Host–parasite genotypic interactions in the honey bee: the dynamics of diversity

Parasites are thought to be a major driving force shaping genetic variation in their host, and are suggested to be a significant reason for the maintenance of sexual reproduction. A leading hypothesis for the occurrence of multiple mating (polyandry) in social insects is that the genetic diversity generated within‐colonies through this behavior promotes disease resistance. This benefit is likely to be particularly significant when colonies are exposed to multiple species and strains of parasites, but host–parasite genotypic interactions in social insects are little known. We investigated this using honey bees, which are naturally polyandrous and consequently produce genetically diverse colonies containing multiple genotypes (patrilines), and which are also known to host multiple strains of various parasite species. We found that host genotypes differed significantly in their resistance to different strains of the obligate fungal parasite that causes chalkbrood disease, while genotypic variation in resistance to the facultative fungal parasite that causes stonebrood disease was less pronounced. Our results show that genetic variation in disease resistance depends in part on the parasite genotype, as well as species, with the latter most likely relating to differences in parasite life history and host–parasite coevolution. Our results suggest that the selection pressure from genetically diverse parasites might be an important driving force in the evolution of polyandry, a mechanism that generates significant genetic diversity in social insects.     

Aphid parasites (Hym., Aphidiidæ) and their relationship to aphid attending ants,with respect to biological control

The author's results of the research on the relationship of aphid parasites to aphid attending ants based both on the study of taxonomy and ecology of the parasites (Hym., Aphidiidæ) have shown that the parasites are disregarded by the aphid attending ants. The ant attendance of the host aphid does not influence the parasite specificity. In biological control praxis, in case of experiments on introduced parasites of pest aphid establishment, the ant attendance, however, is but recommended to be also considered.     

Ant‐following and the prevalence of blood parasites in birds of African rainforests

Blood parasites are widespread in birds, several are pathogenic and may affect the fitness of their hosts, and their evolution. By reanalyzing recently published data I show that parts of the variation in prevalences of parasites in the blood of African rainforest birds and the occurrence of similar or same parasite haplotypes in rather unrelated birds are well understood when considering the ecological aspects of foraging of some of these birds. Specialized ant‐following birds, which regularly follow the massive swarm raids of army ants and feed on insects flushed by the ants, have higher prevalences of nematode microfilariae (~10×), Trypanosoma (~10×), and Plasmodium parasites (~2×) and a much higher probability of infection with multiple parasites than other birds. Moreover, birds regularly attending army ant swarms share identical Trypanosoma haplotypes and show genetically similar microfilariae haplotypes. I conclude that ant‐following increases the probability of birds to get infected with blood parasites and may facilitate the switch of a parasite species from one host species to another. The costs of higher parasite intensities involved when specializing on following ant swarms may have influenced the evolution of foraging behaviour in birds of African rainforests and may help to explain the relatively low number of specialized ant‐following bird species on the African continent.     

Ant cues affect the oviposition behaviour of fruit flies (Diptera: Tephritidae) in Africa

Abstract. Although most studies on fruit fly oviposition behaviour focus on horizontal interactions with competitors and cues from host plants, vertical interactions with predators are poorly documented. The present study provides direct evidence indicating that the oviposition behaviour of the two main mango fruit fly species, Ceratitis cosyra (Walker) and Bactrocera invadens Drew‐Tsurata & White, is affected by secretions of the dominant arboreal ant Oecophylla longinoda (Latreille). When offered ant‐exposed and unexposed mangoes in the absence of the ants, both fly species are reluctant to land on ant‐exposed fruits and, when having landed, often take off quickly and fail to oviposit. The number of puparia collected from unexposed mangoes is approximately eight‐fold higher than from ant‐exposed ones. The results obtained from laboratory experiments and field observations confirm that adult fruit flies are more affected through repellence by ant cues than by direct predation. The use of cues by fruit flies in predator avoidance has implications for evolutionary ecology, behavioural ecology and chemical ecology.     

