The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.     

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.     

Myrmica ants host highly diverse parasitic communities: from social parasites to microbes

Myrmica ants have been model species for studies in a variety of disciplines, including insect physiology, chemical communication, ant social dynamics, ant population, community ecology, and ant interactions with other organisms. Species belonging to the genus Myrmica can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and systematics have been thoroughly studied. These ants serve as hosts to highly diverse parasitic organisms from socially parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in colony fitness. A comprehensive review of the parasitic organisms supported by Myrmica and the effects of these organisms on individuals and on whole ant colonies has not yet been compiled. Here, we provide a review of the interactions of these organisms with Myrmica ants by discussing host and parasite functional, behavioral or physiological adaptations. In addition, for all “symbiont groups” of Myrmica ants described in this paper, we examine the present limitations of the knowledge at present of their impact on individuals and host colony fitness. In conclusion, we argue that Myrmica ants serve as remarkable resource for the evolution of a wide variety of associated organisms.     

Parasitism <Emphasis Type="Italic">versus</Emphasis> mutualism in the ant-garden parabiosis between <Emphasis Type="Italic">Camponotus femoratus</Emphasis> and <Emphasis Type="Italic">Crematogaster levior</Emphasis>

Ant-gardens represent a special type of association between ants and epiphytes. Frequently, two ant species can share the same nest in a phenomenon known as ‘parabiosis’, but the exact nature (i.e., mutualistic or parasitic) of this interaction is the subject of debate. We thus attempted to clarify the mutual costs and benefits for each partner (ants and plants) in the Crematogaster levior/Camponotus femoratus ant-garden parabiosis. The ants’ response to experimental foliar damage to the epiphytes and to the host tree as well as their behavior and interactions during prey capture were investigated to see if the purported parasitic status of Cr. levior could be demonstrated in either the ant-ant or in the ant-plant interactions. The results show that both species take part in protecting the epiphytes, refuting the role of Cr. levior as a parasite of the ant-garden mutualism. During capture of large prey Ca. femoratus took advantage from the ability of Cr. levior to discover prey; by following Cr. levior trails Ca. femoratus workers discover the prey in turn and usurp them during agonistic interactions. Nevertheless, the trade-off between the costs and benefits of this association seems then to be favorable to both species because it is known that Cr. levior benefits from Ca. femoratus building the common carton nests and furnishing protection from vertebrates. Consequently, parabiosis can then be defined as the only mutualistic association existing between ant species, at least in ant-gardens. Received 31 August 2006 ; revised 8 December 2006 ; accepted 12 December 2006     

Host tolerance and resistance to parasitic nest flies differs between two wild bird species

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Performance of Myrmica ant colonies is correlated with the presence of social parasites

1. The performance of ant colonies depends on different factors such as nest site, colony structure or the presence of pathogens and social parasites. Myrmica ants host various types of social parasites, including the larvae of Maculinea butterflies and Microdonmyrmicae (Schönrogge) hoverfly. How these social parasites affect host colony performance is still unexplored. 2. It was examined how the presence of Maculinea teleius Bergsträsser, Maculinea alcon (Denis & Schiffermüller), and M. myrmicae larvae, representing different feeding and growth strategies inside host colonies, is associated with worker survival, the number of foragers, and colony productivity parameters such as growth and reproduction. 3. It was found that the presence of social parasites is negatively associated with total colony production and the production of ant larvae and gynes. Male production was lower only in nests infested by M. teleius, whereas the number of worker pupae was significantly higher in all types of infested colonies than in uninfested colonies. Laboratory observations indicated that nests infested by Maculinea larvae are characterised by a higher number of foragers compared to uninfested nests but we did not find differences in worker survival among nest types. 4. The observed pattern of social parasite influence on colony productivity can be explained by the feeding strategies of parasitic larvae. The most negative effect was found for M. teleius, which feeds on the largest host brood and eliminates a high number of sexual forms. The strong, adverse influence of all studied parasite species on gyne production may result in low queen production in Myrmica populations exposed to these social parasites.     

