The influence of space and time on the evolution of altruistic defence: the case of ant slave rebellion

How can antiparasite defence traits evolve even if they do not directly benefit their carriers? An example of such an indirect defence is rebellion of enslaved Temnothorax longispinosus ant workers against their social parasite Temnothorax americanus, a slavemaking ant. Ant slaves have been observed to kill their oppressors' offspring, a behaviour from which the sterile slaves cannot profit directly. Parasite brood killing could, however, reduce raiding pressure on related host colonies nearby. We analyse with extensive computer simulations for the Temnothorax slavemaker system under what conditions a hypothetical rebel allele could invade a host population, and in particular, how host–parasite dynamics and population structure influence the rebel allele's success. Exploring a wide range of model parameters, we only found a small number of parameter combinations for which kin selection or multilevel selection could allow a slave rebellion allele to spread in the host population. Furthermore, we did not detect any cases in which the reduction of raiding pressure in the close vicinity of the slavemaker nest would substantially contribute to the inclusive fitness of rebels. This suggests that slave rebellion is not costly and perhaps a side‐effect of some other beneficial trait. In some of our simulations, however, even a costly rebellion allele could spread in the population. This was possible when host–parasite interactions led to a metapopulation dynamic with frequent local extinctions and recolonizations of demes by the offspring of few immigrants.     

Colony structure of a slavemaking ant. II. Frequency of slave raids and impact on the host population

The parasite pressure exerted by the slavemaker ant Protomognathus americanus on its host species Leptothorax longispinosus was analyzed demographically and genetically. The origin of slaves found in colonies of the obligate slavemaker was examined with nuclear and mitochondrial DNA markers to make inferences about the frequency and severity of slave raids. Relatedness of enslaved L. longispinosus workers in the same nest was very low, and our data suggest that, on average, each slavemaker nest raids six host colonies per season. Therefore, the influence of slavemaker species on their hosts is much stronger than simple numerical ratios suggest. We also found that slave relatedness was higher in small than in large slavemaker nests; thus, larger nests wield a much stronger influence on the host. We estimated that in the study population, on average, a host nest has a 50% chance of being attacked by a slavemaker colony per year. Free-living Leptothorax colonies in the vicinity of slavemaker nests did not represent the source of slaves working in P. americanus colonies, which suggests that raided nests either do not survive or migrate after being raided. Colony composition and intranest relatedness of free-living L. longispinosus colonies differed markedly between areas with slavemakers and those that are parasite-free. In the presence of slavemakers, host colonies were less likely to be polygynous and had fewer workers and a higher relatedness among worker brood. Host nests with slavemaker neighbors allocated more resources into sexuals, possibly caused by these shifts in nest demography. Finally, enslaved Leptothorax workers in P. americanus nests appeared to be less efficient than their counterparts in free-living colonies. Thus, slavemakers exert a much stronger impact on their hosts than had previously been suspected and represent an unique system to study parasite-host coevolution.     

Raiders from the sky: slavemaker founding queens select for aggressive host colonies

Reciprocal selection pressures in host-parasite systems drive coevolutionary arms races that lead to advanced adaptations in both opponents. In the interactions between social parasites and their hosts, aggression is one of the major behavioural traits under selection. In a field manipulation, we aimed to disentangle the impact of slavemaking ants and nest density on aggression of Temnothorax longispinosus ants. An early slavemaker mating flight provided us with the unique opportunity to study the influence of host aggression and demography on founding decisions and success. We discovered that parasite queens avoided colony foundation in parasitized areas and were able to capture more brood from less aggressive host colonies. Host colony aggression remained consistent over the two-month experiment, but did not respond to our manipulation. However, as one-fifth of all host colonies were successfully invaded by parasite queens, slavemaker nest foundation acts as a strong selection event selecting for high aggression in host colonies.     

