Sexual deception of a beetle pollinator through floral mimicry

Cohen, Callan; Liltved, William; Colville, Jonathan F.; Shuttleworth, Adam; Weißflog, Jerrit; Svatoš, Aleš; Bytebier, Benny; Johnson, Steven D.

doi:10.1016/j.cub.2021.03.037

Cited by 31 publications

(33 citation statements)

References 56 publications

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“…In Australia, several orchid genera have some sexually deceptive species which exhibit this tissue-specific contrast (e.g., within Caladenia , Calochilus ), and in some genera, this is exclusively the case (e.g., Drakaea , Cryptostylis , Paracaleana , Leporella , Caleana ) ( Gaskett, 2011 ). Other examples of tissue-specific dark colors in sexually deceptive species outside Australia are the dark labella of many Ophrys species ( Bradshaw et al, 2010 ) such as Ophrys speculum ( Figure 1F ), the maroon-black callus structure on the pink labellum of Serapias lingua ( Vereecken et al, 2012 ; Pellegrino et al, 2017 ), the large elongated dark maroon labellum of Asian beetle-pollinated Luisia teres ( Arakaki et al, 2016 ), the triangular-shaped dark maroon pigmentation on the labellum of bee-pollinated Mormolyca ringens ( Singer et al, 2004 ), the central dark maroon labellum and column on an otherwise bright yellow corolla of Telipogon peruvianus ( Martel et al, 2016 , 2019 ), a combination of dark maroon-colored floral structures including antennae-like petals, anther, and labellum of south African beetle-pollinated Disa forficaria orchids ( Cohen et al, 2021 ), and the raised black spots on the yellow to bright orange ray florets of some fly pollinated Gorteria diffusa ( Ellis and Johnson, 2010 ) morphotypes ( Figure 1G ). In these cases, the dark pigmentation likely serves several key purposes important for pollination, including mimicking the color of female insects, providing strong chromatic and achromatic contrast, and aiding the exploitation of pollinator sensory biases.…”

Section: Discussionmentioning

confidence: 99%

“…Within the orchids, pollination by sexual deception has evolved independently on four continents and is employed by hundreds of species spanning multiple lineages of the Orchidaceae ( Peakall et al, 2020 ). The types of pollinators involved are also diverse, and include ants, bees and wasps (Hymenoptera), fungus gnats and other flies (Diptera), and beetles (Coleoptera) ( Gaskett, 2011 ; Bohman et al, 2016 ; Peakall et al, 2020 ; Cohen et al, 2021 ; Hayashi et al, 2021 ). In these cases, pollination is achieved during attempted copulation with the labellum, an often highly modified petal of the orchids.…”

Section: Introductionmentioning

confidence: 99%

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Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

2022

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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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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

2022

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“…One of the most specialised pollination strategies is that of sexual deception [1,2], in which pollination typically occurs via sexual attraction of male insects to a flower through chemical mimicry of female sex pheromones [3][4][5][6][7]. While sexual deception has been reported in the Asteraceae [8] and Iridaceae [9], it is most prevalent among the Orchidaceae [10,11]. Due to the high specificity of insect sex pheromones, sexually deceptive orchids frequently have only a single pollinator species, with closely related orchids typically exploiting different pollinator species [12][13][14][15][16].…”

Section: Introductionmentioning

confidence: 99%

Three Chemically Distinct Floral Ecotypes in Drakaea livida, an Orchid Pollinated by Sexual Deception of Thynnine Wasps

Weinstein

Bohman

Flematti

et al. 2022

Plants

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Sexually deceptive orchids are unusual among plants in that closely related species typically attract different pollinator species using contrasting blends of floral volatiles. Therefore, intraspecific variation in pollinator attraction may also be underpinned by differences in floral volatiles. Here, we tested for the presence of floral ecotypes in the sexually deceptive orchid Drakaea livida and investigated if the geographic range of floral ecotypes corresponded to variation in pollinator availability. Pollinator choice trials revealed the presence of three floral ecotypes within D. livida that each attracts a different species of thynnine wasp as a pollinator. Surveys of pollinator distribution revealed that the distribution of one of the ecotypes was strongly correlated with that of its pollinator, while another pollinator species was present throughout the range of all three ecotypes, demonstrating that pollinator availability does not always correlate with ecotype distribution. Floral ecotypes differed in chemical volatile composition, with a high degree of separation evident in principal coordinate analysis. Some compounds that differed between ecotypes, including pyrazines and (methylthio)phenols, are known to be electrophysiologically active in thynnine wasp antennae. Based on differences in pollinator response and floral volatile profile, the ecotypes represent distinct entities and should be treated as such in conservation management.

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“…Once males and females have located each other, individual mating preferences or competition for access to mates may lead to suboptimal decisions during courtship and mating (Trivers, 1972;Andersson, 1994). The willingness to mate is for example exploited by certain insect pollinated flowers (Schiestl et al, 2000;Cohen et al, 2021;Hayashi et al, 2021), which use sexual mimicry to attract pollinators by resembling the opposite sex visually and/or chemically. Exploitation of mate recognition systems can be highly advantageous for obligate pathogens as it increases the chance of pathogen transmission by ensuring contact with new potential hosts of the right species (Hansen and De Fine Licht, 2019).…”

Section: Mainmentioning

confidence: 99%

A pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

Naundrup

Bohman

Kwadha

et al. 2021

Preprint

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To ensure dispersal, many parasites and pathogens behaviourally manipulate infected hosts. Other pathogens and certain insect-pollinated flowers use sexual mimicry and release deceptive mating signals. However, it is unusual for pathogens to rely on both behavioural host manipulation and sexual mimicry. Here, we show that the host-specific and behaviourally manipulating pathogenic fungus, Entomophthora muscae, generates a chemical blend of volatile sesquiterpenes and alters the level of natural host cuticular hydrocarbons in dead infected female house fly (Musca domestica) cadavers. Healthy male house flies respond to the fungal compounds and are enticed into mating with dead female cadavers. This is advantageous for the fungus as close proximity between host individuals leads to an increased probability of infection. The fungus-emitted volatiles thus represent the evolution of an extended phenotypic trait that exploit male flies' willingness to mate and benefit the fungus by altering the behavioural phenotype of uninfected healthy male host flies.

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Sexual deception of a beetle pollinator through floral mimicry

Cited by 31 publications

References 56 publications

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

Anthocyanin and Flavonol Glycoside Metabolic Pathways Underpin Floral Color Mimicry and Contrast in a Sexually Deceptive Orchid

Three Chemically Distinct Floral Ecotypes in Drakaea livida, an Orchid Pollinated by Sexual Deception of Thynnine Wasps

A pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

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