments in question are also expressed in vegetative tissues. In such cases, identifying the target(s) of selection starts with determining the biochemical and molecular basis for the flower color variation and examining any pleiotropic effects manifested in vegetative tissues. Herein, we describe a widespread purple-white flower color polymorphism in the mustard Parrya nudicaulis spanning Alaska. The frequency of white-flowered individuals increases with increasing growing-season temperature, consistent with the role of anthocyanin pigments in stress tolerance. White petals fail to produce the stress responsive flavonoid intermediates in the anthocyanin biosynthetic pathway (ABP), suggesting an early pathway blockage. Petal cDNA sequences did not reveal blockages in any of the eight enzyme-coding genes in white-flowered individuals, nor any color differentiating SNPs. A qRT-PCR analysis of white petals identified a 24-fold reduction in chalcone synthase (CHS) at the threshold of the ABP, but no change in CHS expression in leaves and sepals. This arctic species has avoided the deleterious effects associated with the loss of flavonoid intermediates in vegetative tissues by decoupling CHS expression in petals and leaves, yet the correlation of flower color and climate suggests that the loss of flavonoids in the petals alone may affect the tolerance of white-flowered individuals to colder environments.     

植物交酸系统的进化、资源分配对策与遗传多样性

影响植物自交率进化的选择力量主要体现在两个方面：当外来花粉量不足时,自交可以提高植物的结实率,即雌性适合度（繁殖保障）;而如果进行自交的花粉比异交花粉更易获得使胚珠受精的机会,那么自交也可以提高植物的雄性适合度（自动选择优势）。但是,鉴别什么时候是繁殖保障、什么时候是自动选择优势导致了自交的进化却是极其困难的。花粉贴现降低了自交植物通过异交花粉途径获得的适合度,即减弱了自动选择优势,而近交衰退既减少了自动选择优势也减少了繁残给自交者带来的利益。具有不同交配系统的植物种群将具有不同的资源分配对策。理论研究已经说明,自交率增加将减少植物对雄性功能的资源分配比例,但将使繁殖分配加大,而且在一定条件下交配系统在改变甚至可以导致植物生活史发生剧烈变化,即从多年生变为一年生。文献中支持自交减少植物雄性投入的证据有很多,但是对繁殖分配与自交率的关系目前还没有系统的研究,资源分配理论可以解释植物繁育系统的多样性,尤其是能够3说明为什么大多数植物都是雌雄同体的,自交对植物种群遗传结构的影响是减少种群内的遗传变异,增加种群间的遗传分化,长期以来人们一直猜测,自交者可能会丢掉一些长期进化的潜能,目前这个假说得到了一些支持。     

Antagonistic pleiotropy may help population-level selection in maintaining genetic polymorphism for transmission rate in a model phytopathogenic fungus

It has been shown theoretically that the conditions for the maintenance of polymorphism at pleiotropic loci with antagonistic effects on fitness components are rather restrictive. Here, we use a metapopulation model to investigate whether antagonistic pleiotropy could help maintain polymorphism involving common deleterious alleles in the phytopathogenic fungus Microbotryum violaceum. This fungus causes anther smut disease of the Caryophyllaceae. A previous model has shown that the sex-linked deleterious alleles can be maintained under a metapopulation structure, when intra-tetrad selfing (mating between products of the same meiosis) is high, due to founder effects and selection at the population level. Here, we add two types of pleiotropic advantages to the metapopulation model. A competitive advantage for strains carrying the sex-linked deleterious alleles did not facilitate their maintenance because competitive situations were too rare. In contrast, higher spore production did facilitate the maintenance of the deleterious alleles at low intra-tetrad mating rates and with a large advantage for spore production. These results show that antagonistic pleiotropy may promote the persistence of genetic variation, in combination with other selective forces.     

SMALL AND UGLY? PHYLOGENETIC ANALYSES OF THE “SELFING SYNDROME” REVEAL COMPLEX EVOLUTIONARY FATES OF MONOMORPHIC PRIMROSE FLOWERS

One of the most common trends in plant evolution, loss of self‐incompatibility and ensuing increases in selfing, is generally assumed to be associated with a suite of phenotypic changes, notably a reduction of floral size, termed the selfing syndrome. We investigate whether floral morphological traits indeed decrease in a deterministic fashion after losses of self‐incompatibility, as traditionally expected, using a phylogeny of 124 primrose species containing nine independent transitions from heterostyly (heteromorphic incompatibility) to homostyly (monomorphic self‐compatibility), a classic system for evolution of selfing. We find similar overall variability of homostylous and heterostylous species, except for diminished herkogamy in homostyles. Bayesian mixed models demonstrate differences between homostylous and heterostylous species in all traits, but net effects across species are small (except herkogamy) and directionality differs among traits. Strongly drift‐like evolutionary trajectories of corolla tube length and corolla diameter inferred by Ornstein–Uhlenbeck models contrast with expected deterministic trajectories toward small floral size. Lineage‐specific population genetic effects associated with evolution of selfing may explain that reductions of floral size represent one of several possible outcomes of floral evolution after loss of heterostyly in primroses. Contrary to the traditional paradigm, selfing syndromes may, but do not necessarily evolve in response to increased selfing.     

