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In mutualism, hosts select symbionts via partner choice and preferentially direct more resources to symbionts that provide greater benefits via sanctions. At the initiation of symbiosis, prior to resource exchange, it is not known how the presence of multiple symbiont options (i.e. the symbiont social environment) impacts partner choice outcomes. Furthermore, little research addresses whether hosts primarily discriminate among symbionts via sanctions, partner choice or a combination. We inoculated the legume , Acmispon wrangelianus, with 28 pairs of fluorescently labelled Mesorhizobium strains that vary continuously in quality as nitrogen-fixing symbionts. We find that hosts exert robust partner choice, which enhances their fitness. This partner choice is conditional such that a strain's success in initiating nodules is impacted by other strains in the social environment. This social genetic effect is as important as a strain's own genotype in determining nodulation and has both transitive (consistent) and intransitive (idiosyncratic) effects on the probability that a symbiont will form a nodule. Furthermore, both absolute and conditional partner choice act in concert with sanctions, among and within nodules. Thus, multiple forms of host discrimination act as a series of sieves that optimize host benefits and select for costly symbiont cooperation in mixed symbiont populations.
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This content will become publicly available on May 26, 2026
Synergy, complexity, and the dirty, dirty cheats of the world
ABSTRACT Studies of symbiosis employ the term “parasitism” to connote different sorts of relationships. Within the context of mutualistic symbioses, parasites are otherwise cooperative individuals or strains that appropriate a disproportionate amount of the synergistic products. In the context of antagonistic symbioses, there is no pretence of cooperation, and instead parasites are defined as individuals or strains that derive fitness benefits at a fitness cost to their hosts. In both cases, parasitism is selected for at the lower level (that of the individual symbiont) but selected against at the higher level (the group of symbionts in a single host). Despite these similarities, these different sorts of parasitism likely evolve by different pathways. Once a host–symbiont relationship initiates, if functional synergy is lacking, the relationship will remain exploitative, although parasites may differ in their detrimental effects on the host and the higher‐level unit. If functional synergy is present, however, cooperation may develop with benefits for both host and symbionts (i.e. mutualism). Nevertheless, parasites may still evolve from within these incipient relationships when individuals or strains of symbionts act parasitically by defecting from the common good to further their selfish replication. Levels‐of‐selection dynamics thus underlie both forms of parasitism, but only in the case of latent functional synergy can true symbiotic complexity at the higher level emerge.
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- Award ID(s):
- 2236135
- PAR ID:
- 10593252
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Biological Reviews
- ISSN:
- 1464-7931
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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