Females that experience threat are better teachers

Superb fairy-wren (Malurus cyaneus) females use an incubation call to teach their embryos a vocal password to solicit parental feeding care after hatching. We previously showed that high call rate by the female was correlated with high call similarity in fairy-wren chicks, but not in cuckoo chicks, and that parent birds more often fed chicks with high call similarity. Hosts should be selected to increase their defence behaviour when the risk of brood parasitism is highest, such as when cuckoos are present in the area. Therefore, we experimentally test whether hosts increase call rate to embryos in the presence of a singing Horsfield''s bronze-cuckoo (Chalcites basalis). Female fairy-wrens increased incubation call rate when we experimentally broadcast cuckoo song near the nest. Embryos had higher call similarity when females had higher incubation call rate. We interpret the findings of increased call rate as increased teaching effort in response to a signal of threat.     

Colony pace: a life-history trait affecting social insect epidemiology

Among colonies of social insects, the worker turnover rate (colony ‘pace’) typically shows considerable variation. This has epidemiological consequences for parasites, because in ‘fast-paced’ colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.     

Impact of a social parasite on ant host populations depends on host species,habitat and year

Parasites often affect the abundance and life‐history traits of their hosts. We studied the impact of a social parasite – a slavemaking ant – on host ant communities using two complementary field manipulations. In the first experiment, we analysed the effect of social parasite presence on host populations in one habitat. In a second experiment, conducted in two habitats, we used a cross‐fostering design, analysing the effect of sympatric and allopatric social parasites. In the first experiment, host colonies benefited to some extent from residing in parasite‐free areas, showing increased total production. Yet, in the second experiment, host colonies in plots containing social parasites were more productive, and this effect was most evident in response to allopatric social parasites. We propose several explanations for these inconsistent results, which are related to environmental variability. The discrepancies between the two habitats can be explained well by ecological variation as a result of differences in altitudes and climate. For example, ant colonies in the colder habitat were larger and, for one host species, colonies were more often polygynous. In addition, our long‐term documentation – a total of four measurements of community structure in 6 years – showed temporal variation in abundance and life‐history traits of ant colonies, unrelated to the manipulations. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 559–570.     

Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics

Elevated risk of disease transmission is considered a major cost of sociality, although empirical evidence supporting this idea remains scant. Variation in spatial cohesion and the occurrence of social interactions may have profound implications for patterns of interindividual parasite transmission. We used a social network approach to shed light on the importance of different aspects of group-living (i.e. within-group associations versus physical contact) on patterns of parasitism in a neotropical primate, the brown spider monkey (Ateles hybridus), which exhibits a high degree of fission–fusion subgrouping. We used daily subgroup composition records to create a ‘proximity’ network, and built a separate ‘contact’ network using social interactions involving physical contact. In the proximity network, connectivity between individuals was homogeneous, whereas the contact network highlighted high between-individual variation in the extent to which animals had physical contact with others, which correlated with an individual''s age and sex. The gastrointestinal parasite species richness of highly connected individuals was greater than that of less connected individuals in the contact network, but not in the proximity network. Our findings suggest that among brown spider monkeys, physical contact impacts the spread of several common parasites and supports the idea that pathogen transmission is one cost associated with social contact.     

Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance

The evolutionary interactions between permanently social parasiticspecies and their hosts are of special interest because socialparasites are not only closely dependent on, but are also closelyrelated to, their hosts. The small European slavemaker Harpagoxenussublaevis has evolved several characters that help manipulateits host. In this study we investigated adaptations of thissocial parasite to its local hosts and the geographic patternof host resistance in two main host species from three differentpopulations. In behavioral experiments, we examined whetherhost colonies from three geographically distant Leptothoraxacervorum populations varied in their ability to defend thenest against social parasites. Naive colonies from the unparasitizedEnglish population killed attacking slavemakers more often thandid host colonies from two parasitized populations. We alsofound strong interpopulation variation in the ability of theslavemaker to manipulate host behavior. H. sublaevis uses theDufour gland secretion to induce intracolonial fights and, ingeneral, this "propaganda" substance was most effective againstlocal hosts. Our results suggest that the social parasite isleading the arms race in this aspect. Similar experiments uncovereddifferences between two populations of the second host speciesL. muscorum and could demonstrate that nest defense in bothhost species is similarly efficient. In L. acervorum, monogynouscolonies were more successful in nest defense, whereas socialstructure had no impact in L. muscorum. Colony size did notaffect the efficacy of nest defense in either host species.The caste of the slavemaker had a strong influence on the successof an attack.     

