Mutualistic interactions can be stabilized against invasion by noncooperative individuals by putting such “cheaters” at a selective disadvantage. Selection against cheaters should eliminate genetic variation in partner quality—yet such variation is often found in natural populations. One explanation for this paradox is that mutualism outcomes are determined not only by responses to partner performance but also by partner signals. Here, we build a model of coevolution in a symbiotic mutualism, in which hosts’ ability to sanction noncooperative symbionts and recognition of symbiont signals are determined by separate loci, as are symbionts’ cooperation and expression of signals. In the model, variation persists without destabilizing the interaction, in part because coevolution of symbiont signals and host recognition is altered by the coevolution of sanctions and cooperation, and vice versa. Individual-based simulations incorporating population structure strongly corroborate these results. The dual systems of sanctions and partner recognition converge toward conditions similar to some economic models of mutualistic symbiosis, in which hosts offering the right incentives to potential symbionts can initiate symbiosis without screening for partner quality. These results predict that mutualists can maintain variation in recognition of partner signals or in the ability to sanction noncooperators without destabilizing mutualism, and they reinforce the notion that studies of mutualism should consider communication between partners as well as the exchange of benefits.
Bibliographical noteFunding Information:
(grant 1237993; N. D. Young, principal investigator), and we developed and performed our simulations on computing systems maintained by the Minnesota Supercomputing Institute and Compute Canada’s Westgrid network. J.B.Y. completed this work while a postdoctoral fellow with the CoAdapTree Project, supported by Genome Canada with cofunding from Genome British Columbia and Genome Quebec (S. N. Aitken, Project Leader; S. Yeaman and R. Hamelin, Co-Project Leaders).
This work began as a project for the University of Minnesota Theory Under Construction discussion group. We also thank the Whitlock lab, attendees of the University of British Columbia Biodiversity Lunchtime Informal Seminar Series, S. L. Nuismer, and two anonymous reviewers. This work was funded by a National Science Foundation award to P.T.
- Population genetics