Evidence for differential selection and potential adaptive evolution in the worker caste of an inquiline social parasite

Social parasites exploit the socially managed resources of social insect colonies in order to maximise their own fitness. The inquilines are among the most specialised social parasites, because they are dependent on being fully integrated into their host's colony throughout their lives. They are usually relatives of their host and so share ancestral characteristics (Emery's rule). Closely related inquiline-host combinations offer a rare opportunity to study trade-offs in natural selection. This is because ancestral adaptations to a free-living state (e.g. the production of a worker caste) become redundant and may be replaced by novel, parasitic traits as the inquiline becomes more specialised. The dynamics of such processes are, however, unknown as virtually all extant inquiline social parasites have completely lost their worker caste. An exception is Acromyrmex insinuator, an incipient permanent social parasite of the leaf-cutting ant Acromyrmex echinatior. In the present study, we document the size distribution of parasite and host workers and infer how selection has acted on A. insinuator to reduce, but not eliminate, its investment in a worker caste. We show that the antibiotic producing metapleural glands of these parasite workers are significantly smaller than in their host counterparts and we deduce that the metapleural gland size in the host represents the ancestral state. We further show experimentally that social parasite workers are more vulnerable to the general insect pathogenic fungus Metarhizium than are host workers. Our findings suggest that costly disease resistance mechanisms are likely to have been lost early in inquiline evolution, possibly because active selection for maintaining these traits became less when parasite workers had evolved the ability to exploit the collective immune system of their host societies.