Mechanisms and evolution of deceptive pollination in orchids

The orchid family is renowned for its enormous diversity of pollination mechanisms and unusually high occurrence of non-rewarding flowers compared to other plant families. The mechanisms of deception in orchids include generalized food deception, food-deceptive floral mimicry, brood-site imitation, shelter imitation, pseudoantagonism, rendezvous attraction and sexual deception. Generalized food deception is the most common mechanism (reported in 38 genera) followed by sexual deception (18 genera). Floral deception in orchids has been intensively studied since Darwin, but the evolution of non-rewarding flowers still presents a major puzzle for evolutionary biology. The two principal hypotheses as to how deception could increase fitness in plants are (i) reallocation of resources associated with reward production to flowering and seed production, and (ii) higher levels of cross-pollination due to pollinators visiting fewer flowers on non-rewarding plants, resulting in more outcrossed progeny and more efficient pollen export. Biologists have also tried to explain why deception is overrepresented in the orchid family. These explanations include: (i) efficient removal and deposition of pollinaria from orchid flowers in a single pollinator visit, thus obviating the need for rewards to entice multiple visits from pollinators; (ii) efficient transport of orchid pollen, thus requiring less reward-induced pollinator constancy; (iii) low-density populations in many orchids, thus limiting the learning of associations of floral phenotypes and rewards by pollinators; (iv) packaging of pollen in pollinaria with limited carry-over from flower to flower, thus increasing the risks of geitonogamous self-pollination when pollinators visit many flowers on rewarding plants. All of these general and orchid-specific hypotheses are difficult to reconcile with the well-established pattern for rewardlessness to result in low pollinator visitation rates and consequently low levels of fruit production. Arguments that deception evolves because rewards are costly are particularly problematic in that small amounts of nectar are unlikely to have a significant effect on the energy budget of orchids, and because reproduction in orchids is often severely pollen-, rather than resource-limited. Several recent experimental studies have shown that deception promotes cross-pollination, but it remains unknown whether actual outcrossing rates are generally higher in deceptive orchids. Our review of the literature shows that there is currently no evidence that deceptive orchids carry higher levels of genetic load (an indirect measure of outcrossing rate) than their rewarding counterparts. Cross-pollination does, however, result in dramatic increases in seed quality in almost all orchids and has the potential to increase pollen export (by reducing pollen discounting). We suggest that floral deception is particularly beneficial, because of its promotion of outcrossing, when pollinators are abundant, but that when pollinators are consistently rare, selection may favour a nectar reward or a shift to autopollination. Given that nectar-rewardlessness is likely to have been the ancestral condition in orchids and yet is evolutionarily labile, more attention will need to be given to explanations as to why deception constitutes an 'evolutionarily stable strategy'.     

Physiological diversity of orchids

The Orchidaceae is a diverse and wide spread family of flowering plants that are of great value in ornamental, medical, conservation, and evolutionary research. The broad diversity in morphology, growth form, life history, and habitat mean that the members of Orchidaceae exhibit various physiological properties. Epiphytic orchids are often characterized by succulent leaves with thick cell walls, cuticles, and sunken stomata, whereas terrestrial orchids possess rhizomes, corms, or tubers. Most orchids have a long juvenile period, slow growth rate, and low photosynthetic capacity. This reduced photosynthetic potential can be largely explained by CO₂ diffusional conductance and leaf internal structure. The amount of light required for plant survival depends upon nutritional mode, growth form, and habitat. Most orchids can adapt to their light environments through morphological and physiological adjustments but are sensitive to sudden changes in irradiance. Orchids that originate from warm regions are susceptible to chilling temperatures, whereas alpine members are vulnerable to high temperatures. For epiphytic orchids, rapid water uptake by the velamen radicum, water storage in their pseudobulbs and leaves, slow water loss, and Crassulacean Acid Metabolism contribute to plant-water balance and tolerance to drought stress. The presence of the velamen radicum and mycorrhizal fungi may compensate for the lack of root hairs, helping with quick absorbance of nutrients from the atmosphere. Under cultivation conditions, the form and concentration of nitrogen affect orchid growth and flowering. However, the limitations of nitrogen and phosphorous on epiphytic orchids in the wild, which require these plants to depend on mycorrhizal fungi for nutrients throughout the entire life cycle, are not clearly understood. Because they lack endosperm, seed germination depends upon obtaining nutrients via mycorrhizal fungi. Adult plants of some autotrophic orchids also gain carbon, nitrogen, phosphorus, and other elements from their mycorrhizal partners. Future studies should examine the mechanisms that determine slow growth and flower induction, the physiological causes of variations in flowering behavior and floral lifespan, the effects of nutrients and atmospheric-nitrogen deposition, and practical applications of mycorrhizal fungi in orchid cultivation.     

