Looks matter: changes in flower form affect pollination effectiveness in a sexually deceptive orchid

Rákosy, Demetra; Cuervo, Monica; Paulus, Hannes F.; Ayasse, Manfred

doi:10.1111/jeb.13153

Cited by 23 publications

(27 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The shape and the colour of the flower then induce the male pollinator to land on the flower (e.g. Rakosy et al ., 2012, 2017; Paulus, 2018). The shape (Rakosy et al ., 2017) and the hairiness (Ågren, Kullenberg, & Sensenbaugh, 1984) of the flower orient the body of the male parallel to the longest length of the labellum on the flower.…”

Section: The Bee Orchids and Their Pollinatorsmentioning

confidence: 99%

Why are there so many bee‐orchid species? Adaptive radiation by intra‐specific competition for mnesic pollinators

et al. 2020

View full text Add to dashboard Cite

Adaptive radiations occur mostly in response to environmental variation through the evolution of key innovations that allow emerging species to occupy new ecological niches. Such biological innovations may play a major role in niche divergence when emerging species are engaged in reciprocal ecological interactions. To demonstrate coevolution is a difficult task; only a few studies have confirmed coevolution as driver of speciation and diversification. Herein we review current knowledge about bee orchid (Ophrys spp.) reproductive biology. We propose that the adaptive radiation of the Mediterranean orchid genus Ophrys, comprising several hundred species, is due to coevolutionary dynamics between these plants and their pollinators. We suggest that pollination by sexual swindling used by Ophrys orchids is the main driver of this coevolution. Flowers of each Ophrys species mimic a sexually receptive female of one particular insect species, mainly bees. Male bees are first attracted by pseudo‐pheromones emitted by Ophrys flowers that are similar to the sexual pheromones of their females. Males then are lured by the flower shape, colour and hairiness, and attempt to copulate with the flower, which glues pollen onto their bodies. Pollen is later transferred to the stigma of another flower of the same Ophrys species during similar copulation attempts. In contrast to rewarding pollination strategies, Ophrys pollinators appear to be parasitized. Here we propose that this apparent parasitism is in fact a coevolutionary relationship between Ophrys and their pollinators. For plants, pollination by sexual swindling could ensure pollination efficiency and specificity, and gene flow among populations. For pollinators, pollination by sexual swindling could allow habitat matching and inbreeding avoidance. Pollinators might use the pseudo‐pheromones emitted by Ophrys to locate suitable habitats from a distance within complex landscapes. In small populations, male pollinators would disperse once they have memorized the local diversity of sexual pseudo‐pheromone bouquets or if all Ophrys flowers are fertilized and thus repel pollinators via production of repulsive pheromones that mimic those produced by fertilized female bees. We propose the following evolutionary scenario: Ophrys radiation is driven by strong intra‐specific competition among Ophrys individuals for the attraction of species‐specific pollinators, which is a consequence of the high cognitive abilities of pollinators. Male bees record the pheromone signatures of kin or of previously courted partners to avoid further copulation attempts, thereby inducing strong selection on Ophrys for variation in odour bouquets emitted by individual flowers. The resulting odour bouquets could by chance correspond to pseudo‐pheromones of the females of another bee species, and thus attract a new pollinator. If such pollinator shifts occur simultaneously in several indivuals, pollen exchanges might occur and initiate speciation. To reinforce the attraction of the new pollinator an...

show abstract

Section: The Bee Orchids and Their Pollinatorsmentioning

confidence: 99%

Why are there so many bee‐orchid species? Adaptive radiation by intra‐specific competition for mnesic pollinators

et al. 2020

View full text Add to dashboard Cite

show abstract

“…An important area of future research will be to understand which axes of floral variation experience stronger selection and therefore impose a greater constraint on transitions in pollination strategy to and from sexual deception (e.g. Ellis et al ., ; Rakosy et al ., ). For example, Rakosy et al .…”

Section: Discussionmentioning

confidence: 97%

“…The increase in attempted copulation may reflect more compelling mimicry, as the olfactory and visual cues now coincide, or wasps being more easily able to firmly grasp the fake female rather than struggling to grasp the relatively fine sepal tips. These results suggest that in many sexually deceptive systems, where strong sexual attraction to the labellum may increase the likelihood of pollination (Rakosy et al ., ; de Jager & Peakall, ), producing the odour from the labellum is likely to be the most effective strategy.…”

