From class-specific to individual discrimination: acceptance threshold changes with risk in the partner recognition system of the burying beetle Nicrophorus vespilloides

Abstract

Burying beetles exhibit elaborate biparental care, in which a male and a female bury a carcass upon which they rear their brood and defend it against conspecific competitors. If an intruder succeeds in taking over the carcass, it kills the entire brood and rears its own young on the remaining resource. However, the resident male and female are able to discriminate between an intruder and their breeding partner, and assist their mate in driving off intruders of either sex. Efficient brood guarding requires effective recognition and discrimination mechanisms. Theory predicts that the setting of the optimal acceptance threshold should be affected by the rates of interaction with desirable and undesirable individuals, and shift towards a less permissive threshold when the probability of encountering intruders increases. Here we provide a critical test of acceptance-threshold theory by investigating discrimination rules during reproduction in the burying beetle Nicrophorus vespilloides. The beetles typically discriminate between their breeding partners and conspecific intruders based on a class-specific discrimination rule: they generally accept beetles that are also caring for larvae (whether their own partner or not), but are aggressive towards all nonbreeding beetles. However, we demonstrate that this recognition system is flexible at the level of individual experience and changes with context. After the introduction of an intruder, rejection rate increased, which was manifested as a shift from class-specific to individual-specific discrimination: males suddenly began discriminating between their own breeding partner and novel breeding females, and were more aggressive towards the latter. We show that the plasticity in the recognition system is not caused by template updating, but instead by a flexible acceptance threshold. Our experiments suggest that breeding males learn the individual features of their own breeding partner, but set their acceptance threshold depending on the risk of encountering an intruder.