The MADS and the Beauty: Genes Involved in the Development of Orchid Flowers

Since the time of Darwin, biologists have studied the origin and evolution of the Orchidaceae, one of the largest families of flowering plants. In the last two decades, the extreme diversity and specialization of floral morphology and the uncoupled rate of morphological and molecular evolution that have been observed in some orchid species have spurred interest in the study of the genes involved in flower development in this plant family. As part of the complex network of regulatory genes driving the formation of flower organs, the MADS-box represents the most studied gene family, both from functional and evolutionary perspectives. Despite the absence of a published genome for orchids, comparative genetic analyses are clarifying the functional role and the evolutionary pattern of the MADS-box genes in orchids. Various evolutionary forces act on the MADS-box genes in orchids, such as diffuse purifying selection and the relaxation of selective constraints, which sometimes reveals a heterogeneous selective pattern of the coding and non-coding regions. The emerging theory regarding the evolution of floral diversity in orchids proposes that the diversification of the orchid perianth was a consequence of duplication events and changes in the regulatory regions of the MADS-box genes, followed by sub- and neo-functionalization. This specific developmental-genetic code is termed the "orchid code."     

Research on orchid biology and biotechnology

Orchidaceae constitute one of the largest families of angiosperms. They are one of the most ecological and evolutionary significant plants and have successfully colonized almost every habitat on earth. Because of the significance of plant biology, market needs and the current level of breeding technologies, basic research into orchid biology and the application of biotechnology in the orchid industry are continually endearing scientists to orchids in Taiwan. In this introductory review, we give an overview of the research activities in orchid biology and biotechnology, including the status of genomics, transformation technology, flowering regulation, molecular regulatory mechanisms of floral development, scent production and color presentation. This information will provide a broad scope for study of orchid biology and serve as a starting point for uncovering the mysteries of orchid evolution.     

Evolution and biogeography of the slipper orchids: Eocene vicariance of the conduplicate genera in the Old and New World Tropics

Intercontinental disjunctions between tropical regions, which harbor two-thirds of the flowering plants, have drawn great interest from biologists and biogeographers. Most previous studies on these distribution patterns focused on woody plants, and paid little attention to herbs. The Orchidaceae is one of the largest families of angiosperms, with a herbaceous habit and a high species diversity in the Tropics. Here we investigate the evolutionary and biogeographical history of the slipper orchids, which represents a monophyletic subfamily (Cypripedioideae) of the orchid family and comprises five genera that are disjunctly distributed in tropical to temperate regions. A relatively well-resolved and highly supported phylogeny of slipper orchids was reconstructed based on sequence analyses of six maternally inherited chloroplast and two low-copy nuclear genes (LFY and ACO). We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics. Mexipedium and Phragmipedium from the neotropics are most closely related, and form a clade sister to Paphiopedilum from tropical Asia. According to molecular clock estimates, the genus Selenipedium originated in Palaeocene, while the most recent common ancestor of conduplicate-leaved slipper orchids could be dated back to the Eocene. Ancestral area reconstruction indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions. Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups. In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.     