Climate variation influences host specificity in avian malaria parasites

Parasites with low host specificity (e.g. infecting a large diversity of host species) are of special interest in disease ecology, as they are likely more capable of circumventing ecological or evolutionary barriers to infect new hosts than are specialist parasites. Yet for many parasites, host specificity is not fixed and can vary in response to environmental conditions. Using data on host associations for avian malaria parasites (Apicomplexa: Haemosporida), we develop a hierarchical model that quantifies this environmental dependency by partitioning host specificity variation into region‐ and parasite‐level effects. Parasites were generally phylogenetic host specialists, infecting phylogenetically clustered subsets of available avian hosts. However, the magnitude of this specialisation varied biogeographically, with parasites exhibiting higher host specificity in regions with more pronounced rainfall seasonality and wetter dry seasons. Recognising the environmental dependency of parasite specialisation can provide useful leverage for improving predictions of infection risk in response to global climate change.     

Loss of pathogens in threatened plant species

Global declines in biodiversity create an urgent need to address the impact of infectious disease in the small and fragmented populations that characterize threatened species. However, the paucity of empirical data provides little ability to predict whether disease generally accelerates threatened species towards extinction or becomes less important as populations decline. This study tests whether plant species threatened with extinction exhibit lower disease frequencies and lower overall parasite species richness while also experimentally testing for the effect of physiological disease resistance. Herbarium surveys of the genus Silene revealed that anther‐smut disease was significantly less frequent in threatened species than non‐threatened species, and this effect was not constrained by the host phylogeny or by physiological resistance. Moreover, analysis across a much broader range of plants (using US Federal designations) revealed that species with endangered status had significantly lower species richness of fungal pathogens than closely‐related, non‐endangered species. These results support the role of host ecology, rather than physiological resistance or phylogeny, in determining overall lower incidences and diversity of diseases in plant species threatened by extinction. Low disease incidence accompanied by susceptibility in threatened species may result from selection against costly resistance genes in the absence of disease.     

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.     

Quality and quantity: transitions in antimicrobial gland use for parasite defense

Parasites are a major force in evolution, and understanding how host life history affects parasite pressure and investment in disease resistance is a general problem in evolutionary biology. The threat of disease may be especially strong in social animals, and ants have evolved the unique metapleural gland (MG), which in many taxa produce antimicrobial compounds that have been argued to have been a key to their ecological success. However, the importance of the MG in the disease resistance of individual ants across ant taxa has not been examined directly. We investigate experimentally the importance of the MG for disease resistance in the fungus‐growing ants, a group in which there is interspecific variation in MG size and which has distinct transitions in life history. We find that more derived taxa rely more on the MG for disease resistance than more basal taxa and that there are a series of evolutionary transitions in the quality, quantity, and usage of the MG secretions, which correlate with transitions in life history. These shifts show how even small clades can exhibit substantial transitions in disease resistance investment, demonstrating that host–parasite relationships can be very dynamic and that targeted experimental, as well as large‐scale, comparative studies can be valuable for identifying evolutionary transitions.     

Disease management in two sympatric Apterostigma fungus‐growing ants for controlling the parasitic fungus Escovopsis

Antagonistic interactions between host and parasites are often embedded in networks of interacting species, in which hosts may be attacked by competing parasites species, and parasites may infect more than one host species. To better understand the evolution of host defenses and parasite counterdefenses in the context of a multihost, multiparasite system, we studied two sympatric species, of congeneric fungus‐growing ants (Attini) species and their symbiotic fungal cultivars, which are attacked by multiple morphotypes of parasitic fungi in the genus, Escovopsis. To assess whether closely related ant species and their cultured fungi are evolving defenses against the same or different parasitic strains, we characterized Escovopsis that were isolated from colonies of sympatric Apterostigma dentigerum and A. pilosum. We assessed in vitro and in vivo interactions of these parasites with their hosts. While the ant cultivars are parasitized by similar Escovopsis spp., the frequency of infection by these pathogens differs between the two ant species. The ability of the host fungi to suppress Escovopsis growth, as well as ant defensive responses toward the parasites, differs depending on the parasite strain and on the host ant species.     

