Floral Scent Chemistry and Pollinators of a Sexually Dimorphic Neotropical Orchid.
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ABSTRACT:
SUBMITTER: Milet-Pinheiro P
PROVIDER: S-EPMC9824664 | biostudies-literature | 2022 Dec
REPOSITORIES: biostudies-literature
Publications
Floral Scent Chemistry and Pollinators of a Sexually Dimorphic Neotropical Orchid.
Milet-Pinheiro Paulo P Pinto Carlos E CE Navarro Daniela M A F DMAF Silva João B F JBF Brandt Katharina K Ayasse Manfred M
Plants (Basel, Switzerland) 20221220 1
<i>Catasetum</i> is a speciose Neotropical orchid genus of which male and female flowers emit scents acting both as attractant and reward for their exclusive pollinators, male orchid bees (Euglossini: Apidae). In <i>Catasetum</i>, it is well known that flowers display a remarkably morphological sexual dimorphism. However, it remains poorly investigated whether this is also true for floral scents. Here, we investigated the pollination ecology and floral scent traits (chemistry and total emission) ...[more]
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Project description:Unlabelled•Background and aimsAnimal-pollinated angiosperms have evolved a variety of signalling mechanisms to attract pollinators. Floral scent is a key component of pollinator attraction, and its chemistry modulates both pollinator behaviour and the formation of plant-pollinator networks. The neotropical orchid genus Gongora exhibits specialized pollinator associations with male orchid bees (Euglossini). Male bees visit orchid flowers to collect volatile chemical compounds that they store in hind-leg pouches to use subsequently during courtship display. Hence, Gongora floral scent compounds simultaneously serve as signalling molecules and pollinator rewards. Furthermore, because floral scent acts as the predominant reproductive isolating barrier among lineages, it has been hypothesized that chemical traits are highly species specific. A comparative analysis of intra- and inter-specific variation of floral scent chemistry was conducted to investigate the evolutionary patterns across the genus. •MethodsGas chromatography-mass spectrometry (GC-MS) was used to analyse the floral scent of 78 individuals belonging to 28 different species of Gongora from two of the three major lineages sampled across the neotropical region. Multidimensional scaling and indicator value analyses were implemented to investigate the patterns of chemical diversity within and among taxonomic groups at various geographic scales. Additionally, pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes. •Key resultsA total of 83 floral volatiles, mainly terpenes and aromatic compounds, were detected. Many of the identified compounds are common across diverse angiosperm families (e.g. cineole, eugenol, β-ocimene, β-pinene and terpinen-4-ol), while others are relatively rare outside euglossine bee-pollinated orchid lineages. Additionally, 29 volatiles were identified that are known to attract and elicit collection behaviour in male bees. Floral scent traits were less variable within species than between species, and the analysis revealed exceptional levels of cryptic diversity. Gongora species were divided into 15 fragrance groups based on shared compounds. Fragrance groups indicate that floral scent variation is not predicted by taxonomic rank or biogeographic region. •ConclusionsGongora orchids emit a diverse array of scent molecules that are largely species specific, and closely related taxa exhibit qualitatively and quantitatively divergent chemical profiles. It is shown that within a community, Gongora scent chemotypes are correlated with near non-overlapping bee pollinator assemblies. The results lend support to the hypothesis that floral scent traits regulate the architecture of bee pollinator associations. Thus, Gongora provides unique opportunities to examine the interplay between floral traits and pollinator specialization in plant-pollinator mutualisms.
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Project description:Plant-pollinator systems may be considered as biological markets in which pollinators choose between different flowers that advertise their nectar/pollen rewards. Although expected to play a major role in structuring plant-pollinator interactions, community-wide patterns of flower scent signals remain largely unexplored. Here we show for the first time that scent advertisement is higher in plant species that bloom early in the flowering period when pollinators are scarce relative to flowers than in species blooming later in the season when there is a surplus of pollinators relative to flowers. We also show that less abundant flowering species that may compete with dominant species for pollinator visitation early in the flowering period emit much higher proportions of the generalist attractant ?-ocimene. Overall, we provide a first community-wide description of the key role of seasonal dynamics of plant-specific flower scent emissions, and reveal the coexistence of contrasting plant signaling strategies in a plant-pollinator market.
