Deceptive pollinator lures benefit from physical and perceptual proximity to flowers
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ABSTRACT:
SUBMITTER: White T
PROVIDER: S-EPMC10917580 | biostudies-literature | 2024 Mar
REPOSITORIES: biostudies-literature
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Project description:Botanists have long identified bilaterally symmetrical (zygomorphic) flowers with more specialized pollination interactions than radially symmetrical (actinomorphic) flowers. Zygomorphic flowers facilitate more precise contact with pollinators, guide pollinator behaviour and exclude less effective pollinators. However, whether zygomorphic flowers are actually visited by a smaller subset of available pollinator species has not been broadly evaluated. We compiled 53 609 floral visitation records in 159 communities and classified the plants' floral symmetry. Globally and within individual communities, plants with zygomorphic flowers are indeed visited by fewer species. At the same time, zygomorphic flowers share a somewhat larger proportion of their visitor species with other co-occurring plants and have particularly high sharing with co-occurring plants that also have zygomorphic flowers. Visitation sub-networks for zygomorphic species also show differences that may arise from reduced visitor diversity, including greater connectance, greater web asymmetry and lower coextinction robustness of both plants and visitor species-but these changes do not necessarily translate to whole plant-visitor communities. These results provide context for widely documented associations between zygomorphy and diversification and imply that species with zygomorphic flowers may face a greater risk of extinction due to pollinator loss.
| S-EPMC7532724 | biostudies-literature
Project description:Background and aimsSelection exerted by pollinators on flowers is predicted to occur along two distinct axes. While pollinator attraction to flowers is governed by pollinator preferences, pollen transfer efficiency is mediated by the mechanical fit of pollinators to flower morphology. Although pollinator attraction in sexually deceptive orchids is typically underpinned by floral odour, morphological traits are expected to play a vital role in mechanical fit during floral contact with pollinators.MethodsHere we utilize a comprehensive and novel procedure to test for pollinator-mediated selection through mechanical fit with the flower labellum in the orchid Chiloglottis trapeziformis. This approach combines detailed pollinator observations related to plant reproductive fitness with complementary experimental manipulation and phenotypic selection analysis.Key resultsExperiments with virgin flowers revealed that pollen removal occurs only during vigorous pseudocopulation. This behaviour involves male wasps that grasp the insectiform callus structure on the labellum while probing the labellum tip in a forward orientation. Both orientation and duration of pseudocopulation were significant predictors of pollen removal, confirming a direct relationship between pollinator behaviour and plant fitness. Controlled floral manipulation that either shortened or elongated the distance between the callus and the labellum tip detected no change in pollinator attraction. The duration of pseudocopulation, however, was significantly reduced on flowers with shortened or elongated callus-tip distances, consistent with stabilizing selection. Phenotypic selection analysis confirmed this prediction in natural populations by uncovering evidence for stabilizing selection on the distance between the callus and the labellum tip.ConclusionsOur experimental manipulations and selection analysis in natural populations thus demonstrate stabilizing selection on the distance from the callus to the labellum tip, and illustrate the utility of employing multiple approaches to confirm selection exerted by pollinators on floral form.
| S-EPMC6344214 | biostudies-literature
Project description:In plants, pollinator adaptation is considered to be a major driving force for floral diversification and speciation. However, the genetic basis of pollinator adaptation is poorly understood. The orchid genus Ophrys mimics its pollinators' mating signals and is pollinated by male insects during mating attempts. In many species of this genus, chemical mimicry of the pollinators' pheromones, especially of alkenes with different double-bond positions, plays a key role for specific pollinator attraction. Thus, different alkenes produced in different species are probably a consequence of pollinator adaptation. In this study, we identify genes that are likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturases (SAD), in three closely related Ophrys species, O. garganica, O. sphegodes, and O. exaltata. Combining floral odor and gene expression analyses, two SAD homologs (SAD1/2) showed significant association with the production of (Z)-9- and (Z)-12-alkenes that were abundant in O. garganica and O. sphegodes, supporting previous biochemical data. In contrast, two other newly identified homologs (SAD5/6) were significantly associated with (Z)-7-alkenes that were highly abundant only in O. exaltata. Both molecular evolutionary analyses and pollinator preference tests suggest that the alkenes associated with SAD1/2 and SAD5/6 are under pollinator-mediated divergent selection among species. The expression patterns of these genes in F₁ hybrids indicate that species-specific expression differences in SAD1/2 are likely due to cis-regulation, while changes in SAD5/6 are likely due to trans-regulation. Taken together, we report a genetic mechanism for pollinator-mediated divergent selection that drives adaptive changes in floral alkene biosynthesis involved in reproductive isolation among Ophrys species.
