Abstract
Species pairs that form mutualistic associations are also components of broader organismal community networks. These interaction networks have shaped the evolution of individual mutualisms through interspecific interactions ranging from secondarily mutualistic to intensely antagonistic. Our understanding of this complex context remains limited because characterizing the impacts of species interacting with focal mutualists is often difficult. How is the fitness of mutualists impacted by the co-occurring interactive network of community associates? We investigated this context using a model interaction network comprised of a fig and fig wasp mutualist, eight non-pollinating fig wasp (NPFW) antagonists/commensals and a nematode previously believed to be associated only with the pollinator wasp mutualist. Through repeated sampling and field observations, we characterized the ecological roles of these mutualist-associated organisms to identify key antagonists. We then investigated how potential nematode infection of NPFWs could impact wasp survival across key life stages and, in turn, inferred how this influences the fitness of the fig-pollinator mutualists. Unexpectedly, we found all Ficus petiolaris-associated NPFWs to be the targets for nematode infection, with infection levels sometimes exceeding that of pollinators. Experimental data collected for the most abundant NPFW species suggest that nematode infection significantly reduces their longevity. Further, comparisons of nematode loads for emerging and successfully arriving NPFWs suggest that infection severely limits their dispersal ability. Through these observations, we conclude that this infection could impact NPFWs more severely than either mutualistic partner, suggesting a novel role of density-dependent facultative mutualism between figs, pollinator wasps and the nematode. This antagonist-mediated suppression of other network antagonists may present an ecologically common mechanism through which antagonists can present net benefits for mutualists' fitness.
Highlights
Mutualisms, or reciprocally beneficial interspecific interactions, are ubiquitous in nature and strongly influence ecological processes that, in turn, have shaped the trajectories of organismal evolution (Kiers et al 2010)
We found all Ficus petiolaris‐associated non-pollinating fig wasp (NPFW) to be the targets for nematode infection, with infection levels sometimes exceeding that of pollinators
Percent of wasps excluded due to nematode infection per generation we found that most NPFWs associated with F. petiolaris are targets for nematode infection which may severely limit their dispersal ability and longevity, and suppress their exploitation of the fig–fig wasp mutualism
Summary
Mutualisms, or reciprocally beneficial interspecific interactions, are ubiquitous in nature and strongly influence ecological processes that, in turn, have shaped the trajectories of organismal evolution (Kiers et al 2010). One impediment to investigating the effects of community-level antagonism on mutualism fitness is that lifetime fitness in many systems is difficult to quantify (Bronstein, 2015; West et al 1996) This can be alleviated by focusing on model systems in which all intimately interacting species are known, ecological roles as mutualists and exploiters are well-understood and key components of lifetime reproductive success are estimated. One such model system is the fig–fig wasp obligate nursery– pollination mutualism. We estimate the fitness effects of infection through its potential impacts on key components of NPFW life history such as dispersal ability and longevity
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