Chemical communication is not sufficient to explain reproductive inhibition in the bumblebee Bombus impatiens

Abstract

Reproductive division of labour is a hallmark of eusociality, but disentangling the underlying proximate mechanisms can be challenging. In bumblebees, workers isolated from the queen can activate their ovaries and lay haploid, male eggs. We investigated if volatile, contact, visual or behavioural cues produced by the queen or brood mediate reproductive dominance in Bombus impatiens. Exposure to queen-produced volatiles, brood-produced volatiles and direct contact with pupae did not reduce worker ovary activation; only direct contact with the queen could reduce ovary activation. We evaluated behaviour, physiology and gene expression patterns in workers that were reared in chambers with all stages of brood and a free queen, caged queen (where workers could contact the queen, but the queen was unable to initiate interactions) or no queen. Workers housed with a caged queen or no queen fully activated their ovaries, whereas ovary activation in workers housed with a free queen was completely inhibited. The caged queen marginally reduced worker aggression and expression of an aggression-associated gene relative to queenless workers. Thus, queen-initiated behavioural interactions appear necessary to establish reproductive dominance. Queen-produced chemical cues may function secondarily in a context-specific manner to augment behavioural cues, as reliable or honest signal.

Queen Recognition Signals in Two Primitively Eusocial Halictid Bees: Evolutionary Conservation and Caste-Specific Perception

“…Beside this, it was shown that behavioral interactions of the queens, e.g., aggressive behavior towards workers, is necessary to induce sterility in workers in some primitively eusocial insect species, whereas chemical signals are not sufficient to affect worker's reproductive physiology [52][53][54][55][56][57]. Regarding our recent study on L. malachurum, we could clearly demonstrate that macrocyclic lactones as a chemical signal of the queen are solely sufficient to induce sterility in workers [20].…”

“…However, our recent comparative study on caste differences in cuticular chemical profiles among several halictid bee species with various social levels demonstrated, that castes of facultative eusocial species are chemically less distinct than castes in obligate eusocial species [21]. These smaller caste differences could be a hint for other signals to be involved in the regulation of worker's reproduction, potentially also aggressive behavior as was shown in other primitively eusocial species such as Polistes wasps and bumble bees [52][53][54][55][56][57]. However, more bioassays are needed to prove, if and how other than chemical signals play a role in regulating worker's reproduction in different halictid bee species.…”

Juvenile hormone, but not nutrition or social cues, affects reproductive maturation in solitary alkali bees (Nomia melanderi)

“…This suggests that different components of the endocrine networks influencing reproductive physiology were independently modified during social evolution. Also, nutrition and cues from the social environment are some of the most important factors in reproductive suppression of workers among social bees (Amsalem et al, 2013;Kapheim et al, 2016;Lawson et al, 2016;Padilla et al, 2016), but these factors did not have a significant influence on variation in reproductive activation in solitary alkali bees. This suggests that changes in how nutrient-sensing and environment-sensing pathways regulate reproductive physiology were especially important in the evolutionary origins of reproductive castes.…”

“…Conversely, highly eusocial insects have evolved sophisticated forms of social communication. Within colonies of honey bees, bumble bees and sweat bees, behavior and reproductive physiology are dynamically regulated by the behavior and/or pheromones of nest-mates (Alaux et al, 2009;Amsalem and Hefetz, 2010;Arneson and Wcislo, 2003;Grozinger et al, 2003;Huang et al, 1998;Kapheim et al, 2016;Le Conte et al, 2001;Li-Byarlay et al, 2014;Padilla et al, 2016;Smith et al, 2009). Research with a facultatively eusocial halictid bee, M. genalis, suggests that aggression from older, reproductive females can limit reproductive development via JH suppression in newly emerged females (Kapheim et al, 2016;Smith et al, 2009Smith et al, , 2013.…”

“…Similarly, treatment with the juvenile hormone (JH) analog methoprene leads to accelerated ovarian development in queen paper wasps (Polistes canadensis), but increases foraging activity in workers (Giray et al, 2005). Finally, social cues, such as aggression from the queen, can repress endocrine pathways, and thus ovary maturation, in worker bumble bees (Bombus impatiens) and social halictid bees (Megalopta genalis), but aggression directed from workers toward queens does not have the same effect (Kapheim et al, 2016;Padilla et al, 2016;Smith et al, 2009). Understanding how these differences in sensitivity to physiological and environmental cues arise among females and contribute to variation in reproductive activity is thus key to understanding the origins of social insect castes.…”