Patterns of reproductive isolation in Mediterranean deceptive orchids

The evolution of reproductive isolation is of central interest in evolutionary biology. In plants, this is typically achieved by a combination of pre- and postpollination mechanisms that prevent, or limit, the amount of interspecific gene flow. Here, we investigated and compared two ecologically defined groups of Mediterranean orchids that differ in pollination biology and pollinator specificity: sexually deceptive orchids versus food-deceptive orchids. We used experimental crosses to assess the strength of postmating prezygotic, and postzygotic reproductive isolation, and a phylogenetic framework to determine their relative rates of evolution. We found quantitative and qualitative differences between the two groups. Food-deceptive orchids have weak premating isolation but strong postmating isolation, whereas the converse situation characterizes sexually deceptive orchids. Only postzygotic reproductive isolation among food-deceptive orchids was found to evolve in a clock-like manner. Comparison of evolutionary rates, within a common interval of genetic distance, showed that the contribution of postmating barriers was more relevant in the food-deceptive species than in the sexually deceptive species. Asymmetry in prezygotic isolation was found among food-deceptive species. Our results indicate that postmating barriers are most important for reproductive isolation in food-deceptive orchids, whereas premating barriers are most important in sexually deceptive orchids. The different rate of evolution of reproductive isolation and the relative strength of pre- and postmating barriers may have implication for speciation processes in the two orchid groups.     

广东山区兰科植物的野生花卉资源

经初步统计,广东山区具有较高观赏价值和开发价值的野生兰花资源植物有148种,其中观花类87种,观叶类43种,花叶两赏类18种。介绍广东山区野生兰花资源植物的地理分布情况、生态特点和生长习性。提出保护和开发野生兰花资源的几点建议。     

Bioactive Secondary Metabolites from Orchids (Orchidaceae)

The Orchidaceae family is the largest group of flowering plants in the Angiosperm monocotyledons spread on our planet. Its members, called orchids, are herbs or epiphytes with showy flowers distributed mainly in tropical regions. Several classes of phytoconstituents have been so far isolated from therapeutically‐used orchids showing a great chemical diversity. Among them, phenolic derivatives have been studied for their biological activities, especially in the field of cancer, inflammation, and neurodegeneration. On the other hand, limited information has been so far obtained on the numerous alkaloids and terpenoids isolated from several orchid species. Recent articles revealed pronounced effects of some alkaloids on the CNS. Published literature on orchids that are used in traditional medicine has been reviewed in this work indicating a great potential of such organisms as source of chemical entities for the development of new drugs.     

The impact of life form on the architecture of orchid mycorrhizal networks in tropical forest

Understanding the processes that determine the architecture of interaction networks represents a major challenge in ecology and evolutionary biology. One of the most important interactions involving plants is the interaction between plants and mycorrhizal fungi. While there is a mounting body of research that has studied the architecture of plant–fungus interaction networks, less is known about the potential factors that drive network architecture. In this study, we described the architecture of the network of interactions between mycorrhizal fungi and 44 orchid species that represented different life forms and co‐occurred in tropical forest and assessed the relative importance of ecological, evolutionary and co‐evolutionary mechanisms determining network architecture. We found 87 different fungal operational taxonomic units (OTUs), most of which were members of the Tulasnellaceae. Most orchid species associated with multiple fungi simultaneously, indicating that extreme host selectivity was rare. However, an increasing specificity towards Tulasnellaceae fungal associates from terrestrial to epiphytic and lithophytic orchids was observed. The network of interactions showed an association pattern that was significantly modular (M = 0.7389, M_random = 0.6998) and nested (NODF = 5.53, p < 0.05). Terrestrial orchids had almost no links to modules containing epiphytic or lithophytic orchids, while modules containing epiphytic orchids also contained lithophytic orchids. Within each life form several modules were observed, suggesting that the processes that organize orchid–fungus interactions are independent of life form. The overall phylogenetic signal for both partners in the interaction network was very weak. Overall, these results indicate that tropical orchids associate with a wide number of mycorrhizal fungi and that ecological rather than phylogenetic constraints determine network architecture.     