The role of specialist parasites in structuring host communities

Natural enemies can be a powerful force when structuring natural communities, and in facilitating or preventing species coexistence depending on the nature of the trophic interaction. In particular, “keystone” predators can promote species coexistence, provided they preferentially attack the competitively dominant species. However, it is not clear whether parasites can play a similar structuring role; parasites typically form chronic associations with their victims, reducing their fitness (i.e., fecundity) rather than survival, and allowing infected hosts to remain viable competitors within the community. Therefore the density-dependent suppression of the host is likely to be more subtle than that due to predation. Using a series of simple population-dynamic models we show that specialist parasites can facilitate species coexistence, although possibly less so than predators. These results contrast with those typically found with models of generalist parasites, which can reduce the likelihood of species coexistence through apparent competition. In addition, we show that the likelihood of parasite-facilitated species coexistence depends greatly on the specific type of parasite. In particular, macroparasites (e.g., parasitic helminths) may be less likely to facilitate species coexistence than microparasites (e.g., viruses or bacteria) due to their typically highly aggregated distribution amongst their hosts. Furthermore, species coexistence is more likely if the parasite is relatively benign to its host. Parasitism by apparently “harmless” specialist parasites may provide an important but overlooked factor in the maintenance of species diversity, facilitating species invasions into new communities and the emergence of novel infectious diseases.     

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.     

Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo

Brood parasites dramatically reduce the reproductive successof their hosts, which therefore have developed defenses againstbrood parasites. The first line of defense is protecting thenest against adult parasites. When the parasite has successfullyparasitized a host nest, some hosts are able to recognize andreject the eggs of the brood parasite, which constitutes the secondline of defense. Both defense tactics are costly and would be counteractedby brood parasites. While a failure in nest defense implies successfulparasitism and therefore great reduction of reproductive successof hosts, a host that recognizes parasitic eggs has the opportunityto reduce the effect of parasitism by removing the parasiticegg. We hypothesized that, when nest defense is counteractedby the brood parasite, hosts that recognize cuckoo eggs shoulddefend their nests at a lower level than nonrecognizers becausethe former also recognize adult cuckoos. Magpie (Pica pica) hoststhat rejected model eggs of the brood parasitic great spottedcuckoo (Clamator glandarius) showed lower levels of nest defensewhen exposed to a great spotted cuckoo than when exposed toa nest predator (a carrion crow Corvus corone). Moreover, magpiesrejecting cuckoo eggs showed lower levels of nest defense againstgreat spotted cuckoos than nonrecognizer magpies, whereas differencesin levels of defense disappeared when exposed to a carrion crow.These results suggest that hosts specialize in antiparasitedefense and that different kinds of defense are antagonistically expressed.We suggest that nest-defense mechanisms are ancestral, whereasegg recognition and rejection is a subsequent stage in the coevolutionaryprocess. However, host recognition ability will not be expressedwhen brood parasites break this second line of defense.     

Competition hierarchy and plant defense in a guild of ants on tropical Passiflora

In facultative ant–plant interactions, ants may compete with each other for food provided by extrafloral nectar (EFN) plants. We studied resource competition and plant defense in a guild of ants that use the same EFN resource provided by two species of Passiflora in a seasonal rain forest in tropical China. At least 22 ant species were recorded using the EFN resource, although some of those species were rare. Among these ants, Paratrechina sp.1 and Dolichoderus thoracicus were more aggressive than other species. Ant aggressiveness measured as ant behavioral dominance index (BDI) was positively correlated with ant abundance on the Passiflora species studied. Ant BDI was also positively correlated to the protection that ants provided against herbivory. In Passiflora siamica, the number of workers patrolling on the plants did negatively correlate with average leaf loss per plant. We conclude that in this facultative Passiflora–ant system, plant defense upon herbivore was indeed influenced by the total number of ants present on plant and the aggressiveness of these ants.     

