Nina Hafer

When parasites disagree: Evidence for parasite-induced sabotage of host manipulation

Host manipulation is a common parasite strategy to alter host behavior in a manner to enhance parasite fitness usually by increasing the parasites transmission to the next host. In nature, hosts often harbor multiple parasites with agreeing or conflicting interests over host manipulation. Natural selection might drive such parasites to cooperation, compromise, or sabotage. Sabotage would occur if one parasite suppresses the manipulation of another. Experimental studies on the effect of multi‐parasite interactions on host manipulation are scarce, clear experimental evidence for sabotage is elusive. We tested the effect of multiple infections on host manipulation using laboratory‐bred copepods experimentally infected with the trophically transmitted tapeworm Schistocephalus solidus. This parasite is known to manipulate its host depending on its own developmental stage. Coinfecting parasites with the same aim enhance each others manipulation but only after reaching infectivity. If the coinfecting parasites disagree over host manipulation, the infective parasite wins this conflict: the noninfective one has no effect. The winning (i.e., infective) parasite suppresses the manipulation of its noninfective competitor. This presents conclusive experimental evidence for both cooperation in and sabotage of host manipulation and hence a proof of principal that one parasite can alter and even neutralize manipulation by another.

Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host

BackgroundFor parasites with complex life cycles, size at transmission can impact performance in the next host, thereby coupling parasite phenotypes in the two consecutive hosts. However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably. Using the tapeworm Schistocephalus solidus, we evaluated how parasite size, age, and ontogeny in the copepod first host interact to determine performance in the stickleback second host.MethodsWe raised infected copepods under two feeding treatments (to manipulate parasite growth), and then exposed fish to worms of two different ages (to manipulate parasite ontogeny). We assessed how growth and ontogeny in copepods affected three measures of fitness in fish: infection probability, growth rate, and energy storage.ResultsOur main, novel finding is that the increase in fitness (infection probability and growth in fish) with larval size and age observed in previous studies on S. solidus seems to be largely mediated by ontogenetic variation. Worms that developed rapidly (had a cercomer after 9 days in copepods) were able to infect fish at an earlier age, and they grew to larger sizes with larger energy reserves in fish. Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.ConclusionsTransmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.

Inter- and intraspecific conflicts between parasites over host manipulation.

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.

An experimental conflict of interest between parasites reveals the mechanism of host manipulation

Lay Summary Causing energy drain is enough to fulfill a parasite’s need to change host behavior. A parasite can manipulate host behavior to its own interest either directly or indirectly through increased energy drain driving the host to be risk prone. We can distinguish experimentally between these mechanisms using a potential conflict of interest between 2 simultaneous parasites. We find support for the latter mechanism. An additional experiment with hungry and satiated hosts confirms our interpretation.

Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasites host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasites host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.

Cooperation or Conflict: Host Manipulation in Multiple Infections

Host manipulation is a ubiquitous phenomenon whereby a parasite actively alters its host’s phenotype including host behavior in order to enhance its own fitness beyond benefits gained from exploitation. In nature, hosts are usually infected by multiple parasites. Hence, most manipulating parasites will have to share their host with other parasites some of which might also be manipulators. The interests of these parasites might agree or disagree. Even parasites that do not themselves manipulate might disagree when other parasites manipulate their host’s behavior. If two manipulating parasites agree they could cooperate or free-ride. Especially in parasite species that usually infect their host in high numbers, parasite number seems to affect host manipulation. Conflict can occur between different parasite species with different definitive hosts or different transmission strategies or between different developmental stages of the same parasite species. There is evidence that such conflict can lead to sabotage of one parasite’s manipulation by another. Most studies have focused on intraspecific interactions in complex life cycle parasites and often used only naturally infected hosts. Hence experimental studies of both cooperation and conflict among parasites, especially studies investigating the interaction between different parasite species using the same host are urgently needed.

Differences between populations in host manipulation by the tapeworm Schistocephalus solidus – is there local adaptation?

Host manipulation whereby a parasite increases its transmission to a subsequent host by altering the behaviour of its current host is very far spread. It also occurs in host-parasite systems that are widely distributed. This offers the potential for local adaptation. The tapeworm Schistocephalus solidus modifies its first intermediate copepod hosts predation susceptibility to suit its own needs by reducing its activity before it becomes infective and increasing it thereafter. To investigate potential differences in host manipulation between different populations and test for potential local adaptation with regard to host manipulation, I experimentally infected hosts from two distinct populations with parasites from either population in a fully crossed design. Host manipulation differed between populations mostly once the parasite had reached infectivity. These differences in infective parasites were mostly due to differences between different parasite populations. In not yet infective parasites, however, host population also had a significant effect on host manipulation. There was no evidence of local adaptation; parasites were able to manipulate foreign and local hosts equally well. Likewise, hosts were equally poor at resisting host manipulation by local and foreign parasites.