A generalised mimicry system involving angiosperm flower colour, pollen and bumblebees’ innate colour preferences

Flower colour is a major advertisement signal of zoophilous plants for pollinators. Bees, the main pollinators, exhibit innate colour preferences, which have often been attributed to only one single floral colour, though most flowers display a pattern of two or several colours. The existing studies of floral colour patterns are mostly qualitative studies. Using a model of bee colour vision we quantitatively investigate two questions: whether or not component colours of floral colour patterns may mimic pollen signals, and whether or not bumblebees exhibit innate preferences for distinct parameters of naturally existing floral colour patterns. We analysed the spectral reflectances of 162 plant species with multicoloured flowers and inflorescences, distiniguishing between inner and outer colours of floral colour patterns irrespective of the particular structures so coloured.We found that:– The inner colour of radially symmetrical flowers and inflorescences and of zygomorphic flowers appears less diverse to bees than the peripheral colour.– The inner colour of most radial flowers and inflorescences as well as the inner colour of a large number of non-related zygomorphic flowers appears to bees to be very similar to that of pollen.– Bumblebees (Bombus terrestris) exhibit innate preferences for two-coloured over single-coloured dummy flowers in a spontaneous choice test.– Bumblebees exhibit innate preferences for dummy flowers with a large over those with a small centre area.– Bumblebees exhibit innate preferences for dummy flowers with a centre colour similar to that of pollen over those with another centre colour.Our findings support the hypotheses that the inner component of floral colour patterns could be interpreted as a generalised and little recognised form of mimicry of the colour of visually displayed pollen, that bumblebees exhibit innate preferences regarding colour and size parameters of floral colour patterns, and that these correspond to visually displayed pollen. These findings together suggest a prominent role of floral colour patterns in advertisement to and guidance of naive flower visitors.     

Pollinator response to female and male floral display in a monoecious species and its implications for the evolution of floral dimorphism

Pollinator-mediated selection has been hypothesized as one cause of size dimorphism between female and male flowers. Flower number, ignored in studies of floral dimorphism, may interact with flower size to affect pollinator selectivity. In the present study, we explored pollinator response, and estimated pollen receipt and removal, in experimental populations of monoecious Sagittaria trifolia, in which plants were manipulated to display three, six, nine or 12 female or male flowers per plant. In this species, female flowers are smaller but have a more compressed flowering period than males, creating larger female floral displays. Overall, pollinators preferred to visit male rather than female displays of the same size. Both first visit per foraging bout and visitation rates to female displays increased with display size. However, large male displays did not show increased attractiveness to pollinators. A predicted relationship that pollen removal, rather than pollen receipt, is limited by pollinator visitation was confirmed in the experimental populations. The results suggest that the lack of selection on large male displays may affect the evolution of floral dimorphism in this species.     

Reliance on pollinators predicts defensive chemistry across tobacco species

Defensive traits are typically studied in the context of avoiding antagonists, but may also mediate key interactions with mutualists. Plant chemical defences occur in flowers, suggesting pollinators may be agents of selection on defence. We hypothesised that floral defences would deter pollinators, and therefore, pollinators would select for lower defences in outcrossing than self-pollinating species. We measured pollinator reliance and alkaloid levels in 32 greenhouse-grown Nicotiana species. Using a comparative phylogenetic approach, we found significantly lower nectar, floral and leaf nicotine concentrations in outcrossing than selfing species, with a 15-fold decrease in leaf nicotine levels. Nicotine concentrations were positively correlated across tissues, suggesting that selection against floral defences could constrain the evolution of leaf defences. Thus, pollinators could shape the evolution not only of floral defences but also of defences in other tissues where herbivores have traditionally been considered the dominant agent of selection.     