Increased host aggression as an induced defense against slave-making ants

Slave-making ants reduce the fitness of surrounding host colonies through regular raids, causing the loss of brood and frequently queen and worker death. Consequently, hosts developed defenses against slave raids such as specific recognition and aggression toward social parasites, and indeed, we show that host ants react more aggressively toward slavemakers than toward nonparasitic competitors. Permanent behavioral defenses can be costly, and if social parasite impact varies in time and space, inducible defenses, which are only expressed after slavemaker detection, can be adaptive. We demonstrate for the first time an induced defense against slave-making ants: Cues from the slavemaker Protomognathus americanus caused an unspecific but long-lasting behavioral response in Temnothorax host ants. A 5-min within-nest encounter with a dead slavemaker raised the aggression level in T. longispinosus host colonies. Contrarily, encounters with nonparasitic competitors did not elicit aggressive responses toward non-nestmates. Increased aggression can be adaptive if a slavemaker encounter reliably indicates a forthcoming attack and if aggression increases postraid survival. Host aggression was elevated over 3 days, showing the ability of host ants to remember parasite encounters. The response disappeared after 2 weeks, possibly because by then the benefits of increased aggression counterbalance potential costs associated with it.     

Eco-ethological Factors Affecting the Scouting and Raiding Behaviour of the Slave-making Ant,Polyergus rufescens Latr. (Hymenoptera,Formicidae)

A dulotic colony of the obligatory slave-making ant Polyergus rufescens was monitored daily in the field (Parma, Italy) from 1100–2000 h over the summers of 1991 and 1992. The first P. rufescens workers to emerge from the nest each day were individually marked and their activity was accurately recorded. The path of 47 such individuals (21 over a complete trip) was followed in detail and mapped. Results confirm a clear scouting activity: the route of these workers away from the nest is generally tortuous and time consuming and is followed by a return trip along a different and straighter path. Observations also showed that these scouts recruit nestmates and lead raiding columns towards target nests, confirming their important role in the organization of slave raids. The similarity between routes taken by scouts and raiders during outbound trips indicates the close connection between scouting and raiding activity, which was also recorded in detail since 40 raids were observed. Some experiments analysing the orientation behaviour of inbound columns showed that raiders use a chemical trail (deposited during the outbound run) to lead them back home. The hypothesis of a multiple strategy for the location of host colonies operated by this slave-making species is also discussed.     

Collective defence portfolios of ant hosts shift with social parasite pressure

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.     

The ecological success of a social parasite increases with manipulation of collective host behaviour

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite‐induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour‐treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker‐induced nestmate attack. Slavemakers benefited from altering their hosts’ aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker‐induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T. curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T. longispinosus. Our findings highlight that large‐scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.     

Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus

Slave-making ants are social parasites which exploit the workforce of heterospecific slaves for their own reproduction, and to this end they have developed a variety of morphological and behavioural adaptations. Furthermore, social parasites utilize the chemical communication system of their hosts by breaking their nestmate recognition code, and some slave-maker species additionally employ semiochemicals as weapons during colony foundation and slaveraiding. Here, we demonstrate the use of such a ‘propaganda allomone’ by the North American myrmicine slave-maker Protomognathus americanus. This substance is produced in the Dufour’s gland and may be employed during slave raids to elicit panic among defending host workers. Slave-maker Dufour’s gland secretions evoked agitation and heightened levels of activity among host workers when applied directly on a host nest, and strong aggressive responses of nestmates when applied onto a host worker. Although the hosts own Dufour’s gland secretion also elicits intra-colonial fights, no support for the hypothesis was found that the slave-maker propaganda substance mimics a fertility signal of the host, as the chemical profile of the gland secretions is highly divergent between the two species. Preliminary results on the chemical composition of the secretion obtained by gas chromatography indicate that the propaganda substance of P. americanus differs from that of the related European slavemaker Harpagoxenus sublaevis, and is thus likely to represent an independent evolutionary development. Received 24 February 2005; revised 28 July 2005 and 2 March 2006; accepted 6 March 2006.     