| S-EPMC3852139 | biostudies-literature
Project description:Male and female C57BL/6 J mice were tested on the predator odor response task, where they needed to cross through a chamber of scented bedding to reach a sucrose reward. Following the behavioral testing, mouse brains were immunohistochemically labeled for expression of the immediate early gene c-fos. In the presence of the novel odorant methyl valerate (MV), both males and females exhibited increased exploration behaviors and delayed rewards compared to control bedding. However, in the presence of the predator odor phenylethylamine (PEA), males exhibited increased exploration that strongly resembled their behavior in MV (a non-predator odor) while females behaved very similarly to the clean bedding controls, quickly traversing the chamber to achieve the reward. Expression of c-fos exhibited significant sex by odor condition interactions overall across brain regions and in the anterior piriform cortex, cingulate cortex, and dorsomedial hypothalamus specifically. In all three regions we observed the general pattern that PEA exposure evoked elevated c-fos expression in females but suppressed c-fos expression in males. Taken together these data suggest that males and females may adopt different behavioral strategies in the presence of predator threat.
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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:Speciation is typically accompanied by the formation of isolation barriers between lineages. Commonly, reproductive barriers are separated into pre- and post-zygotic mechanisms that can evolve with different speed. In this study, we measured the strength of different reproductive barriers in two closely related, sympatric orchids of the Ophrys insectifera group, namely Ophrys insectifera and Ophrys aymoninii to infer possible mechanisms of speciation. We quantified pre- and post-pollination barriers through observation of pollen flow, by performing artificial inter- and intraspecific crosses and analyzing scent bouquets. Additionally, we investigated differences in mycorrhizal fungi as a potential extrinsic factor of post-zygotic isolation. Our results show that floral isolation mediated by the attraction of different pollinators acts apparently as the sole reproductive barrier between the two orchid species, with later-acting intrinsic barriers seemingly absent. Also, the two orchids share most of their fungal mycorrhizal partners in sympatry, suggesting little or no importance of mycorrhizal symbiosis in reproductive isolation. Key traits underlying floral isolation were two alkenes and wax ester, present predominantly in the floral scent of O. aymoninii. These compounds, when applied to flowers of O. insectifera, triggered attraction and a copulation attempt of the bee pollinator of O. aymoninii and thus led to the (partial) breakdown of floral isolation. Based on our results, we suggest that adaptation to different pollinators, mediated by floral scent, underlies species isolation in this plant group. Pollinator switches may be promoted by low pollination success of individuals in dense patches of plants, an assumption that we also confirmed in our study.
| S-EPMC5551101 | biostudies-literature
Project description:Background and aimsThe temporal dimensions of floral adaptation to pollinators are not yet well understood, partly because we lack accurate information on the diel rhythms of flower visitation for many pollinators. We investigated whether diel patterns of pollinator visitation to flowers of the African woodland orchid Bonatea polypodantha are synchronized with rhythms of floral anthesis, scent emission and nectar availability.MethodsDirect observations and motion-activated cameras were used to identify pollinators of B. polypodantha and to document their activity periods. The timing of pollinaria removal from flowers, emission of scent and availability of nectar was also measured.ResultsWe found that B. polypodantha is pollinated exclusively by short-tongued hawkmoths. Pollinaria of the orchid are affixed between the labial palps of the moths and brush over the protruding stigmatic arms. The flowers also receive visits by long-tongued hawkmoths, but these act as nectar thieves. Tracking of pollinaria removal from flowers confirmed that pollination occurs only at night. Camera footage revealed a striking crepuscular pattern of foraging by short-tongued hawkmoths with peaks of activity during the twilight periods at dusk and at dawn. In contrast, long-tongued hawkmoths were found to visit flowers throughout the night. Flowers of B. polypodantha exhibit unimodal peaks of anthesis, scent emission (dominated by nitrogenous aromatics) and nectar availability before or around dusk.ConclusionsFlowers of B. polypodantha are pollinated exclusively by short-tongued hawkmoths, which show crepuscular foraging activity at dusk and dawn. Floral phenophases of the orchid are closely synchronized with the peak of pollinator activity at dusk.