Dose-independent virulence in phoretic mites that parasitize burying beetles

Virulence, the negative impact of parasites on their hosts, typically increases with parasite dose. Parasites and hosts often compete for host resources and more parasites will consume more resources. Depending on the mechanism of competition, increasing host resources can benefit the host. Additional resources can also be harmful when the parasites are the main beneficiaries. Then, the parasites will thrive and virulence increases. While parasite dose is often easy to manipulate, it is less trivial to experimentally scale host resources. Here, we study a system with external host resources that can be easily manipulated: Nicrophorus burying beetles reproduce on vertebrate carcasses, with larger carcasses yielding more beetle offspring. Phoretic Poecilochirus mites reproduce alongside the beetles and reduce beetle fitness. The negative effect of mites could be due to competition for the carrion between beetle and mite offspring. We manipulated mite dose and carcass size to better understand the competition between the symbionts. We found that mite dose itself was not a strong predictor of virulence. Instead, the number of mite offspring determined beetle fitness. At larger doses, there was strong competition among adult parental mites as well as mite offspring. While increasing the carcass size increased both host and parasite fitness, it did surprisingly little to alleviate the negative effect that mites had on beetles. Instead, relative virulence was stronger on large carcasses, indicating that the parasites appropriate more of the additional resources. Our results demonstrate an ecological influence on the selection of parasites on their hosts and suggest that virulence can be dose-independent in principle.     

Dissecting the effect of a heterogeneous environment on the interaction between host and parasite fitness traits

Environmental variation can alter the probability of parasitic infection or the fitness consequence of infection, and thus has the potential to dramatically alter the dynamics of host parasite coevolution. Here we investigated the effect of a changing temperature on host-parasite interactions using the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa. By reciprocally varying (1) the temperature at which exposure to parasites occurred and (2) the temperature at which within-host parasite growth occurred, and measuring several fitness-related traits, we show that while there are temperature combinations that favour either host or parasite, there are also conditions that favour neither, that is, negative fitness consequences for the host without fitness benefits for the parasite. This result highlights the importance of considering a heterogeneous rather than static environment in coevolutionary studies, while also showing support for an optimal virulence strategy in castrating parasites.     

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.     

Look before leaping: foraging selectivity of capuchin monkeys on acacia trees in Costa Rica

Acacia trees in Costa Rica have an obligate mutualism with three species of Pseudomyrmex ants, which vigorously defend their host tree from insect and mammalian herbivores. Depending on the size and species of ant colony, individual acacia trees may be differentially protected. For animals able to discern between weakly and highly aggressive ant colonies, costs of ant stings from less active colonies might be offset by nutritional value acquired from feeding on acacia fruit or ant larvae in swollen thorns. We examined foraging selectivity of capuchin monkeys on acacia trees in Santa Rosa National Park, Costa Rica. We measured four characteristics of the acacia trees from which capuchins fed and of acacias immediately adjacent to those in which the monkeys fed: diameter at breast height (DBH), accessibility, species of closest tree and ant species present. We found that capuchins prefer to forage in acacias that are large and accessible. We also made two measurements of ant colony activity on each tree, one before and one after disturbing the ant colony. We found that the three species of mutualistic ants differ in baseline activity levels and that mutualistic ants are more active than non-mutualistic ant species found in acacia trees. We also found that capuchins foraged more frequently in trees colonized by non-mutualistic ants, but the explanatory value (r ²) of this model was low. Furthermore, monkeys did not discriminate between acacias on the basis of baseline ant activity or the ant colony’s response to disturbance. We conclude that these monkeys select acacia trees in which to forage based on characteristics of the trees rather than the ants. In addition, our study suggests that white-faced capuchins act as predators on the acacia ants but they probably benefit the dispersal and reproductive success of acacia trees. Capuchins may in fact function as an additional mutualistic partner for acacia trees via seed dispersal, but they must overcome the ants’ defense of the trees to do so.     

