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Ecology, 85(11), 2004, pp. 2997–3009 q 2004 by the Ecological Society of America

COMMUNITY CONTEXT AND SPECIALIZATION INFLUENCE COEVOLUTION BETWEEN A SLAVEMAKING ANT AND ITS HOSTS MIRIAM BRANDT1

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 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. Key words: arms race; coevolution; community structure; host alternations; host–parasite interactions; Protomognathus americanus; Red Queen process; slavemaking ants; social parasites; specialization.

INTRODUCTION Parasites exhibit the most common lifestyle on earth, and they affect nearly all other living organisms. Therefore, the coevolutionary interactions with their hosts are among the major processes shaping the earth’s biodiversity (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 behavior 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 species 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: [email protected]

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 imprinted on the slavemaker queen and thus accept the parasite colony as their own. Subsequently, the enslaved host workers carry out all necessary tasks of colony maintenance, and they also care for the slavemaker 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 Protomognathus americanus is a small myrmicine ant widely distributed in deciduous forests throughout the northeastern United States and Canada. This social parasite, which enslaves the three closely related Leptothorax species (Temnothorax according to a recent classification by Bolton [2003]), L. longispinosus, L. curvis-

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pinosus, and L. ambiguus, can have a severe impact on its hosts. In some communities, slavemaker colonies conduct about 5–11 raids per year, giving each host colony a .50% chance of being raided. Furthermore, slavemaker attacks are extremely destructive and often result in the death of the host colony (Foitzik and Herbers 2001), and the recurrent slave raids thus impose a strong selection pressure on hosts to evolve defense adaptations. The first evidence that P. americanus and its L. longispinosus host indeed engage in a coevolutionary arms race was recently found by Foitzik and coworkers (2001), who could show that the strength of reciprocal adaptation varies between populations and is linked to local parasite pressure. These interpopulation differences in the progression of the Red Queen process are in accordance with the geographic mosaic of coevolution theory (Thompson 1994, 1999, Gomulkiewicz et al. 2000). This hypothesis suggests that coevolution is not a uniform process over broad geographic ranges, but that the nature and outcome of species interactions are likely to differ between local populations. Under this view, communities differ in the strength of the reciprocal selection pressures (coevolutionary ‘‘hot spots’’ and ‘‘cold spots’’) or in terms of the traits that are actually shaped by an interaction. The existence of geographic structure in the coevolutionary interaction between P. americanus and its host L. longispinosus has been demonstrated on the behavioral (Foitzik et al. 2001), demographic (Herbers and Stuart 1998, Foitzik and Herbers 2001), and ecological level (Herbers and Foitzik 2002). These studies agree that a study site in upstate New York (USA) represents a hot spot of coevolution with strong reciprocal selection pressures. At this site, hosts apparently experience optimal ecological conditions and occur at extremely high densities. Other locations in West Virginia and Vermont (USA), in contrast, were found to be characterized by weaker coevolutionary interactions, thus constituting ‘‘cold spots’’ in the arms race between slavemaker and host. The main explanation for the observed variation in the intensity of coevolution invoked the pronounced differences in parasite prevalence between the studied locations (Foitzik et al. 2001, Herbers and Foitzik 2002). Studies on other model systems, however, have shown that the outcome of coevolutionary interactions is influenced not only by intrinsic parameters such as parasite pressure, but also strongly depends on the community context in which they occur (Thompson and Pellmyr 1992, Benkman 1999, Benkman et al. 2001, 2003, Choo et al. 2003). For example, Benkman and coworkers demonstrated that the arms race between crossbills and pine is disrupted in communities where red squirrels occur as a competing predator. A similar disruption could arise at sites where a parasite uses more than one host species, but studies examining the effect of different degrees of specialization of a parasite

Ecology, Vol. 85, No. 11

on the progression of the arms race with its hosts are as yet lacking. When more than one host species are included in a parasite–host association, one possible outcome is that the parasite population splits into distinct host races, as has been demonstrated for various parasites (Marchetti et al. 1998, Gibbs et al. 2000, McCoy et al. 2001, Dres and Mallet 2002). However, genetic analyses of P. americanus from several populations showed that no distinct host races exist in our study system (degree of population substructure as measured by Fst [st 5 subpopulation total]; Fst between P. americanus with L. curvispinosus and L. longispinosus slaves: 20.009, P 5 0.40; M. Brandt and S. Foitzik, unpublished data). If the possibility of host-race formation is excluded, a parasite confronted with multiple hosts has two options remaining: it can either expand its niche and become more generalistic, or remain specialized on a single host, but alternate its host preferences over time, depending on the defensive abilities of its available host species. Whichever strategy the parasite adopts, theory predicts the association to be weaker and the speed of the coevolutionary arms race to be reduced in the interaction of a parasite with several hosts (Kawecki 1994, 1998, Whitlock 1996, Thompson 1999). Here, we test this hypothesis by comparing the coevolutionary interactions between the slavemaker P. americanus and its hosts from two communities. The first site is the extensively studied hot-spot location in New York, where only a single host species is available as a reliable resource for the parasite; a second cooccurring host is far too rare and patchily distributed to sustain a parasite population. In contrast to earlier studies, we now explicitly searched for a community with comparable parasite and host densities, but a different composition of the host community. We found a suitable site in Ohio (USA), where two host species occur at consistently high densities, giving the parasite a choice between different hosts. In the comparison of these two sites, we could exclude parasite pressure as an important factor for differences in the intensity of the coevolutionary interaction. Slavemaking ants interact with their hosts in various stages of their life cycle. However, the encounters differ with respect to their importance in the coevolutionary arms race. For host colonies, usurpation attempts by slavemaker queens are extremely rare events (Foitzik and Herbers 2001), and, once enslaved, hosts have no possibility of rebellion (Gladstone 1981); therefore these interactions with the parasite are unlikely to select for host counteradaptations. In contrast, slave raids represent the critical interaction for the coevolutionary arms race, not only because they are frequent, but also because post-raid host-colony survival strongly depends on behavioral anti-parasite strategies during a slave raid. Likewise, raiding success is an important fitness component for the slavemaker, who completely depends on the slave labor force for colony growth and

