Tricking Parents: A Review of Mechanisms and Signals of Host Manipulation by Brood-Parasitic Young

Obligate avian brood parasites depend entirely on heterospecific hosts for rearing their offspring. From hatching until independence, the young parasites must deal with the challenge of obtaining sufficient parental care from foster parents that are attuned to provisioning their own offspring. Parent-offspring communication is mediated by complex begging displays in which nestlings and fledglings exhibit visual (e.g., gaping and postures) and vocal (e.g., begging calls) traits that serve as signals to parents to adjust and allocate parental effort. Parasites can manipulate host parental behavior by exploiting these stable parent-offspring communication systems in their favor. During the past 30 years, the study of host exploitation by parasitic chicks has yielded important insights into the function and evolution of manipulative signals in brood parasites. However, despite these major advances, there are still important gaps in our knowledge about how parasitic nestling and fledglings tune into the host’s communication channels and the adaptive value of the visual and acoustic signals they exhibit. Here we review the literature pertaining to host manipulation by parasitic young, focusing on four non-mutually exclusive mechanisms (i.e., host chick mimicry, begging exaggeration, host-attuned begging calls, and sensory exploitation) and the function and evolution of the signals involved, with the aim to summarize and discuss putative adaptations for stimulating parental feeding and escaping host discrimination. Finally, we bring some concluding remarks and suggest directions for future research on the ways in which brood parasites adapt to the communication systems of other birds to exploit the necessary parental care.

Cross-activity of honeybee queen mandibular pheromone in bumblebees provides evidence for sensory exploitation

The evolutionary origin of queen pheromones (QPs), which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect QPs—such as cuticular hydrocarbons—were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on preexisting gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee QP pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.