PARASITES DELAY WORKER REPRODUCTION IN BUMBLEBEES - CONSEQUENCES FOR EUSOCIALITY

Workers in eusocial insects usually tend the brood of the queen and so achieve representation in the next generation through aiding relatives to reproduce. However, workers of some eusocial species, such as bumblebees, are capable of reproductive activity even in the presence of the queen (in queen-right colonies), and worker reproduction is associated with aggressive behaviors and egg cannibalism, both of which reduce colony efficiency. Thus, factors that affect worker ovarian development, a precondition for reproduction, can influence social harmony and colony productivity. Parasites are a ubiquitous and important part of the biotic environment of all organisms. Here we show that parasites play an important role in the reproductive physiology of worker bumblebees in queen-right colonies of Bombus terrestris, affecting the pattern and timing of ovarian development and oviposition. Workers from colonies parasitized with the intestinal trypanosome Crithidia bombi had less developed ovaries than workers of the same age from unparasitized colonies. In addition, parasitized colonies were smaller than unparasitized colonies for about the first half of colony development. This generated further demographic effects such that workers were on average younger in parasitized than in unparasitized colonies around the time of the onset of worker oviposition, and worker oviposition occurred significantly later in parasitized colonies. Workers in parasitized colonies therefore had lower individual reproductive potential and were cooperative for a larger proportion of the colony cycle than those in unparasitized colonies. In this system, where transmission of the parasite between years probably occurs only in infested, young queens, this effect may represent an adaptation on the part of the parasite to ensure its successful passage through the winter. Parasites, by reducing the cost of worker cooperation, may facilitate queen control over her worker force and play an important role in moderating the social organization of eusocial insect colonies.