Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies

Animals commonly leave scent messages by depositing pheromones, faeces, or urine. The intensity of a chemical message may fade over time, but the ‘intention’ remains the same. We argue that house flies, Musca domestica (Diptera: Muscidae), require a message with evolving (sensu changing over time) information content. Gravid females reportedly deploy a pheromone that induces concerted oviposition so that many even-aged larvae ameliorate the resource, such as animal manure. However, continued oviposition by late-arriving females may result in age disparity and cannibalism of larval offspring. Thus, we predicted that house flies have a type of cue that evolves from oviposition induction to inhibition some time after eggs are deposited on a resource. Here we show (1) the existence of such evolving ovipositional cues, (2) the adverse fitness consequences that accrue from ignoring the inhibitory cues and (3) the mechanism by which these cues evolve. The evolving cues depend upon a key bacterial strain, Klebsiella oxytoca, which originates with female M. domestica and which proliferates over time on the surface of deposited eggs. At a threshold density of this strain, further oviposition is inhibited. By deploying such evolving cues, female M. domestica can visit an oviposition site just once and deposit cues that will mediate immediate oviposition induction followed by delayed inhibition, thereby ensuring conditions conducive for offspring development.