A meta‐analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery’s rule

Abstract 1. In ant social parasitism, the process by which parasite–host systems evolved and the types of invasion mechanisms parasites use are being debated. Emery’s rule, for example, states that social parasites are the closest relatives to their hosts. The present study uses previously published data to test whether Emery’s rule applies equally to all parasitism types (i.e. xenobiosis, temporary, dulosis, and inquilinism). In addition, this study also investigates other links between parasite–host relatedness and host biology, which has implications for understanding the invasion mechanisms used by certain parasites. 2. We find that xenobiotic parasites typically use distantly‐related host species that are of at least medium colony size. Temporary parasites often have multiple host species that are very closely related to the parasite and hosts with medium‐size colonies. Dulotic parasites frequently have multiple host species that are slightly less related and of any size. Lastly, inquiline parasites tend to have a single, very closely related, host species with medium‐size colonies. 3. Parasites tend to be more closely related to host species if they have a single host species or when the host has a large colony size. In contrast, parasites with multiple host species or hosts of small colony size tend to be less related to their hosts. 4. This study is the first to examine trends in ant social parasitism across all known parasite species. Our meta‐analysis shows that Emery’s rule applies to inquilinism and temporary parasitism, but not to dulosis and xenobiosis. Our results also suggest that both parasitism type and parasite–host relatedness predict the number of hosts and host colony size. It may be that a chemical mimicry mechanism allows invasion of large host colonies, but requires close relatedness of parasite and host, and concentration on a single host species.     

Differential host defense against multiple parasites in ants

Host–parasite interactions are ideal systems for the study of coevolutionary processes. Although infections with multiple parasite species are presumably common in nature, most studies focus on the interactions of a single host and a single parasite. To the best of our knowledge, we present here the first study on the dependency of parasite virulence and host resistance in a multiple parasite system. We evaluated whether the strength of host defense depends on the potential fitness cost of parasites in a system of two Southeast Asian army ant hosts and five parasitic staphylinid beetle species. The potential fitness costs of the parasites were evaluated by their predation behavior on host larvae in isolation experiments. The host defense was assessed by the ants’ aggressiveness towards parasitic beetle species in behavioral studies. We found clear differences among the beetle species in both host–parasite interactions. Particular beetle species attacked and killed the host larvae, while others did not. Importantly, the ants’ aggressiveness was significantly elevated against predatory beetle species, while non-predatory beetle species received almost no aggression. As a consequence of this defensive behavior, less costly parasites are more likely to achieve high levels of integration in the ant society. We conclude that the selection pressure on the host to evolve counter-defenses is higher for costly parasites and, thus, a hierarchical host defense strategy has evolved that depends on the parasites’ impact.     

Geographic Variation in Social Parasite Pressure Predicts Intraspecific but not Interspecific Aggressive Responses in Hosts of a Slavemaking Ant

Variation in community composition over a species' geographic range leads to divergent selection pressures, resulting in interpopulation variation in trait expression. One of the most pervasive selective forces stems from antagonists such as parasites. Whereas hosts of microparasites developed sophisticated immune systems, social parasites select for behavioural host defences. Here, we investigated the link between parasite pressure exerted by the socially parasitic slavemaking ant Protomognathus americanus and colony‐level aggression in Temnothorax ants from 17 populations. We studied almost the entire geographic range of two host species, including unparasitized populations. As previous studies have demonstrated that host colonies responding highly aggressively towards conspecifics fare better during slavemaker attacks, we predicted higher aggression levels in severely parasitized populations. Indeed, we demonstrate an increase in aggression towards conspecifics with parasite pressure, a pattern that was consistent over the two host species. In contrast to other studies, aggression against the parasite itself did not shift with parasite pressure. This may be explained by an absence of costs of parasite‐specific aggression in parasite‐free populations. The preferred host species T. longispinosus was generally more aggressive; however, the association between parasite pressure and aggression was found for both species, suggesting convergent co‐adaptation. Two potentially confounding factors, colony density and the co‐occurrence of a competing Temnothorax species in the community, could not explain the level of colony aggression in intra‐ and interspecific interactions. Instead, our study points to social parasite pressure as the determining factor shaping antagonistic interactions within, but not between, host species.     