COEVOLUTION IN SLAVEMAKING ANTS

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FIG. 1. Experimental design of the two series of (a) raiding and (b) choice experiments, with sample sizes given next to the arrow for each combination of slavemaker and host. The first trial series was an intrapopulational comparison of host defenses, whereas in the second series, we cross-fostered slavemakers from New York and Ohio with the dominant host species from each site. L. curv. 5 Leptothorax curvispinosus; L. long. 5 L. longispinosus; and L. amb. 5 L. ambiguus.

reproduction; hence slave raids strongly select for reciprocal behavioral adaptations. In this study, we compare the effectiveness of parasite raiding and host defense behavior during this decisive component of the slavemaker–host arms race. We conducted two trial series, investigating first within- and then between-community patterns of virulence and resistance (Fig. 1). In the first series of raiding experiments, we compared the defensive abilities of the two co-occurring host species from each site—L. longispinosus and L. ambiguus in New York and L. curvispinosus and L. longispinosus in Ohio—against attacks by their sympatric slavemaker in staged slave raids in the laboratory. In the second part of this study, we used the same methodology to examine the strength of the reciprocal adaptations in the two communities. Since the outcome of a slave raid is always an interaction between parasite virulence and host defense characters, we used a cross-fostering approach to investigate the effectiveness of the two antagonists: Slavemakers from New York and Ohio were tested against the dominant host species from the two sites. METHODS

Community composition and parasite prevalence We studied two communities of Protomognathus americanus and its hosts in the United States, one in the Huyck Preserve, Rensselaerville, Albany County, New York (42831935.30 N, 7489930.10 W) and the other in Harpersfield, Ashtabula County, Ohio (41845934.20 N, 80857955.70 W). The distance between the two sites is about 600 km. The habitat at both locations is second-growth temperate deciduous forest dominated by maple and oak, with additional beech and hemlock in New York and hickory in Ohio. The New York site is at a slightly higher elevation (400–500 m) than the one in Ohio (250 m). Nevertheless, abiotic conditions are roughly equivalent across the two locations. At the New York site, temperatures range from an average of

26.68C in winter to a mean of 218C in summer (source: Huyck Preserve, Rensselaerville), while in Ohio the mean temperatures in January and July are 248C and 238C, respectively (source: Ohio Department of Development). Mean annual precipitation is 90 cm in New York (NY) and 88 cm in Ohio (OH). Nest densities of P. americanus and its host species were obtained by mapping quadratic plots of 5 3 5 m (N 5 50 plots for NY; N 5 15 plots for OH). These ants nest in small preformed plant cavities such as hollow acorns, nuts, and rotting sticks on the forest floor. During excavation, all potential nest sites were opened, all colonies of P. americanus and its hosts were collected, and the exact locations of the ant nests were mapped. Other ant species that inhabited the same nest sites as the slavemaker and its hosts were also recorded. At both sites, P. americanus was the only socially parasitic species exploiting the co-occurring Leptothorax species. However, we found two fairly common nonleptothoracine ant species that constitute potential competitors for nest sites and food at both locations: Myrmica punctiventris and Lasius alienus (Herbers 1989). In the Ohio community these competing species occur at slightly higher frequencies; however, within-site variation in the density of these species was always much higher than between-site variation. Moreover, the presence of potential competitors did not significantly influence the densities of P. americanus and its hosts, as neither host nor parasite nest densities differed between the two collecting areas (hosts: mean of 1.0 nests/m 2 in NY; 1.2 nests/m2 in OH; t test, NNY 5 50 plots, NOH 5 15 plots, t 5 21.44, P 5 0.15; slavemakers: 0.12 nests/m2 in NY; 0.09 nests/m2 in OH; t test, NNY 5 50 plots, NOH 5 15 plots, t 5 0.80, P 5 0.43). In order to obtain a measure of parasite prevalence, we used our field mapping and collecting data from the years 1998–2003 to calculate the ratio of P. americanus colonies with slaves of a certain host species to the number of free-living host colonies of the respective

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species. Mixed slavemaker colonies, containing slaves of two species (30 colonies with L. longispinosus and L. ambiguus in New York, 8 colonies with L. curvispinosus and L. longispinosus in Ohio) were allocated to one of the host species according to the overall ratio of slaves in mixed colonies.

Collection and maintenance of colonies We collected slavemaker and host colonies in the summers of 2001 and 2002. Colonies were transported to the laboratory in Regensburg (Germany) in their natural nesting sites, censused, and moved to artificial nests in three-chambered plastic boxes (10 3 10 3 1.5 cm) with a moistened plaster floor (Buschinger 1974). We kept slavemaking colonies in an incubator at a cycle of 258C for 14 h light and 178C for 10 h dark. Host colonies were kept at slightly lower temperatures (15 8C for 14 h light, and 88C for 10 h dark) in order to retard the emergence of pupae and thus to elongate the raiding period. Ants were fed pieces of cockroach and honey twice weekly.

Trial series 1: within-community comparisons In order to compare the defensive abilities of the cooccurring host species, the first series of experiments tested the two host species from each site against their sympatric slavemaker. In raiding trials (Fig. 1a), slavemakers from New York were allowed to raid either a L. longispinosus or a L. ambiguus colony. Similarly, we let Ohio parasites raid either a L. curvispinosus or a L. longispinosus colony. Since we found strong differences in parasite prevalence for the two co-occurring host species at the Ohio site, we wanted to investigate possible host preferences of parasites from this location. Thus, we conducted additional choice experiments (Fig. 1b) in which P. americanus colonies from Ohio had the opportunity to choose between their sympatric host species.

Trial series 2: between-community comparisons Our second trial series aimed at comparing the effectiveness of slavemaker raiding and host defense behavior between the two communities. Therefore we cross-fostered slavemakers from the two populations with the dominant host species from each site, L. longispinosus from New York and L. curvispinosus from Ohio. In raiding experiments (Fig. 1a), slavemakers from Ohio conducted raids against L. longispinosus (NY) and against L. curvispinosus (OH), and we analyzed trials of New York slavemakers with L. longispinosus (NY) and with L. curvispinosus (OH). To investigate host preferences of the parasites, we performed choice experiments (Fig. 1b) in which parasites from the two populations were allowed to choose between L. longispinosus (NY) and L. curvispinosus (OH).


