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Research Article

A Role for Parasites in Stabilising the Fig-Pollinator Mutualism

  • Derek W Dunn,

    Affiliations: Division of Biology, Imperial College London, Ascot, United Kingdom, School of Biological Sciences, University of Reading, Reading, United Kingdom, School of Biological Sciences, University of East Anglia, Norwich, United Kingdom

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  • Simon T Segar,

    Affiliations: Division of Biology, Imperial College London, Ascot, United Kingdom, School of Biological Sciences, University of Reading, Reading, United Kingdom

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  • Jo Ridley,

    Affiliation: School of Biological Sciences, University of East Anglia, Norwich, United Kingdom

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  • Ruth Chan,

    Affiliation: Division of Biology, Imperial College London, Ascot, United Kingdom

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  • Ross H Crozier,

    Affiliation: School of Marine and Tropical Biology, James Cook University, Townsville, Queensland, Australia

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  • Douglas W Yu,

    Affiliation: School of Biological Sciences, University of East Anglia, Norwich, United Kingdom

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  • James M Cook mail

    To whom correspondence should be addressed. E-mail: james.cook@reading.ac.uk

    Affiliations: Division of Biology, Imperial College London, Ascot, United Kingdom, School of Biological Sciences, University of Reading, Reading, United Kingdom, Natural Environment Research Council (NERC) Centre for Population Biology, Imperial College London, Ascot, United Kingdom

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  • Published: March 11, 2008
  • DOI: 10.1371/journal.pbio.0060059

Reader Comments (2)

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High diversity of biological traits and colonising strategies of non-pollinating fig wasps

Posted by plosbiology on 07 May 2009 at 22:23 GMT

Author: Rodrigo A. S. Pereira
Position: Professor
Institution: Depto of Biology/FFCLRP-USP
E-mail: raspereira@yahoo.com.br
Additional Authors: Simone de Pádua Teixeira (Depto of Pharmaceutical Sciences/FCFRP-USP); Martine Hossaert-McKey and Finn Kjellberg (CEFE/CNRS-Montpellier)
Submitted Date: March 20, 2008
Published Date: March 21, 2008
This comment was originally posted as a “Reader Response” on the publication date indicated above. All Reader Responses are now available as comments.

Dunn et al. doi:10.1371/journal.pbio.0060059 present welcome empirical data suggesting that parasitic fig wasps, by preferentially parasiting pollinator larvae located close to the fig wall, contribute to the mechanisms stabilising the fig-pollinator mutualism.
The hypothesis that inner ovaries constitute in higher-quality resources for fig wasps was previously proposed for F. microcarpa. Indeed Anstett [1] presented a neat and parsimonious hypothesis that pollinating foundresses were selected to oviposit in inner ovaries, close to the fig cavity as this facilitates offspring emergence and increases female chances of becoming mated. We have observed early and repeated mating of female pollinating wasps located close to the fig cavity and their easy emergence into the fig cavity in diverse fig wasp genera (Platyscapa, Pegoscapus, Alfonsiella, Elisabethiella, Courtella).
The mechanism presented in Dunn et al. is likely to be of importance in a number of species. Nevertheless, the abundance of parasitic fig wasps is variable among fig species (e.g. Ficus beddomei has no parasites [2]) and among fig crops and can be very low in natural environments (R.A.S.P, pers. obs. in Panama and Brazil). Therefore levels of parasitism that prevailed over evolutionary time and hence their importance in shaping pollinator oviposition behavior are rather difficult to evaluate.
However one of the most fascinating emerging aspects of fig-wasp biology is the surprising diversity or plasticity of oviposition strategies within genera and even within species. Previous analysis suggested that parasites of genus Idarnes gall ovules [3] and this is still widely accepted [4]. Indeed, species of Idarnes group flavicollis effectively gall ovules [5, 6]. However, Idarnes species of carme group colonise later and oviposit in pollinator galls [5, 6]. Further and totally unexpectedly, dwarf males of a species of Idarnes carme group were shown to develop feeding on good seeds [7]. Within genus Platyneura some species gall ovules while some species parasitize ovules occupied by pollinator larvae [8]. Dunn et al. took care to focus on parasite genera accepted to be inquilines of the pollinators or parasitoids. However, nobody has checked whether larvae of these species could develop on seeds. What we want to stress here is not that Dunn et al.’s results may not apply but rather that the extreme diversity of fig wasp biological traits should entice us to investigate them very carefully as they provide an exceptionally rich model to understand evolutionary processes. A casual observation in Brazil poses an even more stringent challenge. Ficus benjamina, an introduced species, is usually neither pollinated nor parasitized. R.A.S.P. observed a crop that matured. It had been colonized by Phylotrypesis taiwanensis a species normally associated with F. microcarpa. Hence Philotrypesis can gall ovules! Finally Sycophaga sycomori is a galler ovipositing at the same time as the pollinator. Despite being apparently exposed to the same parasitic pressures as the pollinators it uses all layers of flowers [9].
We hope to have convinced the reader that fig-wasps provide a unique material to investigate evolutionary processes. Their incredible biological diversity is a major asset. However this sheer diversity is also a major challenge to the investigators. The Dunn et al results are important. It is an open invitation to confirm the interpretations by direct biological data.

1. Anstett 2001. Oikos 95: 476-484.
2. Priyadarsanan 2000. Records Zool. Surv. India 182: 1-175.
3. West & Herre 1994. Proc. R. Soc. Lond. B. 258: 67-72.
4. Marussich & Machado 2007. Mol. Ecol. 16: 1925-1946.
5. Elias et al. 2008. Symbiosis 45: in press.
6. Elias 2008. Msc Dissertation. Sao Paulo University, Brazil.
7. Pereira et al. 2007. Biol. J. Linn. Soc. 92: 9-17.
8. Proffit 2007. PhD Thesis. University of Montpellier II, France.
9. Galil & Eisikowitch 1969. Tijdschr. Entomol. 112: 1-13.

No competing interests declared.