How to be a fig wasp parasite on the fig–fig wasp mutualism

https://doi.org/10.1016/j.cois.2015.01.011Get rights and content

Highlights

  • The nursery pollination mutualism between figs and fig wasps is subject to parasitism.

  • Parasites can be gallers, kleptoparasites, seed predators or parasitoids.

  • Host exploitation depends on life history, sensory ecology, and oviposition ability.

  • Parasites exhibit delayed phylogenetic tracking of their hosts.

  • Parasites exhibit less host specificity than previously estimated.

The nursery pollination mutualism between figs and pollinating fig wasps is based on adaptations that allow wasps to enter the enclosed inflorescences of figs, to facilitate seed set, and to have offspring that develop within the nursery and that leave to enter other inflorescences for pollination. This closed mutualistic system is not immune to parasitic fig wasps. Although the life histories and basic biology of the mutualists have been investigated, the biology of the fig wasp parasites has been severely neglected. This review brings together current knowledge of the many different ways in which parasites can enter the system, and also points to the serious lacunae in our understanding of the intricate interactions between gallers, kleptoparasites, seed eaters and parasitoids within this mutualism.

Introduction

Interactions between plants and insects vary from antagonistic (resource–consumer relationships) to mutualistic (resources in exchange for pollination and defence). In some systems, the interaction has evolved into an obligatory or mutualistic one such as the relationship between ants and obligate myrmecophytes and that between pollinating wasps and figs. These highly intimate relationships often require sophisticated adaptations in both partners to secure the interaction. Yet these interactions are often exploited by ‘cheaters’. In this review, I present novel ways in which the mutualistic interaction between figs and fig wasps is exploited by parasites.

Section snippets

The biology of the fig–fig wasp mutualism

The mutualism between figs and their pollinating fig wasps is ancient, originating ca 75 mya in Eurasia [1]. Ficus (Moraceae) has an enclosed globose inflorescence, the syconium, with a single opening, the ostiole. Figs have two breeding systems [2••, 3••, 4••]. In monoecious figs, uniovulate female flowers line the syconium cavity. Pollen-bearing female fig wasps enter the syconium, oviposit into flowers producing galls, and subsequently die. Male offspring eclose first, mate with and release

Non-pollinating fig wasp parasites of the fig–fig wasp mutualism

Figs harbour many kinds of fig wasp parasites [2••]. Pollinating fig wasps occur within the monophyletic agaonid clade of chalcid wasps, and are closely related to non-pollinating fig wasp (NPFW) gallers of the subfamily Sycophaginae [11]. Another chalcid family Pteromalidae contains the majority of other NPFWs within several subfamilies such as Sycoecinae and Sycoryctinae [11] suggesting several independent origins of parasitism. NPFW assemblage size varies from 3 to 30 species on a single fig

Parasites entering syconia for oviposition

Lineages of pollinating wasps can evolve into cheaters [15] with reduced pollen pockets and without the coxal combs that are essential for active pollination [16]; survival of such parasites is greater when they share syconia with congeneric non-cheating pollinators [15]. The mechanism behind the facilitative effect of the mutualistic pollinator on the cheater is unknown. Some sycoecine wasps oviposit into galled flowers already containing pollinator eggs; such parasites are larger than the

Parasites ovipositing into syconia from the outside

Most parasites oviposit into the syconium from its external surface. Since syconium size increases during development, ovipositor lengths of parasite species match the syconial stage of parasitism [17, 18••, 19, 20].

Gallers are the first to attack a syconium. Gallers can oviposit into very small syconia even before floral primordia develop [20]; they gall tissues lining the young syconial lumen and produce very large, thick-walled galls that fill lumen space. Other early gallers oviposit into

Sensory ecology of parasitism

The long-distance attraction of pollinators, as well as NPFW gallers and parasitoids to syconia is mediated by fig VOCs [38]. VOCs emitted by fig trees probably rise in plumes that might spread at different heights depending on the heights of the trees and the prevailing wind conditions. Although wind-blown pollinators have been trapped above tree canopies in forests and cities [39•, 40], fewer NPFWs were trapped at such heights or lower [39], making inferences about heights at which NPFWs

Life history strategies

Parasite life history strategies should match their parasitic strategy. The life history and parasitic strategies of one fig wasp community occupying a single fig species has been investigated [20, 28••]. Gallers exhibited the life history trait of pro-ovigeny, eclosing with a full complement of matured eggs, while parasitoids exhibited synovigeny eclosing with only a few mature eggs. Synovigenic parasitoids continue to develop mature eggs throughout their lifespan. The synovigeny of the

Community organisation of fig wasp parasites

Globally, across fig distributions, there is convergence in the structure of multitrophic communities of fig wasps inhabiting fig syconia [22, 48]. The species richness of gallers strongly influences the diversity of parasitoids [12] as in other systems [49]. Fig species with larger syconia and larger numbers of flowers may provide greater opportunities for niche specialisation, supporting greater NPFW species diversity. There may be trade-offs between life history traits such as fecundity

Do parasites keep pace with the mutualism?