Raiding experiments We conducted the behavioral experiments for trial series 1 in August and September 2002 and for trial series 2 in the same months of 2001. In both trial series, slavemaker and host colonies were assigned to the experimental groups controlling for demographic differences. Thus, slavemaker colonies did not differ in queen number, worker number, amount of brood or number and species of slaves. Similarly, there was no difference in host colonies with regard to queen number, worker number, or amount of brood (Mann-Whitney U tests, all NS at P . 0.10). In the analysis of the effect of slave species on the outcome of raids, mixed slavemaker colonies were allocated to the majority slave species if this host species contributed .80% of the slaves. We observed raids in arenas (43 3 27 3 16 cm) with a moistened plaster floor to regulate humidity. Between two experiments, each arena was carefully cleaned to ensure that all residual odors were removed. We put slavemaker colonies into the arena 12 h prior to the start of the experiment to allow foragers and scouts to get accustomed to the arena. The trial started when we placed a host colony in the arena at a distance of 40 cm from the slavemaker colony. An empty nest site was additionally provided as an escape option for the hosts. Trials were terminated 24 h after the last piece of host brood had been removed from the host nest. Following completion, we censused all ants and brood in the three nest sites and in clusters elsewhere in the arena. Host brood found in the slavemaker nest was counted as ‘‘captured,’’ while brood guarded by host workers, either in the escape nest or in clusters in the arena, was defined as ‘‘salvaged.’’ The number of injured (i.e., having lost legs or antennae) and killed individuals of each species was also recorded.

Choice experiments In these trial series we gave slavemaker colonies the choice between two similarly sized colonies of two host species. In the second trial series, P. americanus colonies from New York and Ohio had the choice between the dominant host species from each site. Slavemaker colonies from the two populations that were used in the choice experiments did not differ in size (MannWhitney U tests; N 5 21 colonies, NOH 5 16 colonies, all NS at P . 0.40). Likewise, the host colonies used contained the same amount of brood and adult workers (Wilcoxon matched-pair tests, N 5 37 colonies, both NS at P . 0.15). For the choice experiments, we reused slavemaker colonies from the raiding experiments and allowed them to raid a second host nest. We assumed these slavemakers were still motivated to raid a second host colony, as naturally occurring P. americanus colonies conduct an average of 5–11 raids per season (Foitzik and Herbers 2001). The choice experiments were con-


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TABLE 1. Composition of Leptothorax host communities and parasite prevalence at the study sites in New York and Ohio (USA).

Host species

No. free-living host colonies

Nest density (no./m2)

No. parasite colonies with enslaved ants

Parasite: host ratio

New York L. longispinosus L. ambiguus

2054 108

0.94 6 0.472 0.06 6 0.085

285 13

1:8.2 1:9.3

Ohio L. curvispinosus L. longispinosus

647 261

0.91 6 0.612 0.30 6 0.272

42 47

1:16.4 1:6.6

Notes: Host nest densities are based on mapping results of 1250 m2 in New York and 375 m2 in Ohio; data are means 6 1 SD. The number of slavemaker and host nests was obtained by combining mapping and collecting data.

ducted in smaller, plastered arenas of 20 3 20 3 9 cm to ensure that scouts would discover both host nests with a high likelihood. We did not observe these trials for the entire period, but checked several times per day whether a raid had taken place. Experiments were stopped as soon as the raid of one host colony was completed or when all slavemaker workers were killed by the hosts.

Data analysis Raiding experiments had three possible outcomes: (1) slavemakers did not attempt to raid the host colony during at least three days; this happened in about 11% of the 159 trials we conducted and occurred predominantly with small parasite nests; (2) a raid was attempted, i.e., at least one slavemaker entered the host nest, but the parasite did not succeed in obtaining any host brood; and (3) slavemakers successfully transported host brood to their own nest. Replicates in category (1) were completely excluded from the data analysis, thus sample sizes given in Fig. 1 refer to the trials in which a raiding attempt took place (categories (2) and (3)). These experiments were used to analyze parameters pertaining to host defenses and participation of slaves in raids. For the analysis of specific raiding parameters, e.g., the proportion of brood captured by the slavemaker, we excluded the unsuccessful raiding attempts and used only trials in category (3). Some parameters could not be obtained for all experiments, thus sample sizes differ slightly between tests. For example, it was not possible to continually observe all raids, so the time until the first extrication of brood by host workers is available only for a subset of trials. Similarly, the proportion of host workers killed could only be assessed in raids where host and slave workers belonged to different species. In order to analyze host defensive abilities, we recorded the number of slavemakers killed during a raiding attempt. However, since P. americanus nests are typically very small, colonies contained a median of only 4 slavemaker workers (quartiles 3–6). Furthermore, there was considerable variance in the number of slavemakers that participated in raids, therefore the

death toll for slavemakers is difficult to express as a meaningful proportion. For this reason, we used the proportion of trials in which hosts succeeded in killing at least one slavemaker worker as a measure of their defensive ability. In the statistical analysis, we tested for accordance with ANOVA assumptions with Kolmogorov-Smirnov and Levene’s tests. If assumptions were violated, data were arcsine transformed, or nonparametric tests were employed. When several tests had to be performed on the same data set, P values given are corrected using sequential Bonferroni correction (Rice 1989). In trial series 1, where the effects of raided host species and slave species were examined for the Ohio community, we employed these two factors in a MANOVA. Two slavemaker colonies contained equal numbers of L. longispinosus and L. curvispinosus slaves and were omitted from the analysis. In experiments with New York slavemakers, which all contained only L. longispinosus slaves, the effect of slave species could not be investigated, therefore these results were analyzed with Mann-Whitney U tests. For the analysis of the cross-fostering experiments in trial series 2, we used the factors host and parasite population in a MANOVA to detect possible interaction effects. In the comparison of the two L. longispinosus populations, we used an ANCOVA with the variable ‘‘slavemaker per host worker in the experiment’’ as a cofactor to control for differences in size between slavemaker colonies from New York and Ohio. RESULTS

