[show abstract][hide abstract] ABSTRACT: Social parasites exploit the brood care behavior of other species and can exert strong selection pressures on their hosts. As a consequence, hosts have developed defenses to circumvent or to lower the costs of parasitism. Recently, a novel, indirect defense trait, termed slave rebellion, has been described for hosts of a slave-making ant: Enslaved Temnothorax longispinosus workers reduce local parasite pressure by regularly killing pupae of their obligatory slavemaking parasite Protomognathus americanus. Subsequently, growth of social parasite nests is reduced, which leads to fewer raids and likely increases fitness of neighboring related host colonies. In this study, we investigate the presence and expression the slave rebellion trait in four communities. We report its presence in all parasitized communities, document strong variation in its expression between different geographic sites and discuss potential explanations for this observed variation.
[show abstract][hide abstract] ABSTRACT: The spatial structure of host-parasite coevolution is shaped by population structure and genetic diversity of the interacting species. We analysed these population genetic parameters in three related ant species: the parasitic slavemaking ant Protomognathus americanus and its two host species Temnothorax longispinosus and T. curvispinosus. We sampled throughout their range, genotyped ants on six to eight microsatellite loci and an MtDNA sequence and found high levels of genetic variation and strong population structure in all three species. Interestingly, the most abundant species and primary host, T. longispinosus, is characterized by less structure, but lower local genetic diversity. Generally, differences between the species were small, and we conclude that they have similar evolutionary potentials. The coevolutionary interaction between this social parasite and its hosts may therefore be less influenced by divergent evolutionary potentials, but rather by varying selection pressures. We employed different methods to quantify and compare genetic diversity and structure between species and genetic markers. We found that Jost D is well suited for these comparisons, as long as mutation rates between markers and species are similar. If this is not the case, for example, when using MtDNA and microsatellites to study sex-specific dispersal, model-based inference should be used instead of descriptive statistics (such as D or G(ST) ). Using coalescent-based methods, we indeed found that males disperse much more than females, but this sex bias in dispersal differed between species. The findings of the different approaches with regard to genetic diversity and structure were in good accordance with each other.
Journal of Evolutionary Biology 02/2011; 24(4):871-86. · 3.48 Impact Factor
[show abstract][hide abstract] ABSTRACT: Parasites and hosts frequently engage in coevolutionary arms races, in which newly developed host defenses will be counteracted by parasite adaptations. Slave-making ants are virulent social parasites that trick enslaved host workers into caring for their brood. These slaves also have to accept stolen host pupae, which slavemakers retrieve during raids. Previously, selection was thought to be unable to act on traits of these enslaved host ants. Yet, a recent study demonstrated rebellion of enslaved Temnothorax workers, which selectively killed female pupae of the slave-making ant Protomognathus americanus. This defensive trait could lower the costs of parasitism because slowed growth of parasite nests reduces raiding impact on related neighboring host colonies. In cross-fostering experiments, we investigated the acceptance of host and parasite pupae by Temnothorax workers in parasitized and unparasitized colonies. Host workers commonly killed transferred pupae, and the presence of the social parasite only increased acceptance of parasite pupae in 1 host species and that of heterospecific host pupae in a second host. Parasite pupae survived better when transferred to sympatric host colonies than to allopatric ones, possibly indicating local adaptation in the parasite P. americanus. Cuticular hydrocarbon analyses explain this with chemical differences in pupae profiles between communities. Overall, parasite and host pupae have highly divergent profiles. Hence, cuticular hydrocarbons can potentially be used by host workers to identify and destroy parasite pupae. The parasite P. americanus should be under strong selection to adapt its pupal recognition cues to those of its hosts to counteract slave rebellion. Copyright 2010, Oxford University Press.
[show abstract][hide abstract] ABSTRACT: Selection and adaptation are important processes in the coevolution between parasites and their hosts. The slave-making ant Protomognathus americanus, an obligate ant social parasite, has previously been shown to evolve morphological, behavioral, and chemical adaptations in the coevolutionary arms race with its Temnothorax hosts. Yet empirical studies have given variable results on the strength of the selection pressure this parasite exerts on its host populations. In this study, we directly investigated the pressure exerted by P. americanus and the reactions of the main host species, T. longispinosus, in two ant communities by manipulating parasite density in the field over several years. In addition, a cross-fostering design with the exchange of parasites between host populations allowed us to investigate local adaptation of parasite or host. We demonstrate a severe impact of the social parasite on the two host populations in West Virginia and New York, but also variation in host reactions between sites, as expected by the geographic mosaic theory of coevolution. Host density decreased at the West Virginia site with the presence of local slave-makers, whereas at the ecologically favorable New York site, density was unaffected. Nevertheless, social organization, colony size, and investment patterns of these host colonies at this site changed in response to our parasite manipulation. The release of P. americanus colonies led to a reduction in the number of resident queens and workers, an increase in intranest relatedness, and lower productivity, but also a higher investment in reproductives. In West Virginia, colony demography did not change, but raiding activity by New York slave-makers caused different investment patterns of host colonies. In addition, the cross-fostering element revealed local adaptation of the parasite P. americanus: slave-making colonies fared better in their sympatric host population, as they contained more slave-making ant workers and slaves at the end of our 27-month experiment.
[show abstract][hide abstract] ABSTRACT: During the process of coevolution, social parasites have evolved sophisticated strategies to exploit the brood care behavior of their social hosts. Slave-making ant queens invade host colonies and kill or eject all adult host ants. Host workers, which eclose from the remaining brood, are tricked into caring for the parasite brood. Due to their high prevalence and frequent raids, following which stolen host broods are similarly enslaved, slave-making ants exert substantial selection upon their hosts, leading to the evolution of antiparasite adaptations. However, all host defenses shown to date are active before host workers are parasitized, whereas selection was thought to be unable to act on traits of already enslaved hosts. Yet, here we demonstrate the rebellion of enslaved Temnothorax workers, which kill two-thirds of the female pupae of the slave-making ant Protomognathus americanus. Thereby, slaves decrease the long-term parasite impact on surrounding related host colonies. This novel antiparasite strategy of enslaved workers constitutes a new level in the coevolutionary battle after host colony defense has failed. Our discovery is analogous to recent findings in hosts of avian brood parasites where perfect mimicry of parasite eggs leads to the evolution of chick recognition as a second line of defense.