Wildfires modify the parasite loads of invasive cane toads

The frequency and severity of wildfires are increasing due to anthropogenic modifications to habitats and to climate. Post-fire landscapes may advantage invasive species via multiple mechanisms, including changes to host–parasite interactions. We surveyed the incidence of endoparasitic lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Rhinella marina) in near-coastal sites of eastern Australia, a year after extensive fires in this region. Both the prevalence of infection and number of worms in infected toads increased with toad body size in unburned areas. By contrast, parasite load decreased with toad body size in burned areas. By killing moisture-dependent free-living lungworm larvae, the intense fires may have liberated adult cane toads from a parasite that can substantially reduce the viability of its host. Smaller toads, which are restricted to moist environments, did not receive this benefit from fires.     

Temperature effects on parasite prevalence in a natural hybrid complex

Both host susceptibility and parasite infectivity commonly have a genetic basis, and can therefore be shaped by coevolution. However, these traits are often sensitive to environmental variation, resulting in genotype-by-environment interactions. We tested the influence of temperature on host–parasite genetic specificity in the Daphnia longispina hybrid complex, exposed to the protozoan parasite Caullerya mesnili. Infection rates were higher at low temperature. Furthermore, significant differences between host clones, but not between host taxa, and a host genotype-by-temperature interaction were observed.     

The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment

While avian chronic haemoparasite infections induce reproductive costs, infection has not previously been shown to affect survival. Here, we experimentally reduced, through medication, the intensity of infection by Haemoproteus parasites in wild-breeding female blue tits Cyanistes caeruleus. However, this treatment did not reduce the intensity of infection in males or the intensity of infection by Leucocytozoon. Medicated females, but not males, showed increased local survival until the next breeding season compared with control birds. To our knowledge, this is the first empirical evidence showing long-term direct survival costs of chronic Haemoproteus infections in wild birds.     

Opposing effects of allogrooming on disease transmission in ant societies

To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour—either performed towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host–pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host–pathogen systems.     

Disappearance of eggs from nonparasitized nests of brood parasite hosts: the evolutionary equilibrium hypothesis revisited

The evolutionary equilibrium hypothesis was proposed to explain variation in egg rejection rates among individual hosts (intra‐ and interspecific) of avian brood parasites. Hosts may sometimes mistakenly reject own eggs when they are not parasitized (i.e. make recognition errors). Such errors would incur fitness costs and could counter the evolution of host defences driven by costs of parasitism (i.e. creating equilibrium between acceptors and rejecters within particular host populations). In the present study, we report the disappearance of host eggs from nonparasitized nests in populations of seven actual and potential hosts of the common cuckoo Cuculus canorus. Based on these data, we calculate the magnitude of the balancing parasitism rate provided that all eggs lost are a result of recognition errors. Importantly, because eggs are known to disappear from nests for reasons other than erroneous host rejection, our data represent the maximum estimates of such costs. Nonetheless, the disappearance of eggs was a rare event and therefore incurred low costs compared to the high costs of parasitism. Hence, costs as a result of recognition errors are probably of minor importance with respect to opposing selective pressure for the evolution of egg rejection in these hosts. We cannot exclude the possibility that low or intermediate egg rejection rates in some host populations may be caused by spatiotemporal variation in the occurrence of parasitism and gene flow, creating a variable influence of opposing costs as a result of recognition errors and the costs of parasitism.     

Crowding does not affect monarch butterflies’ resistance to a protozoan parasite

Host density is an important factor when it comes to parasite transmission and host resistance. Increased host density can increase contact rate between individuals and thus parasite transmission. Host density can also cause physiological changes in the host, which can affect host resistance. Yet, the direction in which host density affects host resistance remains unresolved. It is also unclear whether food limitation plays a role in this effect. We investigated the effect of larval density in monarch butterflies, Danaus plexippus, on the resistance to their natural protozoan parasite Ophryocystis elektroscirrha under both unlimited and limited food conditions. We exposed monarchs to various density treatments as larvae to mimic high densities observed in sedentary populations. Data on infection and parasite spore load were collected as well as development time, survival, wing size, and melanization. Disease susceptibility under either food condition or across density treatments was similar. However, we found high larval density impacted development time, adult survival, and wing morphology when food was limited. This study aids our understanding of the dynamics of environmental parasite transmission in monarch populations, which can help explain the increased prevalence of parasites in sedentary monarch populations compared to migratory populations.     

