Sexual attraction with pollination during feeding behaviour: implications for transitions between specialised strategies.

Orchidaceae evolution nectar pollination sexual deception

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
14 Nov 2023
Historique:
received: 27 08 2023
medline: 14 11 2023
pubmed: 14 11 2023
entrez: 14 11 2023
Statut: aheadofprint

Résumé

Understanding the origin of pollination by sexual deception has proven challenging, as sexually deceptive flowers are often highly modified, making it hard to resolve how any intermediate forms between sexual deception and an ancestral strategy might have functioned. Here, we report the discovery in Caladenia (Orchidaceae) of sexual attraction with pollination during feeding behaviour, which may offer important clues for understanding shifts in pollination strategy. In Caladenia robinsonii, we observed the behaviour of its male wasp pollinator, Phymatothynnus aff. nitidus (Thynnidae), determined the site of release of the sexual attractant, and experimentally evaluated if the position of the attractant influences rates of attempted copulation and feeding behaviour. We applied GC-MS to test for surface sugar on the labellum. To establish if this pollination strategy is widespread in Caladenia, we conducted similar observations and experiments for four other Caladenia species. In C. robinsonii, long-range sexual attraction of the pollinator is via semiochemicals emitted from the glandular sepal tips. Of the wasps landing on the flower, 57 % attempted copulation with the sepal tips, while 27 % attempted to feed from the base of the labellum, the behaviour associated with pollen transfer. A similar proportion of wasps exhibited feeding behaviour when the site of odour release was manipulated. A comparable pollination strategy occurs in another phylogenetically distinct clade of Caladenia. We document a previously overlooked type of sexual deception for orchids involving long-distance sexual attraction, but with pollination occurring during feeding behaviour at the labellum. We show this type of sexual deception operates in other Caladenia species and predict that it is widespread across the genus. Our findings may offer clues about how an intermediate transitional strategy from a food rewarding or food deceptive ancestor operated during the evolution of sexual deception.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Understanding the origin of pollination by sexual deception has proven challenging, as sexually deceptive flowers are often highly modified, making it hard to resolve how any intermediate forms between sexual deception and an ancestral strategy might have functioned. Here, we report the discovery in Caladenia (Orchidaceae) of sexual attraction with pollination during feeding behaviour, which may offer important clues for understanding shifts in pollination strategy.
METHODS METHODS
In Caladenia robinsonii, we observed the behaviour of its male wasp pollinator, Phymatothynnus aff. nitidus (Thynnidae), determined the site of release of the sexual attractant, and experimentally evaluated if the position of the attractant influences rates of attempted copulation and feeding behaviour. We applied GC-MS to test for surface sugar on the labellum. To establish if this pollination strategy is widespread in Caladenia, we conducted similar observations and experiments for four other Caladenia species.
KEY RESULTS RESULTS
In C. robinsonii, long-range sexual attraction of the pollinator is via semiochemicals emitted from the glandular sepal tips. Of the wasps landing on the flower, 57 % attempted copulation with the sepal tips, while 27 % attempted to feed from the base of the labellum, the behaviour associated with pollen transfer. A similar proportion of wasps exhibited feeding behaviour when the site of odour release was manipulated. A comparable pollination strategy occurs in another phylogenetically distinct clade of Caladenia.
CONCLUSIONS CONCLUSIONS
We document a previously overlooked type of sexual deception for orchids involving long-distance sexual attraction, but with pollination occurring during feeding behaviour at the labellum. We show this type of sexual deception operates in other Caladenia species and predict that it is widespread across the genus. Our findings may offer clues about how an intermediate transitional strategy from a food rewarding or food deceptive ancestor operated during the evolution of sexual deception.

Identifiants

pubmed: 37963103
pii: 7420303
doi: 10.1093/aob/mcad178
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company.

Auteurs

Ryan D Phillips (RD)

Department of Environment and Genetics and the Research Centre for Future Landscapes, La Trobe University, Melbourne, Victoria 3086, Australia.
Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
Royal Botanic Gardens Victoria, Science Division, Corner of Ballarto Road and Botanic Drive, Cranbourne, VIC 3977, Australia.
Kings Park and Botanic Garden, The Botanic Garden and Parks Authority, West Perth, WA 6005, Australia.

Björn Bohman (B)

Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
Department of Plant Protection Biology, the Swedish University of Agricultural Sciences, Lomma 23422, Sweden.
School of Molecular Sciences, The University of Western Australia Crawley, WA 6009 Australia; Research School of Chemistry, Australian National University Acton, ACT 2601, Australia.

Rod Peakall (R)

Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.

Noushka Reiter (N)

Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
Royal Botanic Gardens Victoria, Science Division, Corner of Ballarto Road and Botanic Drive, Cranbourne, VIC 3977, Australia.

Classifications MeSH