EVOLUTION OF INCOMPATIBILITY-INDUCING MICROBES AND THEIR HOSTS

In many insect species, males infected with microbes related to Wolbachia pipientis are “incompatible” with uninfected females. Crosses between infected males and uninfected females produce significantly fewer adult progeny than the other three possible crosses. The incompatibility-inducing microbes are usually maternally transmitted. Thus, incompatibility tends to confer a reproductive advantage on infected females in polymorphic populations, allowing these infections to spread. This paper analyzes selection on parasite and host genes that affect such incompatibility systems. Selection among parasite variants does not act directly on the level of incompatibility with uninfected females. In fact, selection favors rare parasite variants that increase the production of infected progeny by infected mothers, even if these variants reduce incompatibility with uninfected females. However, productivity-reducing parasites that cause partial incompatibility with hosts harboring alternative variants can be favored once they become sufficiently abundant locally. Thus, they may spread spatially by a process analogous to the spread of underdominant chromosome rearrangements. The dynamics of modifier alleles in the host are more difficult to predict, because such alleles will occur in both infected and uninfected individuals. Nevertheless, the relative fecundity of infected females compared to uninfected females, the efficiency of maternal transmission and the mutual compatibility of infected individuals all tend to increase under within-population selection on both host and parasite genes. In addition, selection on host genes favors increased compatibility between infected males and uninfected females. Although vertical transmission tends to harmonize host and parasite evolution, competition among parasite variants will tend to maintain incompatibility.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Social organization in a flatworm: trematode parasites form soldier and reproductive castes

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of ‘parthenitae’ within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the ‘recognition of self’ and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.     

Effects of avian malaria on male behaviour and female visitation in lekking blue‐crowned manakins

Avian malaria, the infection by blood parasites of the genus Plasmodium, can reduce host fitness not only through mortality, but also by impairing the expression of sexual selection traits. Although different studies highlight the association of parasitism with a decrease in host reproductive success, few studies have addressed the role of parasites in honest signalling by lekking species. Hence, it is still uncertain which fitness components are affected by parasites in these species. We investigated whether avian malaria is associated with a decrease in mating behaviour of male blue‐crowned manakins Lepidothrix coronata and whether it affects female visitation in leks of a population in the central Amazon. Through behavioural observations, we estimated the rates of total male activity and social interaction, as well as the frequency of female visits at individual perches. We then examined if individuals were infected with Plasmodium spp. using molecular techniques. Avian malaria was associated with a decrease in male mating behaviour in each lek, and mating behaviour correlated with female visitation. Although rates of social interaction were not correlated with avian malaria among males, we observed that interacting with several individuals within a lek may be advantageous for males, as they also vocalized and displayed more, thus increasing their chances of being visited by females. Although female visitation was not associated with avian malaria in individuals or leks, it is still possible that female visitation is indirectly affected by avian malaria through the latter's effects on male activity. We suggest a role for male activity as an honest sexual signal for females. Thus, male display rate could be used by females as cue for the probability of a male being infected.     

Epizootiology of blood parasites in an Australian lizard: a mark-recapture study of a natural population

The dynamics of a naturally endemic blood parasite (Hepatozoon hinuliae) were studied in a lizard (Eulamprus quoyii) host population, using 2 years of longitudinal data. We investigated how parasite abundance in the population varied over time, examined whether certain host sub-populations were more prone to infection, and compared parasite loads in relation to host reproductive behaviour. We recorded blood parasite infections of 331 individuals, obtained in 593 captures. Prevalence (the proportion of the host population infected) of blood parasites was high; approximately 66% of the lizard population was infected. Probability of infection increased with host age and size, but did not differ between the sexes. Within individuals, parasite load (the intensity of infection within individuals) did not vary over time, and was independent of host reproductive behaviour. Parasite load was significantly higher in males compared to females.     

Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae)

Because of their effects on host reproductive behaviour, parasites are theoretically expected to create sometimes assortative mating among hosts, with heavily parasitized individuals pairing together and lightly parasitized ones pairing among themselves. We investigated the influence of protozoan gut parasites on the pairing pattern of the chrysomelid beetle Timarcha maritima. In the field, fecundity was negatively correlated with the parasite load of females, unpaired males were significantly more heavily infected than paired ones and, among pairs, males and females were matched for parasite load. Mate choice experiments in the laboratory showed that males have some ability to avoid heavily infected partners when given the choice between two females. Male competitiveness, measured as their mobility, was also negatively correlated with parasite load. These results indicate that parasite-related assortative pairing in this beetle could result from parasitized females being less fecund and parasitized males less competitive.     