Variation in parasite resistance of Arctic charr,Salvelinus alpinus,between and within sympatric morphs

Genetic variation in resistance against parasite infections is a predominant feature in host–parasite systems. However, mechanisms maintaining genetic polymorphism in resistance in natural host populations are generally poorly known. We explored whether differences in natural infection pressure between resource‐based morphs of Arctic charr (Salvelinus alpinus) have resulted in differentiation in resistance profiles. We experimentally exposed offspring of two morphs from Lake Þingvallavatn (Iceland), the pelagic planktivorous charr (“murta”) and the large benthivorous charr (“kuðungableikja”), to their common parasite, eye fluke Diplostomum baeri, infecting the eye humor. We found that there were no differences in resistance between the morphs, but clear differences among families within each morph. Moreover, we found suggestive evidence of resistance of offspring within families being positively correlated with the parasite load of the father, but not with that of the mother. Our results suggest that the inherited basis of parasite resistance in this system is likely to be related to variation among host individuals within each morph rather than ecological factors driving divergent resistance profiles at morph level. Overall, this may have implications for evolution of resistance through processes such as sexual selection.     

Disease ecology across soil boundaries: effects of below-ground fungi on above-ground host–parasite interactions

Host–parasite interactions are subject to strong trait-mediated indirect effects from other species. However, it remains unexplored whether such indirect effects may occur across soil boundaries and connect spatially isolated organisms. Here, we demonstrate that, by changing plant (milkweed Asclepias sp.) traits, arbuscular mycorrhizal fungi (AMF) significantly affect interactions between a herbivore (the monarch butterfly Danaus plexippus) and its protozoan parasite (Ophryocystis elektroscirrha), which represents an interaction across four biological kingdoms. In our experiment, AMF affected parasite virulence, host resistance and host tolerance to the parasite. These effects were dependent on both the density of AMF and the identity of milkweed species: AMF indirectly increased disease in monarchs reared on some species, while alleviating disease in monarchs reared on other species. The species-specificity was driven largely by the effects of AMF on both plant primary (phosphorus) and secondary (cardenolides; toxins in milkweeds) traits. Our study demonstrates that trait-mediated indirect effects in disease ecology are extensive, such that below-ground interactions between AMF and plant roots can alter host–parasite interactions above ground. In general, soil biota may play an underappreciated role in the ecology of many terrestrial host–parasite systems.     

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

Yellow warblers (Setophaga petechia) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds (Molothrus ater). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.     

The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism

In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.     

Nematode endoparasites do not codiversify with their stick insect hosts

Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.     

The ecological success of a social parasite increases with manipulation of collective host behaviour

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite‐induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour‐treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker‐induced nestmate attack. Slavemakers benefited from altering their hosts’ aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker‐induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T. curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T. longispinosus. Our findings highlight that large‐scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.     

A chemical level in the coevolutionary arms race between an ant social parasite and its hosts

Here we investigate the coevolutionary interactions between the slavemaking ant Protomognathus americanus and its Temnothorax hosts on a chemical level. We show that, although this social parasite is principally well-adapted to its hosts' cuticular hydrocarbon profile, there are pronounced differences in the fine-tuning of this adaptation. Between populations, chemical adaptation varies with host community composition, as the parasite faces a trade-off when confronted with more than one host species. In addition to adaptation of its own chemical signature, the slavemaker causes a reciprocal adjustment in its slaves' cuticular profile, the degree of which depends on the slave species. On the host side, successful parasite defence requires efficient enemy recognition, and in behavioural aggression trials, host colonies could indeed discriminate between invading slaves, which commonly accompany slavemakers on raids, and free-living conspecifics. Furthermore, hosts shifted their acceptance threshold over the seasons, presumably to reduce the costs of defence.