Evolutionary origins of the endosperm in flowering plants

The evolutionary origin of double fertilization and the resultant endosperm tissue in flowering plants remains a puzzle, despite over a century of research. The recent resurgence of approaches to evolutionary developmental biology combining comparative biology with phylogenetics provides new understanding of endosperm origins.     

Effects of floral display and plant abundance on fruit production of Ryncholaelia glauca (Orchidaceae)

Flowering plant density can increase number of visits and fruit set in multi-flowering plants, however this aspect has not been studied on few flower species. We studied the effects of individual floral display and plant density on the fruit production of the epiphytic, moth-pollinated orchid, Ryncholaelia glauca, in an oak forest of Chavarrillo, Veracruz, Mexico. Species is non-autogamous, and produced one flower per flowering shoot each flowering season. We hypothesized that orchids with more flowering shoots and those on trees with clumps of conspecific should develop more fruits than isolated ones. R. glauca population flowers synchronouly, and individual flowers last up to 18 days, with flowers closing rapidly after pollination. Individuals produced few flowers per year, although some plants developed flowers in both seasons and fewer of them developed fruits both years. There was no relationship between flower number per orchid, or per host tree, with the number of fruits developed per plant. Host trees with flowering and fruiting orchids were randomly dispersed and the pattern of distribution of flowering and fruiting plants was not related. Apparently, pollinators visit the flowers randomly, with no evidence of density dependence. The fruit set of R. glauca was as low as fruit set of multi-flowered orchids moth pollinated, suggesting that fruit set on moth pollinated orchids could be independent of the number of flowers displayed.     

Perspective: the origin of flowering plants and their reproductive biology--a tale of two phylogenies

Recently, two areas of plant phylogeny have developed in ways that could not have been anticipated, even a few years ago. Among extant seed plants, new phylogenetic hypotheses suggest that Gnetales, a group of nonflowering seed plants widely hypothesized to be the closest extant relatives of angiosperms, may be less closely related to angiosperms than was believed. In addition, recent phylogenetic analyses of angiosperms have, for the first time, clearly identified the earliest lineages of flowering plants: Amborella, Nymphaeales, and a clade that includes Illiciales/ Trimeniaceae/Austrobaileyaceae. Together, the new seed plant and angiosperm phylogenetic hypotheses have major implications for interpretation of homology and character evolution associated with the origin and early history of flowering plants. As an example of the complex and often unpredictable interplay of phylogenetic and comparative biology, we analyze the evolution of double fertilization, a process that forms a diploid embryo and a triploid endosperm, the embryo-nourishing tissue unique to flowering plants. We demonstrate how the new phylogenetic hypotheses for seed plants and angiosperms can significantly alter previous interpretations of evolutionary homology and firmly entrenched assumptions about what is synapomorphic of flowering plants. In the case of endosperm, a solution to the century-old question of its potential homology with an embryo or a female gametophyte (the haploid egg-producing generation within the life cycle of a seed plant) remains complex and elusive. Too little is known of the comparative reproductive biology of extant nonflowering seed plants (Gnetales, conifers, cycads, and Ginkgo) to analyze definitively the potential homology of endosperm with antecedent structures. Remarkably, the new angiosperm phylogenies reveal that a second fertilization event to yield a biparental endosperm, long assumed to be an important synapomorphy of flowering plants, cannot be conclusively resolved as ancestral for flowering plants. Although substantive progress has been made in the analysis of phylogenetic relationships of seed plants and angiosperms, these efforts have not been matched by comparable levels of activity in comparative biology. The consequence of inadequate comparative biological information in an age of phylogenetic biology is a severe limitation on the potential to reconstruct key evolutionary historical events.     

