Pouyannian mimicry

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Pouyannian mimicry
Dasyscolia ciliata.jpg
Dupe: Dasyscolia ciliata , a scoliid wasp, attempting to copulate with a flower of the orchid Ophrys speculum
Ophrys speculum d (cropped).JPG
Mimic: Ophrys speculum , the mirror bee orchid

Pouyannian mimicry is a form of mimicry in plants that deceives an insect into attempting to copulate with a flower. The flower mimics a potential female mate of a male insect, which then serves the plant as a pollinator. The mechanism is named after the French lawyer and amateur botanist Maurice-Alexandre Pouyanne. The resemblance that he noted is visual, but the key stimuli that deceive the pollinator are often chemical and tactile.

Contents

In orchids, the resemblance is to a species of bee; Pouyanne observed the bee Dasyscolia ciliata pollinating the orchid Ophrys speculum . The flower uses morphology, coloration, and scent to deceive the pollinator. The chemicals secreted from the flower's osmophore glands are indistinguishable from the insect's pheromones. The pollinator is not rewarded with nectar, and may waste significant amounts of sperm while trying to mate with the flower.

Definition

The form of mimicry in plants that deceives an insect into pseudocopulation is called Pouyannian mimicry after the French lawyer and amateur botanist Maurice-Alexandre Pouyanne. [1] [2]

Mimicry typically involves three species, namely a mimic, a model, and a dupe, as seen for example in Batesian mimicry. [1] Floral mimicry involves the imitation of other plants or animals, including of coloration, morphology, egg deposition sites, provoking scents, and mating signals. [3] In the case of Pouyannian mimicry, the model and the dupe are the female and male of the same species, so the mimicry is bipolar, involving only two species, an insect and a flower. [1]

Pouyannian mimicry with pseudocopulation, compared to Batesian mimicry. Pouyannian mimicry is bipolar, with only 2 species involved, as the dupe and the model are of the same species, such as a pollinating bee. Pouyannian mimicry and pseudocopulation.svg
Pouyannian mimicry with pseudocopulation, compared to Batesian mimicry. Pouyannian mimicry is bipolar, with only 2 species involved, as the dupe and the model are of the same species, such as a pollinating bee.

History

In 1916, Pouyanne, with Henry Correvon, described his observations in Algeria: [4] [5]

Pouyanne 1916 [4] Translation
Asseyez-vous, en effet, au soleil, un petit bouquet d' Ophrys speculum à la main, sur un talus au-dessus duquel les mâles de Dasyscolia ciliata exécutent leurs évolutions. Vous ne tardez pas à vous apercevoir qu’ils ont flairé, en quelque sorte, qu’ils ont repéré les fleurs que vous tenez ... Il se pose alors sur le labelle, de manière que sa tête arrive tout près du stigmate, juste sous les pollinies, et que son abdomen plonge, à l’extrémité, dans les poils longs, fauves et épais qui forment comme une couronne barbue au labelle. Le bout de l'abdomen est alors agité, contre ces poils, de mouvements désordonnés, presque convulsifs, et l'insecte tout entier se trémousse; ses mouvements, son attitude paraissent tout à fait semblables à ceux des insectes qui pratiquent des tentatives de copulation.Sit down in the sun, with a small bouquet of Ophrys speculum in your hand, on a slope above which the males of Dasyscolia ciliata are performing their movements. You soon realize that they have scented, in some way, that they have detected the flowers you are holding [...] It then lands on the flower's labellum, so that its head is very close to the stigma, just under the pollinia, and its abdomen plunges, at the end, into the long, tawny and thick hairs which form a kind of bearded crown on the labellum. The tip of the abdomen is then agitated, against these hairs, with disordered, almost convulsive movements, and the entire insect wriggles; its movements, its attitude are like those of insects practising attempts at copulation.