A cost of disease resistance: paradigm or peculiarity?

Disease is one of the main driving forces of biological evolution. Parasites cause natural selection for disease resistance in populations of their hosts. Why then are all organisms susceptible to some parasites? One explanation is that resistance to disease is costly, reducing the fitness of the host in the absence of disease. A recent article shows that such costs might have helped to maintain polymorphism at a resistance locus. Other work, however, has questioned whether the costs of resistance are indeed necessary to account for polymorphism in host–parasite interactions.     

Climate,host phylogeny and the connectivity of host communities govern regional parasite assembly

Aim

Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly.

Location

Australasia and Oceania.

Methods

We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition.

Results

Parasites were more locally distinct (co‐occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co‐occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance.

Main conclusions

Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co‐occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.     

Extrafloral nectar as a driver of arboreal ant communities at the site‐scale in Brazilian savanna

Despite years of study, it remains unclear if and to what extent the effects of extra‐floral nectaries (EFNs) on arboreal ants observed on individual trees scale up to larger spatial scales. Here, we address this issue in Brazilian savanna and tested three predictions: (i) Trees with EFN have higher richness of arboreal ant species than trees without; (ii) Arboreal ant species richness increases with the proportion of total EFN‐bearing trees at the site scale, due to a higher occurrence of non‐core ant species; (iii) Ant species composition changes with the proportion of EFN‐bearing trees at the site scale. We sampled arboreal ants in 32 plots with EFN‐bearing trees ranging from 0% to 60% of all trees. We sampled 72 ant species, from which 17 (mostly belonging to Camponotus, Cephalotes and Crematogaster) were identified as core species in at least one of the ant‐EFN networks in the 32 plots. Ant species richness was significantly higher on EFN‐bearing trees. We identified 11 ant species that preferentially occurred on EFN‐bearing trees, all of which were core partners in networks. Species richness at the site scales increased with the proportion of EFN‐bearing trees, regardless of tree density and richness; this pattern was due to a higher occurrence of non‐core ant species. Finally, species composition also varied with the proportion of EFN‐bearing trees. Therefore, we found that the presence of EFNs not only influences arboreal ants on individual trees but also has a substantial effect on the ant‐EFN network on a broader community scale. The increase in non‐core species site scale reveals that this interaction is unlikely to result in substantially enhanced protection services for EFN‐bearing plants.     

Novel fungal disease in complex leaf‐cutting ant societies

Abstract 1. The leaf‐cutting ants practise an advanced system of mycophagy where they grow a fungus as a food source. As a consequence of parasite threats to their crops, they have evolved a system of morphological, behavioural, and chemical defences, particularly against fungal pathogens (mycopathogens). 2. Specific fungal diseases of the leaf‐cutting ants themselves have not been described, possibly because broad spectrum anti‐fungal defences against mycopathogens have reduced their susceptibility to entomopathogens. 3. Using morphological and molecular tools, the present study documents three rare infection events of Acromyrmex and Atta leaf‐cutting ants by Ophiocordyceps fungi, agenus of entomopathogens that is normally highly specific in its host choice. 4. As leaf‐cutting ants have been intensively studied, the absence of prior records of Ophiocordyceps suggests that these infections may be a novel event and that switching from one host to another is possible. To test the likelihood of this hypothesis, host switching was experimentally induced, and successfully achieved, among five distinct genera of ants, one of which was in a different sub‐family than the leaf‐cutter ants. 5. Given the substantial differences among the five host ants, the ability of Ophiocordyceps to shift between such distant hosts is remarkable; the results are discussed in the context of ant ecological immunology and fungal invasion strategies.     

