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.     

Parasite scouting and host defence behaviours are influenced by colony size in the slave-making ant Protomognathus americanus

In the slave-making ant Protomognathus americanus, scout workers leave their colony, discover host colonies, and initiate slave raids. Captured host pupae subsequently emerge in the slavemaker colony and replenish the slave workforce. The course of these antagonistic encounters can be influenced by the species, aggressivity, or size of the host colony. We asked how the demography of parasite and host colonies influences the initial raiding phase by observing the scouting behaviour of P. americanus slavemakers during 48 raiding attempts. Experiments were performed under controlled laboratory conditions in a Y-shaped experimental arena. The number of active scouts increased with increasing slavemaker worker numbers, but was unaffected by the slave to slavemaker ratio, showing that slavemaker worker numbers are a good indicator for the scouting workforce. Colonies with fewer slaves discovered host colonies faster (colonies with 15 or less slaves: median 9:53 min, colonies with 42 or more slaves: median 18:55 min), suggesting that small slave workforces lead to intensified scouting behaviour. The more scouts were active, the faster a host colony was discovered, but the time between discovery and trial completion was unaffected by slavemaker colony demography. Host colonies were successfully attacked in 79.2 % of the trials, and they fought off an intruding scout only once. Yet host aggression towards slavemaker scouts increased with host colony size, and higher aggression rates delayed a subsequent attack. Our study demonstrates that colony size influences the behaviour and the course of crucial interspecific interactions of a social parasite and its host.     

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.     

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.     

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.     

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.     

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.     

Geographic distribution of the anti-parasite trait “slave rebellion”

Social parasites exploit the brood care behavior of other species and can exert strong selection pressures on their hosts. As a consequence, hosts have developed defenses to circumvent or to lower the costs of parasitism. Recently, a novel, indirect defense trait, termed slave rebellion, has been described for hosts of a slave-making ant: Enslaved Temnothorax longispinosus workers reduce local parasite pressure by regularly killing pupae of their obligatory slavemaking parasite Protomognathus americanus. Subsequently, growth of social parasite nests is reduced, which leads to fewer raids and likely increases fitness of neighboring related host colonies. In this study, we investigate the presence and expression the slave rebellion trait in four communities. We report its presence in all parasitized communities, document strong variation in its expression between different geographic sites and discuss potential explanations for this observed variation.     

FIRST EVIDENCE FOR SLAVE REBELLION: ENSLAVED ANT WORKERS SYSTEMATICALLY KILL THE BROOD OF THEIR SOCIAL PARASITE PROTOMOGNATHUS AMERICANUS

During the process of coevolution, social parasites have evolved sophisticated strategies to exploit the brood care behavior of their social hosts. Slave-making ant queens invade host colonies and kill or eject all adult host ants. Host workers, which eclose from the remaining brood, are tricked into caring for the parasite brood. Due to their high prevalence and frequent raids, following which stolen host broods are similarly enslaved, slave-making ants exert substantial selection upon their hosts, leading to the evolution of antiparasite adaptations. However, all host defenses shown to date are active before host workers are parasitized, whereas selection was thought to be unable to act on traits of already enslaved hosts. Yet, here we demonstrate the rebellion of enslaved Temnothorax workers, which kill two-thirds of the female pupae of the slave-making ant Protomognathus americanus . Thereby, slaves decrease the long-term parasite impact on surrounding related host colonies. This novel antiparasite strategy of enslaved workers constitutes a new level in the coevolutionary battle after host colony defense has failed. Our discovery is analogous to recent findings in hosts of avian brood parasites where perfect mimicry of parasite eggs leads to the evolution of chick recognition as a second line of defense.     

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.     