Infection of the fittest: devil facial tumour disease has greatest effect on individuals with highest reproductive output

Emerging infectious diseases rarely affect all members of a population equally and determining how individuals’ susceptibility to infection is related to other components of their fitness is critical to understanding disease impacts at a population level and for predicting evolutionary trajectories. We introduce a novel state‐space model framework to investigate survival and fecundity of Tasmanian devils (Sarcophilus harrisii) affected by a transmissible cancer, devil facial tumour disease. We show that those devils that become host to tumours have otherwise greater fitness, with higher survival and fecundity rates prior to disease‐induced death than non‐host individuals that do not become infected, although high tumour loads lead to high mortality. Our finding that individuals with the greatest reproductive value are those most affected by the cancer demonstrates the need to quantify both survival and fecundity in context of disease progression for understanding the impact of disease on wildlife populations.     

Complex dynamics of a predator–prey–parasite system: An interplay among infection rate,predator's reproductive gain and preference

Parasites are considered as an important factor in regulating their host populations through trait-mediated effects. On the other hand, predation becomes particularly interesting in host–parasite systems because predation can significantly alter the abundance of parasites and their host population. The combined effects of parasites and predator on host population and community structure therefore may have larger effect. Different field experiments confirm that predators consume disproportionately large number of infected prey in comparison to their susceptible counterpart. There are also substantial evidences that predator has the ability to distinguish prey that have been infected by a parasite and avoid such prey to reduce fitness cost. In this paper we study the predator–prey dynamics, where the prey species is infected by some parasites and predators consume both the susceptible and infected prey with some preference. We demonstrate that complexity in such systems largely depends on the predator's selectivity, force of infection and predator's reproductive gain. If the force of infection and predator's reproductive gain are low, parasites and predators both go to extinction whatever be the predator's preference. The story may be totally different in the opposite case. Survival of species in stable, oscillatory or chaotic states, and their extinction largely depend on the predator's preference. The system may also show two coexistence equilibrium points for some parameter values. The equilibrium with lower susceptible prey density is always stable and the equilibrium with higher susceptible prey density is always unstable. These results suggest that understanding the consequences of predator's selectivity or preference may be crucial for community structure involving parasites.     

The effect of the acanthocephalan parasite Pomphorhynchus laevis on the lipid and glycogen content of its intermediate host Gammarus pulex

Besides conspicuous changes in behaviour, manipulative parasites may also induce subtle physiological effects in the host that may also be favourable to the parasite. In particular, parasites may be able to influence the re-allocation of resources in their own favour. We studied the association between the presence of the acanthocephalan parasite, Pomphorhynchus laevis, and inter-individual variation in the lipid and glycogen content of its crustacean host, Gammarus pulex (Amphipoda). Infected gravid females had significantly lower lipid contents than uninfected females, but there was no difference in the lipid contents of non-gravid females and males that were infected with P. laevis. In contrast, we found that all individuals that were parasitised by P. laevis had significantly increased glycogen contents, independent of their sex and reproductive status. We discuss our results in relation to sex-related reproductive strategies of hosts, and the influence they may have on the level of conflict over energy allocation between the host and the parasite.     

Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host

Parasitic infection has a direct physiological cost to hosts but may also alter how hosts interact with other individuals in their environment. Such indirect effects may alter both host fitness and the fitness of other individuals in the host''s social network, yet the relative impact of direct and indirect effects of infection are rarely quantified. During reproduction, a host''s social environment includes family members who may be in conflict over resource allocation. In such situations, infection may alter how resources are allocated, thereby redistributing the costs of parasitism between individuals. Here, we experimentally reduce parasite burdens of parent and/or nestling European shags (Phalacrocorax aristotelis) infected with Contracaecum nematodes in a factorial design, then simultaneously measure the impact of an individual''s infection on all family members. We found no direct effect of infection on parent or offspring traits but indirect effects were detected in all group members, with both immediate effects (mass change and survival) and longer-term effects (timing of parents’ subsequent breeding). Our results show that parasite infection can have a major impact on individuals other than the host, suggesting that the effect of parasites on population processes may be greater than previously thought.     

