Density‐dependent fitness effects stabilize parasitic hitchhiking within a mutualism

Abstract

Mutualisms are often subject to perturbations by parasitism arising from third‐party interactions. How third‐party perturbations are dampened is a fundamental question pertaining to mutualism stability. Phoretic organisms that turn parasitic within a mutualism may destabilize it. If the fitness cost of such phoresy is high, then density‐dependent effects could be one mechanism to stabilize these interactions. We experimentally examined the fitness effects of a phoretic nematode community on a brood‐site pollination mutualism involving a pollinating fig wasp (the vehicle) and its associated fig species (the host for wasp and nematode development). We comprehensively investigated fitness impacts of phoresy on wasp lifespan, lifetime reproductive success, dispersal ability and predation risk as well as on host brood‐site volume and seed number. We employed a range of hitchhiker densities that encompassed natural and overloading levels for two nematode taxa (one plant‐ and one animal‐parasitic type). None of the plant host and vehicle fitness parameters were affected by wasps with low nematode transportation loads for either type of nematode. Furthermore, wasps arriving at their destinations carried lower densities of both animal‐ and plant‐parasitic nematodes compared to dispersing wasps, suggesting that there is selection on hitchhiker numbers during the dispersal process and that wasps loaded with a greater density of nematodes do not successfully disperse. Overloaded wasps had shorter flight durations, suggesting limited dispersal ability; on arrival at their destination, they suffered greater predation risk. Such overloaded wasps delivered impaired pollination services and produced fewer offspring resulting in lower lifetime fitness. Therefore, the direct and indirect effects of nematodes on their vehicles are strong. These effects also translated into impacts on host plant fitness, with the overloaded pollinators promoting the development of smaller brood sites with fewer seeds, thus reducing fig tree reproductive success. The effects of the animal parasites were greater than that of the plant parasite in this study. The third‐party interaction is therefore self‐limited and exhibits density dependence. The strong negative effects of overloading likely explain the low number of nematodes found in nature on dispersing and arriving fig wasps. Consequently, parasitic hitchhikers are unlikely to destabilize the mutualism. A free Plain Language Summary can be found within the Supporting Information of this article.

The enemy of my enemy is my friend: Nematode infection of pollinating and non-pollinating fig wasps has net benefits for the fig-fig wasp pollination mutualism

“…Importantly, these GLMMs also suggest that nematode infection, while significantly negatively associated with pollinator wasp offspring production, is a relatively benign effect that only limits an estimated 1% of the pollinator population every generation even though this infection is relatively common (consistent with Van Goor et al 2018, Gupta andBorges 2019, andShi et al 2019). In F. petiolaris, we have previously observed that nematode infection does not appear to limit pollinator longevity, dispersal ability, or offspring production unless many nematode individuals attempt to infect the same host (Van Goor et al 2018).…”

“…The life history of Parasitodiplogaster is tightly coupled with that of their pollinating wasp hosts, which they rely upon for energy, transport to a new fig, and subsequent reproductive success. For a description of the lifecycle of figs, their pollinator wasps, NPFWs, and Parasitodiplogaster see is thus necessary that their impacts on female pollinator wasp survival are not so great as to prohibit successful dispersal to trees bearing receptive stage figs (Herre 1995, Van Goor et al 2018, Gupta and Borges 2019, Shi et al 2019. Despite this constraint, the virulence of nematode infection varies across species as a function of host-wasp species population density (Herre 1993) and can range from avirulent or commensal (Herre 1995, Ramirez-Benavides and Salazar-Figueroa 2015, Van Goor et al 2018, Shi et al 2019 to virulent (Herre 1993(Herre , 1995, reducing host offspring production by up to 15%.…”

Phoresy in animals: review and synthesis of a common but understudied mode of dispersal

“…how many individuals are physically attached to the host) play in the effects of phoronts on their hosts (e.g. Moser, 1976; Gupta & Borges, 2019)? Answering these and related questions will help develop a better understanding of the evolution of these interactions from the viewpoint of both phoronts and hosts.…”

Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms

“…In a few vehicle–hitchhiker relationships, high hitchhiker density severely compromised the behaviour and physiology of the vehicle, affecting its dispersal (Gupta & Borges, 2019; Kinn, 1970). Therefore, under an overcrowding scenario (Figure 1a), whether caused by heterospecific or conspecific travellers, the probability of successful dispersal of the hitchhiker may decrease with co‐traveller numbers.…”

“…and Schistonchus sp.) interaction effects with the mutualistic partners but also show variation in hitchhiker density per vehicle within the dispersing wasp population (Gupta & Borges, 2019; Jauharlina et al., 2012; Van Goor et al., 2018).…”