Parasitism and queen presence interactively shape worker behaviour and fertility in an ant host

Abstract

Parasites with complex life cycles regularly alter host traits in their own interest. In social hosts, phenotypic alterations induced by parasites can also affect uninfected group members. The tapeworm Anomotaenia brevis uses Temnothorax nylanderi ants as intermediate hosts, reducing host activity and behavioural repertoire, but increasing life span. Uninfected nestmates are less active and less aggressive and suffer from higher mortality. Next to parasites, the social environment, such as the queen, influences worker behaviour, reproduction and longevity. Here, we studied how tapeworm parasitism interacts with the queen to affect the behaviour and reproductive potential of ant workers. We collected naturally parasitized and unparasitized ant colonies, and experimentally removed the sole queen in half of each colony type to induce worker reproduction. We examined the behaviour and ovary development of tapeworm-infected workers, uninfected nurses and uninfected foragers from parasitized and unparasitized colonies living under queenright and queenless conditions. Remarkably, fertility induction was most pronounced in tapeworm-infected workers, which quickly responded to queen removal by developing their ovaries. The fertility of nurses, known to have the highest reproductive potential and to be in close contact with infected workers, was not reduced by tapeworm parasitism. However, their behaviour was impacted by an interaction between parasitism and queen removal: nurses from parasitized, queenless colonies became less active, whereas no behavioural changes were observed in nurses from unparasitized colonies. Behaviour and ovary development of foragers were unaffected by the presence of tapeworm-infected workers and the queen. Our findings indicate that parasitism by a tapeworm increases rather than decreases the reproductive potential of infected workers. We further show that parasites and the presence of dominant group members interactively shape fertility and behaviour of infected and healthy group members.