Population structure and the co-evolution between social parasites and their hosts

Co-evolutionary trajectories of host-parasite interactions are strongly affected by the antagonists' evolutionary potential, which in turn depends on population sizes as well as levels of recombination, mutation, and gene flow. Under similar selection pressures, the opponent with the higher evolutionary rate is expected to lead the co-evolutionary arms race and to develop local adaptations. Here, we use mitochondrial DNA sequence data and microsatellite markers to assess the amount of genetic variability and levels of gene flow in two host-parasite systems, each consisting of an ant social parasite--the European slavemaker Harpagoxenus sublaevis and the North American slavemaker Protomognathus americanus--and its two main host species. Our population genetic analyses revealed limited gene flow between individual populations of both host and parasite species, allowing for a geographic mosaic of co-evolution. In a between-system comparison, we found less genetic variability and more pronounced structure in Europe, where previous behavioural studies demonstrated strong local adaptation. Within the European host-parasite system, the larger host species Leptothorax acervorum exhibited higher levels of both genetic variability and gene flow, and previous field data showed that it is less affected by the social parasite H. sublaevis than the smaller host Leptothorax muscorum, which has genetically depleted and isolated populations. In North America, the parasite P. americanus showed higher levels of gene flow between sites, but overall less genetic diversity than its hyper-variable main host species, Temnothorax longispinosus. Interestingly, recent ecological and chemical studies demonstrated adaptation of P. americanus to local host populations, indicating the importance of migration in co-evolutionary interactions.     

The role of an attractive brood pheromone in the obligatory,slavemaking ant,Polyergus breviceps (hymenoptera: Formicidae)

Freeliving workers of Formica occulta, an ant species enslaved by the obligatory slavemaking ant Polyergus breviceps, retrieve and nurse Polyergus pupaejust as well as conspecific pupae in a choice test. No such attraction was found toward pupae of the facultative slavemaker; Formica wheeleri,which also enslaves F. occulta. Formica neogagates,a sympatric species which is not parasitized by either slavemaker, preferentially retrieves and tends conspecific brood over that of Polyergusand F. wheeleri.It is proposed that brood of obligatory slavemaking species must possess an attractive pheromone for slavemaker colony foundation to be successful, since slavemaker brood must be nursed by adult slave workers with no prior exposure to slavemaker brood. An attractive pheromone is not necessary in the brood of facultative slavemakers, since this brood is cared for by newly eclosed slave workers who imprint on the slavemaker brood.     

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.     

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.     

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.     

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.     

Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system

The geographical mosaic theory of coevolution predicts differences in the advance or trajectory of the coevolutionary process between local communities due to their composition and the strength of ecological selection pressures through competition and resource availability. In this study, we investigate local co-adaptation in different populations of a social parasite. We conducted cross-fostering experiments to test for interpopulational differences in raiding efficiency between various populations of a slave-making ant and the defence abilities of local hosts. Here, we demonstrate that the success of raids strongly depends on the combination of populations of the parasite Harpagoxenus sublaevis and its host Leptothorax acervorum, indicating very localized coevolution. We found no absolute differences between slave-maker populations; the outcome of an encounter depended more on whether the two opponents occur in sympatry or allopatry. Furthermore, this study supports the results of our earlier work, that the unparasitized English L. acervorum population is most aggressive against the parasite.     

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.     

PARASITES AND THE EVOLUTION OF SELF-FERTILIZATION

Abstract.— Assuming all else is equal, an allele for selfing should spread when rare in an outcrossing population and rapidly reach fixation. Such an allele will not spread, however, if self‐fertilization results in inbreeding depression so severe that the fitness of selfed offspring is less that half that of outcrossed offspring. Here we consider an ecological force that may also counter the spread of a selfing allele: coevolution with parasites. Computer simulations were conducted for four different genetic models governing the details of infection. Within each of these models, we varied both the level of selfing in the parasite and the level of male‐gamete discounting in the host (i.e., the reduction in outcrossing fitness through male function due to the selfing allele). We then sought the equilibrium level of host selfing under the different conditions. The results show that, over a wide range of conditions, parasites can select for host reproductive strategies in which both selfed and outcrossed progeny are produced (mixed mating). In addition, mixed mating, where it exits, tends to be biased toward selfing.