Parasites decrease host fitness and can induce changes in host behavior, morphology, and physiology. When parasites exploit social insects, they influence not only infected individuals but also the society as a whole. Workers of the ant Temnothorax nylanderi are an intermediate host for the cestode Anomotaenia brevis. We studied a heavily parasitized population and found that, although parasite infection had strong and diverse consequences for individual workers, colony fitness remained unchanged. At the individual level, we uncovered differences among the three worker types, infected and healthy workers from parasitized colonies and healthy workers from nonparasitized colonies. Infected workers were smaller than healthy ones and had smaller heads as parasite load increased. Behavioral changes extended to all workers from parasitized colonies; such workers were less active than workers in nonparasitized colonies but engaged in more grooming. Healthy workers from parasitized colonies showed behavioral patterns intermediate to those of infected workers and healthy workers from nonparasitized colonies. Despite the lower activity level found in ants from parasitized colonies, an important fitness parameter, per-worker productivity, remained unaltered in parasitized colonies. However, the investment strategies of parasitized colonies changed as their sex ratio became male biased and as male body size increased. In short, ant colonies can buffer the drain of resources by the parasite despite strong effects on individual workers.

Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nest-mates and do not contribute to colony fitness, but are tolerated in their colonies and well cared for. Here, we investigated how tapeworminfected workers affect colony aggression by manipulating their presence in ant colonies and analysing whether their absence or presence resulted in behavioural alterations in their nest-mates. We report a parasite-induced shift in colony aggression, shown by lower aggression of uninfected nest-mates from parasitized colonies towards conspecifics, potentially explaining the tolerance towards infected ants. We also demonstrate that tapeworm-infected workers showed a reduced flight response and higher survival, while their presence caused a decrease in survival of uninfected nest-mates. This anomalous behaviour of infected ants, coupled with their increased survival, could facilitate the parasites' transmission to its definitive hosts, woodpeckers. We conclude that parasites exploiting individuals that are part of a society not only induce phenotypic changes within their individual hosts, but in uninfected group members as well.

Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.

Many parasites manipulate their hosts' phenotype. In particular, parasites with complex life cycles take control of their intermediate hosts' behaviour and life history to increase transmission to their definitive host. The proximate mechanisms underlying these parasite-induced alterations are poorly understood. The cestode Anomotaenia brevis affects the behaviour, life history and morphology of parasitized Temnothorax nylanderi ants and indirectly of their unparasitized nestmates. To gain insights on how parasites alter host phenotypes, we contrast brain gene expression patterns of T. nylanderi workers parasitized with the cestode, their unparasitized nestmates and unparasitized workers from unparasitized colonies. Over 400 differentially expressed genes between the three groups were identified, with most uniquely expressed genes detected in parasitized workers. Among these are genes that can be linked to the increased lifespan of parasitized workers. Furthermore, many muscle (functionality) genes are downregulated in these workers, potentially causing the observed muscular deformations and their inactive behaviour. Alterations in lifespan and activity could be adaptive for the parasite by increasing the likelihood that infected workers residing in acorns are eaten by their definitive host, a woodpecker. Our transcriptome analysis reveals numerous gene expression changes in parasitized workers and their uninfected nestmates and indicates possible routes of parasite manipulation. Although causality still needs to be established, parasite-induced alterations in lifespan and host behaviour appear to be partly explained by morphological muscle atrophy instead of central nervous system interference, which is often the core of behavioural regulation. Results of this study will shed light upon the molecular basis of antagonistic species interactions.

Social insects are hosts of diverse parasites, but the influence of these parasites on phenotypic host traits is not yet well understood. Here, we tracked the survival of tapeworm-infected ant workers, their uninfected nest-mates and of ants from unparasitized colonies. Our multi-year study on the ant Temnothorax nylanderi, the intermediate host of the tapeworm Anomotaenia brevis, revealed a prolonged lifespan of infected workers compared with their uninfected peers. Intriguingly, their survival over 3 years did not differ from those of (uninfected) queens, whose lifespan can reach two decades. By contrast, uninfected workers from parasitized colonies suffered from increased mortality compared with uninfected workers from unparasitized colonies. Infected workers exhibited a metabolic rate and lipid content similar to young workers in this species, and they received more social care than uninfected workers and queens in their colonies. This increased attention could be mediated by their deviant chemical profile, which we determined to elicit more interest from uninfected nest-mates in a separate experiment. In conclusion, our study demonstrates an extreme lifespan extension in a social host following tapeworm infection, which appears to enable host workers to retain traits typical for young workers.