Changes in host phenotype are often attributed to manipulation that enables parasites to complete trophic transmission cycles. We characterized changes in host phenotype in a colonial host–endoparasite system that lacks trophic transmission (the freshwater bryozoan Fredericella sultana and myxozoan parasite Tetracapsuloides bryosalmonae). We show that parasitism exerts opposing phenotypic effects at the colony and module levels. Thus, overt infection (the development of infectious spores in the host body cavity) was linked to a reduction in colony size and growth rate, while colony modules exhibited a form of gigantism. Larger modules may support larger parasite sacs and increase metabolite availability to the parasite. Host metabolic rates were lower in overtly infected relative to uninfected hosts that were not investing in propagule production. This suggests a role for direct resource competition and active parasite manipulation (castration) in driving the expression of the infected phenotype. The malformed offspring (statoblasts) of infected colonies had greatly reduced hatching success. Coupled with the severe reduction in statoblast production this suggests that vertical transmission is rare in overtly infected modules. We show that although the parasite can occasionally infect statoblasts during overt infections, no infections were detected in the surviving mature offspring, suggesting that during overt infections, horizontal transmission incurs a trade-off with vertical transmission.

This study begins to redress our lack of knowledge of the interactions between colonial hosts and their parasites by focusing on a novel host-parasite system. Investigations of freshwater bryozoan populations revealed that infection by myxozoan parasites is widespread. Covert infections were detected in all 5 populations studied and were often at high prevalence while overt infections were observed in only 1. Infections were persistent in populations subject to temporal sampling. Negative effects of infection were identified but virulence was low. Infection did not induce mortality in the environmental conditions studied. However, the production of statoblasts (dormant propagules) was greatly reduced in bryozoans with overt infections in comparison to uninfected bryozoans. Overtly-infected bryozoans also grew more slowly and had low fission rates relative to colonies lacking overt infection. Bryozoans with covert infections were smaller than uninfected bryozoans. High levels of vertical transmission were achieved through colony fission and the infection of statoblasts. Increased fission rates may be a strategy for hosts to escape from parasites but the parasite can also exploit the fragmentation of colonial hosts to gain vertical transmission and dispersal. Our study provides evidence that opportunities and constraints for host-parasite co-evolution can be highly dependent on organismal body plans and that low virulence may be associated with exploitation of colonial hosts by endoparasites.