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Project description:Background and Aims:Floral scent is considered an integral component of pollination syndromes, and its composition and timing of emission are thus expected to match the main pollinator type and time of activity. While floral scent differences among plant species with different pollination systems can be striking, studies on intraspecific variation are sparse, which limits our understanding of the role of pollinators in driving scent divergence. Methods:Here, we used dynamic headspace sampling to quantify floral scent emission and composition during the day and at night in the natural habitat of six Scandinavian populations of the fragrant orchid Gymnadenia conopsea. We tested whether diel scent emission and composition match pollinator type by comparing four populations in southern Sweden, where nocturnal pollinators are more important for plant reproductive success than are diurnal pollinators, with two populations in central Norway, where the opposite is true. To determine to what extent scent patterns quantified in the field reflected plasticity, we also measured scent emission in a common growth chamber environment. Key Results:Both scent composition and emission rates differed markedly between day and night, but only the latter varied significantly among populations. The increase in scent emission rate at night was considerably stronger in the Swedish populations compared with the Norwegian populations. These patterns persisted when plants were transferred to a common environment, suggesting a genetic underpinning of the scent variation. Conclusions:The results are consistent with a scenario where spatial variation in relative importance of nocturnal and diurnal pollinators has resulted in selection for different scent emission rhythms. Our study highlights the importance of adding a characterization of diel variation of scent emission rates to comparative studies of floral scent, which so far have often focused on scent composition only.
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Project description:The floral traits of bisexual flowers may evolve in response to selection on both male and female functions, but the relative importance of selection associated with each of these two aspects is poorly resolved. Sexually dimorphic traits in plants with unisexual flowers may reflect gender-specific selection, providing opportunities for gaining an increased understanding of the evolution of specific floral traits. We examined sexually dimorphic patterns of floral traits in perfect and female flowers of the gynodioecious species Cyananthus delavayi. A special corolla appendage, the throat hair, was investigated experimentally to examine its influences on male and female function. We found that perfect flowers have larger corollas and much longer throat hairs than female flowers, while female ones have much exerted stigmas. The presence of throat hairs prolonged the duration of pollen presentation by restricting the amount of pollen removed by pollen-collecting bees during each visit. Floral longevity was negatively related to the rate of pollen removal. When pollen removal rate was limited in perfect flowers, the duration of the female phases diminished with the increased male phase duration. There was a weak negative correlation between throat hair length and seed number per fruit in female flowers, but this correlation was not significant in perfect flowers. These results suggest that throat hairs may enhance male function in terms of prolonged pollen presentation. However, throat hairs have no obvious effect on female function in terms of seed number per fruit. The marked sexual dimorphism of this corolla appendage in C. delavayi is likely to have evolved and been maintained by gender-specific selection.
| S-EPMC4300179 | biostudies-literature
Project description:Sexually deceptive plants secure pollination by luring specific male insects as pollinators using a combination of olfactory, visual, and morphological mimicry. Flower color is a key component to this attraction, but its chemical and genetic basis remains poorly understood. Chiloglottis trapeziformis is a sexually deceptive orchid which has predominantly dull green-red flowers except for the central black callus projecting from the labellum lamina. The callus mimics the female of the pollinator and the stark color contrast between the black callus and dull green or red lamina is thought to enhance the visibility of the mimic. The goal of this study was to investigate the chemical composition and genetic regulation of temporal and spatial color patterns leading to visual mimicry, by integrating targeted metabolite profiling and transcriptomic analysis. Even at the very young bud stage, high levels of anthocyanins were detected in the dark callus, with peak accumulation by the mature bud stage. In contrast, anthocyanin levels in the lamina peaked as the buds opened and became reddish-green. Coordinated upregulation of multiple genes, including dihydroflavonol reductase and leucoanthocyanidin dioxygenase, and the downregulation of flavonol synthase genes (FLS) in the callus at the very young bud stage underpins the initial high anthocyanin levels. Conversely, within the lamina, upregulated FLS genes promote flavonol glycoside over anthocyanin production, with the downstream upregulation of flavonoid O-methyltransferase genes further contributing to the accumulation of methylated flavonol glycosides, whose levels peaked in the mature bud stage. Finally, the peak anthocyanin content of the reddish-green lamina of the open flower is underpinned by small increases in gene expression levels and/or differential upregulation in the lamina in select anthocyanin genes while FLS patterns showed little change. Differential expression of candidate genes involved in specific transport, vacuolar acidification, and photosynthetic pathways may also assist in maintaining the distinct callus and contrasting lamina color from the earliest bud stage through to the mature flower. Our findings highlight that flower color in this sexually deceptive orchid is achieved by complex tissue-specific coordinated regulation of genes and biochemical pathways across multiple developmental stages.
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