The rules for symbiont community assembly change along a mutualism–parasitism continuum

Symbiont community assembly is driven by host–symbiont and symbiont–symbiont interactions. The effects that symbionts exert on their hosts are often context‐dependent, and existing theoretical frameworks of symbiont community assembly do not consider the implications of variable outcomes to assembly processes. We hypothesized that symbiont–symbiont interactions become increasingly important along a parasitism/mutualism continuum because; (i) negative outcomes favour host resistance which in turn reduces symbiont colonization and subsequently reduce symbiont–symbiont interactions, whereas (ii) positive host outcomes favour tolerance and consequently higher symbiont colonization rates, leading to stronger interactions among symbionts. We found support for this hypothesis in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. The symbiosis between crayfish and their worms can shift from parasitism/commensalism to mutualism as crayfish age. Here, field surveys identified changes in worm density, diversity and composition that were concomitant to changing symbiosis outcomes. We conducted several laboratory experiments and behavioural assays to relate patterns from the field to their likely causal processes. Young crayfish typically hosted only two relatively small worm species. Older crayfish hosted two additional larger species. In laboratory experiments, young crayfish exhibited a directed grooming response to all worm species, but were unable to remove small species. Conversely, adult crayfish did not exhibit grooming responses to any worm species. Relaxed grooming allowed the colonization of large worm species and initiated symbiont–symbiont intraguild predation that reduced the abundance and altered the behaviour of small worm species. Thus, the dominant processes of symbiont community assembly shifted from host resistance to symbiont–symbiont interactions through host ontogeny and a concomitant transition towards mutualism. This work shows that host resistance can have a prevailing influence over symbiont community assembly when symbiosis is disadvantageous to the host. However, when symbiosis is advantageous and resistance is relaxed, symbiont colonization rate and consequently abundance and diversity increases and interactions among symbionts become increasingly important to symbiont community assembly.