Ontogenetic shift in host tolerance controls initiation of a cleaning symbiosis

When the interests of mutualists are not perfectly aligned, control mechanisms that modulate interactions can maintain mutually beneficial outcomes and stabilize mutualisms over evolutionary time. However, the costs and benefits of symbiosis often change with ontogeny and whether control mechanisms are adjusted to reflect ontogenetic changes is largely unknown. We examined the recently described cleaning symbiosis between crayfish Cambarus chaugaensis and ectosymbiotic annelids (Xironodrilus appalachius) for evidence of ontogenetic changes in symbiont control. Xironodrilus appalachius provide a beneficial cleaning service to C. chaugaensis by removing epibiotic accumulations from the gills, but crayfish also incur costs via density‐dependent facultative parasitism of gill tissue. A series of laboratory experiments using crayfish from three size (age) – classes demonstrated that crayfish use grooming to limit cleaner density and grooming effects on cleaners varied with crayfish age. Small crayfish quickly removed essentially all of their cleaners. Intermediate crayfish removed most of their cleaners, but some cleaners persisted at a location apparently inaccessible to grooming and far from the gill chamber. Large crayfish removed a smaller proportion of cleaners and cleaners were allowed access to the gill chamber, thus initiating the cleaning symbiosis. Cleaner removal was not dependent on cleaner density, suggesting that crayfish do not regulate cleaners to a specific density. Experimental results were corroborated by patterns observed during a field survey. We argue decreased cleaner removal and relaxed control of cleaner attachment sites corresponds to ontogenetic changes in the costs and benefits of symbiosis. This study integrates two major theoretical perspectives from ecological literature; control mechanisms and ontogenetic shifts, and illustrates how changes in control mechanisms with ontogeny may favor life‐long positive outcomes of symbiosis. Ontogenetic shifts in the costs and benefits of symbiosis may be common; therefore future theoretical and empirical studies of symbioses should incorporate both perspectives.