Evolutionary consequences of deception: Complexity and informational content of colony signature are favored by social parasitism

Nestmate recognition codes show remarkable chemical complexity, involving multiple biochemical pathways. This complexity provides the opportunity to evaluate the ecological and social conditions that favor the evolution of complex signaling. We investigated how the chemical signatures of three populations of the social paper wasp Polistes biglumis differed in terms of concentration of hydrocarbons, proportions of branched hydrocarbons and overall variation. We tested whether the variation in chemical signatures among populations could be explained by the prevalence of social parasites or whether this was just an effect of local abiotic conditions which influenced the composition of the hydrocarbon cuticular layer. We studied the chemical signature in three populations in which obligate social parasites differed in the selection pressures they imposed on host populations. Within each population, we restricted our analyses to non-parasitized hosts, to avoid potential short-term effects of parasite presence on the host chemical signatures. We found that host colonies in parasitized populations had more diverse profiles than the parasite-free population. Moreover, the overall concentration of hydrocarbons and the relative proportion of branched hydrocarbons were larger in the parasitized populations, relative to the non-parasitized one. This is to our knowledge the first evidence in favour of the hypothesis that different traits in the host chemical signatures as a whole undergo evolutionary changes resulting from directional or balancing selection imposed by social parasites. We conclude that obligate social parasites act as 'engines of diversity' on host chemical signatures and operate in favor of a geographic mosaic of diverging communication codes.