The co-optimization of floral display and nectar reward

In most insect-pollinated flowers, pollinators cannot detect the presence of nectar without entering the flower. Therefore, flowers may cheat by not producing nectar and may still get pollinated. Earlier studies supported this ‘cheater flower’ hypothesis and suggested that the cost saving by cheater flowers could be the most predominant selective force in the evolution of nectarless flowers. Previous models as well as empirical studies have addressed the problem of optimizing the proportion of nectarless and nectarful flowers. However, there has been no attempt to optimize the investment in nectar production along with that in floral display. One of the key questions that arises is whether the floral display will evolve to be an honest indicator of nectar reward. We use a mathematical model to cooptimize the investments in nectar and floral display in order to achieve maximum reproductive success. The model assumes that pollinators rely on a relative rather than an absolute judgement of reward. A conspicuous floral display attracts naïve pollinators on the one hand and enhances pollinator learning on the other. We show that under these assumptions, plant-pollinator co-evolution leads to honest signalling, i.e. a positive correlation between display and reward.     

Temporal stability of pollinator preference in an alpine plant community and its implications for the evolution of floral traits

A traditional view of diverse floral traits is that they reflect differences in foraging preferences of pollinators. The role of pollinators in the evolution of floral traits has been questioned recently by broad community surveys, especially studies concerning variation in pollinator assemblages and visitation frequency, which suggest a diminished role of pollinators in floral evolution. Here, we investigate the relationships between six categories of floral traits of 29 species and 10 pollinator functional groups in an alpine meadow in the Hengduan Mountains of China, over three consecutive years. Simpson’s diversity index was used to estimate the level of pollinator generalization of each plant species by considering both pollinator groups and their relative visitation frequencies. Multivariate analyses indicated that eight of the ten pollinator groups showed constant preferences for at least two floral traits, leading to a relatively stable level of ecological generalization for most floral traits (two out of three categories), despite the fact that the level of generalization of the entire community varied across years. Shape preferences of butterflies, honeybees and beeflies varied such that open flowers exhibited a lower level of ecological generalization in 2007 than closed flowers, in contrast with the other 2 years. These results suggest that temporally stabilized preferences of diverse pollinators may contribute to the evolution of specialized versus generalized floral traits; however, their role may be moderated by variation in community structure, including both the composition and abundance of plants and pollinators.     

The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards

1.  The evolution of flowering plants has undoubtedly been influenced by a pollinator's ability to learn to associate floral signals with food. Here, we address the question of 'why' flowers produce scent by examining the ways in which olfactory learning by insect pollinators could influence how floral scent emission evolves in plant populations.
2.  Being provided with a floral scent signal allows pollinators to learn to be specific in their foraging habits, which could, in turn, produce a selective advantage for plants if sexual reproduction is limited by the income of compatible gametes. Learning studies with honeybees predict that pollinator-mediated selection for floral scent production should favour signals which are distinctive and exhibit low variation within species because these signals are learned faster. Social bees quickly learn to associate scent with the presence of nectar, and their ability to do this is generally faster and more reliable than their ability to learn visual cues.
3.  Pollinators rely on floral scent as a means of distinguishing honestly signalling flowers from deceptive ones. Furthermore, a pollinator's sensitivity to differences in nectar rewards can bias the way that it responds to floral scent. This mechanism may select for flowers that provide olfactory signals as an honest indicator of the presence of nectar or which select against the production of a detectable scent signal when no nectar is present.
4.  We expect that an important yet commonly overlooked function of floral scent is an improvement in short-term pollinator specificity which provides an advantage to both pollinator and plant over the use of a visual signal alone. This, in turn, impacts the evolution of plant mating systems via its influence on the species-specific patterns of floral visitation by pollinators.     

