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

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

Oh sister,where art thou? Spatial population structure and the evolution of an altruistic defence trait

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post‐enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites’ offspring. As enslaved workers do not reproduce, they gain no direct fitness benefit from this ‘rebellion’ behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to ‘rebel’ nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers’ killing behaviour. We use a simple mathematical model to examine whether the small‐scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study, we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small‐scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of ‘rebellion’ by kin selection.     

Phylogeography and the geographic cline in the armament of a seed-predatory weevil: effects of historical events vs. natural selection from the host plant

Japanese camellia (Camellia japonica) and its seed predator, the camellia weevil (Curculio camelliae), provide a notable example of a geographic mosaic of coevolution. In the species interaction, the offensive trait of the weevil (rostrum length) and the defensive trait of the plant (pericarp thickness) are involved in a geographically-structured arms race, and these traits and selective pressures acting on the plant defence vary greatly across a geographical landscape. To further explore the geographical structure of this interspecific interaction, we tested whether the geographical variation in the weevil rostrum over an 800-km range along latitude is attributed to local natural selection or constrained by historical (phylogeographical) events of local populations. Phylogeographical analyses of the mitochondrial DNA sequences of the camellia weevil revealed that this species has experienced differentiation into two regions, with a population bottleneck and subsequent range and/or population expansion within each region. Although these phylogeographical factors have affected the variation in rostrum length, analyses of competing factors for the geographical variation revealed that this pattern is primarily determined by the defensive trait of the host plant rather than by the effects of historical events of populations and a climatic factor (annual mean temperature). Thus, our study suggests the overwhelming strength of coevolutionary selection against the effect of historical events, which may have limited local adaptation.     

Population structure and the co-evolution between social parasites and their hosts

Co-evolutionary trajectories of host-parasite interactions are strongly affected by the antagonists' evolutionary potential, which in turn depends on population sizes as well as levels of recombination, mutation, and gene flow. Under similar selection pressures, the opponent with the higher evolutionary rate is expected to lead the co-evolutionary arms race and to develop local adaptations. Here, we use mitochondrial DNA sequence data and microsatellite markers to assess the amount of genetic variability and levels of gene flow in two host-parasite systems, each consisting of an ant social parasite--the European slavemaker Harpagoxenus sublaevis and the North American slavemaker Protomognathus americanus--and its two main host species. Our population genetic analyses revealed limited gene flow between individual populations of both host and parasite species, allowing for a geographic mosaic of co-evolution. In a between-system comparison, we found less genetic variability and more pronounced structure in Europe, where previous behavioural studies demonstrated strong local adaptation. Within the European host-parasite system, the larger host species Leptothorax acervorum exhibited higher levels of both genetic variability and gene flow, and previous field data showed that it is less affected by the social parasite H. sublaevis than the smaller host Leptothorax muscorum, which has genetically depleted and isolated populations. In North America, the parasite P. americanus showed higher levels of gene flow between sites, but overall less genetic diversity than its hyper-variable main host species, Temnothorax longispinosus. Interestingly, recent ecological and chemical studies demonstrated adaptation of P. americanus to local host populations, indicating the importance of migration in co-evolutionary interactions.     

Low host-pathogen specificity in the leaf-cutting ant-microbe symbiosis

Host-parasite associations are shaped by coevolutionary dynamics. One example is the complex fungus-growing ant-microbe symbiosis, which includes ancient host-parasite coevolution. Fungus-growing ants and the fungi they cultivate for food have an antagonistic symbiosis with Escovopsis, a specialized microfungus that infects the ants' fungus gardens. The evolutionary histories of the ant, cultivar and Escovopsis are highly congruent at the deepest phylogenetic levels, with specific parasite lineages exclusively associating with corresponding groups of ants and cultivar. Here, we examine host-parasite specificity at finer phylogenetic levels, within the most derived clade of fungus-growing ants, the leaf-cutters (Atta spp. and Acromyrmex spp.). Our molecular phylogeny of Escovopsis isolates from the leaf-cutter ant-microbe symbiosis confirms specificity at the broad phylogenetic level, but reveals frequent host-switching events between species and genera of leaf-cutter ants. Escovopsis strains isolated from Acromyrmex and Atta gardens occur together in the same clades, and very closely related strains can even infect the gardens of both ant genera. Experimental evidence supports low host-parasite specificity, with phylogenetically diverse strains of Escovopsis being capable of overgrowing all leaf-cutter cultivars examined. Thus, our findings indicate that this host-pathogen association is shaped by the farming ants having to protect their cultivated fungus from phylogenetically diverse Escovopsis garden pathogens.     

The behaviour of an omnivorous protozoan affects the extent of induced morphological defence in a protozoan prey

1. The ciliate Euplotes octocarinatus responds to the presence of Stylonychia mytilus with a morphological transformation rendering its ingestion more difficult. Predation on Euplotes is reduced when an alternative prey, the flagellate Chlorogonium elongatum, is available. Lower predation is accompanied by reduced induction in Euplotes. 2. We quantified the motility of both ciliates in the presence and absence of Chlorogonium to test the hypothesis that the differential response in Euplotes is a consequence of behavioural changes affecting the encounter rate of the prey and the predator. 3. The results indicate that S. mytilus uses different feeding strategies for each prey. It is a filter feeder when small food particles (Chlorogonium) are abundant, however, it becomes a raptorial feeder when large prey with an escape capability (Euplotes) is available and small alternative prey are absent. 4. As the mobility of filter feeding Stylonychia is strongly limited, the presence of the flagellate may indirectly affect the defence level in Euplotes by reducing the frequency of contacts with the predator. 5. An experiment with Chaetogaster diastrophus, a more specialised predator not affected by the presence of Chlorogonium, as well as direct manipulation of the encounter rate by changing the surface area available for the crawling ciliates, supported the encounter rate hypothesis.     

