The evolution of host protection by vertically transmitted parasites

Hosts are often infected by a variety of different parasites, leading to competition for hosts and coevolution between parasite species. There is increasing evidence that some vertically transmitted parasitic symbionts may protect their hosts from further infection and that this protection may be an important reason for their persistence in nature. Here, we examine theoretically when protection is likely to evolve and its selective effects on other parasites. Our key result is that protection is most likely to evolve in response to horizontally transmitted parasites that cause a significant reduction in host fecundity. The preponderance of sterilizing horizontally transmitted parasites found in arthropods may therefore explain the evolution of protection seen by their symbionts. We also find that protection is more likely to evolve in response to highly transmissible parasites that cause intermediate, rather than high, virulence (increased death rate when infected). Furthermore, intermediate levels of protection select for faster, more virulent horizontally transmitted parasites, suggesting that protective symbionts may lead to the evolution of more virulent parasites in nature. When we allow for coevolution between the symbiont and the parasite, more protection is likely to evolve in the vertically transmitted symbionts of longer lived hosts. Therefore, if protection is found to be common in nature, it has the potential to be a major selective force on host–parasite interactions.     

The evolution of parasite manipulation of host dispersal

We investigate the evolution of manipulation of host dispersal behaviour by parasites using spatially explicit individual-based simulations. We find that when dispersal is local, parasites always gain from increasing their hosts' dispersal rate, although the evolutionary outcome is determined by the costs-to-benefits ratio. However, when dispersal can be non-local, we show that parasites investing in an intermediate dispersal distance of their hosts are favoured even when the manipulation is not costly, due to the intrinsic spatial dynamics of the host-parasite interaction. Our analysis highlights the crucial importance of ecological spatial dynamics in evolutionary processes and reveals the theoretical possibility that parasites could manipulate their hosts' dispersal.     

Host manipulation by parasites: a multidimensional phenomenon

The diversity of ways in which parasites manipulate the phenotype of their hosts to increase their transmission has been well‐documented during the past decades. Parasites clearly have the potential to alter a broad range of phenotypic traits in their hosts, extending from behaviour and colour to morphology and physiology. While the vast majority of studies have concentrated on few, often only one, host characters, there is increasing evidence that manipulative parasites alter multiple characteristics of their host's phenotype. These alterations can occur simultaneously and/or successively through time, making parasitically modified organisms undoubtedly more complex than traditionally viewed. Here, we briefly review the multidimensionality of host manipulation by parasites, discuss its possible significance and evolution, and propose directions for further research. This view should prove to be an extremely useful approach, generating a series of testable hypotheses regarding the ecology of parasitized hosts, and leading to a better comprehension of complex host–parasite relationships.     

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host–parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.     

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.     

Play and the evolution of fairness: a game theory model

Bekoff [J. Consci. Stud. 8 (2001) 81] argued that mammalian social play is a useful behavioral phenotype on which to concentrate in order to learn more about the evolution of fairness. Here, we build a game theoretical model designed to formalize some of the ideas laid out by Bekoff, and to examine whether ‘fair’ strategies can in fact be evolutionarily stable. The models we present examine fairness at two different developmental stages during an individual's ontogeny, and hence we create four strategies—fair at time 1/fair at time 2, not fair at time 1/not fair at time 2, fair at time 1/not fair at time 2, not fair at time 1/fair at time 2. Our results suggest that when considering species where fairness can be expressed during two different developmental stages, acting fairly should be more common than never acting fairly. In addition, when no one strategy was evolutionarily stable, we found that all four strategies we model can coexist at evolutionary equilibrium. Even in the absence of an overwhelming database from which to test our model, the general predictions we make have significant implications for the evolution of fairness.     

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.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia

One of the most striking characteristics of gall-forming insects is the variability in gall position, morphology, and complexity. Our knowledge of the driving forces behind the evolutionary divergence of gall types is limited. Natural enemies, competition, and behavioral constraints might be involved. We present a cladogram, based on sequences of COI and COII (1952bp), of mitochondrial DNA for the evolution of 14 species of gall-forming aphids (Fordinae). These insects induce five gall types with remarkable morphological variation on Pistacia spp. hosts. The parsimony cladogram divides the Fordinae into three lineages, Fordini and Baizongiini, and a third (new) sister group including the previously Fordini member, Smynthurodes betae (West). We then use ecological data to trace and explain the evolution of gall morphology. The aphids seem to have evolved gradually towards better ability to manipulate their host plant, induce stronger sinks, and gain higher reproductive success. We suggest that the ancestral gall type was a simple, open, "pea"-sized gall located on the leaflet midvein. Some Fordini and S. betae evolved a two-gall life cycle, inducing a new gall type on the leaflet margin. The Baizongiini improved the manipulation of their host by inducing larger galls near the midvein, with stronger sinks supporting thousands of aphids. Similar gall types are induced at similar sites on different Pistacia hosts suggesting control of the aphids on gall morphology and frequent host shifts. Thus, even extreme specialization (specific gall and host) is flexible.     