兰科植物欺骗性传粉

植物与传粉动物的互利关系在生态系统中非常普遍。然而,有许多植物不为传粉者提供任何报酬,而是利用各种欺骗方式诱骗昆虫拜访,从而实现传粉,即欺骗性传粉。兰科是被子植物大科之一,其高度特化的繁殖器官和适应于昆虫传粉的精巧结构令人称奇。进化论创始人达尔文描述了许多兰花与昆虫精巧的传粉系统,但他忽视了欺骗性传粉的存在。事实上,近1/3的兰科植物都依赖于欺骗性传粉。欺骗性传粉可能是导致兰科植物多样性的重要原因之一。兰花利用或操作昆虫觅食、交配、产卵和栖息等行为,演化出各种各样的欺骗性传粉机制,常见的类型包括泛化的食源性欺骗、Batesian拟态、性欺骗、产卵地拟态和栖息地拟态。花的颜色、形态和气味在欺骗性传粉的成功实现中起到了重要作用。欺骗性兰花与传粉昆虫之间的演化可能是不同步的,兰花追踪昆虫的行为信号而发生分化,然而欺骗性传粉可能对昆虫造成一定的伤害,从而对昆虫也施加选择压力。由于昆虫的学习行为,欺骗性的兰花一般具有低的昆虫拜访率和结实率,其繁殖成功率受各种因素的影响。欺骗性加剧了兰花对传粉昆虫的依赖,使其具有更高的灭绝风险,传粉生物学的研究能为兰科植物的有效保护提供指导。在欺骗性传粉系统中,有报酬的伴生植物、拟态模型和其他拟态信号提供者对传粉成功有重要影响。因此,研究欺骗性传粉兰花、传粉昆虫和相关的生物和生态因子的网状进化关系具有重要理论和实践意义。     

Pollinators and seed predators generate conflicting selection on Dalechampia blossoms

Plant–pollinator relationships are often mediated by floral traits that advertise the presence or amount of rewards. However, herbivores may also use these traits to find their hosts. In Dalechampia scandens, we tested whether floral advertisements that attract pollinators were also used by seed predators, and whether this generated conflicting selection pressures. We studied the influence of natural variation in the size of showy bracts, amount of reward, and two shape traits on pollinator visitation, pollen arrival on stigmas, seed production and seed predation. We then built a multivariate fitness function for these traits to estimate selection generated by pollinators and seed predators. Blossoms with larger bracts were visited by bees more frequently and received more pollen on their stigmas. Seed predators laid more eggs on blossoms with larger bracts and also on blossoms later producing more seeds. Consequently, selection for larger bract size exerted by pollinators was counteracted by the selection exerted by seed predators. As a result, net selection on bract size tended to be stabilizing. Additionally, we found selection on traits that increased the rate of self‐pollination (assuming uniform seed quality). These results illustrate the importance of both mutualists and antagonists in floral evolution, as well as the value of taking an integrative approach to assessing selection on floral traits.     

Corolla herbivory, pollination success and fruit predation in complex flowers: an experimental study with Linaria lilacina (Scrophulariaceae)

BACKGROUND AND AIMS: Herbivory on floral structures has been postulated to influence the evolution of floral traits in some plant species, and may also be an important factor influencing the occurrence and outcome of subsequent biotic interactions related to floral display. In particular, corolla herbivory may affect structures differentially involved in flower selection by pollinators and fruit predators (specifically, those ovopositing in ovaries prior to fruit development); hence floral herbivores may influence the relationships between these mutualistic and antagonistic agents. METHODS: The effects of corolla herbivory in Linaria lilacina (Scrophulariaceae), a plant species with complex flowers, were considered in relation to plant interactions with pollinators and fruit predators. Tests were made as to whether experimentally created differences in flower structure (resembling those occurring naturally) may translate into differences in reproductive output in terms of fruit or seed production. KEY RESULTS: Flowers with modified corollas, particularly those with lower lips removed, were less likely to be selected by pollinators than control flowers, and were less likely to be successfully visited and pollinated. As a consequence, fruit production was also less likely in these modified flowers. However, none of the experimental treatments affected the likelihood of visitation by fruit predators. CONCLUSIONS: Since floral herbivory may affect pollinator visitation rates and reduce seed production, differences among plants in the proportion of flowers affected by herbivory and in the intensity of the damage inflicted on affected flowers may result in different opportunities for reproduction for plants in different seasons.     