Global warming will reshuffle the areas of high prevalence and richness of three genera of avian blood parasites

The importance of parasitism for host populations depends on local parasite richness and prevalence: usually host individuals face higher infection risk in areas where parasites are most diverse, and host dispersal to or from these areas may have fitness consequences. Knowing how parasites are and will be distributed in space and time (in a context of global change) is thus crucial from both an ecological and a biological conservation perspective. Nevertheless, most research articles focus just on elaborating models of parasite distribution instead of parasite diversity. We produced distribution models of the areas where haemosporidian parasites are currently highly diverse (both at community and at within‐host levels) and prevalent among Iberian populations of a model passerine host: the blackcap Sylvia atricapilla; and how these areas are expected to vary according to three scenarios of climate change. On the basis of these models, we analysed whether variation among populations in parasite richness or prevalence are expected to remain the same or change in the future, thereby reshuffling the geographic mosaic of host‐parasite interactions as we observe it today. Our models predict a rearrangement of areas of high prevalence and richness of parasites in the future, with Haemoproteus and Leucocytozoon parasites (today the most diverse genera in blackcaps) losing areas of high diversity and Plasmodium parasites (the most virulent ones) gaining them. Likewise, the prevalence of multiple infections and parasite infracommunity richness would be reduced. Importantly, differences among populations in the prevalence and richness of parasites are expected to decrease in the future, creating a more homogeneous parasitic landscape. This predicts an altered geographic mosaic of host‐parasite relationships, which will modify the interaction arena in which parasite virulence evolves.     

Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.     

Inferring associations among parasitic gamasid mites from census data

Within a community, the abundance of any given species depends in large part on a network of direct and indirect, positive and negative interactions with other species, including shared enemies. In communities where experimental manipulations are often impossible (e.g., parasite communities), census data can be used to evaluate the strength or frequency of positive and negative associations among species. In ectoparasite communities, competitive associations can arise because of limited space or food, but facilitative associations can also exist if one species suppresses host immune defenses. In addition, positive associations among parasites could arise merely due to shared preferences for the same host, without any interaction going on. We used census data from 28 regional surveys of gamasid mites parasitic on small mammals throughout the Palaearctic, to assess how the abundance of individual mite species is influenced by the abundance and diversity of other mite species on the same host. After controlling for several confounding variables, the abundance of individual mite species was generally positively correlated with the combined abundances of all other mite species in the community. This trend was confirmed by meta-analysis of the results obtained for separate mite species. In contrast, there were generally no consistent relationships between the abundance of individual mite species and either the species richness or taxonomic diversity of the community in which they occur. These patterns were independent of mite feeding mode. Our results indicate either that synergistic facilitative interactions among mites increase the host’s susceptibility to further attacks (e.g., via immunosuppression) and lead to different species all having increased abundance on the same host, or that certain characteristics make some host species preferred habitats for many parasite species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The role of kin recognition in the evolution of conspecific brood parasitism

Conspecific brood parasitism (CBP) is a common strategy in several species of birds. Currently, some studies suggest that relatedness between host and parasite enhances CBP, since indirect fitness benefits could select for acceptance of related eggs by hosts. Conversely, parasites should avoid laying eggs in nests of relatives if this is costly for the host. Based on the latter argument, kinship should not promote brood parasitism. A recent model clarified this relationship, and showed that kinship can promote brood parasitism, assuming kin recognition. However, in that model kin recognition was assumed perfect. Here we present a model that addresses the role of relatedness and kin selection in CBP, when kin recognition is not perfect and hosts do not always detect parasitism. We consider both the indirect fitness of the parasite and the possible responses of the host. Our results indicate that the existence and accuracy of a kin recognition system is crucial to the final outcome. When CBP represents a cost to the host, a parasitic female that has the choice should avoid parasitizing relatives, unless (1) the costs are not too high and (2) hosts can accurately enough recognize eggs laid by relatives, rejecting them less often than eggs laid by nonkin. But if ‘parasitism’ enhances the direct fitness of the host (which is possible in species with precocial young) parasites should choose relatives whenever possible, even if hosts do not recognize kin eggs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

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.