RESISTANCE IS FUTILE BUT TOLERANCE CAN EXPLAIN WHY PARASITES DO NOT ALWAYS CASTRATE THEIR HOSTS

The disease caused by parasites and pathogens often causes sublethal effects that reduce host fecundity. Theory suggests that if parasites can "target" the detrimental effects of their growth on either host mortality or fecundity, they should always fully sterilize. This is because a reduction in host fecundity does not reduce the infectious period and is therefore neutral to a horizontally transmitted infectious organism. However, in nature fully castrating parasites are relatively rare, no doubt in part because of defense mechanisms in the host. Here, we examine in detail the evolution of host defense to the sterilizing effects of parasites and show that intermediate levels of sterility tolerance are found to evolve for a wide range of cost structures. Our key result arises when the host and parasite coevolve. Investment in tolerance by the host may prevent castration, but if host defense is through resistance (by controlling the parasite's growth rate) coevolution by the parasite results in the complete loss of infected host fecundity. Resistance is therefore a waste of resources, but tolerance can explain why parasites do not castrate their hosts. Our results further emphasize the importance of tolerance as opposed to resistance to parasites.     

The ecology of host immune responses to chronic avian haemosporidian infection

Host responses to parasitism in the wild are often studied in the context of single host–parasite systems, which provide little insight into the ecological dynamics of host–parasite interactions within a community. Here we characterized immune system responses to mostly low-intensity, chronic infection by haemosporidian parasites in a sample of 424 individuals of 22 avian host species from the same local assemblage in the Missouri Ozarks. Two types of white blood cells (heterophils and lymphocytes) were elevated in infected individuals across species, as was the acute-phase protein haptoglobin, which is associated with inflammatory immune responses. Linear discriminant analysis indicated that individuals infected by haemosporidians occupied a subset of the overall white blood cell multivariate space that was also occupied by uninfected individuals, suggesting that these latter individuals might have harbored other pathogens or that parasites more readily infect individuals with a specific white blood cell profile. DNA sequence-defined lineages of haemosporidian parasites were sparsely distributed across the assemblage of hosts. In one well-sampled host species, the red-eyed vireo (Vireo olivaceus), heterophils were significantly elevated in individuals infected with one but not another of two common parasite lineages. Another well-sampled host, the yellow-breasted chat (Icteria virens), exhibited no differences in immune response to different haemosporidian lineages. Our results indicate that while immune responses to infection may be generalized across host species, parasite-specific immune responses may also occur.     

Dynamic changes in host–virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta)

The dynamics of host – parasite interactions can change dramatically over the course of a chronic infection as the internal (physiological) and external (environmental) conditions of the host change. When queens of social insects found a colony, they experience changes in both their physiological state (they develop their ovaries and begin laying eggs) and the social environment (they suddenly stop interacting with the other members of the mother colony), making this an excellent model system for examining how these factors interact with chronic infections. We investigated the dynamics of host – viral interactions in queens of Solenopsis invicta (fire ant) as they transition from mating to colony founding/brood rearing to the emergence of the first workers. We examined these dynamics in naturally infected queens in two different social environments, where queens either founded colonies as individuals or as pairs. We hypothesized that stress associated with colony founding plays an important role in the dynamics of host – parasite interactions. We also hypothesized that different viruses have different modalities of interaction with the host that can be quantified by physiological measures and genomic analysis of gene expression in the host. We found that the two most prevalent viruses, SINV‐1 and SINV‐2, are associated with different fitness costs that are mirrored by different patterns of gene expression in the host. In fact SINV‐2, the virus that imposes the significant reduction of a queen's reproductive output is also associated with larger changes of global gene expression in the host. These results show the complexity of interactions between S. invicta and two viral parasites. Our findings also show that chronic infections by viral parasites in insects are dynamic processes that may pose different challenges in the host, laying the groundwork for interesting ecological and evolutionary considerations.     