Community composition and parasite prevalence At the New York site, the host community was almost exclusively composed of Leptothorax longispinosus colonies (95%, Table 1), with the minority host L. ambiguus being extremely rare (5%). Furthermore, an extensive earlier study has shown that while L. longispinosus is virtually ubiquitous in this study area, L. ambiguus shows an extremely patchy spatial distribution (Herbers and Foitzik 2002). At the location in Ohio, L. curvispinosus was the main host species (71%,


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TABLE 2. Within-community comparisons. During staged raids in the laboratory Leptothorax longispinosus colonies from Ohio killed fewer slavemaking workers and suffered higher losses among their own worker force compared to sympatric L. curvispinosus colonies; in New York, the co-occurring host species did not differ in their fighting abilities. Host species New York L. longispinosus L. ambiguus Ohio L. curvispinosus L. longispinosus

Leptothorax killed Percentage 14.6 6 9.8 16.1 6 7.9 16.5 6 10.1 24.1 6 11.2

Trials with slavemakers killed

P

Percentage†

0.57

P 0.28

33.3 (8/24) 19.0 (4/21) 0.03

0.043 60.0 (12/20) 22.2 (4/18)

Note: We show mean 6 1 SD for percentage of Leptothorax killed and the percentage of trials with slavemakers killed out of the total number of raids. † Percentage calculated as no. of trials with slavemakers killed out of total raids (shown in parentheses).

Table 1), but L. longispinosus occurred at substantial densities as well (29%). The relative frequencies of the primary and secondary host species differed highly significantly between the two communities (x2 test, N 5 3070 total host colonies, x21 5 321.1, P , 0.00001).

FIG. 2. Outcome of successful raids conducted by slavemakers from Ohio and New York. Presented are the relative amounts of brood captured by slavemakers and salvaged by hosts for the two sympatric Leptothorax host species from each site. Sample sizes: Ohio, L. curvispinosus (N 5 16 raids) and L. longispinosus (N 5 17 raids); New York, L. longispinosus (N 5 20 raids) and L. ambiguus (N 5 17 raids).

At each location, P. americanus nests contained enslaved workers of both sympatric host species. However, whereas in the New York community, the slavemaker did not preferentially use either of the two host species (Table 1; x2 test, N 5 2460 colonies, x21 5 0.22, P 5 0.64), parasite–host ratios differed markedly between the two host species at the Ohio site. There, the secondary host L. longispinosus was more frequently exploited by the slavemaker than was the dominant L. curvispinosus (Table 1; N 5 997 colonies, x21 5 21.99, P , 0.00001).

Trial series 1: within-community comparisons Within the New York community, we found no significant differences between L. longispinosus and L. ambiguus colonies in anti-parasite defense. The failure rate of raiding attempts by the slavemaker—i.e., the number of trials in which no brood was successfully transported to the slavemaker nest—was not influenced by host species (failure rate: 4 out of 24 raiding attempts against L. longispinosus; 4 out of 21 attempts against L. ambiguus; x2 test with Yates correction, N 5 45 raiding attempts, x21 5 0.03, P 5 0.86). Survival rate of host and parasite (Table 2) and the amount of brood captured by the slavemaker or salvaged by the host did not differ between the two host species (Fig. 2; Mann-Whitney U tests, N 5 20 raids against L. longispinosus, N 5 17 raids against L. ambiguus, all NS at P . 0.40). Neither of the two host species in the Ohio community was able to entirely prevent Protomognathus americanus from raiding their colonies, and slavemakers were able to steal at least part of the host brood in the majority of the trials (failure rate: 4 out of 20 raiding attempts against L. curvispinosus, 1 out of 18 attempts against L. longispinosus). The slavemaker’s failure rate was not influenced by the species of the host colony (x2 test with Yates correction, N 5 38 raiding attempts, x21 5 0.70, P 5 0.40). However, host species differed considerably regarding their ability to defend themselves in the event of a raid, with the minority host L. longispinosus exhibiting much less effective

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defenses. The latter host lost on average 3 times as many larvae and pupae to the slavemaker as L. curvispinosus (Fig. 2; MANOVA, N 5 32 raids, F1 5 7.57, P , 0.02) and consequently rescued much less brood (Fig. 2; F1 5 7.43, P , 0.02). The outcome of raids against the two host species also differed in terms of death toll for the slavemaker: Whereas L. longispinosus only rarely harmed a P. americanus worker, L. curvispinosus colonies killed at least one slavemaker worker during most raids (Table 2; x2 test with Yates correction, x21 5 4.1, P , 0.05). In summary, we found a pronounced asymmetry in the degree of resistance between the locally co-occurring host species at the site in Ohio, but no difference between the primary and secondary host in New York. The contribution of slaves of different species to the outcome of the raids could only be assessed in trials with Ohio slavemakers, because, due to the extreme rarity of L. ambiguus in the New York community, none of the slavemaker colonies we used in the behavioral trials comprised a majority of L. ambiguus slaves. In our experiments, enslaved Leptothorax workers were often recruited by slavemakers and subsequently participated in the raiding activities. L. curvispinosus and L. longispinosus slaves did not differ in their disposition to accompany slavemakers on raids (L. curvispinosus: participation in 8 out of 16 raids; L. longispinosus: 13 out of 20 raids; x2 test with Yates correction, N 5 36 raiding attempts, x21 5 0.32, P 5 0.57). Nevertheless, the two slave species differed in terms of aggressiveness, as raids involving L. longispinosus slaves resulted in more Leptothorax workers being killed (MANOVA, N 5 32 raids, F1 5 5.10, P , 0.04) and tended to have fewer hosts escaping from the raid (F1 5 4.01, P 5 0.055). Concerning the proportion of brood captured by the parasite or salvaged by the host, there was neither an effect of slave species nor an interaction between the factors host and slave species ( P . 0.15 in all cases). Consequently, the observed differences in the success of raids are entirely attributable to the interaction between P. americanus and the raided host species. In the choice trials, slavemakers from Ohio preferentially attacked L. longispinosus colonies (in 17 out of 20 trials, x2 test, x21 5 9.80, P 5 0.002). However, this preference was not absolute, as in six cases, the slavemakers later raided the second host colony as well. This result indicates that P. americanus choose to raid L. longispinosus if presented with a choice, but attack L. curvispinosus nests as well if there is no alternative.

