The scent of infanticide risk? Behavioural allocation to current and future reproduction in response to mating opportunity and familiarity with intruder

The killing of young by unrelated males is widespread in the animal kingdom. In short-lived small rodents, females can mate immediately after delivery (post-partum oestrus) and invest in future reproduction, but infanticide may put the nestlings, their current reproductive investment, at risk. Here, we investigated the behavioural trade-offs between mating interest and nest protection in an arena experiment with bank voles (Myodes glareolus). Non-gravid females (n = 33) were housed at one end of a large structured arena with their nestlings. Different scents (cage bedding) were presented to each female in a replicated design. Three combinations of mating opportunities and male-female familiarity were simulated using different scent donors: mating opportunity with the sire of the nestlings with whom the female was familiar; mating opportunity with a male unrelated to the offspring and unfamiliar to the female, thus posing a higher risk to the offspring; and neither risk nor mating opportunity (clean control). Most females investigated male scents, regardless of familiarity, leaving their litter unprotected. During control treatment, females with larger litters spent less time at the scent area, indicating increasing nursing demands or better protection. Females with older litters visited scents more often, suggesting an increased interest in reproduction while they are non-gravid alongside the decreased risk of infanticide for older young. In the presence of unfamiliar scents, females spent more time protecting their nests, supporting the perceived association of unfamiliarity with infanticide risk. Thus, rodent females flexibly allocate time spent between searching for a mate and protecting their nest, which is modulated by their familiarity with a potential intruder. Infanticide by conspecific males is an extreme form of sexual conflict and has large costs on females, abolishing their investment into current offspring. In an experimental approach, we exposed lactating female bank voles to different combinations of mating opportunity and familiarity to a (simulated) intruder: (1) the sire of the nestlings with whom the female was familiar and, therefore, potentially less risky in terms of infanticide; (2) a male which was unrelated and unfamiliar to the female and thus posed a higher risk to the offspring; or (3) as a control, cage bedding, which posed neither risk of infanticide nor a mating opportunity. We show that females flexibly allocated pup protection and mating interest based on their familiarity with the male, indicating that the unfamiliar males pose a threat to offspring, which is perceived by the females. Females further adjusted their behaviour to the size and/or age of their current litter, investing more time in male scents when offspring were older, thus balancing future and current investments into reproduction.