The evolution of altruism: game theory in multilevel selection and inclusive fitness

Although the prisoner's dilemma (PD) has been used extensively to study reciprocal altruism, here we show that the n-player prisoner's dilemma (NPD) is also central to two other prominent theories of the evolution of altruism: inclusive fitness and multilevel selection. An NPD model captures the essential factors for the evolution of altruism directly in its parameters and integrates important aspects of these two theories such as Hamilton's rule, Simpson's paradox, and the Price covariance equation. The model also suggests a simple interpretation of the Price selection decomposition and an alternative decomposition that is symmetrical and complementary to it. In some situations this alternative shows the temporal changes in within- and between-group selection more clearly than the Price equation. In addition, we provide a new perspective on strong vs. weak altruism by identifying their different underlying game structures (based on absolute fitness) and showing how their evolutionary dynamics are nevertheless similar under selection (based on relative fitness). In contrast to conventional wisdom, the model shows that both strong and weak altruism can evolve in periodically formed random groups of non-conditional strategies if groups are multigenerational. An integrative approach based on the NPD helps unify different perspectives on the evolution of altruism.     

Behavior out of control: Experimental evolution of resistance to host manipulation

Many parasites alter their host's phenotype in a manner that enhances their own fitness beyond the benefits they would gain from normal exploitation. Such host manipulation is rarely consistent with the host's best interests resulting in suboptimal and often fatal behavior from the host's perspective. In this case, hosts should evolve resistance to host manipulation. The cestode Schistocephalus solidus manipulates the behavior of its first intermediate copepod host to reduce its predation susceptibility and avoid fatal premature predation before the parasite is ready for transmission to its subsequent host. Thereafter, S. solidus increases host activity to facilitate transmission. If successful, this host manipulation is necessarily fatal for the host. I selected the copepod Macrocyclops albidus, a first intermediate host of S. solidus, for resistance or susceptibility to host manipulation to investigate their evolvability. Selection on the host indeed increased host manipulation in susceptible and reduced host manipulation in resistant selection lines. Interestingly, this seemed to be at least partly due to changes in the baseline levels of the modified trait (activity) rather than actual changes in resistance or susceptibility to host manipulation. Hence, hosts seem restricted in how rapidly and efficiently they can evolve resistance to host manipulation.     

The effect of spatial heterogeneity and parasites on the evolution of host diversity

Both spatial heterogeneity and exploiters (parasites and predators) have been implicated as key ecological factors driving population diversification. However, it is unclear how these factors interact. We addressed this question using the common plant-colonizing bacterium Pseudomonas fluorescens, which has been shown to diversify rapidly into spatial niche-specialist genotypes when propagated in laboratory microcosms. Replicate populations were evolved in spatially homogeneous and heterogeneous environments (shaken and static microcosms, respectively) with and without viral parasites (bacteriophage) for approximately 60 bacterial generations. Consistent with previous findings, exploiters reduced diversity in heterogeneous environments by relaxing the intensity of resource competition. By contrast, exploiters increased diversity in homogeneous environments where there was little diversification through resource competition. Competition experiments revealed this increase in diversity to be the result of fitness trade-offs between exploiter resistance and competitive ability. In both environments, exploiters increased allopatric diversity, presumably as a result of divergent selection for resistance between populations. Phage increased total diversity in homogeneous environments, but had no net effect in heterogeneous environments. Such interactions between key ecological variables need to be considered when addressing diversification and coexistence in future studies.     

Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

The evolution game

Theories of human evolution should be so constituted that they promote progress. This has not been the case in the past, as vividly shown in the controversies over the Taung skull. The “facts” of human evolution are so uncertain that it may be best to regard the study of human evolution as a game, rather than as a science.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation

Parasite survival in hosts mainly depends on the capacity to circumvent the host immune response. Acanthocephalan infections in gammarids are linked with decreased activity of the prophenoloxidase (ProPO) system, suggesting an active immunosuppression process. Nevertheless, experimental evidence for this hypothesis is lacking: whether these parasites affect several immune pathways is unknown and the consequences of such immune change have not been investigated. In particular, the consequences for other pathogens are not known; neither are the links with other parasite-induced manipulations of the host. Firstly, using experimental infections of Pomphorhynchus laevis we confirmed that the lower immune activity in parasitised Gammarus pulex is induced by the parasite infection. Second, using natural infections of three different parasites, P. laevis, Pomphorhynchus tereticollis and Polymorphus minutus, we showed that acanthocephalan infection was associated with reduction of the activity of the ProPO system and the haemocyte concentration (two major parameters of crustacean immunity) suggesting that immune depression is a phenomenon affecting several immunological activities. This was confirmed by the fact that acanthocephalan infection (whatever the parasite species) was linked to a lower efficiency to eliminate a bacterial infection. The result suggests a cost of parasite immune depression. Finally, acanthocephalans are also known to induce behavioural alterations in the intermediate host which favour their transmission to definitive hosts. We did not find any correlation between behavioural and immunological alterations in both experimentally and naturally-infected gammarids. Overall, this study suggests that whilst immune depression might be beneficial to acanthocephalan survival within the intermediate gammarid host, it might also be costly if it increases host mortality to additional infections before transmission of the parasite.