Susanne Foitzik

Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts.

Recently, avian brood parasites and their hosts have emerged as model systems for the study of host–parasite coevolution. However, empirical studies of the highly analogous social parasites, which use the workers of another eusocial species to raise their own young, have never explicitly examined the dynamics of these systems from a coevolutionary perspective. Here, we demonstrate interpopulational variation in behavioural interactions between a socially parasitic slave–maker ant and its host that is consistent with the expectations of host–parasite coevolution. Parasite pressure, as inferred by the size, abundance and raiding frequency of Protomognathus americanus colonies, was highest in a New York population of the host Leptothorax longispinosus and lowest in a West Virginia population. As host–parasite coevolutionary theory would predict, we found that the slave–makers and the hosts from New York were more effective at raiding and defending against raiders, respectively, than were conspecifics from the West Virginia population. Some of these variations in efficacy were brought about by apparently simple shifts in behaviour. These results demonstrate that defence mechanisms against social parasites can evolve, and they give the first indications of the existence of a coevolutionary arms race between a social parasite and its host.

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

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

Diverse societies are more productive: a lesson from ants

The fitness consequences of animal personalities (also known as behavioural syndromes) have recently been studied in several solitary species. However, the adaptive significance of collective personalities in social insects and especially of behavioural variation among group members remains largely unexplored. Although intracolonial behavioural variation is an important component of division of labour, and as such a key feature for the success of societies, empirical links between behavioural variation and fitness are scarce. We investigated aggression, exploration and brood care behaviour in Temnothorax longispinosus ant colonies. We focused on two distinct aspects: intercolonial variability and its consistency across time and contexts, and intracolonial variability and its influence on productivity. Aggressiveness was consistent over four to five months with a new generation of workers emerging in between trial series. Other behaviours were not consistent over time. Exploration of novel environments responded to the sequence of assays: colonies were faster in discovering when workers previously encountered opponents in aggression experiments. Suites of correlated behaviours (e.g. aggression–exploration syndrome) present in the first series did not persist over time. Finally, colonies with more intracolonial behavioural variation in brood care and exploration of novel objects were more productive under standardized conditions than colonies with less variation.

Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones.

Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood‐tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood‐tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood‐tenders and foragers (~300 genes). The expression profile of fertile workers is more worker‐like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.

COLONY STRUCTURE OF A SLAVEMAKING ANT. I. INTRACOLONY RELATEDNESS, WORKER REPRODUCTION, AND POLYDOMY

Colony and population structure of the obligate slavemaker ant Protomognathus americanus was analyzed via four nuclear microsatellite loci and mitochondrial DNA (mtDNA) markers. Colonies of P. americanus usually contain a single queen, and here we show that she is singly inseminated. Nestmate workers are generally full sisters and their relatedness does not deviate from the expected value of 0.75. Even though colonies were strictly monogynous, we were able to infer that colony takeover by related queens was common and queen replacement by unrelated queens was rare. Polydomy is widespread, with neighboring nests having the same genetic composition. Although we found no evidence of population viscosity or inbreeding from nuclear markers, mtDNA markers provided evidence for small‐scale genetic structuring. Haplotype structuring and takeover by related queens suggest philopatry of newly mated queens. In this species, workers reproduce in queenright and queenless nests and worker reproduction accounts for more than 70% of all males. Although sex‐ratio theory points to slavemaking ants as important systems for studying queen‐worker conflict, our results indicate no basis for such conflict in P. americanus, because extensive worker reproduction generates shifts in relatedness values. Rather, the dual effects of independent polydomous nest units and local resource competition among queens produce male‐biased allocation ratios in this species.

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.

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.

Six origins of slavery in formicoxenine ants

Summary.Slave-making (dulotic) ants have long fascinated biologists because of their intriguing behavior and highly specialized lifestyle. Dulosis evolved convergently several times within the two ant subfamilies Myrmicinae and Formicinae. Here, we demonstrate that it originated at least six times independently within the small myrmicine tribe Formicoxenini alone. Our phylogenetic trees, based on 1386 base pairs of the mitochondrial cytochrome oxidase gene, document different degrees of genetic divergence between different monophyla of slave-makers and their host species, which suggests that they evolved from non-parasitic Formicoxenini at different times. Two nearctic slave-makers, Temnothorax duloticus and a new species still to be formally described, appear to be of particularly recent origin. In contrast, the other parasitic monophyla clearly diverged much earlier from their nonparasitic ancestors and have a much longer evolutionary history.

Nestmate recognition and intraspecific chemical and genetic variation in Temnothorax ants

The evolutionary stability of social cooperation requires altruistic acts to be directed mainly towards related individuals. To maintain significant intragroup relatedness, social insects have evolved sophisticated recognition systems. We compared nestmate recognition abilities of three native European species of the ant genus Temnothorax in relation to variation in cuticular chemicals and intraspecific genetic diversity. Colony take-over and fusions are common in two sibling species T. nylanderi and T. crassispinus, but rare in T. unifasciatus, suggesting relatively inefficient nestmate recognition in the former species. Temnothorax nylanderi and T. crassispinus discriminated less effectively between nestmates and non-nestmates than T. unifasciatus. While chemical profiles of different colonies strongly overlapped in T. crassispinus and T. nylanderi, 97% of all T. unifasciatus samples were, in a discriminant analysis, correctly assigned to their respective colony. Chemical distances between colonies correlated with aggression levels in T. unifasciatus, but not in the other two species. Finally, preliminary genetic results indicated that haplotype divergence within T. nylanderi and T. crassispinus is remarkably low, whereas T. unifasciatus and other congeners are genetically more variable. In theory, loss of genetic variation, including depletion at loci involved in the production of cuticular hydrocarbons, could decrease colony recognition efficiency. We suggest that this might be the case in T. nylanderi and T. crassispinus, leading to colony fusions in the field. Despite their different life histories, these native species show similarities to invasive ants where genetic bottlenecks arising from founder effects are thought to result in a loss of colony boundaries.

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.