Trial series 2: between-community comparisons There was no difference between slavemakers from the two populations concerning the success rate of their raiding attempts (failure rates: 4 out of 21 raids for New York slavemakers, 7 out of 37 raids for Ohio; x2 test, x21 5 0.00, P 5 0.99). However, in the successful raiding attempts there were pronounced differences in

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FIG. 3. Number of slaves and slavemaker workers in Protomognathus americanus colonies from New York (open squares, N 5 321 colonies) and Ohio (solid triangles, N 5 92 colonies). The slopes of the regression lines, which denote the number of slaves per slavemaker, differ significantly between the two sites (see Results: Trial series 2 . . . ).

effectiveness between the two slavemaker populations. P. americanus from New York were more effective and destructive as raiders, independent of host species. They successfully delayed the extrication of brood by host workers (Mann-Whitney U test, NNY 5 16 raids, NOH 5 27 raids, U 5 128.5, P , 0.03), and let a smaller proportion of host workers escape than their counterparts from Ohio (mean of 25% compared to 42%; MANOVA, NNY 5 17 raids, NOH 5 30 raids, F1 5 13.41, P , 0.001). Additionally, New York slavemakers were killed less often during raids (NY: at least 1 slavemaker killed in 7 out of 21 trials, OH: 24 out of 37 trials included killings; x2 test, x21 5 5.35, P , 0.03). The demography of parasite colonies from the two locations corroborates these results: P. americanus colonies from New York contained more slaves per slavemaker (Fig. 3; ANCOVA on log-transformed data, NNY 5 321 slavemaker colonies, NOH 5 92 slavemaker colonies, F1 5 35.12, P , 0.02), indicating they were more proficient at recruiting new slaves. Since colonies of New York slavemakers contained more slaves per slavemaker, one possibility is that the observed differences in slavemaker effectiveness were attributable not to the slavemakers themselves, but to the slaves that accompanied them on the raids. However, the proportion of raids with participation of slaves did not differ between New York and Ohio (6 out of 21 raids for New York, 12 out of 37 raids for Ohio; x2 test, x21 5 0.05, P 5 0.82). Similarly, there was no difference in the number of slaves that engaged in raiding activities (Mann-Whitney U test, NNY 5 6 and NOH 5 12 (number of raids with participating slaves), Z 5 20.66, P 5 0.51). Accordingly, the higher effectiveness of New York parasites cannot be explained by the participation of slaves in the raids, but reflects a true

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FIG. 4. Success of raids involving sympatric and allopatric hosts, measured as percentage of host brood obtained by the slavemakers and salvaged by the hosts. Protomognathus americanus colonies from New York (NY; N 5 17 experiments) acquired more brood in raids against their sympatric Leptothorax longispinosus hosts, whereas Ohio slavemakers (OH; N 5 30 experiments) captured a similar percentage of brood from colonies of sympatric and allopatric hosts. Data are means with 95% confidence intervals. L. long 5 L. longispinosus; L. curv. 5 L. curvispinosus.

difference between the two populations of P. americanus. The differences between slavemaker populations were mirrored in the effectiveness of host defense. While on average one fourth of all L. curvispinosus workers from Ohio were killed during the slavemaker attack, only 10% of the L. longispinosus workers from New York endured the same fate (MANOVA, N 5 22 raids against L. curvispinosus [OH], N 5 10 raids against L. longispinosus [NY], F1 5 5.41, P , 0.03). In the test of slavemaker effectiveness in raids against sympatric and allopatric hosts, the outcome of slave raids, measured as the proportion of brood obtained by slavemakers and hosts, differed highly significantly between the four possible combinations of slavemaker population and host species (MANOVA; brood captured by slavemaker, N 5 47 raids, F1 5 18.89, P , 0.0001; brood salvaged by hosts, F1 5 5.51, P , 0.03). P. americanus colonies from Ohio obtained a similar proportion of brood from colonies of both the allopatric L. longispinosus from New York and the sympatric L. curvispinosus from Ohio (Fig. 4; Tukey test for unequal N, N 5 14 raids against L. longispinosus [NY], N 5 16 raids against L. curvispinosus [OH]; brood captured, NS; brood salvaged, NS). In contrast, New York slavemakers managed to steal about twice as much brood in raids against their sympatric L. longispinosus hosts (Fig. 4; Tukey test for unequal N, N 5 8 raids against L. longispinosus [NY], N 5 9 raids against L. curvispinosus [OH]; brood captured, P , 0.001; brood salvaged, NS). This result indicates a


higher degree of specialization of the parasite in the New York community. As we showed in trial series 1, within the Ohio community, L. longispinosus had weaker defenses against slave raids than the sympatric L. curvispinosus. In the second trial series, we found that L. curvispinosus from Ohio were in turn less efficient defenders than L. longispinosus from New York. The combination of the results from the two studies thus suggests that the two L. longispinosus populations differ strongly in their level of anti-parasite defense. Indeed, a direct comparison of raids by Ohio slavemakers against L. longispinosus from New York and Ohio indicated more effective host defenses in the New York community. During slave raids, New York L. longispinosus retained more brood (Fig. 5; ANCOVA, N 5 15 raids against NY L. longispinosus, N 5 18 raids against L. longispinosus from OH, F1 5 5.29, P , 0.05), and consequently P. americanus raiders captured fewer larvae and pupae (Fig. 5; F1 5 10.10, P , 0.01). Furthermore, L. longispinosus from New York had fewer of their workers killed during raids (NY, mean 12.3%, OH, 28.6%; F1 5 5.57, P , 0.04), and killed at least one slavemaker worker in most of the trials (12 out of 18 trials vs. 4 out of 18 trials for L. longispinosus from Ohio; x2 test with Yates correction, x21 5 6.4, P , 0.02). When P. americanus colonies were simultaneously given the possibility to raid colonies of L. longispinosus from New York and L. curvispinosus from Ohio, they primarily attacked L. curvispinosus colonies from Ohio (N 5 37 trials, x2 test, x21 5 6.08, P , 0.02). Slavemaker colonies from Ohio and New York did not differ in their preference (N 5 21 trials with slavemaker colonies from OH, N 5 16 trials with slavemaker colonies from NY, x21 5 0.30, P 5 0.58). Our field data from the two sites yielded that L. longispinosus is the main host species for P. americanus at the site in New York, and the preferentially used species in the Ohio community (Table 1). This finding

