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.     

Evolution of the selfing syndrome: Anther orientation and herkogamy together determine reproductive assurance in a self‐compatible plant

Capacity for autonomous self‐fertilization provides reproductive assurance, has evolved repeatedly in the plant kingdom, and typically involves several changes in flower morphology and development (the selfing syndrome). Yet, the relative importance of different traits and trait combinations for efficient selfing and reproductive success in pollinator‐poor environments is poorly known. In a series of experiments, we tested the importance of anther–stigma distance and the less studied trait anther orientation for efficiency of selfing in the perennial herb Arabis alpina. Variation in flower morphology among eight self‐compatible European populations was correlated with efficiency of self‐pollination and with pollen limitation in a common‐garden experiment. To examine whether anther–stigma distance and anther orientation are subject to directional and/or correlational selection, and whether this is because these traits affect pollination success, we planted a segregating F2 population at two native field sites. Selection strongly favored a combination of introrse anthers and reduced anther–stigma distance at a site where pollinator activity was low, and supplemental hand‐pollination demonstrated that this was largely because of their effect on securing self‐pollination. The results suggest that concurrent shifts in more than one trait can be crucial for the evolution of efficient self‐pollination and reproductive assurance in pollinator‐poor habitats.     

Divergence in pollen performance between Clarkia sister species with contrasting mating systems supports predictions of sexual selection

Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on postcopulatory male traits affecting siring success. In plants, closely related self‐ and cross‐pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse‐raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self‐pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We tested for the effects of species, population, pollen type (self vs. outcross), the number of competing pollen grains, and temperature on pollen performance. Clarkia unguiculata exhibited higher mean PTGR than C. exilis; pollen type had no effect on performance in either taxon. The difference between these species in PTGR is consistent with predictions of sexual selection theory.     

滨海湿地植物种群Allee效应驱动机制研究进展

Allee效应是指生物个体适应度与种群规模或密度之间呈正向关联的现象,因与植物种群动态和种群灭绝密切相关而受到生态学家的普遍重视。阐释多重胁迫下滨海湿地植物种群响应机制,从保护生物多样性和维持生态系统稳定性层面发展系统性生态修复措施成为相关研究关注的重点。本研究分别从遗传过程、花粉扩散过程和生物互作关系不同层面,总结分析了植物种群Allee效应驱动机制的研究进展。一方面,植物因遗传过程中近交衰退、遗传变异丧失、有害突变累积等遗传结构改变造成繁殖失败而引发Allee效应;另一方面,植物花粉扩散过程和动植物互作关系影响下的花粉限制也通过影响植物种群繁殖力成为驱动Allee效应的关键因素。滨海湿地水盐梯度变异及格局破碎化影响下,植物种群遭受Allee效应的风险需引起关注,维持滨海湿地植物种群适宜分布格局和生物连通过程成为缓解Allee效应的重要手段。结合生理学与化学生态学研究手段和长时间尺度动态监测技术,有助于进一步阐释环境及生物等多重胁迫下Allee效应的非线性驱动机制。     

Microgametophyte population sizes and plant reproductive output in the insect-pollinated Prunella grandiflora (Lamiaceae)

Intraspecific variation in pollen deposition and number of pollen tubes per style is rarely quantified, but is essential for assessing the occurrence of pollen limitation and pollen competition and their evolutionary implications. Moreover, pollen deposition, pollen tube growth, and the fate of fertilized ovules are rarely distinguished in field studies. Here we present such a study in eight natural populations of Prunella grandiflora. We quantified microgametophyte population sizes and inferred pollen limitation when the number of fertilizable ovules exceeded pollen tubes, and assessed seed set and fate after open pollination. Two and three populations had on average significantly fewer pollen grains and pollen tubes per flower, respectively, than the fixed number of fertilizable ovules per fruit, while one population experienced significant pollen competition. Style length was positively correlated with the number of pollen tubes. While pollen availability was very variable, seed abortion was significantly less frequent in denser populations, and in one population the proportion of well-developed seeds was significantly, positively correlated with the number of pollen tubes in the style. Less pollen deposition, lower numbers of pollen tubes reaching the base of the style, lower pollen quality and therefore increased abortion of fertilized ovules can all reduce seed set in natural P. grandiflora stands. Substantial intraspecific variability implies that microgametophyte competition also occurs in this species. Finally, style morphology may affect pollen receipt.     

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.     

Morph-ratio variation, population size and female reproductive success in distylous Pulmonaria officinalis (Boraginaceae)

Theory predicts that morph ratios in heterostylous populations are governed by negative frequency-dependent selection typically resulting in equal morph ratios at equilibrium. Previous work on the distylous perennial herb Pulmonaria officinalis, however, showed asymmetric mating between floral morphs and a weak self-incompatibility system, with the long-styled morph (L-morph) producing significantly higher seed set following intramorph crosses and even selfing than the short-styled morph (S-morph), two aspects thought to affect female fecundity and morph-ratio variation. Here, we evaluated morph ratios and population size of all known P. officinalis populations in the northern part of Belgium. Morph ratios deviated significantly from 1:1 (range 0.09-1 L-morph frequency, mean = 0.58). Relative fecundity of the S-morph (i.e. mean seed set of the S-morph/mean seed set of the L-morph) was on average 0.73, was positively related to the frequency of the L-morph, and reached 1 (similar levels of female fecundity) at an average L-morph frequency of 0.66 in the population. As some small populations had the S-morph in majority, our results suggest that local morph ratios are influenced both by the relative fecundity of L- and S-morph individuals and by stochastic processes in small populations.     

