Coevolution between slave‐making ants and their hosts: host specificity and geographical variation

Blatrix, Rumsaïs

doi:10.1046/j.1365-294x.2003.01947.x

Cited by 25 publications

(41 citation statements)

References 30 publications

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“…Such interspecific differences in host defence strategies have also been reported in hosts of brood parasites [30] and social parasitic hosts [46] and may reflect host preference by the parasite [46]. Although we cannot rule out that differences in defence strategies and efficiencies between our two host species resulted from the use of different slavemaker populations, it could provide a mechanistic explanation for P. americanus' preference for its primary host, T. longispinosus [20,24].…”

Section: Discussionsupporting

confidence: 51%

“…The slave raid that follows is often initiated by only one or few slavemakers, which recruit nest-mates before or during the raiding attack. As host workers and the queen are often killed during a raid, few colonies survive a slavemaker attack [19,20]. Hence, frontline defences, directed to fend off slavemaker scouts or raiding parties, are likely to be selected for.…”

Section: Introductionmentioning

confidence: 99%

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Collective defence portfolios of ant hosts shift with social parasite pressure

et al. 2014

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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.

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Section: Discussionsupporting

confidence: 51%

Section: Introductionmentioning

confidence: 99%

Collective defence portfolios of ant hosts shift with social parasite pressure

et al. 2014

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“…This has indeed been demonstrated for several slavemaking ant hosts, which respond to social parasite pressure with behavioural defences against slave raids, improved recognition of intruding slavemakers, or changes in reproductive strategies Foitzik et al, 2003). Moreover, behavioural and ecological studies have demonstrated the occurrence of strong geographic variation in the interactions between slavemakers and their hosts Herbers & Foitzik, 2002;Blatrix & Herbers, 2003;Brandt & Foitzik, in press). This finding is in accordance with the geographic mosaic of coevolution theory, which states that the nature and outcome of species interactions is likely to differ between local populations, resulting in a mosaic of coevolutionary ' hot spots' and ' cold spots' (Thompson, 1994.…”

Section: Introductionmentioning

confidence: 87%

The coevolutionary dynamics of obligate ant social parasite systems – between prudence and antagonism

et al. 2005

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In this synthesis we apply coevolutionary models to the interactions between socially parasitic ants and their hosts. Obligate social parasite systems are ideal models for coevolution, because the close phylogenetic relationship between these parasites and their hosts results in similar evolutionary potentials, thus making mutual adaptations in a stepwise fashion especially likely to occur. The evolutionary dynamics of host-parasite interactions are influenced by a number of parameters, for example the parasite's transmission mode and rate, the genetic structure of host and parasite populations, the antagonists' migration rates, and the degree of mutual specialisation. For the three types of obligate ant social parasites, queen-tolerant and queen-intolerant inquilines and slavemakers, several of these parameters, and thus the evolutionary trajectory, are likely to differ. Because of the fundamental differences in lifestyle between these social parasite systems, coevolution should further select for different traits in the parasites and their hosts. Queen-tolerant inquilines are true parasites that exert a low selection pressure on their host, because of their rarity and the fact that they do not conduct slave raids to replenish their labour force. Due to their high degree of specialisation and the potential for vertical transmission, coevolutionary theory would predict interactions between these workerless parasites and their hosts to become even more benign over time. Queen-intolerant inquilines that kill the host queen during colony take-over are best described as parasitoids, and their reproductive success is limited by the existing worker force of the invaded host nest. These parasites should therefore evolve strategies to best exploit this fixed resource. Slavemaking ants, by contrast, act as parasites only during colony foundation, while their frequent slave raids follow a predator prey dynamic. They often exploit a number of host species at a given site, and theory predicts that their associations are best described in terms of a highly antagonistic coevolutionary arms race.

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“…However, recent studies show that avian brood parasites can significantly reduce lifetime reproductive output of their heterospecific hosts, sometimes even threatening host populations (e.g., Rothstein andRobinson 1994, Lotem andRothstein 1995). Hymenopteran social parasites show similar impacts on host populations (Herbers and Stuart 1998, Foitzik et al 2001, 2003, Foitzik and Herbers 2001a, Hare and Alloway 2001, Herbers and Foitzik 2002, Blatrix and Herbers 2003. Often within the same class as their host, if not closely related phylogenetically (Emery's rule;Emery 1909), social parasite-host systems are more susceptible to cyclical reciprocal selection dynamics compared to micro-and macroparasites and have become a new model system for host-parasite coevolution (Rothstein 1990).…”

Section: Introductionmentioning

confidence: 99%

Impact of Parasite Sympatry on the Geographic Mosaic of Coevolution

Johnson

2006

Ecology

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Abstract. Slave-making ants are specialized social parasites that steal the young from colonies of their host species to augment their slave supply. The degree of parasite-host specialization has been shown to shape the trajectory along which parasites and hosts coevolve and is a prime contributor to the geographic mosaic of coevolution. However, virtually nothing is known about extrinsic influences on parasite-host dynamics, although the simple addition of a competing slave-maker may significantly alter selection pressures. Here we report the effect of two sympatric slave-makers on a single host. We measured temporal and spatial changes in colonies of the primary host Temnothorax curvispinosus that had been placed in field enclosures along with a single colony of either one or both species of the North American slave-making ants Protomognathus americanus and Temnothorax duloticus. Each slave-maker species alone had a negative impact on its hosts, although one slave-maker species more frequently decimated its host assemblage and then went extinct. Nevertheless, the combined effect in mixed-parasite enclosures was, surprisingly, greatly attenuated. Virulent slave-maker growth and prudent slave-maker decay in these shared enclosures, together with field data showing an inverse proportional relationship between the two slave-makers in natural populations, suggest that their checkered distribution is a consequence of direct asymmetrical antagonism between parasites. Thus, our results imply a tripartite coevolutionary arms race, whereby intraguild interactions among social parasites strongly affect the realized selection pressures on hosts and contribute to the geographic mosaic of coevolution.

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Coevolution between slave‐making ants and their hosts: host specificity and geographical variation

Cited by 25 publications

References 30 publications

Collective defence portfolios of ant hosts shift with social parasite pressure

Collective defence portfolios of ant hosts shift with social parasite pressure

The coevolutionary dynamics of obligate ant social parasite systems – between prudence and antagonism

Impact of Parasite Sympatry on the Geographic Mosaic of Coevolution

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