NPFWs are much less ancient than pollinators, exhibiting delayed phylogenetic tracking of their hosts [55•, 56, 57, 58], much less close co-cladogenesis with the figs and much more host shifting than exhibited by pollinators and figs [55•, 56]. The same parasites were found on more than one fig species [59], suggesting less specificity than previously believed.

How opportunistic or how generalist are parasites? Since NPFWs are attracted by fig VOCs, gallers or parasitoids could exploit a set of

Future prospects

Successful parasitism of the fig–fig wasp mutualism is clearly a challenge. Although many aspects of the fig–pollinator association have been examined, the biology of NPFWs has been severely neglected. Explaining the patterns that are emerging on the presence or absence of co-diversification between figs, their pollinators, and their parasites will only be possible when dietary ecology, life history traits and sensory ecology are investigated. The fig system is not readily amenable to yielding

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Our work on figs has received support from the Ministry of Environment and Forests, the Department of Science and Technology, the Department of Biotechnology, Government of India, and the Indo-French Centre for the Promotion for Advanced Research for which I am grateful. I thank Rieta Gols for inviting me to contribute this review. I am grateful to Anusha Krishnan, Vignesh Venkateswaran and Pratibha Yadav for help with the figures.

References (59)

  • C.C.L. Soler et al.

    Evidence for intersexual mimicry in a dioecious plant

    Ecol Lett

    (2012)
  • M.J. McLeish et al.

    Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism

    BMC Evol Biol

    (2012)
  • C.T. Darwell et al.

    Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity

    BMC Evol Biol

    (2014)
  • G.D. Weiblen

    How to be a fig wasp

    Annu Review Entomol

    (2002)
  • S. van Noort et al.

    Convergent evolution of agaonine and sycoecine (Agaonidae, Chalcidoidea) head shape in response to the constraints of host fig morphology

    J Biogeogr

    (1996)
  • M. Hossaert-McKey et al.

    Floral scents: their roles in nursery pollination mutualisms

    Chemoecology

    (2010)
  • J.M. Heraty et al.

    A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera)

    Cladistics

    (2013)
  • S.G. Compton et al.

    Determinants of species richness in southern African fig wasp assemblages

    Oecologia

    (1992)
  • A. Cruaud et al.

    A multilocus phylogeny of the world Sycoecinae fig wasps (Chalcidoidea: Pteromalidae)

    PLoS ONE

    (2013)
  • H.-H. Chen et al.

    Secondary galling: a novel feeding strategy among ‘non-pollinating’ fig wasps from Ficus curtipes

    Ecol Entomol

    (2013)
  • J.-B. Zhao et al.

    A switch from mutualist to exploiter is reflected in smaller egg loads and increased larval mortalities in a ‘cheater’ fig wasp

    Acta Oecol

    (2014)
  • Y.-Q. Peng et al.

    Co-occurrence of two Eupristina species on Ficus altissima in Xishuangbanna, SW China

    Symbiosis

    (2008)
  • G.D. Weiblen et al.

    Speciation in fig pollinators and parasites

    Mol Ecol

    (2002)
  • M. Ghara et al.

    Nature's Swiss army knives: ovipositor structure mirrors ecology in a multitrophic fig wasp community

    PLoS ONE

    (2011)
  • S. al-Beidh et al.

    Parasites and mutualism: measuring enemy-free space in a fig–pollinator symbiosis

    Oikos

    (2012)
  • M. Ghara et al.

    Divvying up an incubator: how parasitic and mutualistic fig wasps use space within their nursery microcosm

    Arthropod-Plant Interac

    (2014)
  • A. Cruaud et al.

    Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea)

    BMC Evol Biol

    (2011)
  • S. Jansen-González et al.

    Mutualism from the inside: coordinated development of plant and insect in an active pollinating fig wasp

    Arthropod-Plant Interac

    (2012)
  • S. Jansen-González et al.

    Same but different: larval development and gall-inducing process of a non-pollinating fig wasp compared to that of pollinating fig-wasps

    Acta Oecol

    (2014)
  • Cited by (0)

    View full text