Floral symmetry affects speciation rates in angiosperms

Despite much recent activity in the field of pollination biology, the extent to which animal pollinators drive the formation of new angiosperm species remains unresolved. One problem has been identifying floral adaptations that promote reproductive isolation. The evolution of a bilaterally symmetrical corolla restricts the direction of approach and movement of pollinators on and between flowers. Restricting pollinators to approaching a flower from a single direction facilitates specific placement of pollen on the pollinator. When coupled with pollinator constancy, precise pollen placement can increase the probability that pollen grains reach a compatible stigma. This has the potential to generate reproductive isolation between species, because mutations that cause changes in the placement of pollen on the pollinator may decrease gene flow between incipient species. I predict that animal-pollinated lineages that possess bilaterally symmetrical flowers should have higher speciation rates than lineages possessing radially symmetrical flowers. Using sister-group comparisons I demonstrate that bilaterally symmetric lineages tend to be more species rich than their radially symmetrical sister lineages. This study supports an important role for pollinator-mediated speciation and demonstrates that floral morphology plays a key role in angiosperm speciation.     

POLLINATORS DISCRIMINATE AMONG FLORAL HEIGHTS OF A SEXUALLY DECEPTIVE ORCHID: IMPLICATIONS FOR SELECTION

Pollinators have influenced the evolution of many morphological floral traits, although few studies have shown that pollinators have influenced plant height. Chiloglottis trilabra is one of many Australian orchids that deceive and attract male pollinators by mimicking the sex pheromones and morphology of females insects. Orchids in this genus have unusually short flowers whose peduncle elongates dramatically after pollination to approximately twice the original height. In a series of choice experiments in the field, we show that pollinators of C. trilabra strongly discriminate among floral heights, preferring flowers presented at 15 cm-20 cm over flowers presented at lower and higher positions (ranging from 2 cm-100 cm). Our results suggested pollinators have the potential to mediate stabilizing selection for floral height when pollination is limiting. However, the natural height range of the orchid (mean = 10 cm, range 5 cm–15 cm) was lower than the experimentally determined optimum for visitation frequency. This difference may indicate that pollinator-mediated selection does not occur in this species, perhaps because seed set is not sufficiently limited. Alternatively, other life-history factors may counteract pollinator-mediated selection, yielding an evolutionary compromise in height.     

Pollinators and nectar robbers cause directional selection for large spur circle in Impatiens oxyanthera (Balsaminaceae)

Nectar spurs have an important role in floral evolution and plant–pollinator coadaptation. The flowers of some species possess spurs curving into a circle. However, it is unclear whether spur circle diameter is under direct selection pressure from different sources, such as pollinators and nectar robbers. In this study, we quantified selection on some floral traits, such as spur circle diameter in Impatiens oxyanthera (Balsaminaceae) using phenotypic selection analysis and compared the relative importance of pollinators and nectar robbers as selective agents using mediation analysis. The study showed that pollinators caused significant selection on corolla length, spur curvature and spur circle diameter while nectar robbers only imposed strong selection on spur circle diameter. Pollinators favored flowers with large corolla, curly spurs and large spur circle while nectar robbers preferred flowers with small spur circle. More pollinator visits resulted in higher female reproductive success, while robbery reduced female fitness. Conflicting selection on spur traits from pollinators and nectar robbers was not found. Mediation analysis showed that selection on floral traits through nectar robbing was stronger than selection through pollination. The results suggested that pollinators and nectar robbers jointly mediated the directional selection for large spur circle, and nectar robbers caused stronger selection than pollinators on floral traits.     

Morning floral heat as a reward to the pollinators of the Oncocyclus irises

Relationships between flowering plants and their pollinators are usually affected by the amount of reward, mainly pollen or nectar, offered to pollinators by flowers, with these amounts usually positively correlated with floral display. The large Oncocyclus iris flowers, despite being the largest flowers in the East Mediterranean flora, are nectarless and have hidden pollen. No pollinators visit the flowers during daytime, and these flowers are pollinated only by night-sheltering solitary male bees. These iris flowers are partially or fully dark-colored, suggesting that they gather heat by absorbing solar radiation. Here we test the hypothesis that the dark-colored flowers of the Oncocyclus irises offer heat reward to their male solitary bee pollinators. Floral temperature was higher by 2.5°C than ambient air after sunrise. Solitary male bees emerged earlier after sheltering in Oncocyclus flowers than from other experimental shelter types. Pollination tunnels facing east towards the rising sun hosted more male bees than other aspects. We suggest that floral heat reward can explain the evolution of dark floral colors in Oncocyclus irises, mediated by the pollinators’ behavior.     

Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of Tabebuia aurea (Bignoniaceae): effects of floral display size and habitat fragmentation

Large floral displays favour pollinator attraction and the import and export of pollen. However, large floral displays also have negative effects, such as increased geitonogamy, pollen discounting and nectar/pollen robber attraction. The size of the floral display can be measured at different scales (e.g. the flower, inflorescence or entire plant) and variations in one of these scales may affect the behaviour of flower visitors in different ways. Moreover, the fragmentation of natural forests may affect flower visitation rates and flower visitor behaviour. In the present study, video recordings of the inflorescences of a tree species (Tabebuia aurea) from the tropical savannah of central Brazil were used to examine the effect of floral display size at the inflorescence and tree scales on the visitation rate of pollinators and nectar robbers to the inflorescence, the number of flowers approached per visit, the number of visits per flower of potential pollinators and nectar robbers, and the interaction of these variables with the degree of landscape disturbance. Nectar production was quantified with respect to flower age. Although large bees are responsible for most of the pollination, a great diversity of flower insects visit the inflorescences of T. aurea. Other bee and hummingbird species are highly active nectar robbers. Increases in inflorescence size increase the visitation rate of pollinators to inflorescences, whereas increases in the number of inflorescences on the tree decrease visitation rates to inflorescences and flowers. This effect has been strongly correlated with urban environments in which trees with the largest floral displays are observed. Pollinating bees (and nectar robbers) visit few flowers per inflorescence and concentrate visits to a fraction of available flowers, generating an overdispersed distribution of the number of visits per inflorescence and per flower. This behaviour reflects preferential visits to young flowers (including flower buds) with a greater nectar supply.     

花部特征演化的最有效传粉者原则:证据与疑问

自然界千姿百态的花是如何演化而来?前人曾提出花部特征是由当地最频繁的、最有效的传粉者所塑造的观点,但是吸引传粉者的特征也可能吸引植物的敌人——植食动物。花的特征与其他特征一样也经受着环境因子的选择作用。论述了支持花部特征演化的最有效传粉者原则的证据,该原则受到质疑的论点;再从植食作用、环境、传粉后的选择等方面,就花部特征选择的生态因子,列举了一些前人和作者提出的证据,以及需要深入研究的问题。     

Are pollinators the agents of selection on flower colour and size in irises?

Plant–pollinator interactions are believed to play a major role in the evolution of floral traits. Flower colour and flower size are important for attracting pollinators, directly influencing reproduction, and thus expected to be under pollinator‐mediated selection. Pollinator‐mediated selection is also proposed to play a role in maintaining flower colour polymorphism within populations. However, pigment concentrations, and thus flower colour, are also under selective pressures independent of pollinators. We quantified phenotypic pollinator‐mediated selection on flower colour and size in two colour polymorphic Iris species. Using female fitness, we estimated phenotypic selection on flower colour and size, and tested for pollinator‐mediated selection by comparing selection gradients between flowers open to natural pollination and supplementary pollinated flowers. In both species, we found evidence for pollen limitation, which set the base for pollinator‐mediated selection. In the colour dimorphic Iris lutescens, while pigment concentration and flower size were found to be under selection, this was independent of pollinators. For the polymorphic Iris pumila, pigment concentration is under selective pressure by pollinators, but only for one colour morph. Our results suggest that pollinators are not the main agents of selection on floral traits in these irises, as opposed to the accepted paradigm on floral evolution. This study provides an opposing example to the largely‐accepted theory that pollinators are the major agent of selection on floral traits.     