A chemical level in the coevolutionary arms race between an ant social parasite and its hosts

Here we investigate the coevolutionary interactions between the slavemaking ant Protomognathus americanus and its Temnothorax hosts on a chemical level. We show that, although this social parasite is principally well-adapted to its hosts' cuticular hydrocarbon profile, there are pronounced differences in the fine-tuning of this adaptation. Between populations, chemical adaptation varies with host community composition, as the parasite faces a trade-off when confronted with more than one host species. In addition to adaptation of its own chemical signature, the slavemaker causes a reciprocal adjustment in its slaves' cuticular profile, the degree of which depends on the slave species. On the host side, successful parasite defence requires efficient enemy recognition, and in behavioural aggression trials, host colonies could indeed discriminate between invading slaves, which commonly accompany slavemakers on raids, and free-living conspecifics. Furthermore, hosts shifted their acceptance threshold over the seasons, presumably to reduce the costs of defence.     

Geographic Variation in Social Parasite Pressure Predicts Intraspecific but not Interspecific Aggressive Responses in Hosts of a Slavemaking Ant

Variation in community composition over a species' geographic range leads to divergent selection pressures, resulting in interpopulation variation in trait expression. One of the most pervasive selective forces stems from antagonists such as parasites. Whereas hosts of microparasites developed sophisticated immune systems, social parasites select for behavioural host defences. Here, we investigated the link between parasite pressure exerted by the socially parasitic slavemaking ant Protomognathus americanus and colony‐level aggression in Temnothorax ants from 17 populations. We studied almost the entire geographic range of two host species, including unparasitized populations. As previous studies have demonstrated that host colonies responding highly aggressively towards conspecifics fare better during slavemaker attacks, we predicted higher aggression levels in severely parasitized populations. Indeed, we demonstrate an increase in aggression towards conspecifics with parasite pressure, a pattern that was consistent over the two host species. In contrast to other studies, aggression against the parasite itself did not shift with parasite pressure. This may be explained by an absence of costs of parasite‐specific aggression in parasite‐free populations. The preferred host species T. longispinosus was generally more aggressive; however, the association between parasite pressure and aggression was found for both species, suggesting convergent co‐adaptation. Two potentially confounding factors, colony density and the co‐occurrence of a competing Temnothorax species in the community, could not explain the level of colony aggression in intra‐ and interspecific interactions. Instead, our study points to social parasite pressure as the determining factor shaping antagonistic interactions within, but not between, host species.     

Reproductive strategy of the slave antFormica podzolica relative to raiding efficiency of enslaver species

Summary Formica podzolica serves as host to slave-making ants in North America. We propose thatF. podzolica may respond to slavery by two alternative colony-growth and reproductive strategies depending on the raiding ability of the slavemaker: (1) Rapid colony growth at the expense of producing sexuals to a stage where raiding by unspecialized, facultative slavemakers, capable of exploiting only small colonies, becomes unlikely owing to a strong work force and (2) Early production of sexual offspring at the cost of colony growth to secure some sexual production in an environment with specialized obligate enslavers, capable of raiding large colonies. We tested the strategies by excavating 30 small to moderately large mounds ofF. podzolica and measured reproductive parameters of colonies in relation to mound size, worker number, and worker size. Mound area predicted worker number satisfactorily. Worker number correlated significantly with worker head width and with number of worker and sexual offspring. With a growing work force, the proportion of sexual offspring increased in the total offspring. Two thirds of the colonies producing sexuals emitted single sex, sex being independent of colony size. Some of the large colonies produced both sexes with a strong bias toward either sex. The unweighted population-level sex ratio did not differ from even, being 0.52 (numerical) or 0.54 (biomass). Very large mounds (not excavated) had small workers and highly male-biased sex ratios, probably owing to energy constraints set by central-place foraging. Population-level colony ontogeny data did not fit either one of the suggested strategies, but imply a mixture of the two. We discuss an alternative, still untested raid-independent explanation to the ontogeny pattern.     

Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species

The speed and the dynamics of the co-evolutionary process strongly depend on the relative strengths of reciprocal selection pressures exerted by the interacting species. Here, we investigate the influence of an obligate social parasite, the slave-making ant Harpagoxenus sublaevis, on populations of the two main host species Leptothorax acervorum and Leptothorax muscorum from a German ant community. A combination of genetic and demographic data allowed us to analyse the consequences of raiding pressure on the hosts' life history and possible host preferences of the parasite. We can demonstrate that slave raids during which the social parasite pillages brood from neighbouring host colonies are both frequent and extremely destructive for both host species. Microsatellite analysis showed that, on average, a single slave-maker colony conducts more than three raids per year and that host colonies mostly perish in the aftermath of these parasite attacks. Only in few cases, surviving nests of previously raided host colonies were found in the surroundings of slave-maker colonies. As a consequence of the high prevalence of parasites and their recurrent and devastating slave raids on host colonies, the life expectancy of host colonies was severely reduced. Combining our results on host-specific parasitic colony founding and raiding frequencies with the post-raid survival rate, we can demonstrate an overall higher mortality rate for the smaller host species L. muscorum. This might be caused by a preference of H. sublaevis for this secondary host species as demographic data on host species usage indicate.     

Eco-ethological Study on Raiding Behaviour of the European Amazon Ant,Polyergus rufescens Latr. (Hymenoptera: Formicidae)

In this paper we report the results of a detailed study on the behavioural ecology of slave raiding in the European amazon ant, Polyergus rufescens Latr. The field study, supported also by a video-tape recording technique, was conducted over an unbroken period of 53 days, during which observations of the activity of the residents (both slave-makers and slaves) were made for 10 h each day. It was possible to observe 38 slave raids distributed over 32 days, among which 27 were followed by the sack of 10 different nests of Formica cunicularia Latr., whereas 11 failed because of various reasons. Simple, compound and multiple raids occurred. We recorded the timing, frequency, distance, and direction of slave raids, including the number of participants and the type of captured brood. Moreover, particular attention was paid to the atmospheric conditions present at the moment of the raid onset. Information was also collected about the behaviour of the “activators” and the scouts before and during the movement of the storming column. Both dealate and winged P. rufescens queens, having emerged from the mixed colony during 6 sexual flights, were seen following the outbound raiding column during 4 raids. Finally, some peculiar behaviour, such as digging out the soil near the target nest to facilitate the entry of the raiding swarm, and the pillage of adult ants (eudulosis) was recorded and described. Data have been compared with what is known about the other species of the genus Polyergus.     

Comparing Reversal-Learning Abilities,Sucrose Responsiveness,and Foraging Experience Between Scout and Non-Scout Honey bee (Apis mellifera) Foragers

Honey bee (Apis mellifera) colonies divide foraging activities between scouts, who search for new sources of food, and non-scouts, who rely on information from waggle dances to find food sources. Molecular analyses of scouts and non-scouts have revealed differences in the expression of numerous genes, including several related to neurotransmitter signaling. Despite this progress, we know almost nothing about cognitive, sensory, or behavioral differences that underlie scouting. We tested three hypotheses related to differences between scouts and non-scouts. First, we tested whether scouts and non-scouts differ in their reversal-learning abilities and found that scouts showed a significantly faster reversal in their response to an odor that was punished and then rewarded. The results also suggested an interaction between the effects of foraging role (scout or non-scout) and seasonal effects on reversal-learning abilities. Second, we tested whether scouts and non-scouts show differences in responsiveness to sucrose rewards and found no difference. Third, we hypothesized that scouts have more foraging experience than do non-scouts. We tested this by comparing wing damage and found that non-scouts showed greater wing damage in the early summer but not the late summer. Together, these three results contribute to our understanding of the underpinnings of scouting behavior.     