Molecular analysis of orchid pollinaria and pollinaria-remains found on insects

Direct observations of pollinator visits to orchids are often difficult and time consuming, especially in orchids with a deceptive pollination system where seed set is typically pollinator-limited. This lack of direct observations greatly inhibits our understanding of orchid-pollinator relationships and especially the degree of pollinator-specificity. Here we describe a molecular approach to the study of orchid-pollinator relationships based on the analysis of DNA recovered from pollinaria found on insects. The insects were collected from nectar-rich plants flowering near natural orchid populations, or taken from museum collections. Sequence analysis of the nuclear ribosomal ITS region allowed the identification of the orchid species or species-group from which the pollinaria originated. Four out of eight orchid-pollinator relationships established with this approach have not been reported previously, which highlights the value of molecular tools for the study of orchid pollination biology.     

Orthoptera, a new order of pollinator

Background and Aims

Pollinator-mediated selection and evolution of floral traits have long fascinated evolutionary ecologists. No other plant family shows as wide a range of pollinator-linked floral forms as Orchidaceae. In spite of the large size of this model family and a long history of orchid pollination biology, the identity and specificity of most orchid pollinators remains inadequately studied, especially in the tropics where the family has undergone extensive diversification. Angraecum (Vandeae, Epidendroideae), a large genus of tropical Old World orchids renowned for their floral morphology specialized for hawkmoth pollination, has been a model system since the time of Darwin.

Methods

The pollination biology of A. cadetii, an endemic species of the islands of Mauritius and Reunion (Mascarene Islands, Indian Ocean) displaying atypical flowers for the genus (white and medium-size, but short-spurred) was investigated. Natural pollinators were observed by means of hard-disk camcorders. Pollinator-linked floral traits, namely spur length, nectar volume and concentration and scent production were also investigated. Pollinator efficiency (pollen removal and deposition) and reproductive success (fruit set) were quantified in natural field conditions weekly during the 2003, 2004 and 2005 flowering seasons (January to March).

Key Results

Angraecum cadetii is self-compatible but requires a pollinator to achieve fruit set. Only one pollinator species was observed, an undescribed species of raspy cricket (Gryllacrididae, Orthoptera). These crickets, which are nocturnal foragers, reached flowers by climbing up leaves of the orchid or jumping across from neighbouring plants and probed the most ‘fresh-looking’ flowers on each plant. Visits to flowers were relatively long (if compared with the behaviour of birds or hawkmoths), averaging 16·5 s with a maximum of 41·0 s. At the study site of La Plaine des Palmistes (Pandanus forest), 46·5 % of flowers had pollen removed and 27·5 % had pollinia deposited on stigmas. The proportion of flowers that set fruit ranged from 11·9 % to 43·4 %, depending of the sites sampled across the island.

Conclusions

Although orthopterans are well known for herbivory, this represents the first clearly supported case of orthopteran-mediated pollination in flowering plants.     

The evolution of plant sexual diversity

Charles Darwin recognized that flowering plants have an unrivalled diversity of sexual systems. Determining the ecological and genetic factors that govern sexual diversification in plants is today a central problem in evolutionary biology. The integration of phylogenetic, ecological and population-genetic studies have provided new insights into the selective mechanisms that are responsible for major evolutionary transitions between reproductive modes.     

Tourism and recreation a global threat to orchids

Orchidaceae is a mega diverse family accounting for 10% of the world’s flowering plants. Due to factors such as small dispersed populations, specific symbiosis with fungi and with pollinators and their desirability for collecting, many orchids are threatened with extinction. Tourism and recreation is increasingly recognised as a global threat for plants, but is it an issue for orchids? When data on orchids from the International Union for Nature Conservation (IUCN) Red List was reviewed, we found that 149 (40%) of the 442 orchid species with threat data were at risk from tourism and recreation. This included: 98 (22%) species threatened by residential and commercial development for tourism and recreation, 75 (17%) by intentional collecting within protected areas, and 90 (20%) by human intrusions and disturbance from recreational activities. The three threats often co-occurred and hence can be treated as a threat syndrome. The proportion of species threatened varied among locations with 80% of the 65 species in East Asia, 32% of 68 species in South and Southeast Asia and 94% of 16 orchid species in Europe threatened by tourism and recreation. Terrestrial orchids and those growing in forests were more likely to be at risk from these threats. With so many species at risk, increased awareness and recognition of these threats combined with improved management to reduce impacts is needed. Gaps and inconsistencies in the IUCN Red List must also be addressed to obtain a better understanding of the extent of this, and other threats to plants.     

