Host sanctions and pollinator cheating in the fig tree–fig wasp mutualism

Abstract

Theory predicts that mutualisms should be vulnerable to invasion by cheaters, yet mutualistic interactions are both ancient and diverse. What prevents one partner from reaping the benefits of the interaction without paying the costs? Using field experiments and observations, we examined factors affecting mutualism stability in six fig tree-fig wasp species pairs. We experimentally compared the fitness of wasps that did or did not perform their most basic mutualistic service, pollination. We found host sanctions that reduced the fitness of non-pollinating wasps in all derived, actively pollinated fig species (where wasps expend time and energy pollinating), but not in the basal, passively pollinated fig species (where wasps do not). We further screened natural populations of pollinators for wasp individuals that did not carry pollen ('cheaters'). Pollen-free wasps occurred only in actively pollinating wasp species, and their prevalence was negatively correlated with the sanction strength of their host species. Combined with previous studies, our findings suggest that (i) mutualisms can show coevolutionary dynamics analogous to those of 'arms races' in overtly antagonistic interactions; (ii) sanctions are critical for long-term mutualism stability when providing benefits to a host is costly, and (iii) there are general principles that help maintain cooperation both within and among species.

The Coexistence of Hosts with Different Abilities to Discriminate against Cheater Partners: An Evolutionary Game-Theory Approach

“…While Foster and Kokko (2006) have demonstrated the importance of variability in partner cooperation to maintain host discrimination, our model proposes that cheaters can facilitate host species coexistence. The existence of host species with different capacities to discriminate against cheater partners has recently been demonstrated to occur in a wide variety of mutualisms (Pellmyr 1994;Keirs et al 2007;Bever et al 2009;Heil et al 2009;Jandér and Herre 2010;Kiers et al 2011;Grman 2012), suggesting these population dynamics may be a general feature of mutualisms. In this context, giving and discriminating hosts act as reservoirs of the cheater and mutualist partners each requires to coexist.…”

“…Several recent studies suggest that discriminating hosts derive relatively less benefit from cooperative partners than their giving competitors. For example, fig species associated with strong sanctions against cheater wasps have floral traits that reduce their maximum achievable seed yield relative to figs that tolerate cheating (Herre 1989;Jandér and Herre 2010). Acacia species that are better at promoting vigilant defensive ant species invest more resources into costly extrafloral nectaries than species that tolerate cheater, nondefensive ants (Heil et al 2009).…”

“…An alternative mechanism is one that involves negative feedbacks among coexisting species, such that giver hosts act as a susceptible reservoir for the production of cheater partners, while discriminator hosts sustain sufficient mutualists to prevent cheaters from driving the givers extinct. Indeed, the requisite cheaters and variability in host species' ability to discriminate is documented in the mutualisms between figs and pollinator wasps (Jandér and Herre 2010), Acacia and herbivore defense ants (Heil et al 2009), and plants and mycorrhiza that enhance nutrient acquisition Kiers et al 2011;Grman 2012).…”

Major evolutionary transitions in individuality

“…Sanction mechanisms seem to be more common in partnerships when symbionts transmit horizontally, where we predict that there will be more conflict to resolve, such as in partnerships with root symbionts, luminous symbionts, and pollinator mutualisms (24,25,48,49).…”

Economic contract theory tests models of mutualism

“…23, p 63), whereas both PFF and HS are differential rewards or punishments implemented after exploitation is possible. Here, we argue that a failure to clearly define the differences between PFF and HS has led to their conflation, with the result that experiments demonstrating what appears to be the punishment of cheating in a wide range of mutualisms, including those between yucca plants and yucca moths (24), legumes and nitrogen-fixing bacteria (25,26), ants and plants (27), plants and mycorrhizal fungi (28), and figs and fig wasps (29), have been generally accepted as evidence for HS (1,9,13,(26)(27)(28)(29), whereas PFF is the more likely explanation.…”