FIG. 5. Percentage of brood captured by the slavemaker and salvaged by the hosts in raids of Ohio slavemakers against Leptothorax longispinosus from New York (N 5 15 raids) and Ohio (N 5 18 raids). Data are means 6 1 SE.


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could be interpreted as evidence for an innate preference of the slavemaker for L. longispinosus hosts. However, combining the results of the choice experiments with P. americanus colonies from Ohio in our two trial series, we can clearly reject this possibility. Ohio slavemakers preferred L. longispinosus over L. curvispinosus colonies in the first trial series, where both hosts came from the same location (L. longispinosus nest raided in 17 out of 20 trials). In our second trial series, in contrast, where the two offered host colonies came from different sites, Ohio slavemakers preferentially exploited the L. curvispinosus colonies from Ohio rather than the L. longispinosus from New York (L. curvispinosus nest raided in 14 out of 21 trials). This highly significant difference (x2 test, x21 5 9.72, P , 0.002) indicates that the decision criterion for P. americanus is not host species, but the level of nest defense encountered by raiding slavemakers. DISCUSSION Our study revealed strong interpopulational variation in the degree of specialization of Protomognathus americanus. In the New York community, where only one of the host species constitutes a reliably exploitable resource, P. americanus was more specialized compared to the Ohio site with two available hosts. These differences have a pronounced impact on the progression of the arms race between parasite and host, as the Red Queen process was more advanced in the New York community compared to the one in Ohio. Our first trial series demonstrated the absence of differences in anti-parasite defenses between the two hosts in New York, and the demographic data showed the lack of a slavemaker preference for either host species in the field. At the Ohio site, in contrast, the minority host Leptothorax longispinosus showed weaker defenses against P. americanus. Furthermore, L. longispinosus colonies from Ohio were preferentially attacked in our choice experiments, and this species was also more frequently exploited by the slavemaker in the field. Our second series of experiments revealed strong differences in the intensity of the coevolutionary interaction between the communities in New York and Ohio. Slavemakers from the New York community raided host colonies more efficiently and survived raids better, but were also more destructive, letting only very few host workers escape from a raid. As a result, New York P. americanus colonies succeeded in acquiring a higher number of slaves per slavemaker worker. Furthermore, slavemakers from New York exhibited a higher degree of specialization than their counterparts from Ohio, as they performed less well against allopatric than sympatric hosts. The high effectiveness of slavemakers from New York was mirrored in a high level of colony defense in the majority host L. longispinosus from this location. In contrast, at the Ohio site, both slavemakers and hosts were less effective at their

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respective tasks than their counterparts from New York. The weaker defenses of L. curvispinosus from Ohio were apparent not only in the cross-fostering experiments, but also in the choice trials. Slavemakers from both populations preferentially raided this host species when given a choice between it and the well defended New York L. longispinosus, indicating that slavemaker scouts may have been discouraged to attack the L. longispinosus hosts from New York by a stronger colony defense.

Different levels of host defense Of the host species in Ohio, L. curvispinosus appears to have evolved better defenses against the slavemaker. However, it is the L. longispinosus that are presently under higher parasite pressure, so why have they not developed equally effective counteradaptations? According to the evolutionary-lag hypothesis (Rothstein 1975, 1990), host defenses would principally be adaptive, but require sufficient time and genetic variation to evolve. The ineffective nest defense of L. longispinosus from Ohio could thus be due to a lack of time for the evolution of counteradaptations. The contrasting evolutionary-equilibrium hypothesis (Rohwer and Spaw 1988, Lotem et al. 1992, Takasu 1998) proposes that the level of host defense is determined by a cost–benefit balance, which is influenced not only by parasite pressure, but also by ecological factors. Host defenses in our social-parasite system should generally be lower for the secondary host species, which suffers higher costs due to selection pressures from environmental conditions or interspecific competition. This is indeed what we find in the Ohio community, where the minority host L. longispinosus is more poorly defended. In the New York community, the secondary host is much rarer than at the site in Ohio and is probably inhibited by even more adverse conditions; thus the differences in the defensive abilities of the two sympatric host species should still be more pronounced in this system. However, we did not detect any such differences in the New York community. This finding can be explained by the higher degree of specialization exhibited by the P. americanus from this population, who, in contrast to their counterparts from Ohio, performed much worse against allopatric L. curvispinosus than against their usual host L. longispinosus. Thus, in the New York community, the slavemaker, due to its specialization on the dominant L. longispinosus, does not cope well with L. ambiguus, even though this minority host probably cannot afford costly counteradaptations because of constraints set by the unfavorable ecological conditions.