| S-EPMC3420943 | biostudies-literature
Project description:BACKGROUND:Sexually deceptive orchids of the genus Ophrys attract their pollinators, male insects, on a highly specific basis through the emission of odour blends that mimic the female sex pheromone of the targeted species. In this study, we have investigated a contact site between Ophrys arachnitiformis and O. lupercalis, two sympatric orchid species that are usually reproductively isolated via the exploitation of different pollinator "niches", but occasionally hybridise despite their apparent combination of ethological and mechanical isolation barriers. In particular, we have investigated the extent to which these Ophrys hybrids generate "emergent" combinations (i.e. novel and unpredictable from the parents' phenotypes) of floral traits, and how these phenotypic novelties, particularly the odour blends emitted by the flower, could facilitate the invasion of a novel pollinator "niche" and induce the rapid formation of reproductive isolation, a prerequisite for adaptive evolutionary divergence. RESULTS:Our chemical analyses of floral scents show that the Ophrys F1 hybrids investigated here produce more compounds, significantly different ratios (% of odour compounds in the total blend), as well as new compounds in their floral odour compared to their progenitors. When tested for their attractiveness to the pollinator of each parent orchid species, we found that floral scent extracts of the hybrids triggered less inspecting flights and contacts by the male bees with the scented dummy than those of the parental orchid species. However, a series of additional behavioural bioassays revealed that the novel floral scent of the hybrids was significantly more attractive than either of the two parents to a pollinator species not initially involved in the pollination of any of the parent Ophrys species. CONCLUSIONS:Collectively, our results illustrate that the process of hybridisation can lead to the generation of evolutionary novelties, and that novel combinations of floral traits can drive pollinator shifts and rapid reproductive isolation in highly specific plant-pollinator interactions.
| S-EPMC2875231 | biostudies-literature
Project description:BackgroundSexually deceptive orchids of the genus Ophrys mimic the mating signals of their pollinator females to attract males as pollinators. This mode of pollination is highly specific and leads to strong reproductive isolation between species. This study aims to identify candidate genes responsible for pollinator attraction and reproductive isolation between three closely related species, O. exaltata, O. sphegodes and O. garganica. Floral traits such as odour, colour and morphology are necessary for successful pollinator attraction. In particular, different odour hydrocarbon profiles have been linked to differences in specific pollinator attraction among these species. Therefore, the identification of genes involved in these traits is important for understanding the molecular basis of pollinator attraction by sexually deceptive orchids.ResultsWe have created floral reference transcriptomes and proteomes for these three Ophrys species using a combination of next-generation sequencing (454 and Solexa), Sanger sequencing, and shotgun proteomics (tandem mass spectrometry). In total, 121 917 unique transcripts and 3531 proteins were identified. This represents the first orchid proteome and transcriptome from the orchid subfamily Orchidoideae. Proteome data revealed proteins corresponding to 2644 transcripts and 887 proteins not observed in the transcriptome. Candidate genes for hydrocarbon and anthocyanin biosynthesis were represented by 156 and 61 unique transcripts in 20 and 7 genes classes, respectively. Moreover, transcription factors putatively involved in the regulation of flower odour, colour and morphology were annotated, including Myb, MADS and TCP factors.ConclusionOur comprehensive data set generated by combining transcriptome and proteome technologies allowed identification of candidate genes for pollinator attraction and reproductive isolation among sexually deceptive orchids. This includes genes for hydrocarbon and anthocyanin biosynthesis and regulation, and the development of floral morphology. These data will serve as an invaluable resource for research in orchid floral biology, enabling studies into the molecular mechanisms of pollinator attraction and speciation.
| S-EPMC3667177 | biostudies-literature
Project description:Parasites are important actors within ecosystems. However, a key aspect to unraveling parasite epidemiology is understanding transmission. The bee pollinator community harbors several multihost parasites, which have been shown to be able to spread between species via flowers. Hence the plant-pollinator network can provide valuable information on the transmission of these parasites between species. Although several controlled experiments have shown that flowers function as a transmission hub for parasites, the link with the plant-pollinator network has rarely been addressed in the field. Here, one can hypothesize that the most central flowers in the network are more likely to enable parasite transmission between species. In this study, we test this hypothesis in three local plant-pollinator networks and show that the centrality of a plant in a weighted plant-pollinator network is a good predictor of the presence of multihost pollinator parasites on the plant's flowers.
