2997 Ecology, 85(11), 2004, pp. 2997–3009  2004 by the Ecological Society of America COMMUNITY CONTEXT AND SPECIALIZATION INFLUENCE COEVOLUTION BETWEEN A SLAVEMAKING ANT AND ITS HOSTS MIRIAM BRANDT 1 AND SUSANNE FOITZIK Department Biology I, University of Regensburg, Universita ¨tsstrasse 31, 93040 Regensburg, Germany 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 Pro- tomognathus 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. Key words: arms race; coevolution; community structure; host alternations; host–parasite in- teractions; Protomognathus americanus; Red Queen process; slavemaking ants; social parasites; spe- cialization. INTRODUCTION Parasites exhibit the most common lifestyle on earth, and they affect nearly all other living organisms. There- fore, the coevolutionary interactions with their hosts are among the major processes shaping the earth’s bio- diversity (Thompson 1994, 1999). These antagonistic species interactions are often assumed to result in an endless process of reciprocal coadaptation that has been described in the ‘‘arms race’’ (Dawkins and Krebs 1979) and ‘‘Red Queen’’ (Van Valen 1973) metaphors. In contrast to the traditionally known parasites that exploit the physiology of an individual host, ‘‘social parasites’’ are social insects that parasitize complete societies. By taking advantage of the brood-care be- havior of other social insect species, thereby reducing the host’s fitness considerably, social parasites avoid the costs of parental care in an analogous fashion to avian brood parasites such as cuckoos and cowbirds (Davies et al. 1989). Of the approximately 10 000 spe- cies of ants, about 200 are social parasites, 50 of which in turn are dulotic, or slavemaking, species (Ho ¨lldobler and Wilson 1990). Dulosis can be facultative, when the parasitic species is still able to maintain its colonies without a heterospecific work force, or obligate, such as in the species studied here. Obligate slavemakers are dependent on their hosts in all stages of their life cycle. A slavemaker colony is initiated when a mated Manuscript received 24 November 2003; revised 4 May 2004; accepted 5 May 2004. Corresponding Editor: P. Nonacs. 1 E-mail: miriam.brandt@web.de parasite queen invades a host colony, kills or expels all adult individuals, and appropriates the larvae and pupae (Wesson 1939). Because ants learn their colony odor in a sensitive phase in early adult life (Breed and Bennett 1987, Vander Meer and Morel 1998), host workers that emerge from the usurped brood are im- printed on the slavemaker queen and thus accept the parasite colony as their own. Subsequently, the en- slaved host workers carry out all necessary tasks of colony maintenance, and they also care for the slave- maker queen’s brood. Obligate slavemaker workers, in contrast, are specialized on only a single task: they regularly conduct raids on neighboring host colonies, steal their brood, and carry it back to their own nest in order to replenish their supply of slaves (Wesson 1939, Alloway 1979, Buschinger et al. 1980, Topoff et al. 1989, Schumann 1992). For a long time it was generally accepted that social parasites were too rare to exert significant selection pressure on their hosts. However, recent studies on the Formicoxenine slavemaking ants have invalidated this assumption (Herbers and Stuart 1998, Foitzik et al. 2001, Foitzik and Herbers 2001, Hare and Alloway 2001, Herbers and Foitzik 2002, Blatrix and Herbers 2003, Foitzik et al. 2003). The slavemaker Protomog- nathus americanus is a small myrmicine ant widely distributed in deciduous forests throughout the north- eastern United States and Canada. This social parasite, which enslaves the three closely related Leptothorax species (Temnothorax according to a recent classifi- cation by Bolton [2003]), L. longispinosus, L. curvis-