Degree of specialization of the parasite Our results indicate profound differences in the degree of specialization of the slavemakers from New York and Ohio. How can we explain these findings? Mechanisms that are commonly invoked to explain the

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phenomenon of host specificity and other forms of niche restriction include competition (MacArthur 1972), predation or parasitism (Colwell and Fuentes 1975), and an increase in the chances of finding a mate (Rohde 1979, Combes and The´ron 2000). In our communities, competition can probably be ruled out as a factor, as we did not find other social parasites cooccurring with P. americanus. Likewise, it does not seem plausible that predation should be higher on parasites with one slave species compared to the other. Finally, in P. americanus, our genetic analyses show that the usage of different host species does not result in increased reproductive isolation (M. Brandt and S. Foitzik, unpublished data). Additional arguments in favor of specialization derive from a large body of theoretical work. In accordance with the intuitively appealing assumption that ‘‘a jack of all trades is a master of none,’’ several models predict that specialized species have an advantage over generalized ones under a broad range of conditions. A popular hypothesis that could explain the high degree of specialization exhibited by many parasitic species is the existence of tradeoffs, such that traits leading to increased fitness on one host are detrimental on others (Rausher 1984, CastilloChavez et al. 1988, Futuyma and Moreno 1988, Jaenike 1990, Via 1990). It has been shown that alleles need not even be deleterious on other hosts for specialization to be favored by selection; it is sufficient if the alleles are neutral, or even just less strongly positively selected on other hosts (Fry 1996). However, there are also factors opposing these advantages of specialization; these include search costs and variations in host quality and availability over time (Fry 1996, McPeek 1996). For slavemaking ants, both arguments apply. Having to raid host colonies at large distances incurs energy costs, is likely to reduce raiding efficiency, and exposes the raiding party to higher predation risks. Consequently, the parasites are dependent on host colonies in the vicinity of their nest. Due to the fact that many raided host colonies do not survive the slavemaker attack (Foitzik and Herbers 2001), each raiding season creates a sink patch of empty nest sites within the raiding radius of the slavemaker nest that can be recolonized by immigrating hosts. If, as in the Ohio community, two host species co-occur at densities in the same order of magnitude, the number and species of host colonies within raiding distance of a parasite nest probably changes unpredictably from year to year, making specialization on only a single host a risky strategy. Thus, for a slavemaker it might pay to raid whatever host colonies occur in the vicinity, and only exert a host preference if there are more potential sources of new slaves than are needed for the replenishment of the colony’s labor force. This is exactly what we find in the raiding and choice experiments with P. americanus from Ohio: the slavemaker exhibits a predisposition to raid L. longispinosus, but this preference is not absolute, and the parasite is still able to exploit both po-


tential host species. Slavemakers in New York, in contrast, have an extremely low chance of ever encountering a colony of the secondary host, thus the dominant host L. longispinosus constitutes a predictable, stable resource, and the parasite should be selected to become specialized (Ward 1992, Sasal et al. 1999, Desdevises et al. 2002).

Specialization and the progression of the arms race In accordance with the results of previous studies (Foitzik et al. 2001, Foitzik and Herbers 2001, Herbers and Foitzik 2002, Blatrix and Herbers 2003), our data confirm the existence of a geographic mosaic of coevolution in P. americanus and its hosts (Thompson 1994, 1999). However, in contrast to previous results that attributed geographic variation in the strength of reciprocal adaptation to differences in selection pressure exerted by the parasite, the comparison of L. longispinosus hosts from New York and Ohio shows that our present findings cannot be explained by current parasite pressure. The L. longispinosus from the two populations have evolved markedly different levels of anti-parasite defense, in spite of the fact that slavemaker / host ratios for this species did not differ between the two communities (x2 test, x21 5 0.7, P 5 0.41). Intrinsic parameters of the interaction thus cannot account for the observed differences, and so it may be the community context that critically influences the coevolutionary arms race (Thompson and Pellmyr 1992, Benkman 1999, Benkman et al. 2001, 2003). Our results indicate that the progression of the Red Queen process depends on the number of antagonists involved in the interaction. In the New York community, the slavemaker engages in an arms race almost exclusively with only one opponent, and the coevolutionary interaction is very tight. At the Ohio site, in contrast, the inclusion of a second host species appears to disrupt the arms race and thus to decelerate the progression of the Red Queen. Possible explanations for this finding may come from the fact that P. americanus is characterized by different niche breadth in the two populations. Theoretical models have suggested that, under the assumption of roughly equal population sizes, species with a narrower niche can have a faster rate of evolutionary response than generalized ones, as they have a higher probability of fixing beneficial alleles and take less time to do so (Whitlock 1996). Conversely, since alleles in generalist species are exposed to selection in only part of the species’ niche, these species are more prone to accumulate deleterious mutations (Kawecki 1994). In addition, it was shown that if trade-offs exist between the virulence of a generalist parasite on different host species, host heterogeneity can prevent virulence from escalating (Regoes et al. 2000). This prediction is in accordance with the intuitive rationale that a parasitic lineage that evolves a preference for a particular host species automatically becomes more consistently ex-

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posed to selection on that host. As a result, provided that performance on different host species is at least partially genetically independent, the specialized lineage evolves faster responses to the evolution of host defenses than a generalist one that undergoes selection on several host species (Kawecki 1998). The above explanations are valid under the assumption that a parasite confronted with more than one host species expands its niche and becomes a true generalist. However, this is not the only evolutionary option for a parasite in this situation. As an alternative explanation, Davies and Brooke (1989) were the first to suggest from their data on Common Cuckoos and their hosts that the proportion of brood parasites preferring a particular host may oscillate over time as the most commonly used avian hosts evolve increased defenses and uncommonly used hosts evolve decreased defenses. Thompson (1994, 1999) generalized from this hypothesis that parasite populations are often specialized on particular host species, but are able to evolve preferences for new hosts through frequency-dependent selection if their currently used hosts develop counteradaptations. Under these circumstances, the parasite actually remains more or less specialized but has the option to alternate between the available host species. Our study provides evidence that this may be a plausible scenario for the P. americanus population in Ohio. As L. curvispinosus from this site exhibit high levels of colony defense, it is possible that P. americanus in this community only recently underwent a host switch caused by the development of anti-parasite adaptations by the majority host. Since Ohio slavemakers are more successful in raids against L. longispinosus, they should presently be selected to shift their focus to this host species, and indeed we find that L. longispinosus is preferentially exploited by the parasite in the field as well as in laboratory experiments. As a consequence of the increased usage of the alternative host, parasite pressure on L. curvispinosus would be relaxed, leading to a decrease in the adaptive value of previously acquired resistance characters. Under the changed selection regime, L. longispinosus should develop counteradaptations, while at the same time L. curvispinosus should lower their defenses. The slavemaker, in turn, should always be selected to exploit the host species with the weaker defenses, setting the stage for repeated host switches and coevolutionary cycles (Thompson 1999). The recurrent loss of adaptations and counteradaptations that arises from such a series of host switches is eventually expected to lead to a reduced progression of the Red Queen process in this system, and thus could also explain the lower degree of effectiveness we found in both hosts and parasites from the Ohio community. From our choice experiments, we have indications that the slavemaker does not even have to change its host preferences over time to induce host switches, but that in our social-parasite system host alternations may

