Mutualism is a relationship between two organisms or species in which both benefit from the association. Flowering plants and pollinator interactions are a classic example of mutualism. Mutualisms are ubiquitous in nature and biologists have been fascinated by them for a long time. For example, how does mutualism evolve? What maintains mutualism? Theory predicts that mutualism is susceptible to breakdown (May 1981) and vulnerable to anthropogenic environmental change (Six 2009, Verbruggen and Kiers 2010). However, mutualism has been maintained for a really long time. But how? There have to be mechanisms that limit invasion of uncooperative cheaters (partners that reap the benefits of mutualism but don’t provide benefits to the other partner). One potential mechanism is a host sanction of less-beneficial symbionts. Some organisms, such as rhizobia and mycorrhizae, can sanction their uncooperative symbionts by reducing resource allocation (Kiers et al. 2003, Bever et al. 2009). What is not clear is how precisely host sanction can act against the “cheaters”. When there is a cheater in the system, the host has three main options: 1) do nothing, 2) sanction at the “module” level or 3) sanction at the individual level (figure below). Option 3) is the most precise sanction but there might be cost associated with precision.
(modified Figure 1 from Jandér et al 2012)
What they did
Jandér and her colleagues explored these hypotheses using the fig-fig wasp mutualism as a study system. They asked at which level does host sanction against uncooperative wasps occur? To appreciate this really cool study, we first need to know a little bit about the biology of fig-fig wasp interactions. Fig trees produce a collection of tiny flowers inside each hollow inflorescence (i.e. fig). Female wasps can enter a fig to pollinate flowers and oviposit eggs in the flowers. Interestingly, a small fraction of individual wasps in nature do not carry pollen, but do oviposit eggs (i.e. uncooperative cheaters).
They conducted a field experiment in Panama to test the precision of fig sanction. They applied three wasp treatments on non-pollinated figs: 1) two pollen-free wasps (P-P-), 2) one pollen-free wasp and another with pollen-carrying wasp (P-P+), and 3) two pollen-carrying wasps (P+P+). Just before the wasps emerged, they collected the figs and quantified all the wasp offspring. For P-P+ treatment, they identified their maternal lineages using molecular markers.
Prior to conducting the experiment, they came up with four competing hypotheses (p. 1363 Jandér et al. 2012):
Hyp1: Fig-level sanctions; 1P+ sufficient. Pollination by one wasp ensures sufficient resources for all developing wasp larvae in the fig.
Hyp 2: Fig-level sanctions; pollen-dependent. Resource allocation to the fig increases linearly with pollination level.
Hyp 3: Flower & nearby level. Sanctions act on the flower level, but without a sharp distinction between pollinated and unpollinated flowers – benefits from pollinated flowers ‘leak’ to nearby flowers.
Hyp 4: Flower-level sanctions only. For example, resources might be strictly allocated to pollinated flowers only.
What they found
-They found that adding one pollinator increased seed numbers dramatically, as they expected. Adding the second pollinator further increased the seed production, suggesting that figs are pollen limited.
– They also found that sanctions act on the fig level rather than on individual flowers inside each fig (Hypothesis 1 or 2, but they cannot distinguish between them with the current dataset). In other words, if a cheater wasp oviposits with a pollen-carrying wasp, then the fitness of cheater is as good as the cooperative ones.
Why I liked it:
-Host sanction is difficult to test. Their experiment was elegant and they laid out their multiple competing hypotheses well.
-They don’t really highlight it in the paper very much, but I like how they quantified fitness of both the plants and wasps. From the plants’ perspective, the cost of only associating with cheater wasps is high (fitness ≈0). But host sanction does not drive wasps’ fitness to zero; cheater wasps (P-P-) can still have offspring (Figure 5).
-This study generates more interesting questions about mutualism. For example, what is the variation in costs and benefits of host sanction among species that differ in sanction precision? How common are figs pollinated by cooperative and uncooperative pollinators (P-P+) in nature? If the host sanction is not efficient, how do they limit cheaters?
-Jen also liked the paper and says “This paper combined the approaches of Q and Macgyver (high tech and low tech) – used DNA-based approaches to estimate parentage, but also the brute force methods of manipulating pollen on wasps by removing pollen.”