Covariance of floral and vegetative traits in four species of Ranunculaceae: a comparison between specialized and generalized pollination systems

Theory predicts that tighter correlation between floral traits and weaker relationship between floral and vegetative traits more likely occur in specialized flowers than generalized flowers,favoring by precise fit with pollinators.However,traits and trait correlations frequently vary under different environments.Through detecting spatiotemporal variation in phenotypic traits (floral organ size and vegetative size) and trait correlations in four Ranunculaceae species,we examined four predictions.Overall,our results supported these predictions to a certain degree.The mean coefficient of variation (CV) of floral traits in two specialized species (Delphinium kamaonense and Aconitum gymnandrum) was marginally significantly lower than that of another two generalized species (Trollius ranunculoides and Anemone obtusiloba).The two specialized species also showed marginally significantly smaller CV in floral traits than vegetative size across the two species.The absolute mean correlation between floral and vegetative traits,or that between floral traits in species with specialized flowers was not significantly lower,or higher than that in generalized plants,weakly supporting the predictions.Furthermore,we documented a large variation in trait correlations of four species among different seasons and populations.Study of covariance of floral and vegetative traits will benefit from the contrast of results obtained from generalized and specialized pollination systems.     

克隆生长对被子植物传粉过程的影响

克隆植物与其传粉者的相互作用是植物繁殖生态学的重要研究领域之一。植物克隆生长与有性繁殖通常相伴进行, 往往产生较大的花展示与复杂的克隆空间结构, 通过传粉过程对有性繁殖过程产生影响, 共同决定植物的适合度。本文回顾了克隆生长对被子植物传粉过程影响的国内外研究进展, 从植物克隆大小、花资源空间配置、克隆构型与种群遗传结构四个方面讨论了克隆生长对传粉过程的影响及其生态学与进化生物学意义。早期研究预期, 随着克隆增大, 同株异花授粉水平增加, 因而通过增大自交率或花粉阻塞效应降低植物的适合度。但是, 后来的一些模拟与野外实验研究发现, 传粉者在同一克隆内访问的花数量并不会随克隆增大而一直增加, 访花行为也主要发生在分株内; 而且分子标记的自交率组分分析也表明自交主要发生在分株内。另一方面, 人工模型模拟以及传粉者访问行为研究表明, 当花朵数量相同时, 与所有花集中生长在同一分株上相比, 将花朵分散在多个分株上的克隆生长方式不会增加, 反而降低了同株异花授粉的发生水平。如果花序内花雌雄同熟, 花朵同时提供与接收花粉, 克隆生长会使植物接收到更高比例的异交花粉, 在提高后代质量的同时不增加同株异花授粉概率。这是从传粉生物学角度对植物克隆生长习性进化的一个全新的解释。今后, 克隆植物传粉生物学研究需要针对传粉者与克隆生长之间的相互作用建立理论模型, 探究克隆大小、克隆构型、花资源空间配置模式对传粉者访问频率和行为、花粉散布、交配格局的影响。同时, 需要在自然种群中, 尤其是克隆与非克隆的近缘类群、同一物种克隆与非克隆种群开展比较研究, 利用更高效的分子标记来研究克隆生长的生态与进化意义。     

IS FLORAL SPECIALIZATION AN EVOLUTIONARY DEAD‐END? POLLINATION SYSTEM TRANSITIONS IN RUELLIA (ACANTHACEAE)

Pollination systems frequently reflect adaptations to particular groups of pollinators. Such systems are indicative of evolutionary specialization and have been important in angiosperm diversification. We studied the evolution of pollination systems in the large genus Ruellia. Phylogenetic analyses, morphological ordinations, ancestral state reconstructions, and a character mapping simulation were conducted to reveal key patterns in the direction and lability of floral characters associated with pollination. We found significant floral morphological differences among species that were generally associated with different groups of floral visitors. Floral evolution has been highly labile and also directional. Some specialized systems such as hawkmoth or bat pollination are likely evolutionary dead-ends. In contrast, specialized pollination by hummingbirds is clearly not a dead-end. We found evidence for multiple reverse transitions from presumed ancestral hummingbird pollination to more derived bee or insect pollination. These repeated origins of insect pollination from hummingbird-pollinated ancestors have not evolved without historical baggage. Flowers of insect-pollinated species derived from hummingbird-pollinated ancestors are morphologically more similar to hummingbird flowers than they are to other more distantly related insect-pollinated flowers. Finally, some pollinator switches were concomitant with changes in floral morphology that are associated with those pollinators. These observations are consistent with the hypothesis that some transitions have been adaptive in the evolution of Ruellia.