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.     

Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae)

Most models of mating system evolution predict mixed mating to be unstable, although it is commonly reported from nature. Ecological interactions with mutualistic pollinators can help account for this discrepancy, but antagonists such as herbivores are also likely to play a role. In addition, inbreeding can alter ecological interactions and directly affect selfing rates, which may also contribute to maintaining mating system variation. We explored herbivore and inbreeding effects on pollinator behavior and selfing rates in Mimulus guttatus. First, individual spittlebug (Philaenus spumarius) herbivores were applied to native plants in two populations. Spittlebugs reduced flower size, increased anther-stigma distance, and increased selfing rates. A second experiment factorially crossed spittlebug treatment with inbreeding history (self- vs. cross-fertilized), using potted plants in arrays. Spittlebugs did not affect pollinator behavior, but they reduced flower size and nearly doubled the selfing rate. Inbreeding reduced the frequency of pollinator visits and increased flower-handling time, and this may be the first report that inbreeding affects pollinator behavior. Selfing rates of inbred plants were reduced by one half, which may reflect early inbreeding depression or altered pollinator behavior. The contrasting effects of herbivory and inbreeding on selfing rates may help maintain mating system variation in M. guttatus.     

Role of parasite transmission in promoting inbreeding: I. Infection intensities drive individual parasite selfing rates

Among parasitic organisms, inbreeding has been implicated as a potential driver of host–parasite co‐evolution, drug‐resistance evolution and parasite diversification. Yet, fundamental topics about how parasite life histories impact inbreeding remain to be addressed. In particular, there are no direct selfing‐rate estimates for hermaphroditic parasites in nature. Our objectives were to elucidate the mating system of a parasitic flatworm in nature and to understand how aspects of parasite transmission could influence the selfing rates of individual parasites. If there is random mating within hosts, the selfing rates of individual parasites would be an inverse power function of their infection intensities. We tested whether selfing rates deviated from within‐host random mating expectations with the tapeworm Oochoristica javaensis. In doing so, we generated, for the first time in nature, individual selfing‐rate estimates of a hermaphroditic flatworm parasite. There was a mixed‐mating system where tapeworms self‐mated more than expected with random mating. Nevertheless, individual selfing rates still had a significant inverse power relationship to infection intensities. The significance of this finding is that the distribution of parasite infection intensities among hosts, an emergent property of the transmission process, can be a key driver in shaping the primary mating system, and hence the level of inbreeding in the parasite population. Moreover, we demonstrated how potential population selfing rates can be estimated using the predicted relationship of individual selfing rates to intensities and showed how the distribution of parasites among hosts can indirectly influence the primary mating system when there is density‐dependent fecundity.     

Relatively weak inbreeding depression in selfing but also in outcrossing populations of North American Arabidopsis lyrata

Hermaphroditic plants can potentially self‐fertilize, but most possess adaptations that promote outcrossing. However, evolutionary transitions to higher selfing rates are frequent. Selfing comes with a transmission advantage over outcrossing, but self‐progeny may suffer from inbreeding depression, which forms the main barrier to the evolution of higher selfing rates. Here, we assessed inbreeding depression in the North American herb Arabidopsis lyrata, which is normally self‐incompatible, with a low frequency of self‐compatible plants. However, a few populations have become fixed for self‐compatibility and have high selfing rates. Under greenhouse conditions, we estimated mean inbreeding depression per seed (based on cumulative vegetative performance calculated as the product of germination, survival and aboveground biomass) to be 0.34 for six outcrossing populations, and 0.26 for five selfing populations. Exposing plants to drought and inducing defences with jasmonic acid did not magnify these estimates. For outcrossing populations, however, inbreeding depression per seed may underestimate true levels of inbreeding depression, because self‐incompatible plants showed strong reductions in seed set after (enforced) selfing. Inbreeding‐depression estimates incorporating seed set averaged 0.63 for outcrossing populations (compared to 0.30 for selfing populations). However, this is likely an overestimate because exposing plants to 5% CO₂ to circumvent self‐incompatibility to produce selfed seed might leave residual effects of self‐incompatibility that contribute to reduced seed set. Nevertheless, our estimates of inbreeding depression were clearly lower than previous estimates based on the same performance traits in outcrossing European populations of A. lyrata, which may help explain why selfing could evolve in North American A. lyrata.