Effective population size,reproductive success and sperm precedence in the butterfly,Bicyclus anynana,in captivity

A pedigree approach is used to estimate the effective population size yn two population cages of the butterfly, Bicyclus anynana. Each cage was founded with 54 individually marked adults of each sex. Matings were recorded over a 3‐day period. Eggs were then collected from each female over a similar period before the numbers of hatching larvae were counted to assess progeny number. The males showed a higher variance in reproductive success than the females. Since about one‐quarter of all females mated more than once, we also examined the pattern of sperm precedence using molecular markers or, in separate crossing experiments, wing pattern mutants. Both instances of complete first and last male sperm precedence, as well as of sperm mixing, were found. In some crosses a ‘leakiness’ was found in which some of the early eggs laid by a female were fertilized by a male partner which was subsequently completely unsuccessful. However, the estimates of effective population size were largely unaffected by the pattern of sperm precedence. Estimates for N_e : N in each cage were close to 0.60. The possibility of obtaining comparable estimates in selected natural populations of butterflies is discussed.     

Pollination efficiency and reproductive patterns in relation to local plant density,population size,and floral display in the rewarding Listera ovata (Orchidaceae)

Pollination efficiency and reproductive success vary strongly among populations of most animal‐pollinated plant species, depending on their size and local density, whereas individual plants within populations experience varying levels of reproductive output as a result of differences in floral display. Although most orchid species have been shown to be severely pollination limited, few studies have investigated the impact of the above‐mentioned factors on pollination success and reproduction, especially in rewarding species. In this study, the impact of population size, local density of flowering plants, and floral display on the rates of pollinia export and fruit production was investigated in 13 natural populations of the rewarding terrestrial orchid Listera ovata. In addition, an emasculation experiment was set up to examine how floral display and local density of flowering plants affected the relative importance of cross‐ vs. geitonogamous pollination in determining fruit set. In the studied populations, pollination efficiency, pollen removal, and fruit set increased with increasing population size until a threshold value of 30–40 flowering plants was reached, above which pollination efficiency and reproductive output decreased again. On average, plants with large floral displays showed higher proportional pollinia removal and fruit set compared with smaller plants. Fruit production was also significantly and positively related to local plant density, whereas emasculation did not affect the relationship between local plant density and fruit set, suggesting that geitonogamous pollination did not affect the outcome of female function. The results of this study are discussed in the light of the flowering mechanism of the species and its generalized pollination system. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 157 , 713–721.     

Effects of reproductive compensation, gamete discounting and reproductive assurance on mating-system diversity in hermaphrodites

Hermaphroditism allows considerable scope for contributing genes to subsequent generations through various mixtures of selfed and outcrossed offspring. The fitness consequences of different family compositions determine the evolutionarily stable mating strategy and depend on the interplay of genetic features, the nature of mating, and factors that govern offspring development. This theoretical article considers the relative contributions of these influences and their interacting effects on mating-system evolution, given a fixed genetic load within a population. Strong inbreeding depression after offspring gain independence selects for exclusive outcrossing, regardless of the intensity of predispersal inbreeding depression, unless insufficient mating limits offspring production. The extent to which selfing evolves under weak postdispersal inbreeding depression depends on predispersal inbreeding depression and the opportunity for resource limitation of offspring production. Mixed selfing and outcrossing is an evolutionarily stable strategy (ESS) if selfed zygotes survive poorly, but selfed offspring survive well, and maternal individuals produce enough "extra" eggs that deaths of unviable outcrossed embryos do not impact offspring production (reproductive compensation). Mixed mating can also be an ESS, despite weak lifetime inbreeding depression, if self-mating reduces the number of male gametes available for outcrossing (male-gamete discounting). Reproductive compensation and male-gamete discounting act largely independently on mating-system evolution. ESS mating systems always involve either complete fertilization or fertilization of enough eggs to induce resource competition among embryos, so although reproductive assurance is adaptive with insufficient mating, it is never an ESS. Our results illustrate the theoretical importance of different constraints on offspring production (availability of male gametes, egg production, and maternal resources) for both the course and outcome of mating-system evolution, whereas unequal competition between selfed and outcrossed embryos has limited effect. These results also underscore the significance of heterogeneity in the nature and intensity of inbreeding depression during the life cycle for the evolution of hermaphrodite mating systems.     