Parasitic castration: a perspective from a model of dynamic energy budgets

Models of the evolution of virulence have typically focusedon increased mortality, one of two negative effects that parasitescan inflict on their host. Those that consider the other effect,fecundity reduction, can predict that parasites should completelysterilize their hosts. Although this prediction seems extreme,sterilization features prominently in a fascinating strategy,parasitic castration. Such castration can be accompanied bygigantism (unusually large growth of infected hosts), long infectiousperiods, and fecundity compensation (where, before heavy parasiteburdens ensue, newly infected hosts reproduce earlier/more thanthey would if not infected). Using a model of dynamic energybudgets (DEB), we show how these results readily emerge, assumingthat parasites consume energy reserves of the host. The simple,but mechanistic, DEB model follows energy flow though hostsand parasites, starting with ingestion, and continuing withstorage of assimilated energy, and use of those reserves forgrowth and reproduction, as allocated by the host accordingto the "-rule". Using this model, we compare and contrast twostrategies for parasites. "Consumers" only steal energy fromtheir hosts, thereby indirectly altering allocation of energyto growth and reproduction, reducing fecundity, and enhancingmortality. "Castrators" steal energy but also directly modifythe scheme by which hosts allocate reserve energy, shuntingresources from reproduction to growth. Not surprisingly, themodel predicts that this strategy should promote gigantism,but it also forecasts longer infectious periods and fecunditycompensation. Thus, commonly observed characteristics of parasiticcastration readily emerge from a mechanistic model of energyflow using a minimal number of assumptions. Finally, the DEBmodel for both "consumers" and "castrators" highlight that variationin resources supplied to hosts promotes variation in virulencein a given host-parasite system, holding all else equal. Suchpredictions highlight the potential importance of resource ecologyfor virulence in disease systems.     

Avian malaria is associated with increased reproductive investment in the blue tit

Haemosporidians causing avian malaria are very common parasites among bird species. Their negative effects have been repeatedly reported in terms of deterioration in survival prospects or reproductive success. However, a positive association between blood parasites and avian fitness has also been reported. Here, we studied a relationship between presence of malaria parasites and reproductive performance of the host, a hole‐breeding passerine – the blue tit Cyanistes caeruleus. Since the malaria parasites might affect their hosts differently depending on environmental conditions, we performed brood size manipulation experiment to differentiate parental reproductive effort and study the potential interaction between infection status and brood rearing conditions on reproductive performance. We found individuals infected with malaria parasites to breed later in the season in comparison with uninfected birds, but no differences were detected in clutch size. Interestingly, infected parents produced heavier and larger offspring with stronger reaction to phytohemagglutinin. More importantly, we found a significant interaction between infection status and brood size manipulation in offspring tarsus length and reaction to phytohemagglutinin: presence of parasites had stronger positive effect among birds caring for experimentally enlarged broods. Our results might be interpreted either in the light of the parasite‐mediated selection or terminal investment hypothesis.     

Reproductive compensation

The reproductive compensation hypothesis says that individuals constrained by ecological or social forces to reproduce with partners they do not prefer compensate for likely offspring viability deficits. The reproductive compensation hypothesis assumes that (i) pathogens and parasites evolve more rapidly than their hosts, (ii) mate preferences predict variation in health and viability of offspring, (iii) social and ecological factors keep some individuals from mating with their preferred partners (some are constrained to mate with partners they do not prefer), (iv) all individuals may be induced to compensate, so that (v) variation in compensation is due to environmental and developmental factors affecting between-individual abilities to express compensatory mechanisms. Selection favouring compensation may act through variation in prezygotic physiological mechanisms, zygotic mechanisms, or parental care to eggs or young that enhance offspring health, increasing the likelihood that some offspring survive to reproductive age, often at a survival cost to the parents. Compensation may be through increased number of eggs laid or offspring born, a compensatory effort working during a single reproductive bout that sometimes will match the number of offspring surviving to reproductive age produced by unconstrained parents during the same bout. The reproductive compensation hypothesis therefore predicts trade-offs in components of fitness for breeders, such that parents constrained to mating with a nonpreferred partner, but who compensate sometimes match their current productivity (number of offspring at reproductive age) to unconstrained parents (those breeding with their preferred partners), and, when all else is equal, die faster than unconstrained parents. The reproductive compensation hypothesis emphasizes that reproductive competition is not just between constrained and unconstrained individuals, but also among constrained individuals who do and do not compensate. The reproductive compensation hypothesis may thus explain previously unexplained between-population and within-population, between-individual variation in reproductive success, survival, physiology and behaviour.     

