Community Context and Specialization Influence Coevolution Between a Slavemaking Ant and Its Hosts

Abstract

The dynamics of host–parasite coevolution are thought to be influenced not only by inherent parameters, but also by their community context. Here we report strong differences in the degree of specialization of a social parasite at different geographic sites. Furthermore, we provide the first empirical evidence for a deceleration of the coevolutionary arms race caused by the inclusion of a second host species into a parasite–host association. We compare two communities, each including the North American slavemaking ant Protomognathus americanus and two Leptothorax host species, with similar parasite and host densities. At the first site, the minority host species occurred at frequencies too low to sustain the parasite, whereas at the second location, both hosts constituted an exploitable resource. Thus, only in the latter community does the parasite have the options to expand its niche or to alternate between the available host species. During slave raids, which represent the crucial parasite–host encounter, hosts and slavemakers from the second site were less efficient at defending and raiding, respectively. Thus, we demonstrate a higher degree of reciprocal adaptation at the location where the parasite specializes on a single host, indicating a more advanced stage of the arms race.

Collective defence portfolios of ant hosts shift with social parasite pressure

“…To assess whether slavemaker sympatry affected colony responses, we tested each of the 64 experimental T. longispinosus colonies from New York and West Virginia against both a sympatric and an allopatric slavemaker in random order with a 7-day interval. As in previous behavioural studies [10,24], we found no effect of slavemaker sym-or allopatry (GLMMs with colony identity, nested in population identity as random factor: number of aggressive workers: x 2 ¼ 0.01, p ¼ 0.931; evacuation probability: We assessed whether collective defences to an intruding slavemaker and the efficiency of such responses were associated with parasite pressure, host species identity and host colony size. Hereto, we analysed the likelihood of collective immobilization (i.e.…”

“…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”

“…It is not easy to quantify parasite pressure, because it depends on several parameters such as parasite prevalence, raid frequency and destructiveness as well as community composition. Previous studies have shown that parasite prevalence is very similar in the three focal communities (Table 1), but slavemaker colonies in NY seem to have a higher frequency of successful raids as compared to WV and OH (Foitzik et al 2001, Brandt & Foitzik 2004). …”

“…We study hosts from three well-studied communities in New York (NY), West Virginia (WV) and Ohio (OH), which differ in their community composition, but are very similar in parasite prevalence (Herbers and Foitzik 2002;Brandt and Foitzik 2004). Previous studies have found differences between the three communities which may be important for our study.…”

“…Indeed, population genetic analyses based on neutral markers detected strong structuring in the host and the parasite (Brandt et al 2007;Pennings et al 2011). In addition, geographic differences in other defence behaviours have been documented (Brandt and Foitzik 2004). of host pupae vary, restrictive non-parasitized workers would be at risk to reject a proportion of their own pupae.…”