Immune challenge reduces the production of queen-specific compounds and fertility signals in honey bee queens.

Abstract

Abstract In social insect species, the majority of individuals in each colony – the workers forego reproduction – or produce but a few descendants, while a small minority of individuals, the queens (or a single queen) produce large numbers of offspring – a phenomenon known as reproductive skew. In this situation the workers’ inclusive fitness depends to a large extent on the reproductive capacity of the queen. To maximize their indirect fitness, the workers need to accurately assess the queen’s physiological quality and reproductive capacity. Communication between queens and workers in social insects relies heavily on chemical signals produced by several exocrine glands. Honesty of these signals remains a subject of scientific debate, and the physiological mechanisms maintaining their honesty are not yet well understood. Our study explores how immune challenge affects the chemical profile of honey bee queens. Here, we focus on the mandibular and Dufour’s glands that are critical to production of honey bee queens’ chemical profile. We find that queens subjected to an immune challenge display lower proportions of the esters signaling fertility in their Dufour’s gland as well as lower proportions of queen-like substances in their mandibular glands, suggesting that these chemical signals are honest. Furthermore, we observe that queens subjected to immune challenge switch to production of worker-like compounds, which apparently serve as anti-microbial agents. Our findings suggest that production of queen-specific signaling compounds requires a tradeoff with production of defensive chemicals, suggesting that honey bee queen signals are physiologically costly to produce. Signals that advertise an individual’s physiological quality through the cost of their production, referred to as handicaps, have been documented in sexual communication but not queen-worker communication, which provides the basis of reproductive regulation in insect societies. Our findings may provide the first indication of a handicap signal in insect queen-worker communication.