Mating with an allopatric male triggers immune response and decreases longevity of ant queens.

In species with lifelong pair bonding, the reproductive interests of the mating partners are aligned, and males and females are expected to jointly maximize their reproductive success. Mating increases both longevity and fecundity of female reproductives (queens) of the ant Cardiocondyla obscurior, indicating a tight co-evolution of mating partners. Here, we show that mating with a male from their own population increases lifespan and reproductive success of queens more than mating with a male from a different population, with whom they could not co-evolve. A comparison of transcriptomes revealed an increased expression of genes involved in immunity processes in queens, which mated with males from a different population. Increased immune response might be proximately associated with decreased lifespan. Our study suggests a synergistic co-evolution between the sexes and sheds light on the proximate mechanisms underlying the decreased fitness of allopatrically mated queens.