Section: Discussionmentioning

confidence: 99%

“…For example, Rakosy et al . () showed that in Ophrys, parts of the labellum used as gripping points affect the duration of copulation and thus may be under stronger selection for shape than other parts of the labellum. Similarly, de Jager & Peakall () show strong evidence for stabilizing selection on the distance from the callus to the labellum tip of Chiloglottis trapeziformis , but not other morphological traits of the labellum.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

An experimental evaluation of traits that influence the sexual behaviour of pollinators in sexually deceptive orchids

Phillips

Peakall

2018

J of Evolutionary Biology

View full text Add to dashboard Cite

Pollination by sexual deception of male insects is perhaps one of the most remarkable cases of mimicry in the plant kingdom. However, understanding the influence of floral traits on pollinator behaviour in sexually deceptive plants is challenging, due to the risk of confounding changes in floral odour when manipulating morphology. Here, we investigated the floral traits influencing the sexual response of male Zaspilothynnus nigripes (Tiphiidae) wasps, a pollinator of two distantly related sexually deceptive orchids with contrasting floral architecture, Caladenia pectinata and Drakaea livida. In D. livida, the chemical sexual attractant is emitted from the labellum, whereas in C. pectinata, it is produced from the distal sepal tips, allowing manipulative experiments. When controlling for visual cues, there was no difference in long-distance attraction, although the floral odour of D. livida induced copulation more frequently than that of C. pectinata. The role of colour in pollinator sexual attraction was equivocal, indicating that colour may not be a strong constraint on the initial evolution of sexual deception. The frequency of wasp visitors landing on C. pectinata decreased when the amount of floral odour was reduced, but attempted copulation rates were enhanced when the source of floral odour was associated with the labellum. These latter variables may represent axes of selection that operate across many sexually deceptive species. Nonetheless, the observed variation in floral traits suggests flexibility among species in how sexual deception can be achieved.

show abstract

“…However, in both deceptive strategies, it has also been reported that this variation may also be retained through genetic mechanisms in combination with other selective agents (Rakosy et al . ; Xu et al . ).…”

Section: Discussionmentioning

confidence: 99%

Does size really matter? A comparative study on floral traits in orchids with two different pollination strategies

et al. 2019

View full text Add to dashboard Cite

The lock and key hypothesis assumes that male and female genitalia match in a unique system to prevent interspecific crosses. This hypothesis is largely investigated in animals, while there is a distinct lack of studies on plants. Nevertheless, we expect the lock and key hypothesis could apply to plants with complex floral morphologies, such as orchids.• Here we apply a comparative approach to examine the variation of floral functional traits in food-and sex-deceptive orchids. To understand if a specific deception strategy is related to a specific variation in floral traits evaluated the variation in sterile and fertile traits among species and subsequently examined the correlations between male and female reproductive organs of the same species with the aim of investigating the role of the lock and key hypothesis in deceptive orchids.• Our results show that the functional morphology of fertile traits plays a pivotal role in limiting gene flow in species that grow in sympatry. In particular, it was observed that the Reproductive Standardisation Index (RSI) is significantly different in the two pollination strategies and that the correlation between pollinarium length and stigmatic cavity length is stronger in food-deceptive species when compared to the sex-deceptive species.• These results reveal that the lock and key hypothesis contributes to maintain boundaries in plants with very complex floral morphology.Plant Biology 21 (2019) 961-966

show abstract

Looks matter: changes in flower form affect pollination effectiveness in a sexually deceptive orchid

Cited by 23 publications

References 38 publications

Why are there so many bee‐orchid species? Adaptive radiation by intra‐specific competition for mnesic pollinators

Why are there so many bee‐orchid species? Adaptive radiation by intra‐specific competition for mnesic pollinators

An experimental evaluation of traits that influence the sexual behaviour of pollinators in sexually deceptive orchids

Does size really matter? A comparative study on floral traits in orchids with two different pollination strategies

Contact Info

Product

Resources

About