Mating system and the evolution of quantitative traits: an experimental study of Mimulus guttatus

Abstract The mating system of a population profoundly influences its evolution. Inbreeding alters the balance of evolutionary forces that determine the amount of genetic variation within a population. It redistributes that variation among individuals, altering heritabilities and genetic correlations. Inbreeding even changes the basic relationships between these genetic statistics and response to selection. If populations differing only in mating system are exposed to the same selection pressures, will they respond in qualitatively different ways? Here, we address this question by imposing selection on an index of two negatively correlated traits (flower size and development rate) within experimental populations that reproduce entirely by outcrossing, entirely by self‐fertilizing, or by a mixture of outcrossing and selfing. Entirely selfing populations responded mainly by evolving larger flowers whereas outcrossing populations also evolved more rapid development. Divergence occurred despite an equivalent selection regime and no direct effect of mating system on fitness. The study provides an experimental demonstration of how the interaction of selection, genetic drift, and mating system can produce dramatic short‐term changes in trait means, variances, and covariances.     

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.     

Pronounced reproductive skew in a natural population of green swordtails, Xiphophorus helleri

For many species in nature, a sire's progeny may be distributed among a few or many dams. This poses logistical challenges--typically much greater across males than across females--for assessing means and variances in mating success (number of mates) and reproductive success (number of progeny). Here we overcome these difficulties by exhaustively analyzing a population of green swordtail fish (Xiphophorus helleri) for genetic paternity (and maternity) using a suite of highly polymorphic microsatellite loci. Genetic analyses of 1476 progeny from 69 pregnant females and 158 candidate sires revealed pronounced skews in male reproductive success both within and among broods. These skews were statistically significant, greater than in females, and correlated in males but not in females with mating success. We also compare the standardized variances in swordtail reproductive success to the few such available estimates for other taxa, notably several mammal species with varied mating systems and degrees of sexual dimorphism. The comparison showed that the opportunity for selection on male X. helleri is among the highest yet reported in fishes, and it is intermediate compared to estimates available for mammals. This study is one of a few exhaustive genetic assessments of joint-sex parentage in a natural fish population, and results are relevant to the operation of sexual selection in this sexually dimorphic, high-fecundity species.     

Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus

In flowering plants, pollen limitation has been proposed to intensify selection on floral characters important in pollinator attraction, but may also select for traits that increase seed set through autonomous selfing. Here, a factorial design (+/- pollen addition, +/- pollinator removal) was used to investigate how the pollination environment affects selection on floral morphology via female fitness in a mixed-mating population of the yellow monkeyflower, Mimulus guttatus (Phrymaceae). Female fitness was strongly pollen-limited, with supplementally pollinated plants setting 37% more seeds than open-pollinated individuals. Strong positive selection was found on flower length, weak positive selection on flower width : length ratio and no selection on stigma-anther distance in both open-pollinated and supplementally pollinated treatments. By contrast, flowers with relatively narrow corollas and low stigma-anther distances were favored in the pollinator exclusion treatment. These results provide mixed support for the idea that pollen limitation intensifies selection on floral characters. Despite strong phenotypic selection, natural pollen limitation did not mediate selection on characters associated with either pollinator attraction or self-fertilization. However, the novel pattern of selection on severely pollen-limited plants suggests that reproductive assurance against pollinator loss may have been directly involved in the floral evolution of closely related selfing taxa.     

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

Although a large portion of plant and animal species exhibit intermediate levels of outcrossing, the factors that maintain this wealth of variation are not well understood. Natural enemies are one relatively understudied ecological factor that may influence the evolutionary stability of mixed mating. In this paper, we aim for a conceptual unification of the role of enemies in mating system expression and evolution in both hermaphroditic animals and plants. We review current theory and detail the potential effects of enemies on fundamental mating system parameters. In doing so, we identify situations in which consideration of enemies alters expectations about the stability of mixed mating. Generally, we find that inclusion of the enemy dimension may broaden conditions in which mixed mating systems are evolutionarily stable. Finally, we highlight avenues ripe for future theoretical and empirical work that will advance our understanding of enemies in the expression and evolution of mixed mating in their hosts/victims, including examination of feedback cycles between victims and enemies and quantification of mating system-related parameters in victim populations in the presence and absence of enemies.     

Ecological components and evolution of selfing in the freshwater snail Galba truncatula

The reproductive assurance hypothesis emphasizes that self-fertilization should evolve in species with reduced dispersal capability, low population size or experiencing recurrent bottlenecks. Our work investigates the ecological components of the habitats colonized by the snail, Galba truncatula, that may influence the evolution of selfing. Galba truncatula is a preferential selfer inhabiting freshwater habitats, which vary with respect to the degree of permanence. We considered with a population genetic approach the spatial and the temporal degree of isolation of populations of G. truncatula. We showed that patches at distances of only a few meters are highly structured. The effective population sizes appear quite low, in the order of 10 individuals or less. This study indicates that individuals of the species G. truncatula are likely to be alone in a site and have a low probability of finding a partner from a nearby site to reproduce. These results emphasize the advantage of selfing in this species.