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Oviposition strategies, host coercion and the stable exploitation of figs by wasps.

ABSTRACT: A classic example of a mutualism is the one between fig plants (Ficus) and their specialized and obligate pollinating wasps. The wasps deposit eggs in fig ovules, which the larvae then consume. Because the wasps derive their fitness only from consumed seeds, this mutualism can persist only if the wasps are prevented from laying eggs in all ovules. The search for mechanisms that can limit oviposition and stabilize the wasp-seed conflict has spanned more than three decades. We use a simple foraging model, parameterized with data from two Ficus species, to show how fig morphology reduces oviposition rates and helps to resolve the wasp-seed conflict. We also propose additional mechanisms, based on known aspects of fig biology, which can prevent even large numbers of wasps from ovipositing in all ovules. It has been suggested that in mutualistic symbioses, the partner that controls the physical resources, in this case Ficus, ultimately controls the rate at which hosts are converted to visitors, regardless of relative evolutionary rates. Our approach provides a mechanistic implementation of this idea, with potential applications to other mutualisms and to theories of virulence.

SUBMITTER: Yu DW

PROVIDER: S-EPMC1691705 | biostudies-literature | 2004 Jun

REPOSITORIES: biostudies-literature

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Oviposition strategies, host coercion and the stable exploitation of figs by wasps.

Yu Douglas W DW Ridley Jo J Jousselin Emmanuelle E Herre Edward Allen EA Compton Stephen G SG Cook James M JM Moore Jamie C JC Weiblen George D GD

Proceedings. Biological sciences 20040601 1544

A classic example of a mutualism is the one between fig plants (Ficus) and their specialized and obligate pollinating wasps. The wasps deposit eggs in fig ovules, which the larvae then consume. Because the wasps derive their fitness only from consumed seeds, this mutualism can persist only if the wasps are prevented from laying eggs in all ovules. The search for mechanisms that can limit oviposition and stabilize the wasp-seed conflict has spanned more than three decades. We use a simple foragin ...[more]

PMID: 15306369

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Project description:It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.].

Project description:BACKGROUND:Biotic interactions are ubiquitous and require information from ecology, evolutionary biology, and functional genetics in order to be understood. However, study systems that are amenable to investigations across such disparate fields are rare. Figs and fig wasps are a classic system for ecology and evolutionary biology with poor functional genetics; Caenorhabditis elegans is a classic system for functional genetics with poor ecology. In order to help bridge these disciplines, here we describe the natural history of a close relative of C. elegans, Caenorhabditis inopinata, that is associated with the fig Ficus septica and its pollinating Ceratosolen wasps. RESULTS:To understand the natural context of fig-associated Caenorhabditis, fresh F. septica figs from four Okinawan islands were sampled, dissected, and observed under microscopy. C. inopinata was found in all islands where F. septica figs were found. C.i nopinata was routinely found in the fig interior and almost never observed on the outside surface. C. inopinata was only found in pollinated figs, and C. inopinata was more likely to be observed in figs with more foundress pollinating wasps. Actively reproducing C. inopinata dominated early phase figs, whereas late phase figs with emerging wasp progeny harbored C. inopinata dauer larvae. Additionally, C. inopinata was observed dismounting from Ceratosolen pollinating wasps that were placed on agar plates. C. inopinata was not found on non-pollinating, parasitic Philotrypesis wasps. Finally, C. inopinata was only observed in F. septica figs among five Okinawan Ficus species sampled. CONCLUSION:These are the first detailed field observations of C. inopinata, and they suggest a natural history where this species proliferates in early phase F. septica figs and disperses from late phase figs on Ceratosolen pollinating fig wasps. While consistent with other examples of nematode diversification in the fig microcosm, the fig and wasp host specificity of C. inopinata is highly divergent from the life histories of its close relatives and frames hypotheses for future investigations. This natural co-occurrence of the fig/fig wasp and C. inopinata study systems sets the stage for an integrated research program that can help to explain the evolution of interspecific interactions.

Dataset Information

Oviposition strategies, host coercion and the stable exploitation of figs by wasps.

Publications

Oviposition strategies, host coercion and the stable exploitation of figs by wasps.

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