Nest relocation in the slavemaking ants Formica subintegra and Formica pergandei: a response to host nest availability that increases raiding success

Social insects typically occupy spatially fixed nests which may thus constrain their mobility. Nevertheless, colony movements are a frequent component of the life cycle of many social insects, particularly ants. Nest relocation in ants may be driven by a variety of factors, including nest deterioration, seasonality, disturbances, changes in microclimate, and local depletion of resources. The colony movements of slavemaking ants have been noted anecdotally, and in recent studies such relocations were primarily attributed to nest deterioration or shifts to overwintering locations. In this study we explore nest relocations in large colonies of formicine slavemakers which occupy stable and persistent earthen nest mounds. We investigate the hypothesis that colony relocations of these slavemakers are best explained by efforts to improve raiding success by seeking areas of higher host availability. Five summers of monitoring the raiding behavior of 11–14 colonies of the slavemakers Formica subintegra and Formica pergandei revealed relatively frequent nest relocations: of 14 colonies that have been tracked for at least three of 5 years, all but one moved at least once by invading existing host nests. Movements tended to occur in the middle of the raiding season and were typically followed by continued raiding of nearby host colonies. Spatial patterns of movements suggest that their purpose is to gain access to more host colonies to raid: the distance moved is typically farther than the mean raiding distance before the move, which may indicate an effort to escape their local neighborhood. Furthermore, the mean distance of raids after relocation is shorter than the distance before relocation. For many slavemaking ant colonies, particularly those on the verge of relocating, raiding distance increased as the raiding season progressed. In addition, movements tended to be toward areas of higher local host density. Nest relocation is likely an important component of the ecology of slavemaking ants that contributes to the dynamic nature of their interaction with the host ant population.     

Differential Response of Ant Colonies to Intruders: Attack Strategies Correlate With Potential Threat

Animals are often threatened by predators, parasites, or competitors, and attacks against these enemies are a common response, which can help to remove the danger. The costs of defense are complex and involve the risk of injury, the loss of energy/time, and the erroneous identification of a friend as a foe. Our goal was to study the specificity of defense strategies. We analyzed the aggressive responses of ant colonies by confronting them with workers of an unfamiliar congeneric species, a non‐nestmate conspecific, a co‐occurring congeneric competitor species, and a social parasite—a slave‐making ant. As expected, the latter species, which can inflict dramatic fitness losses to the colony, was treated with most aggression. A co‐occurring competitor was also attacked, but the ants used different behaviors in their responses to both enemies. While the slavemaker was attacked by biting and stinging and was approached with spread mandibles, the competitor was dragged, a behavioral strategy only possible if the defending ant is similar in size and strength to the opponent. Non‐nestmate conspecifics were treated aggressively as well, but less than the slavemaker and the co‐occurring competitor, presumably because they are less easily recognized as enemies. An unfamiliar congeneric species was rarely attacked. This first detailed study comparing the aggressive responses of ant colonies toward slave‐making ants to other species posing different threats indicates that the responses of ant colonies are adjusted to the risk each opponent poses to the colony.     

Raiding behavior of the dulotic antChalepoxenus muellerianus (Finzi) in the field (Hymenoptera: Formicidae,Myrmicinae)

Summary Little information is available regarding the raiding behavior in nature of dulotic ants belonging to the tribeLeptothoracini. Between July 17 and 24, 1991, several raids ofChalepoxenus muellerianus (Finzi) were observed in nature near Tignale/Lago di Garda, Italy. Apparently, this species raids frequently during its summer raiding season (5 raids were observed during 7 days spent observing 8 colonies). A singleChalepoxenus colony sometimes raids more than one host colony more or less simultaneously. Observations during which oneChalepoxenus colony raided another and captured slavemaker brood indicate that intraspecific raids can occur either accidentally, or as a result of competition or territoriality when there is a sufficient dense slavemaker population.     

Oh sister,where art thou? Spatial population structure and the evolution of an altruistic defence trait

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post‐enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites’ offspring. As enslaved workers do not reproduce, they gain no direct fitness benefit from this ‘rebellion’ behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to ‘rebel’ nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers’ killing behaviour. We use a simple mathematical model to examine whether the small‐scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study, we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small‐scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of ‘rebellion’ by kin selection.     

The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.