Adaptive social immunity in leaf-cutting ants

Social insects have evolved a suite of sophisticated defences against parasites. In addition to the individual physiological immune response, social insects also express ‘social immunity’ consisting of group-level defences and behaviours that include allogrooming. Here we investigate whether the social immune response of the leaf-cutting ant Acromyrmex echinatior reacts adaptively to the virulent fungal parasite, Metarhizium anisopliae. We ‘immunized’ mini-nests of the ants by exposing them twice to the parasite and then compared their social immune response with that of naive mini-nests that had not been experimentally exposed to the parasite. Ants allogroomed individuals exposed to the parasite, doing this both for those freshly treated with the parasite, which were infectious but not yet infected, and for those treated 2 days previously, which were already infected but no longer infectious. We found that ants exposed to the parasite received more allogrooming in immunized mini-nests than in naive mini-nests. This increased the survival of the freshly treated ants, but not those that were already infected. The results thus indicate that the social immune response of this leaf-cutting ant is adaptive, with the group exhibiting a greater and more effective response to a parasite that it has previously been exposed to.     

Fitness consequences of nest infiltration by the mutualist‐exploiter Megalomyrmex adamsae

1. Fungus‐growing ants are obligate mutualists. Their nutrient‐rich fungus garden provides a valuable food store that sustains the ant hosts, but can also attract social parasites. 2. The ‘guest ant' Megalomyrmex adamsae Longino parasitises the fungus‐growing Trachymyrmex zeteki Weber queen just after nest founding. The parasitic queen infiltrates the incipient nest, builds a cavity in the fungal garden, and lays eggs that develop into workers and reproductive males and females. 3. This study compared young parasitised and non‐parasitised laboratory colonies by measuring garden growth and biomass, and the number of host workers and reproductives. Host queen survival and parasite colony growth were also monitored. 4. Parasitised Trachymyrmex colonies had reduced host worker and alate numbers, as well as lower garden biomass, compared with non‐parasitised control colonies, confirming that M. adamsae is a xenobiotic social parasite. Host queen survival was not significantly different between parasitised and control colonies. 5. This is the first study that experimentally infects host colonies with a xenobiotic social parasite to measure fitness cost to the host. The natural history of M. adamsae and the fungus‐growing ant mutualism are evaluated in the context of three general predictions of (Bronstein, Ecology Letters, 4 , 277–287, 2001a) regarding the cost of mutualism exploiters.     

Plant Ontogeny as a Conditionality Factor in the Protective Effect of Ants on a Neotropical Tree

The outcome of any interspecific interaction is often determined by the ecological context in which the interacting species are embedded. Plant ontogeny may represent an important source of variation in the outcome of ant–plant mutualisms, as the level of investment in ant rewards, in alternative (non‐biotic) defenses, or both, may be modulated by the plant's developmental stage. In addition, the abundance and identities of the ants involved in the interaction may change during ontogeny of the host‐plant. Here, we evaluated if plant ontogeny affects the interaction between ants and a savanna tree species (Caryocar brasiliense) that produces extrafloral nectar. We found fewer ants per branch and fewer species of ants per tree in juvenile than in reproductive trees of medium and large size. In addition, large‐sized reproductive trees were more likely to host more aggressive ants than were medium‐sized reproductive or juvenile trees. Such differences strongly affected the outcome of the interaction between ants and their host‐plants, as the magnitude of the effect of ants on herbivory was much stronger for large trees than for juvenile ones. The fact that we did not find significant ontogenetic variation in the concentration of leaf tannins suggests that the observed differences in herbivory did not result from a differential investment in chemical defenses among different‐sized plants. Overall, the results of our study indicate that the developmental stage of the host plant is an important factor of conditionality in the interaction between C. brasiliense and arboreal foraging ants.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.