重要观赏兰科植物的分子生物学研究进展

兰科植物是开花植物中最大的家族之一,分子标记技术应用于兰科植物的分类鉴定和品种鉴别,为兰花的分类提供了分子水平的证据,也为兰花保护策略和措施的制定提供了理论基础。兰科植物表现有高度特异的形态、结构和生理特性,是研究花着色机理和子房发育的理想对象。兰花离体培养开花系统的建立,可以用来探明兰花从营养生长向生殖生长的转变机制,是研究花的分化和发育的理想材料。兰花具有特异的查尔酮合成酶（CHS）基因和二氢叶酸还原酶（DFR）基因等控制花色素的合成,DOH1基因控制石斛兰花芽的形成和提早开花,PHAL.039基因和ACC合成酶基因在蝴蝶兰授粉后的子房发育中起着重要的调控作用,这些特异基因的分离和克隆为兰花花的分化、发育及着色机制提供了分子基础。蝴蝶兰属、大花蕙兰(Cymbidium hybridium)、石斛兰属、文心兰属、五唇兰属和万代兰属等兰科植物都有转基因的研究报道,主要以原球茎为材料采用基因枪或农杆菌法转化,部分研究获得了转化植株。     

Specificity and mutual dependency of the orchid-euglossine bee interaction

Seasonal and geographic relationships, and host pollinator specificities are examined for indications of interdependency in the orchid-euglossine bee interaction. The orchids are dependent on the bees for pollination, and their flowering seasonality corresponds well with peak activity of their pollinators. However, there is little evidence that the bees are dependent on these fragrance hosts. The orchids tap the majority of euglossine species and individuals for pollinator services during any given season, but most of those bee species that temporarily lack orchid fragrance hosts persist in the area, continually emerge from nests, and seek floral fragrance compounds. Pollinator specificity occurs in less than half of the orchids, and host specificity is rare. Geographic distributions of nearly all orchid-pollinator pairs are not mutually inclusive. Moreover, nearly a third of the local male euglossine bee species censused are not pollinators of any fragrance orchids in the area. Local alternative fragrance sources occur. The orchid-male euglossine bee interaction does not appear to represent a mutually obligatory relationship. The orchids may have exploited a preexisting behavioural phenomenon of the bees, and reciprocal evolutionary responses may not have occurred.     

Generalized food-deceptive orchid species flower earlier and occur at lower altitudes than rewarding ones

Aims Food-deceptive pollination, in which plants do not offer any food reward to their pollinators, is common within the Orchidaceae. As food-deceptive orchids are poorer competitors for pollinator visitation than rewarding orchids, their occurrence in a given habitat may be more constrained than that of rewarding orchids. In particular, the success of deceptive orchids strongly relies on several biotic factors such as interactions with co-flowering rewarding species and pollinators, which may vary with altitude and over time. Our study compares generalized food-deceptive (i.e. excluding sexually deceptive) and rewarding orchids to test whether (i) deceptive orchids flower earlier compared to their rewarding counterparts and whether (ii) the relative occurrence of deceptive orchids decreases with increasing altitude.Methods To compare the flowering phenology of rewarding and deceptive orchids, we analysed data compiled from the literature at the species level over the occidental Palaearctic area. Since flowering phenology can be constrained by the latitudinal distribution of the species and by their phylogenetic relationships, we accounted for these factors in our analysis. To compare the altitudinal distribution of rewarding and deceptive orchids, we used field observations made over the entire Swiss territory and over two Swiss mountain ranges.Important findings We found that deceptive orchid species start flowering earlier than rewarding orchids do, which is in accordance with the hypotheses of exploitation of naive pollinators and/or avoidance of competition with rewarding co-occurring species. Also, the relative frequency of deceptive orchids decreases with altitude, suggesting that deception may be less profitable at high compared to low altitude.