Evolutionary transition to a semelparous life history in the socially parasitic ant Acromyrmex insinuator

The recently discovered social parasite Acromyrmex insinuator ( 25 ) exploits colonies of the leafcutter ant A. echinatior. We document that A. insinuator represents a rare early stage in the evolution of social parasitism, because a worker caste is still partially present and mating phenology has remained at least partially similar to that of the host. A. insinuator is tolerant of host queens, and sexual offspring produced in parasitized colonies can be either exclusively A. insinuator or a mix of A. insinuator and A. echinatior. The remarkably high abundance of A. insinuator in nests of the investigated Panamanian host population and the fact that A. insinuator colonies readily reproduce under laboratory conditions allowed us to test evolutionary predictions on reproductive life history evolution that are not possible in most other socially parasitic ants. We show that (1) A. insinuator has a semelparous ‘big bang’ reproductive life history which exploits host colonies without leaving reserves for survival; (2) social parasite sexuals are significantly smaller than A. echinatior host sexuals, but still large compared to host workers, confirming an evolutionary scenario of gradual size reduction and loss of the worker caste after transition towards a socially parasitic life history; (3) major changes in the life history of ants can evolve relatively quickly compared to adaptations in morphology, caste differentiation and mating phenology.     

Characterization of 24 microsatellite markers in 11 species of fire ants in the genus Solenopsis (Hymenoptera: Formicidae)

The social parasite ant Solenopsis daguerrei infests colonies of several mound-building fire ant species. Twenty-four microsatellite markers were isolated from a repeat-enriched genomic library of S. daguerrei. Eleven loci were polymorphic in this ant with two to six alleles per locus. Expected heterozygosity ranged from 0.0222 to 0.7940 among loci. Most microsatellites amplified successfully across the 11 Solenopsis species tested and will be useful for evolutionary genetic studies in this diverse ant group.     

The impact of environmental change on host-parasite coevolutionary dynamics

Environmental factors are known to affect the strength and the specificity of interactions between hosts and parasites. However, how this shapes patterns of coevolutionary dynamics is not clear. Here, we construct a simple mathematical model to study the effect of environmental change on host-parasite coevolutionary outcome when interactions are of the matching-alleles or the gene-for-gene type. Environmental changes may effectively alter the selective pressure and the level of specialism in the population. Our results suggest that environmental change altering the specificity of selection in antagonistic interactions can produce alternating time windows of cyclical allele-frequency dynamics and cessation thereof. This type of environmental impact can also explain the maintenance of polymorphism in gene-for-gene interactions without costs. Overall, our study points to the potential consequences of environmental variation in coevolution, and thus the importance of characterizing genotype-by-genotype-by-environment interactions in natural host-parasite systems, especially those that change the direction of selection acting between the two species.     

Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host?

Many parasites show fidelity to a set of hosts in ecological time but not evolutionary time and the determinants of this pattern are poorly understood. Malarial parasites use vertebrate hosts for the asexual stage of their life cycle but use Dipteran hosts for the sexual stage. Despite the potential evolutionary importance of Dipteran hosts, little is known of their role in determining a parasite's access to vertebrate hosts. Here, we use an avian malarial system in Panama to explore whether mosquitoes act as an access filter that limits the range of vertebrate hosts used by particular parasite lineages. We amplified and sequenced Plasmodium mitochondrial DNA (mtDNA) from Turdus grayi (clay-coloured robin) and from mosquitoes at the same study site. We trapped and identified to species 123 141 female mosquitoes and completed polymerase chain reaction (PCR) screening for Plasmodium parasites in 435 pools of 20 mosquitoes per pool (8700 individuals total) spanning the 11 most common mosquito species. Our primers amplified nine Plasmodium lineages, whose sequences differed by 1.72%–10.0%. Phylogenetic analyses revealed partial clustering of lineages that co-occurred in mosquito hosts. However PAN3 and PAN6, the two primary parasite lineages of T. grayi , exhibited sequence divergence of 8.59% and did not cluster in the phylogeny. We detected these two lineages exclusively in mosquitoes from different genera — PAN3 was found only in Culex (Melanoconion) ocossa , and PAN6 was found only in Aedeomyia squamipennis . Furthermore, each of these two parasite lineages co-occurred in mosquitoes with other Plasmodium lineages that were not found in the vertebrate host T. grayi . Together, this evidence suggests that parasite–mosquito associations do not restrict the access of parasites to birds but instead may actually facilitate the switching of vertebrate hosts that occurs over evolutionary time.     

Genetic diversity,population structure and sex‐biased dispersal in three co‐evolving species

Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost’s D_est ), we detected strong population structuring in all species and less male‐biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post‐glacial colonization routes – northern populations are as variable as more southern populations. We conclude that conditions for Thompson’s geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.