Animals that cooperate with nonrelatives represent a challenge to inclusive fitness theory, unless cooperative behavior is shown to provide direct fitness benefits. Inheritance of breeding resources could provide such benefits, but this route to cooperation has been little investigated in the social insects. We show that nest inheritance can explain the presence of unrelated helpers in a classic social insect model, the primitively eusocial wasp Polistes dominulus. We found that subordinate helpers produced more direct offspring than lone breeders, some while still subordinate but most after inheriting the dominant position. Thus, while indirect fitness obtained through helping relatives has been the dominant paradigm for understanding eusociality in insects, direct fitness is vital to explain cooperation in P. dominulus.

Semiochemicals influence many aspects of insect behavior, including interactions between parasites and their hosts. We studied the chemical recognition system of bumblebees (Bombus) by examining the cuticular hydrocarbon cues of 14 species, including five species of social parasites, known as cuckoo bees (subgenus Psithyrus). We found that bumblebees possess species-specific alkene positional isomer profiles that are stable over large geographical regions and are mimicked by three host-specific cuckoo parasites. In three host-cuckoo associations where mimicry is poor, possibly due to recent host shifts, these cuckoos produce dodecyl acetate a known chemical repellent that allows the cuckoos to invade their host colonies. Our findings indicate cuckoos use two chemical mechanisms, mimicry and repellents, to invade their hosts, and this may reflect different stages of an ongoing dynamic arms race.

The paper wasp Polistes dominulus is unique among the social insects in that nearly one-third of co-foundresses are completely unrelated to the dominant individual whose offspring they help to rear and yet reproductive skew is high. These unrelated subordinates stand to gain direct fitness through nest inheritance, raising the question of whether their behaviour is adaptively tailored towards maximizing inheritance prospects. Unusually, in this species, a wealth of theory and empirical data allows us to predict how unrelated subordinates should behave. Based on these predictions, here we compare helping in subordinates that are unrelated or related to the dominant wasp across an extensive range of field-based behavioural contexts. We find no differences in foraging effort, defense behaviour, aggression or inheritance rank between unrelated helpers and their related counterparts. Our study provides no evidence, across a number of behavioural scenarios, that the behaviour of unrelated subordinates is adaptively modified to promote direct fitness interests.