| S-EPMC7762566 | biostudies-literature
Project description:Biotic interactions play an important role in species distribution models, whose ignorance may cause an overestimation of species' potential distributions. Species of the family Orchidaceae are almost totally dependent on mycorrhizal symbionts and pollinators, with sexually deceptive orchids being often highly specialized, and thus the interactions with their pollinators are expected to strongly affect distribution predictions. We used Maxent algorithm to explore the extent of current and future habitat suitability for two Greek endemic sexually deceptive orchids (Ophrys argolica and Ophrys delphinensis) in relation to the potential distribution of their unique pollinator (Anthophora plagiata). Twelve climate change scenarios were used to predict future distributions. Results indicated that the most important factors determining potential distribution were precipitation seasonality for O. argolica and geological substrate for O. delphinensis. The current potential distribution of the two orchids was almost of the same extent but spatially different, without accounting for their interaction with A. plagiata. When the interaction was included in the models, their potentially suitable area decreased for both species. Under future climatic conditions, the effects of the orchid-pollinator interaction were more intense. Specifically, O. argolica was restricted in specific areas of southern Greece, whereas O. delphinensis was expected to become extinct. Our findings highlighted the significant role of plant-pollinator interactions in species distribution models. Failing to study such interactions might expose plant species to serious conservation issues.
| S-EPMC7327032 | biostudies-literature
Project description:Can plants sense natural airborne sounds and respond to them rapidly? We show that Oenothera drummondii flowers, exposed to playback sound of a flying bee or to synthetic sound signals at similar frequencies, produce sweeter nectar within 3 min, potentially increasing the chances of cross pollination. We found that the flowers vibrated mechanically in response to these sounds, suggesting a plausible mechanism where the flower serves as an auditory sensory organ. Both the vibration and the nectar response were frequency-specific: the flowers responded and vibrated to pollinator sounds, but not to higher frequency sound. Our results document for the first time that plants can rapidly respond to pollinator sounds in an ecologically relevant way. Potential implications include plant resource allocation, the evolution of flower shape and the evolution of pollinators sound. Finally, our results suggest that plants may be affected by other sounds as well, including anthropogenic ones.
| S-EPMC6852653 | biostudies-literature
Project description:Background and aimsPterostylis is an Australasian terrestrial orchid genus of more than 400 species, most of which use a motile, touch-sensitive labellum to trap dipteran pollinators. Despite studies dating back to 1872, the mechanism of pollinator attraction has remained elusive. This study tested whether the fungus gnat-pollinated Pterostylis sanguinea secures pollination by sexual deception.MethodsThe literature was used to establish criteria for confirming sexual deception as a pollination strategy. Observations and video recordings allowed quantification of each step of the pollination process. Each floral visitor was sexed and DNA barcoding was used to evaluate the degree of pollinator specificity. Following observations that attraction to the flowers is by chemical cues, experimental dissection of flowers was used to determine the source of the sexual attractant and the effect of labellum orientation on sexual attraction. Fruit set was quantified for 19 populations to test for a relationship with plant density and population size.Key resultsA single species of male gnat (Mycetophilidae) visited and pollinated the rewardless flowers. The gnats often showed probing copulatory behaviour on the labellum, leading to its triggering and the temporary entrapment of the gnat in the flower. Pollen deposition and removal occurred as the gnat escaped from the flower via the reproductive structures. The labellum was the sole source of the chemical attractant. Gnats always alighted on the labellum facing upwards, but when it was rotated 180 ° they attempted copulation less frequently. Pollination rate showed no relationship with orchid population size or plant density.ConclusionsThis study confirms for the first time that highly specific pollination by fungus gnats is achieved by sexual deception in Pterostylis. It is predicted that sexual deception will be widespread in the genus, although the diversity of floral forms suggests that other mechanisms may also operate.
| S-EPMC3936588 | biostudies-literature
Project description:Dioecy, the specialization of individuals into either male-only or female-only sexual function, has multiple evolutionary origins in plants. One proposed ancestral mating system is heterodichogamy, two morphs of cross-fertilizing hermaphrodite flowers that differ in their timing of flowering. Previous research suggested that small specializations in these morphs' functional genders could facilitate their evolution into separate sexes. We tested the possible role of pollinators in driving such specializations. Ziziphus spina-christi is an insect-pollinated heterodichogamous tree with self-incompatible flowers and two sympatric flowering morphs. We compared the flower development patterns, floral food rewards, pollinator visits, and fruit production between the two morphs. Male-phase flowers of Z. spina-christi's "Early" and "Late" morphs open before dawn and around noon, respectively, and transition into female-phase 7-8 h later. Flowers of both morphs contain similar nectar and pollen rewards, and receive visits by flies (their ancestral pollinators) at similar rates, mostly during the morning. Consequently, the Early morph functions largely as pollen donor. The Late morph, functioning as female in the morning, produces more fruit. We developed an evolutionary probabilistic model, inspired by Z. spina-christi's reproductive system, to test whether pollinator visit patterns could potentially play a role in an evolutionary transition from heterodichogamy towards dioecy. The model predicts that reproductive incompatibility within flowering morphs promotes their evolution into different sexes. Furthermore, the pollinators' morning activity drives the Early and Late morphs' specialization into male and female functions, respectively. Thus, while not required for transitioning from heterodichogamy to dioecy, pollinator-mediated selection is expected to influence which sexual specialization evolves in each of the flowering morphs.
| S-EPMC6813929 | biostudies-literature