In orchids

Several orchids (Orchidaceae) make use of floral mimicry. Using sex-based deception, these species imitate female mating signals of certain pollinator species. [6] This results in attempted copulation by males of the pollinator species, facilitating pollen transfer. Bee orchids ( Ophrys apifera ) and fly orchids ( Ophrys insectifera ), specifically, utilize flower morphology, coloration, and scent to deceive their respective pollinators. These orchids have evolved traits matching the preferences of specific pollinator niches, leading to adaptive speciation. [7]

The mimicry involves secreting chemicals from glands (osmophores) in the sepals, petals, or labellum, that are indistinguishable from the insect's natural pheromones. The flower attaches a pollinium to the pollinator's body; the insect transfers the pollinium to the stigma of another flower when it makes its next copulation attempt. Pollinators are often bees, wasps, or flies. [8]

The cost to the pollinating insects might be seen as negligible, but pollinators of the Australian orchid Cryptostylis can waste significant amounts of sperm by ejaculating onto the flower. Thus there could be antagonistic coevolution such that pollinators become better at identifying their own species correctly, while orchids become better mimics. [9]

One mechanism in pollination is to use incentives or rewards. These are beneficial offerings to a pollinator, enticing it to engage with the reward and thus transfer pollen. Flowering plants that do not produce such rewards can instead attract pollinators through mimicry — a form of convergent evolution. [3] Such plants are called "deceptive plants" as they mimic the characteristics or rewards of other species without providing any benefit to the pollinator. [10] [11]

Although bee and fly orchids are visual mimics of their pollinators, visual traits are not the only (nor the most important) ones mimicked to increase attraction. [12] [10] Floral odours have been identified as the most prominent way of attracting pollinators, because these odours imitate the sex pheromones of females of the pollinator species. [6] Male pollinators then track these scents over long distances. [10] The proportions of such odour compounds have been found to be varied in different populations of orchids (in a variety of locations), playing a crucial role in attracting specific pollinators at the population level. The evolution of these interactions between plants and pollinators involves natural selection favoring local adaptation, leading to a more precise imitation of the scents produced by local pollinators. [6]

Chemical compounds (more specifically, alkanes and alkenes), while used for sexual deception, are produced in many species of Ophrys, and likely were preadapted for other functions before being co-opted for mimicry. [3] These orchids increased ancestral levels of alkene production to mimic the female pheromones that attract male pollinators, a form of sensory exploitation called a sensory trap. [13]

Although mimetic plants typically receive fewer interactions with pollinators than truly-rewarding plants do, the evolution of sexual deception appears to be linked to benefits associated with mating behavior. Sex-based mimicry results in pollinator fidelity, the continued revisiting of flowers of the same species by a pollinator, as a result of sexual deception. In support of this, sex-based deception in an Australian orchid results in a higher proportion of pollen reaching stigmas than food-based deception. In another study, deception of male pollinators results in a long-distance dispersal of pollen. [10]

Related Research Articles

<i>Ophrys apifera</i> Species of flowering plant in the orchid family Orchidaceae

Ophrys apifera, known in Europe as the bee orchid, is a perennial herbaceous plant of the genus Ophrys, in the family of Orchidaceae. It serves as an example of sexually deceptive pollination and floral mimicry, a highly selective and highly evolved plant–pollinator relationship.

<span class="mw-page-title-main">Pollinator</span> Animal that moves pollen from the male anther of a flower to the female stigma

A pollinator is an animal that moves pollen from the male anther of a flower to the female stigma of a flower. This helps to bring about fertilization of the ovules in the flower by the male gametes from the pollen grains.

<i>Ophrys</i> Genus of orchids

The genus Ophrys is a large group of orchids from the alliance Orchis in the subtribe Orchidinae. They are widespread across much of Europe, North Africa, Caucasus, the Canary Islands, and the Middle East as far east as Turkmenistan.

