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A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown.
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Partner dependency alters patterns of coevolutionary selection in mutualisms
Coevolution is a ubiquitous driver of diversification in both mutualistic and antagonistic interactions between species. In mutualisms, coevolution can result in trait complementarity between partners that facilitates their persistence. Despite its importance, most of what we know about coevolution in mutualism comes from obligate interactions, whereas we know comparatively little about facultative interactions, arguably the most common type of mutualism. To evaluate coevolutionary dynamics in facultative mutualism and test how it compares with obligate mutualisms, we used a synthetic yeast mutualism where the partners exchange essential nutrient resources. We manipulated mutualism dependency by controlling the availability of mutualistic resources in the environment and measured coevolution via time-shift assays and tracking the evolution of mutualistic traits over time. In addition, we genotyped the evolved and ancestral mutualists to test for differences in the strength of coevolutionary selection between facultative and obligate mutualisms. We found evidence of coevolution in both facultative and obligate mutualisms, but coevolution was weaker and slower in facultative mutualisms. We also found evidence for evolution of trait complementarity in obligate mutualisms but not in facultative mutualisms. Furthermore, obligate mutualists had more SNPs under positive selection than facultative mutualists. Together, these results provide strong evidence that mutualism dependency impacts both the strength of coevolution and the rate of trait evolution.
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- Award ID(s):
- 2137555
- PAR ID:
- 10670887
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 122
- Issue:
- 21
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1073/pnas.2424983122
