Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite

The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus . A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with local parasite pressure, we found parasite success to be much more important. Our chemical and behavioural analyses revealed that parasites from high prevalence sites carry lower concentrations of recognition cues and are less often attacked by hosts. This link was further supported by gene expression analysis. Our study reveals that host–parasite interactions are strongly influenced by social parasite strategies, so that variation in parasite prevalence is determined by parasite traits rather than the efficacy of host defence. Gene functions associated with parasite success indicated strong neuronal responses in hosts, including long-term changes in gene regulation, indicating an enduring impact of parasites on host behaviour. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Gene expression is stronger associated with behaviour than with age and fertility in ant workers

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is strongly influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and corpulent. Here, we experimentally disentangle behaviour from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. Our transcriptome analysis reveals four times more genes associated with behaviour than with age and only few fertility-associated genes. Brood carers exhibited an upregulation of genes involved in lipid biosynthesis, whereas foragers invested in metabolism. Additional simulations revealed that the experimental disassociation of co-varying factors reduces transcriptomic noise, potentially explaining discrepancies between transcriptomic studies on worker behaviour in other social insects. Our study highlights the influence of nutritional status on task choice in ant workers.

Fitness costs of worker specialization for ant societies

Division of labour is of fundamental importance for the success of societies, yet little is known about how individual specialization affects the fitness of the group as a whole. While specialized workers may be more efficient in the tasks they perform than generalists, they may also lack the flexibility to respond to rapid shifts in task needs. Such rigidity could impose fitness costs when societies face dynamic and unpredictable events, such as an attack by socially parasitic slavemakers. Here, we experimentally assess the colony-level fitness consequences of behavioural specialization in Temnothorax longispinosus ants that are attacked by the slavemaker ant T. americanus . We manipulated the social organization of 102 T. longispinosus colonies, based on the behavioural responses of all 3842 workers. We find that strict specialization is disadvantageous for a colony's annual reproduction and growth during slave raids. These fitness costs may favour generalist strategies in dynamic environments, as we also demonstrate that societies exposed to slavemakers in the field show a lower degree of specialization than those originating from slavemaker-free populations. Our findings provide an explanation for the ubiquity of generalists and highlight their importance for the flexibility and functional robustness of entire societies.

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.

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.