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.     

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.     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

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.     

Do host species evolve a specific response to slave-making ants?

Background

Social parasitism is an important selective pressure for social insect species. It is particularly the case for the hosts of dulotic (so called slave-making) ants, which pillage the brood of host colonies to increase the worker force of their own colony. Such raids can have an important impact on the fitness of the host nest. An arms race which can lead to geographic variation in host defenses is thus expected between hosts and parasites. In this study we tested whether the presence of a social parasite (the dulotic ant Myrmoxenus ravouxi) within an ant community correlated with a specific behavioral defense strategy of local host or non-host populations of Temnothorax ants. Social recognition often leads to more or less pronounced agonistic interactions between non-nestmates ants. Here, we monitored agonistic behaviors to assess whether ants discriminate social parasites from other ants. It is now well-known that ants essentially rely on cuticular hydrocarbons to discriminate nestmates from aliens. If host species have evolved a specific recognition mechanism for their parasite, we hypothesize that the differences in behavioral responses would not be fully explained simply by quantitative dissimilarity in cuticular hydrocarbon profiles, but should also involve a qualitative response due to the detection of particular compounds. We scaled the behavioral results according to the quantitative chemical distance between host and parasite colonies to test this hypothesis.

Results

Cuticular hydrocarbon profiles were distinct between species, but host species did not show a clearly higher aggression rate towards the parasite than toward non-parasite intruders, unless the degree of response was scaled by the chemical distance between intruders and recipient colonies. By doing so, we show that workers of the host and of a non-host species in the parasitized site displayed more agonistic behaviors (bites and ejections) towards parasite than toward non-parasite intruders.

Conclusions

We used two different analyses of our behavioral data (standardized with the chemical distance between colonies or not) to test our hypothesis. Standardized data show behavioral differences which could indicate qualitative and specific parasite recognition. We finally stress the importance of considering the whole set of potentially interacting species to understand the coevolution between social parasites and their hosts.

     

Can infection by eugregarine parasites mediate species coexistence in Calopteryx damselflies?

1. Parasitism may be an important factor determining the coexistence of closely related species. Although host–parasite interactions can affect the ecology and distribution of the host species, virtually nothing is known about how other interspecific interactions affecting the host, such as competition or predation, relate to the parasite burden of the host. 2. We studied parasite‐mediated competition between two closely related Calopteryx damselflies, C. virgo L. and C. splendens Harris. We investigated a total of 31 populations, including 18 allopatric and 13 sympatric populations. We measured the occurrence of gut parasites, eugregarines. 3. We found that the prevalence of gregarines was higher in C. virgo than in C. splendens. On average, more than half of the C. virgo individuals were infected by eugregarines both in allopatric and sympatric populations. However, hardly any allopatric C. splendens populations had gregarines, but most of sympatric populations had infected individuals. 4. According to our results, co‐existence of the host species affects the likelihood of the subordinate species showing higher levels of parasitism. Interspecific aggression, lower species genetic heterozygosity, and the difference in host species immunity are proposed as possible explanations for greater parasite burdens in the inferior species at sympatric sites.     

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.     

Interspecific relationships in co‐occurring populations of social parasites and their host ants

Myrmica ant colonies host numerous insect species, including the larvae of Maculinea butterflies and Microdon myrmicae hoverflies. Little is known about the interspecific relationships among these social parasites and their host ants occurring in sympatric populations. We investigated communities of social parasites to assess the strategies allowing them to share the same pool of resources (i.e. Myrmica colonies). The present study was carried out at five sites inhabited by different social parasite communities, each comprising varying proportions of Maculinea teleius, Maculinea nausithous, Maculinea alcon, and Microdon myrmicae. We investigated their spatial distributions, host segregation, the degree of chemical similarity between social parasites and hosts, and temporal overlaps in colony resource exploitation. Spatial segregation among social parasites was found in two populations and it arises from microhabitat preferences and biological interactions. Local conditions can drive selection on one social parasite to use a Myrmica host species that is not exploited by other social parasites. Myrmica scabrinodis and Myrmica rubra nests infested by larvae of two social parasite species were found and the most common co‐occurrence was between Ma. teleius and Mi. myrmicae. The successful coexistence of these two species derives from their exploitation of the host colony resources at different times of the year. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 699–709.     

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.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

Bottom‐up regulation of malaria population dynamics in mice co‐infected with lung‐migratory nematodes

When and how populations are regulated by bottom up vs. top down processes, and how those processes are affected by co‐occurring species, are poorly characterised across much of ecology. We are especially interested in the community ecology of parasites that must share a host. Here, we quantify how resources and immunity affect parasite propagation in experiments in near‐replicate ‘mesocosms’’ – i.e. mice infected with malaria (Plasmodium chabaudi) and nematodes (Nippostrongylus brasiliensis). Nematodes suppressed immune responses against malaria, and yet malaria populations were smaller in co‐infected hosts. Further analyses of within‐host epidemiology revealed that nematode co‐infection altered malaria propagation by suppressing target cell availability. This is the first demonstration that bottom‐up resource regulation may have earlier and stronger effects than top‐down immune mechanisms on within‐host community dynamics. Our findings demonstrate the potential power of experimental ecology to disentangle mechanisms of population regulation in complex communities.     

Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail

Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its co‐evolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus‐infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used an F_ST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in the P. antipodarum‐Microphallus interaction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.     

Populations of the damselfly Coenagrion hastulatum at the edge of the species range have fewer gregarine and water mite parasites

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Population‐level dynamics in experimental mixed infections: evidence for competitive exclusion among bacterial parasites of Paramecium caudatum

Parasites frequently share their host populations with other parasites. However, little is known about how different parasites respond to competition with diverse competitor species in the within‐host and between‐host environments. We explored the repeatability of competition by simultaneously exposing microcosm populations of the ciliate Paramecium caudatum to pairs of parasites from the Holospora species complex (H. undulata, H. caryophila and H. obtusa). We measured how competition affected the persistence and prevalence of each compared to single infections, across three host genotypes. Three weeks post‐inoculation we identified the presence of each parasite using fluorescence in situ hybridisation (FISH). Competitive exclusion (62/72) was more common than co‐existence (10/72) in populations inoculated with two parasites. There was a clear pattern of competitive superiority, with H. caryophila persisting in all doubly inoculated populations (with either H. undulata or H. obtusa), and H. undulata tending to exclude H. obtusa. This mirrored infection success in single infections, with H. caryophila having a higher infection prevalence in single inoculations, followed by H. undulata then H. obtusa. The probability of persistence in co‐inoculations did not change across the different host genotypes, and prevalence was the same as in single infections. Our results are consistent with superinfection models, which assume the competitive exclusion of parasites upon contact within the same host. Furthermore, such non‐random competitive epidemiological dynamics, where one parasite always wins, may be of interest for public health management, especially if the winning parasite is avirulent, as is seemingly the case here.     

Host diversity drives parasite diversity: meta‐analytical insights into patterns and causal mechanisms

Statistical correlations of biodiversity patterns across multiple trophic levels have received considerable attention in various types of interacting assemblages, forging a universal understanding of patterns and processes in free‐living communities. Host–parasite interactions present an ideal model system for studying congruence of species richness among taxa as obligate parasites are strongly dependent upon the availability of their hosts for survival and reproduction while also having a tight coevolutionary relationship with their hosts. The present meta‐analysis examined 38 case studies on the relationship between species richness of hosts and parasites, and is the first attempt to provide insights into the patterns and causal mechanisms of parasite biodiversity at the community level using meta‐regression models. We tested the distinct role of resource (i.e. host) availability and evolutionary co‐variation on the association between biodiversity of hosts and parasites, while spatial scale of studies was expected to influence the extent of this association. Our results demonstrate that species richness of parasites is tightly correlated with that of their hosts with a strong average effect size (r= 0.55) through both host availability and evolutionary co‐variation. However, we found no effect of the spatial scale of studies, nor of any of the other predictor variables considered, on the correlation. Our findings highlight the tight ecological and evolutionary association between host and parasite species richness and reinforce the fact that host–parasite interactions provide an ideal system to explore congruence of biodiversity patterns across multiple trophic levels.     

The effect of density on aggression between a highly invasive and native fish

Population densities of invasive species fluctuate spatially and temporally, suggesting that the intensity of their aggressive interactions with native species is similarly variable. Although inter‐specific aggression is often thought to increase with population density, it is often theorized that it should be exceeded by intra‐specific aggression since conspecifics share a greater degree of resource overlap. Yet, the magnitude of intra‐specific aggression is seldom considered when examining aggressive interactions, particularly those between invasive and native species. Here, we manipulated the density of the invasive eastern mosquitofish, Gambusia holbrooki, and observed its aggressive interactions with juveniles of the native Australian bass, Macquaria novemaculeata in a laboratory setting. For both species, the magnitudes of intra‐ and inter‐specific aggression were recorded. Regardless of density, the native M. novemaculeata was more aggressive towards heterospecifics than G. holbrooki was. In addition to this, M. novemaculeata was more aggressive to G. holbrooki than towards conspecifics, at both low‐ and high‐density conditions. In contrast, G. holbrooki was similarly aggressive towards M. novemaculeata and G. holbrooki at a high density, yet at low density, displayed significantly more aggression towards conspecifics than M. novemaculeata. These findings demonstrate the importance of considering intra‐specific aggression when exploring behavioural interactions between native and invasive species.     

