Locally adapted social parasite affects density, social structure, and life history of its ant hosts

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.

The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons

“…A reduction in recognition cues through higher relative abundances of n-alkanes is a more versatile strategy, as it facilitates the exploitation of multiple host species. All of our focal slavemakers can indeed exploit several host species, and they occasionally enslave workers of different host species in the same nest [41,48]. They may profit from the absence of slavemaker-specific hydrocarbons, such that the differences to their host species are only quantitative.…”

“…These ants have small colonies with a few dozen workers and inhabit cavities in acorns or small sticks on the forest floor. Slavemaker colonies contain on average only two to five slavemakers and 30 slaves and are, in contrast to their facultative polygynous hosts, invariably monogynous [41,48]. Each slavemaker parasitizes multiple hosts, but shows a clear preference for a single host species [37,45] (electronic supplementary material, S1 for community composition and slavemaker preference).…”

Collective defence portfolios of ant hosts shift with social parasite pressure

“…Whenever possible, we therefore included long-term collection data on parasite pressure from previously studied communities (i.e. Ohio North, West Virginia, Vermont and New York [23][24][25][26]). Moreover, we have evidence for consistent parasite occurrence from some other communities that have been sampled sporadically in the past (i.e.…”

Geographic distribution of the anti-parasite trait “slave rebellion”

“…In birds, fish and insects these requirements are met, and indeed brood parasitism originated in all three taxonomic groups (Sato 1986;Rothstein 1990;Davies 1999, Buschinger 2009). In the wellstudied avian systems (Kruger 2007) as well as in social insects (Hare and Alloway 2001;Fischer-Blass et al 2006;Foitzik et al 2009) severe fitness costs for the host have been demonstrated, resulting in strong selection pressures on the host species. In response, they have developed defence mechanisms either to avoid parasitic exploitation (Alloway 1990; 45 50 55 60 Moksnes et al 1991;Roskaft et al 2002) or to reduce its costs once parasitized (Langmore et al 2003;Kruger 2007;Achenbach and Foitzik 2009).…”

“…Due to high raiding frequency and the destructiveness of these raiding events (Foitzik and Herbers 2001;Foitzik et al 2009) this evolutionary old social parasite (Beibl et al 2005) exerts high selection pressure on its three host ant species of the genus…”