Proximate Determinants of Reproductive Skew in Polygyne Colonies of the Ant Formica fusca

Understanding the determinants of reproductive skew (the partitioning of reproduction among co‐breeding individuals) is one of the major questions in social evolution. In ants, multiple‐queen nests are common and reproductive skew among queens has been shown to vary tremendously both within and between species. Proximate determinants of skew may be related to both queen and worker behaviour. Queens may attempt to change their reproductive share through dominance interactions, egg eating and by changing individual fecundity. Conversely, workers are in a position to regulate the reproductive output of queens when rearing the brood. This paper investigates queen behaviour at the onset of egg laying and the effect of queen fecundity and worker behaviour on brood development and reproductive shares of multiple queens in the ant Formica fusca. The study was conducted in two‐queen laboratory colonies where the queens produced only worker offspring. The results show that in this species reproductive apportionment among queens is not based on dominance behaviour and aggression, but rather on differences in queen fecundity. We also show that, although the queen fecundity at the onset of brood rearing is a good indicator of her final reproductive output, changes in brood composition occur during brood development. Our results highlight the importance of queen fecundity as a major determinant of her reproductive success. They furthermore suggest that in highly derived polygyne species, such as the Formica ants, direct interactions as a means for gaining reproductive dominance have lost their importance.     

Effects of parasites on fish behaviour: a review and evolutionary perspective

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of these parasites are passed directly between ultimate hosts, others need to navigate through a series of intermediate hosts before reaching a host in (or on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten by specific predators to ensure transmission, has renewed interest in the evolutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and parasitic infections have been demonstrated to have consequences for almost every aspect of fish behaviour. Despite a scarcity of knowledge regarding the mechanistic basis of such behaviour changes in most cases, and an even lower understanding of their ecological consequences, there can be little doubt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency, time budget, habitat selection, competitive ability, predator-prey relationships, swimming performance and sexual behaviour and mate choice have all been associated with – and in some cases been shown to be a result of – parasite infections, and are reviewed here in some detail. Since the behavioural consequences of infections are exposed to evolutionary selection pressures in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found little conclusive evidence for the Parasite Increased Trophic Transmission (PITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of the many behavioural changes described have rarely been quantified, their evolutionary and ecological significance is effectively unknown.Potential hosts may also change their behaviour in the presence of infective parasite stages, if they adopt tactics to reduce exposure risk. Such `behavioural resistance', which may take the form of habitat avoidance, prey selectivity or avoidance of infected individuals, can be viewed as behavioural change associated with the threat of being parasitised, and so is included here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, although the efficacy of the latter as a parasite removal strategy is currently subject to a good deal of debate.The effects parasites have on shoaling behaviour of host fish have attracted a good deal of attention from researchers, and we have provided a case study to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individual's foraging ability. It therefore seems unsurprising that, in a number of species avoidance of parasitised individuals has evolved which may explain the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tendency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for parasitised hosts and their parasites are not always easy to predict, yet an understanding of these is important before we can make predictions regarding the ecological impact of infections on host fish populations.Clearly, there remain many gaps in our knowledge regarding the effects of parasites on the behaviour of host fish. We believe that a much greater understanding of the importance of infection-associated behaviour changes in fish could be gained from high quality research in comparatively few areas. We have completed our review by highlighting the key research topics that we believe should attract new research in this field.     

Rodent sociality and parasite diversity

The risk of parasitism is considered to be a general cost of sociality and individuals living in larger groups are typically considered to be more likely to be infected with parasites. However, contradictory results have been reported for the relationship between group size and infection by directly transmitted parasites. We used independent contrasts to examine the relationship between an index of sociality in rodents and the diversity of their macroparasites (helminths and arthropods such as fleas, ticks, suckling lice and mesostigmatid mites). We found that the species richness of directly transmitted ectoparasites, but not endoparasites, decreased significantly with the level of rodent sociality. A greater homogeneity in the biotic environment (i.e. a reduced number of cohabiting host species) of the more social species may have reduced ectoparasites' diversity by impairing ectoparasites transmission and exchange. Our finding may also result from beneficial outcomes of social living that include behavioural defences, like allogrooming, and the increased avoidance of parasites through dilution effects.