Pseudocopulation Explained

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.

A non-mimetic form of pseudocopulation has been observed in some parthenogenetic, all-female species of lizard. The behaviour does not appear to be necessary to trigger parthenogenesis.

Definition

In zoology, pseudocopulation is attempted copulation that serves a reproductive function for one or both participants but does not involve actual sexual union between the individuals. In the case where an insect pollinator attempts to copulate with a flower, the process involves mimicry of an insect by the plant concerned. 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, a mimic, a model, and a dupe. 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]

History

In 1916, Pouyanne, with Henry Correvon, described his observations in Algeria:[3] [4]

In orchids

Several orchids (Orchidaceae) make use of floral mimicry. Using sex-based deception, these species imitate female mating signals of certain pollinator species.[5] 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.[6]

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.[7]

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.[8]

One mechanism is through the use of 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. Floral mimicry, which has independently evolved in a diverse range of plant species, involves the imitation of other plants or animals, including of coloration, morphology, egg deposition sites, provoking scents, and mating signals.[9] 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 odors have been identified as the most prominent way of attracting pollinators, because these odors imitate the sex pheromones of females of the pollinator species.[5] Male pollinators then track these scents over long distances.[10] The proportions of such odor 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 involve natural selection favoring local adaptation, leading to a more precise imitation of the scents produced by local pollinators.[5]

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.[9] 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]

In lizards

Some lizard species, such as the Laredo striped whiptail (Aspidoscelis [Cnemidophorus] laredoensis) and the Desert grassland whiptail lizard (A. uniparens), consist only of females, which reproduce by parthenogenesis. Some of these species have been observed to practise pseudocopulation in captivity, but it does not appear to be required to trigger parthenogenesis.[14] [15]

Notes and References

  1. Pasteur . Georges . A Classificatory Review of Mimicry Systems . 1982 . . 13 . 169–199 . 10.1146/annurev.es.13.110182.001125 . 2097066.
  2. Web site: Orchids Today and Yesterday . South Coast Orchid Society . 5 August 2024 . April 2021.
  3. Correvon . Henry . Pouyanne . Maurice-Alexandre . Un curieux cas de mimétisme chez les orchidées . fr . Journal de la Société Nationale d'Horticulture de France . 4 . 1916 . 29–47 .
  4. Correvon . Henry . Pouyanne . Maurice-Alexandre . Nouvelles observations sur le mimétisme et la fécondation chez les Ophrys speculum et lutea . fr . Journal de la Société Nationale d'Horticulture de France . 4 . 1923 . 372–377 .
  5. Vereecken . Nicolas J. . Schiestl . Florian P. . The evolution of imperfect floral mimicry . . 105 . 21 . 27 May 2008 . 18508972 . 2396721 . 10.1073/pnas.0800194105 . 7484–7488 . 2008PNAS..105.7484V . free .
  6. Schlüter . Philipp M. . Schiestl . Florian P. . Molecular mechanisms of floral mimicry in orchids . . 13 . 5 . 2008 . 10.1016/j.tplants.2008.02.008 . 228–235 . 18424223 . 2008TPS....13..228S .
  7. Pramanik . Dewi . Dorst . Nemi . Meesters . Niels . Spaans . Marlies . Smets . Erik . Welten . Monique . Gravendeel . Barbara . 3 . Evolution and development of three highly specialized floral structures of bee-pollinated Phalaenopsis species . EvoDevo . 11 . 1 . 2020 . 16 . 32793330 . 7418404 . 10.1186/s13227-020-00160-z . free .
  8. Gaskett . A. C. . Winnick . C. G. . Herberstein . M. E. . Orchid Sexual Deceit Provokes Ejaculation . 2008 . . 171 . E206-12 . 18433329 . 6 . 16443767 . 10.1086/587532.
  9. Schiestl . Florian P. . Cozzolino . Salvatore . Evolution of sexual mimicry in the orchid subtribe orchidinae: the role of preadaptations in the attraction of male bees as pollinators . . 8 . 1 . 2008 . 18226206 . 2267782 . 10.1186/1471-2148-8-27 . 27 . 2008BMCEE...8...27S . free .
  10. Ellis . Allan G. . Johnson . Steven D. . Floral Mimicry Enhances Pollen Export: The Evolution of Pollination by Sexual Deceit Outside of the Orchidaceae . . 176 . 5 . 2010 . 10.1086/656487 . E143–E151 . 20843263 . 45076899 .
  11. Goodrich . Katherine R. . Jürgens . Andreas . Pollination systems involving floral mimicry of fruit: aspects of their ecology and evolution . . 217 . 1 . 2018 . 10.1111/nph.14821 . 74–81 . 28980704 . free .
  12. Book: Leendert . van der Pijl . Calaway H. . Dodson . Orchid Flowers: Their Pollination and Evolution . Chapter 11: Mimicry and Deception . University of Miami Press . 1966 . 129–141 . 0-87024-069-2 . 310489511 . https://archive.org/details/orchidflowersthe0000pijl_y8t7/page/129 .
  13. Edwards . David P. . Yu . Douglas W. . The roles of sensory traps in the origin, maintenance, and breakdown of mutualism . Behavioral Ecology and Sociobiology . 61 . 9 . 2007 . 10.1007/s00265-007-0369-3 . 1321–1327 . 2007BEcoS..61.1321E . 43863247 .
  14. Paulissen . Mark A. . Walker . James M. . Pseudocopulation in the Parthenogenetic Whiptail Lizard Cnemidophorus laredoensis (Teiidae) . The Southwestern Naturalist . 34 . 2 . 1989 . 10.2307/3671747 . 296. 3671747 .
  15. Dias . Brian George . Crews . David . Regulation of Pseudosexual Behavior in the Parthenogenetic Whiptail Lizard, Cnemidophorus uniparens . Endocrinology . 149 . 9 . 1 September 2008 . 18483155 . 2553382 . 10.1210/en.2008-0214 . 4622–4631.