<span class="mw-page-title-main">Mimicry</span> Evolutionary strategy

In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. In the simplest case, as in Batesian mimicry, a mimic resembles a model, so as to deceive a dupe, all three being of different species. A Batesian mimic, such as a hoverfly, is harmless, while its model, such as a wasp, is harmful, and is avoided by the dupe, such as an insect-eating bird. Birds hunt by sight, so the mimicry in that case is visual, but in other cases mimicry may make use of any of the senses. Most types of mimicry, including Batesian, are deceptive, as the mimics are not harmful, but Müllerian mimicry, where different harmful species resemble each other, is honest, as when species of wasps and of bees all have genuinely aposematic warning coloration. More complex types may be bipolar, involving only two species, such as when the model and the dupe are the same; this occurs for example in aggressive mimicry, where a predator in wolf-in-sheep's-clothing style resembles its prey, allowing it to hunt undetected. Mimicry is not limited to animals; in Pouyannian mimicry, an orchid flower is the mimic, resembling a female bee, its model; the dupe is the male bee of the same species, which tries to copulate with the flower, enabling it to transfer pollen, so the mimicry is again bipolar. In automimicry, another bipolar system, model and mimic are the same, as when blue lycaenid butterflies have 'tails' or eyespots on their wings that mimic their own heads, misdirecting predator dupes to strike harmlessly. Many other types of mimicry exist.

<span class="mw-page-title-main">Pseudocopulation</span> Biological process

Pseudocopulation is a behavior similar to copulation that serves a reproductive function for one or both participants but does not involve actual sexual union between the individuals. It is most generally applied to a pollinator attempting to copulate with a flower adapted to mimic a potential female mate. The resemblance may be visual, but the key stimuli are often chemical and tactile. The form of mimicry in plants that deceives an insect into pseudocopulation is called Pouyannian mimicry after the French lawyer and amateur botanist Maurice-Alexandre Pouyanne.

<span class="mw-page-title-main">Entomophily</span> Form of pollination by insects

Entomophily or insect pollination is a form of pollination whereby pollen of plants, especially but not only of flowering plants, is distributed by insects. Flowers pollinated by insects typically advertise themselves with bright colours, sometimes with conspicuous patterns leading to rewards of pollen and nectar; they may also have an attractive scent which in some cases mimics insect pheromones. Insect pollinators such as bees have adaptations for their role, such as lapping or sucking mouthparts to take in nectar, and in some species also pollen baskets on their hind legs. This required the coevolution of insects and flowering plants in the development of pollination behaviour by the insects and pollination mechanisms by the flowers, benefiting both groups. Both the size and the density of a population are known to affect pollination and subsequent reproductive performance.

<span class="mw-page-title-main">Euglossini</span> Tribe of bees

The tribe Euglossini, in the subfamily Apinae, commonly known as orchid bees or euglossine bees, are the only group of corbiculate bees whose non-parasitic members do not all possess eusocial behavior.

<i>Ophrys insectifera</i> Species of flowering plant in the orchid family Orchidaceae

Ophrys insectifera, the fly orchid, is a species of orchid and the type species of the genus Ophrys. It is remarkable as an example of the use of sexually deceptive pollination and floral mimicry, as well as a highly selective and highly evolved plant–pollinator relationship.

<i>Drakaea</i> Genus of orchids

Drakaea is a genus of 10 species in the plant family Orchidaceae commonly known as hammer orchids. All ten species occur only in the south-west of Western Australia. Hammer orchids are characterised by an insectoid labellum that is attached to a narrow, hinged stem, which holds it aloft. The stem can hinge only backwards, where the broadly winged column carries the pollen and stigma. Each species of hammer orchid is pollinated by a specific species of thynnid wasp. Thynnid wasps are unusual in that the female is flightless and mating occurs when the male carries a female away to a source of food. The labellum of the orchid resembles a female thynnid wasp in shape, colour and scent. Insect pollination involving sexual attraction is common in orchids but the interaction between the male thynnid wasp and the hammer orchid is unique in that it involves the insect trying to fly away with a part of the flower.