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be caused by a much simpler mechanism. We found that P. americanus, when presented with a choice between two host colonies, chooses the nest where it encounters the weaker defenses. In our trials, slavemakers preferred L. curvispinosus from Ohio over L. longispinosus from New York, and, within the Ohio community, they primarily attacked L. longispinosus rather than L. curvispinosus. This kind of preference, not for a certain host species but for whatever host offers the least resistance, could ensure that the slavemaker always exploits the host with the weaker defenses. Since in the New York community the slavemaker engages in an arms race almost exclusively with only one opponent and thus does not have the option of host alternations, the resulting coevolutionary interaction is tighter and progresses faster. This community may thus represent a snapshot of a more advanced stage in the coevolution between P. americanus and its hosts (Davies and Brooke 1989, Davies et al. 1996). This view fits in with the evolutionary-lag hypothesis (Rothstein 1975, 1990), according to which interacting antagonists are permanently under selection pressure to increase their virulence or resistance, and thus become locked in the process of a coevolutionary arms race. Under the evolutionary-equilibrium view (Rohwer and Spaw 1988, Lotem et al. 1992), in contrast, once the equilibrium stage is reached, there would be no further coevolutionary development and no continuing arms race (Rohwer and Spaw 1988, Lotem et al. 1992, 1995, Winfree 1999, Servedio and Lande 2003). The evolutionary-lag hypothesis assumes that the development of defenses is constrained by time and genetic variation; the currently observed level of resistance in a population may thus not be adaptive, which makes this hypothesis difficult to test. Furthermore, since costs and benefits of anti-parasite defenses are extremely hard to assess, there has so far been no study that was able to provide conclusive evidence for either one (Winfree 1999) or a mixture of the two hypotheses (Soler et al. 1998). Nevertheless, in accordance with the view of Davies et al. (1996), we would argue that parasite and host populations are still under soft selection and should permanently be driven to better mutual adaptations by intraspecific competition. An improvement by one of the antagonists will shift the cost– benefit ratio for the opponent and should thus trigger a coevolutionary response. Therefore, equilibrium balances should themselves be subject to evolutionary change, and consequently are not incompatible with the idea of a progressing arms race.

Conclusions Our results show that the coevolutionary trajectory of a host–parasite interaction is critically dependent on its community context. In our social parasite system we can directly examine the effect of the incorporation of a third species into the interaction without phylogenetic constraints. Whereas an arms race between two

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players results in a high degree of specialization and advanced reciprocal co-adaptations, we show that the inclusion of a second host species in the community loosens the association by opening new coevolutionary options for the parasite. ACKNOWLEDGMENTS We would like to thank R. and B. Meyer, T. Wittig, T. Santl, and H. Sturm for support in the field. We are also indebted to S. Praha, who conducted the cross-fostering experiments. We are grateful to N. Davies, C. DeHeer, B. Fischer, J. Heinze, J. Herbers, J. Korb, P. Nonacs, and J. Strassmann for helpful comments on an earlier version of this manuscript. This study was supported by the E. N. Huyck Preserve, Rensselaerville, New York, and the Deutsche Forschungsgemeinschaft Fo 298/2. LITERATURE CITED Alloway, T. M. 1979. Raiding behavior of two species of slavemaking ants, Harpagoxenus americanus (Emery) and Leptothorax duloticus Wesson (Hymenoptera: Formicidae). Animal Behaviour 27:202–210. Benkman, C. W. 1999. The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. American Naturalist 153:S75–S91. Benkman, C. W., W. C. Holimon, and J. W. Smith. 2001. The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282–294. Benkman, C. W., T. L. Parchman, A. Favis, and A. M. Siepielski. 2003. Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. American Naturalist 162:182–194. Blatrix, R., and J. M. Herbers. 2003. Coevolution between slave-making ants and their hosts: host specificity and geographical variation. Molecular Ecology 12:2809–2816. Bolton, B. 2003. Synopsis and classification of Formicidae. Memoirs of the American Entomological Institute. Volume 71. American Entomological Institute, Gainesville, Florida, USA. Breed, M. D., and B. Bennett. 1987. Kin recognition in highly eusocial insects. Pages 243–285 in D. J. C. Fletcher and C. D. Michener, editors. Kin recognition in animals. J. Wiley and Sons, Chichester, UK. Buschinger, A. 1974. Experimente und Beobachtungen zur Gru¨ndung und Entwicklung neuer Sozieta¨ten der sklavenhaltenden Ameise Harpagoxenus sublaevis (Nyl.). Insectes Sociaux 21:381–350. Buschinger, A., W. Ehrhardt, and U. Winter. 1980. The organization of slave raids in dulotic ants—a comparative study (Hymenoptera; Formicidae). Zeitschrift fu¨r Tierpsychologie 53:245–264. Castillo-Chavez, C., S. A. Levin, and F. Gould. 1988. Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42:986–994. Choo, K., P. D. Williams, and T. Day. 2003. Host mortality, predation and the evolution of parasite virulence. Ecology Letters 6:310–315. Colwell, R. K., and E. R. Fuentes. 1975. Experimental studies of the niche. Annual Review of Ecology and Systematics 6:281–310. Combes, C., and A. The´ron. 2000. Metazoan parasites and resource heterogeneity: constraints and benefits. International Journal for Parasitology 30:299–304. Davies, N. B., A. F. G. Bourke, and M. D. L. Brooke. 1989. Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends in Ecology and Evolution 4:274–278. Davies, N. B., and M. D. L. Brooke. 1989. An experimental study of co-evolution between the cuckoo, Cuculus cano-


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