Diversity begets diversity: do parasites promote variation in protective symbionts?

Insects commonly possess heritable microbial symbionts that increase their resistance to particular parasites. A diverse community of defensive symbionts may thus provide hosts with effective and specific protection against multiple parasites, although costs might constrain the accumulation of many symbionts. In parallel to the allelic diversity in the MHC complex of the vertebrate immune system, parasite diversity could be the driving force behind symbiont diversity. There is indeed evidence that parasites have the ability to drive frequencies of defensive symbionts in their hosts, and that these symbionts influence parasite communities, but direct evidence that parasite diversity can promote symbiont diversity is still lacking. We provide suggestions to investigate this potential link.

Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes.

Females choose specific mates in order to produce fitter offspring. However, several factors interfere with females' control over fertilization of their eggs, including sneaker males and phenotypically unpredictable allele segregation during meiosis. Mate choice at the individual level thus provides only a poor approximation for obtaining the best genetic match. Consequently, postcopulatory sperm selection by female oocytes has been proposed as a mechanism to achieve complementary combinations of parental haplotypes. Here, using controlled in vitro fertilization of three-spined stickleback eggs, we find haplotype-specific fertilization bias toward gametes with complementary major histocompatibility complex (MHC) immunogenes. The resulting zygote (and thus offspring) genotypes exhibit an intermediate level of individual MHC diversity that was previously shown to confer highest pathogen resistance. Our finding of haplotype-specific gamete selection thus represents an intriguing mechanism for fine-tuned optimization of the offspring's immune gene composition and an evolutionary advantage in the Red Queen dynamics of host-parasite coevolution.

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 host's 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.

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 parasite's 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 parasite's 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.

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

Parasites can increase their host's predation susceptibility. It is a long-standing puzzle, whether this is caused by host manipulation, an evolved strategy of the parasite, or by side effects due to, for example, the parasite consuming energy from its host thereby changing the host's trade-off between avoiding predation and foraging toward foraging. Here, we use sequential infection of three-spined sticklebacks with the cestode Schistocephalus solidus so that parasites have a conflict of interest over the direction of host manipulation. With true manipulation, the not yet infective parasite should reduce rather than enhance risk taking because predation would be fatal for its fitness; if host behavior is changed by a side effect, the 2 parasites would add their increase of predation risk because both drain energy. Our results support the latter hypothesis. In an additional experiment, we tested both infected and uninfected fish either starved or satiated. True host manipulation should act independently of the fish's hunger status and continue when energy drain is balanced through satiation. Starvation and satiation affect the risk averseness of infected sticklebacks similarly to that of uninfected starved and satiated ones. Increased energy drain rather than active host manipulation dominates behavioral changes of S. solidus-infected sticklebacks.

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.

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 parasite's 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 other's 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.

BACKGROUND: For 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. METHODS: We 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. RESULTS: Our 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. CONCLUSIONS: Transmission 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.

Transgenerational effects of food availability on age at maturity and reproductive output in an asexual collembolan species.

Transgenerational effects of environmental conditions can have several important ecological and evolutionary implications. We conducted a fully factorial experiment manipulating food availability across three generations in the collembolan Folsomia candida, a springtail species that inhabits soil and leaf litter environments which vary in resource availability. Maternal and grandmaternal food availability influenced age at maturity and reproductive output. These effects appear to be cumulative rather than adaptive transgenerational life-history adjustments. Such cumulative effects can profoundly influence eco-evolutionary dynamics in both stable and fluctuating environments.

Shape change in viable eggs of the collembolan Folsomia candida provides insight into the role of Wolbachia endosymbionts.

The endosymbiotic bacteria of the genus Wolbachia that infect the collembolan species Folsomia candida are responsible for facilitating parthenogenetic reproduction in their hosts. This study made empirical observations of the development of eggs of F. candida which contained normal populations of Wolbachia and of eggs which were cured of Wolbachia by treatment with the antibiotic rifampicin. A marked increase in egg size accompanied by a significant change in shape from spherical to discoid occurred in viable eggs three to four days after laying. These changes did not occur in the universally inviable eggs which came from the antibiotic treatment or in the 7% of untreated eggs which were naturally inviable. We infer that Wolbachia plays a critical role in zygotic or embryonic development during or before the first three days after laying and we draw on existing knowledge in speculating on the developmental mechanisms that Wolbachia may influence.