Sexual mimicry occurs when one sex mimics the opposite sex in its behavior, appearance, or chemical signalling.

<i>Hymenopus coronatus</i> Species of praying mantis

Hymenopus coronatus is a mantis from the tropical forests of Southeast Asia. It is known by various common names, including walking flower mantis, orchid-blossom mantis and (pink) orchid mantis. It is one of several species known as flower mantis, a reference to their unique physical form and behaviour, which often involves moving with a “swaying” motion, as if being “blown” in the breeze. Several species have evolved to mimic orchid flowers as a hunting and camouflaging strategy, “hiding” themselves in plain view and preying upon pollinating insects that visit the blooms. They are known to grab their prey with blinding speed.

<span class="mw-page-title-main">Chemical mimicry</span> Biological mimicry using chemicals

Chemical mimicry is a type of biological mimicry involving the use of chemicals to dupe an operator.

<span class="mw-page-title-main">Mimicry in plants</span>

In evolutionary biology, mimicry in plants is where a plant evolves to resemble another organism physically or chemically. Mimicry in plants has been studied far less than mimicry in animals. It may provide protection against herbivory, or may deceptively encourage mutualists, like pollinators, to provide a service without offering a reward in return.

<span class="mw-page-title-main">Pollination trap</span> Plant flower structures

Pollination traps or trap-flowers are plant flower structures that aid the trapping of insects, mainly flies, so as to enhance their effectiveness in pollination. The structures of pollination traps can include deep tubular corollas with downward pointing hairs, slippery surfaces, adhesive liquid, attractants, flower closing and other mechanisms.

<i>Ophrys speculum</i> Species of orchid

Ophrys speculum, the mirror orchid, is a species of Ophrys distributed throughout the Mediterranean that is pollinated exclusively by a single species of scoliid wasp.

<span class="mw-page-title-main">Advertising in biology</span> Use of displays by organisms to signal for selective advantage

Advertising in biology means the use of displays by organisms such as animals and plants to signal their presence for some evolutionary reason.

<i>Argogorytes mystaceus</i> Species of wasp

Argogorytes mystaceus is a species of solitary wasp in the family Crabronidae.

Floral biology is an area of ecological research that studies the evolutionary factors that have moulded the structures, behaviours and physiological aspects involved in the flowering of plants. The field is broad and interdisciplinary and involves research requiring expertise from multiple disciplines that can include botany, ethology, biochemistry, and entomology. A slightly narrower area of research within floral biology is sometimes called pollination biology or anthecology.

<span class="mw-page-title-main">Floral isolation</span>

Floral Isolation is a form of reproductive isolation found in angiosperms. Reproductive isolation is the process of species evolving mechanisms to prevent reproduction with other species. In plants, this is accomplished through the manipulation of the pollinator’s behavior or through morphological characteristics of flowers that favor intraspecific pollen transfer. Preventing interbreeding prevents hybridization and gene flow between the species (introgression), and consequently protects genetic integrity of the species. Reproductive isolation occurs in many organisms, and floral isolation is one form present in plants. Floral isolation occurs prior to pollination, and is divided into two types of isolation: morphological isolation and ethological isolation. Floral isolation was championed by Verne Grant in the 1900s as an important mechanism of reproductive isolation in plants.

<span class="mw-page-title-main">Pollination of orchids</span>

The pollination of orchids is a complex chapter in the biology of this family of plants that are distinguished by the complexity of their flowers and by intricate ecological interactions with their pollinator agents. It has captured the attention of numerous scientists over time, including Charles Darwin, father of the theory of evolution by natural selection. Darwin published in 1862 the first observations of the fundamental role of insects in orchid pollination, in his book The Fertilization of Orchids. Darwin stated that the varied stratagems orchids use to attract their pollinators transcend the imagination of any human being.

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