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Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: How does flower-specific variation of odor signals influence reproductive success?

Ayasse, Manfred ; Schiestl, Florian P ; Paulus, H F ; Löfstedt, Christer LU ; Hansson, Bill S ; Ibarra, F and Francke, Wittko (2000) In Evolution 54(6). p.1995-2006
Abstract
The orchid Ophrys sphegodes Miller is pollinated by sexually excited males of the solitary bee Andrena nigroaenea, which are lured to the flowers by visual cues and volatile semiochemicals. In O. sphegodes, visits by pollinators are rare. Because of this low frequency of pollination, one would expect the evolution of strategies that increase the chance that males will visit more than one flower on the same plant; this would increase the number of pollination events on a plant and therefore the number of seeds produced. Using gas chromatography-mass spectrometry (GC-MS) analyses, we identified more than 100 compounds in the odor bouquets of labellum extracts from O. sphegodes; 24 compounds were found to be biologically active in male... (More)
The orchid Ophrys sphegodes Miller is pollinated by sexually excited males of the solitary bee Andrena nigroaenea, which are lured to the flowers by visual cues and volatile semiochemicals. In O. sphegodes, visits by pollinators are rare. Because of this low frequency of pollination, one would expect the evolution of strategies that increase the chance that males will visit more than one flower on the same plant; this would increase the number of pollination events on a plant and therefore the number of seeds produced. Using gas chromatography-mass spectrometry (GC-MS) analyses, we identified more than 100 compounds in the odor bouquets of labellum extracts from O. sphegodes; 24 compounds were found to be biologically active in male olfactory receptors based on gas chromatography with electroantennographic detection (GC-EAD). Gas chromatography (GC) analyses of odors from individual flowers showed less intraspecific variation in the odor bouquets of the biologically active compounds as compared to nonactive compounds. This can be explained by a higher selective pressure on the pollinator-attracting communication signal. Furthermore, we found a characteristic variation in the GC-EAD active esters and aldehydes among flowers of different stem positions within an inflorescence and in the n-alkanes and n-alkenes among plants from different populations. In our behavioral field tests, we showed that male bees learn the odor bouquets of individual flowers during mating attempts and recognize them in later encounters. Bees thereby avoid trying to mate with flowers they have visited previously, but do not avoid other flowers either of a different or the same plant. By varying the relative proportions of saturated esters and aldehydes between flowers of different stem positions, we demonstrated that a plant may take advantage of the learning abilities of the pollinators and influence flower visitation behavior. Sixty-seven percent of the males that visited one flower in an inflorescence returned to visit a second flower of the same inflorescence. However, geitonogamy is prevented and the likelihood of cross-fertilization is enhanced by the time required for the pollinium deposited on the pollinator to complete its bending movement, which is necessary for pollination to occur. Cross-fertilization is furthermore enhanced by the high degree of odor variation between plants. This variation minimizes learned avoidance of the flowers and increases the likelihood that a given pollinator would visit several to many different plants within a population. (Less)
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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
chemical communication, learning behavior, Ophrys sphegodes, pollination by sexual deception, scent variation, reproductive success, Andrena nigroaenea
in
Evolution
volume
54
issue
6
pages
1995 - 2006
publisher
Wiley-Blackwell
ISSN
1558-5646
DOI
10.1554/0014-3820(2000)054[1995:EORSIT]2.0.CO;2
language
English
LU publication?
yes
id
22a50c6e-4528-48d9-b987-4cd727d0e6e6 (old id 146222)
alternative location
http://www.bioone.org/bioone/?request=get-document&issn=0014-3820&volume=054&issue=06&page=1995
date added to LUP
2016-04-01 15:27:00
date last changed
2021-01-06 06:22:46
@article{22a50c6e-4528-48d9-b987-4cd727d0e6e6,
  abstract     = {{The orchid Ophrys sphegodes Miller is pollinated by sexually excited males of the solitary bee Andrena nigroaenea, which are lured to the flowers by visual cues and volatile semiochemicals. In O. sphegodes, visits by pollinators are rare. Because of this low frequency of pollination, one would expect the evolution of strategies that increase the chance that males will visit more than one flower on the same plant; this would increase the number of pollination events on a plant and therefore the number of seeds produced. Using gas chromatography-mass spectrometry (GC-MS) analyses, we identified more than 100 compounds in the odor bouquets of labellum extracts from O. sphegodes; 24 compounds were found to be biologically active in male olfactory receptors based on gas chromatography with electroantennographic detection (GC-EAD). Gas chromatography (GC) analyses of odors from individual flowers showed less intraspecific variation in the odor bouquets of the biologically active compounds as compared to nonactive compounds. This can be explained by a higher selective pressure on the pollinator-attracting communication signal. Furthermore, we found a characteristic variation in the GC-EAD active esters and aldehydes among flowers of different stem positions within an inflorescence and in the n-alkanes and n-alkenes among plants from different populations. In our behavioral field tests, we showed that male bees learn the odor bouquets of individual flowers during mating attempts and recognize them in later encounters. Bees thereby avoid trying to mate with flowers they have visited previously, but do not avoid other flowers either of a different or the same plant. By varying the relative proportions of saturated esters and aldehydes between flowers of different stem positions, we demonstrated that a plant may take advantage of the learning abilities of the pollinators and influence flower visitation behavior. Sixty-seven percent of the males that visited one flower in an inflorescence returned to visit a second flower of the same inflorescence. However, geitonogamy is prevented and the likelihood of cross-fertilization is enhanced by the time required for the pollinium deposited on the pollinator to complete its bending movement, which is necessary for pollination to occur. Cross-fertilization is furthermore enhanced by the high degree of odor variation between plants. This variation minimizes learned avoidance of the flowers and increases the likelihood that a given pollinator would visit several to many different plants within a population.}},
  author       = {{Ayasse, Manfred and Schiestl, Florian P and Paulus, H F and Löfstedt, Christer and Hansson, Bill S and Ibarra, F and Francke, Wittko}},
  issn         = {{1558-5646}},
  keywords     = {{chemical communication; learning behavior; Ophrys sphegodes; pollination by sexual deception; scent variation; reproductive success; Andrena nigroaenea}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{1995--2006}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Evolution}},
  title        = {{Evolution of reproductive strategies in the sexually deceptive orchid <i>Ophrys sphegodes</i>: How does flower-specific variation of odor signals influence reproductive success?}},
  url          = {{http://dx.doi.org/10.1554/0014-3820(2000)054[1995:EORSIT]2.0.CO;2}},
  doi          = {{10.1554/0014-3820(2000)054[1995:EORSIT]2.0.CO;2}},
  volume       = {{54}},
  year         = {{2000}},
}