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

TLDR

Mutualisms are theoretically vulnerable to cheaters, yet they persist across diverse, ancient systems, raising the question of what mechanisms prevent partners from exploiting the interaction without incurring costs. The authors conducted field experiments and observational surveys on six fig tree–fig wasp species pairs, comparing the fitness of pollinating versus non‑pollinating wasps and screening natural populations for pollen‑free individuals. They found that host sanctions lowered the fitness of non‑pollinating wasps in all actively pollinated species but not in passively pollinated ones, that pollen‑free wasps were restricted to actively pollinating species and inversely related to sanction strength, and that these results, together with prior work, support sanctions as essential for long‑term mutualism stability and reveal arms‑race dynamics in cooperative systems.

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.