North‐African house martins endure greater haemosporidian infection than their European counterparts

Afro‐Palearctic migrant species are exposed to parasites at both breeding and over‐wintering grounds. The house martin Delichon urbicum is one such migratory species facing high instances of blood parasite infection. In an attempt to determine whether breeding European house martins harbour similar blood parasite communities to populations breeding in North Africa, birds were sampled at their breeding grounds in Switzerland and Algeria. Moreover, haemosporidian prevalence and parasite communities were compared to published data sets on Spanish and Dutch breeding populations. This study furthermore wanted to establish whether co‐infection with multiple genera or lineages of parasites had negative e?ects on host body condition. Breeding house martins caught in Algeria showed a higher prevalence of avian haemosporidian parasites than did European populations. Swiss house martins showed a prevalence comparable to that of Spanish and Dutch populations. There were slight differences in the haemosporidian community between European and North‐African populations in terms of composition and abundance of each lineage. Similar to the Dutch house martins, but in contrast to the Spanish population, infection status and number of genera of parasites infecting single hosts did not in?uence Swiss house martin body condition.     

Temperature and multiple parasites combine to alter host community structure

Predicting the effects of climate change requires understanding complex interactions among multiple abiotic and biotic factors. By influencing key interactions among host species, parasites can affect community and ecosystem structuring. Yet, our understanding of how multiple parasites and abiotic factors interact to alter ecosystem structure remains limited. To empirically test the role of temperature variation and parasites in shaping communities, we used a multigenerational mesocosm experiment composed of four sympatric freshwater crustacean species (isopods and amphipods) that share up to four parasite species. Mesocosms were assigned to one of four different treatments with contrasting seasonal temperatures (normal and elevated) and parasite exposure levels (continuous and arrested (presence or absence of parasite larvae in mesocosm)). We found that parasite exposure and water temperature had interactive effects on the host community. Continuous exposure to parasites altered the community structure and differences in water temperature altered species abundance. The abundance of the amphipod Paracalliope fluviatilis decreased substantially when experiencing continuous parasite exposure and elevated water temperatures. Elevated temperatures also led to parasite-induced mortality in another amphipod host, Paracorophium excavatum. Contrastingly, isopod hosts were affected much less, suggesting increasing temperatures in conjunction with higher parasite exposure might increase their relative abundance in the community. Changes in invertebrate host populations have implications for other species such as fish and birds that consume crustaceans as well as having impacts on ecosystem processes, such as aquatic primary production and nutrient cycling. In light of climate change predictions, parasite exposure and rise in average temperatures may have substantial impacts on communities and ecosystems, altering ecosystem structure and dynamics.     

Compositional turnover in host and parasite communities does not change network structure

Decreasing similarity between ecological communities with increasing geographic distance (i.e. distance‐decay) is a common biogeographical observation in free‐living communities, and a slightly less common observation for parasite communities. Ecological networks of interacting species may adhere to a similar pattern of decreasing interaction similarity with increasing geographic distance, especially if species interactions are maintained across space. We extend this further, examining if host–parasite networks – independent of host and parasite species identities – become more structurally dissimilar with increasing geographic distance. Utilizing a global database of helminth parasite occurrence records, we find evidence for distance‐decay relationships in host and parasite communities at both regional and global scales, but fail to detect similar relationships in network structural similarity. Host and parasite community similarity were strongly related, and both decayed rapidly with increasing geographic distance, typically resulting in complete dissimilarity after approximately 2500 km. Our failure to detect a decay in network structural similarity suggests the possibility that different host and parasite species are filling the same functional roles in interaction networks, or that variation in network similarity may be better explained by other geographic variables or aspects of host and parasite ecology.     

Diverse avian malaria and other haemosporidian parasites in Andean house wrens: evidence for regional co‐diversification by host‐switching

Recent research has revealed well over 1000 mtDNA lineages of avian haemosporidian parasites, but the extent to which this diversity is caused by host–parasite coevolutionary history or environmental heterogeneity is unclear. We surveyed haemosporidian and host mtDNA in a geographically structured, ecological generalist species, the house wren Troglodytes aedon, across the complex landscape of the Peruvian Andes. We detected deep genetic structure within the house wren across its range, represented by seven clades that were between 3.4–5.7% divergent. From muscle and liver tissue of 140 sampled house wrens we found 23 divergent evolutionary lineages of haemosporidian mtDNA, of which ten were novel and apparently specific to the house wren based on searches of haemosporidian databases. Combined and genus‐specific haemosporidian abundance differed significantly across environments and elevation, with Leucocytozoon parasites strongly associated with montane habitats. We observed spatial stratification of haemosporidians along the west slope of the Andes where five lineages were restricted to non‐overlapping elevational bands. Individual haemosporidian lineages varied widely with respect to host specificity, prevalence, and geographic distribution, with the most host‐generalist lineages also being the most prevalent and widely distributed. Despite the deep divergences within the house wren, we found no evidence for host‐specific co‐diversification with haemosporidians. Instead, host‐specific haemosporidian lineages in the genus Haemoproteus were polyphyletic with respect to the New World parasite fauna and appeared to have diversified by periodic host‐switches involving distantly related avian species within the same region. These host‐specific lineages appeared to have diversified contemporaneously with Andean house wrens. Taken together, these findings suggest a model of diffuse co‐diversification in which host and parasite clades have diversified over the same time period and in the same geographic area, but with parasites having limited or ephemeral host specificity.