Notch signalling mediates reproductive constraint in the adult worker honeybee

Abstract

The hallmark of eusociality is the reproductive division of labour, in which one female caste reproduces, while reproduction is constrained in the subordinate caste. In adult worker honeybees (Apis mellifera) reproductive constraint is conditional: in the absence of the queen and brood, adult worker honeybees activate their ovaries and lay haploid male eggs. Here, we demonstrate that chemical inhibition of Notch signalling can overcome the repressive effect of queen pheromone and promote ovary activity in adult worker honeybees. We show that Notch signalling acts on the earliest stages of oogenesis and that the removal of the queen corresponds with a loss of Notch protein in the germarium. We conclude that the ancient and pleiotropic Notch signalling pathway has been co-opted into constraining reproduction in worker honeybees and we provide the first molecular mechanism directly linking ovary activity in adult worker bees with the presence of the queen.

Long-lived rodents reveal signatures of positive selection in genes associated with lifespan and eusociality

“…Notch signaling regulates interactions between physically adjacent cells and has a central role in the development of many tissues, including neurons 97 . It was demonstrated that Notch signaling represses reproduction in worker honeybees depending on the presence of the queen and that chemical inhibition of Notch signaling can overcome the repressive effect of queen pheromone in regard to the worker ovary activity 98 .…”

Brain microRNAs among social and solitary bees

“…The presence of this miRNA in the solitary bee genomes suggests that an evolutionary shift in expression pattern has accompanied at least two independent origins of eusociality in bees. This miRNA coordinates Insulin and Notch signaling in D. melanogaster , and both of these pathways are important regulators of social dynamics in insects [56–60]. Interestingly, this miRNA is also upregulated in worker-destined compared to queen-destined honey bee larvae, and may thus play a role in caste differentiation [22].…”

From gene list to gene network: Recognizing functional connections that regulate behavioral traits

“…Cardoen et al () found further overlap from 2D‐DIGE against the gene screens of Grozinger et al (; n = 3 genes) and Cardoen et al (; n = 31 genes), strongly suggesting that several gene‐level components of the regulatory networks are directly connected to the protein level above it. Additional studies on protein‐level interactions that mediate sterility are necessary to identify hub proteins implicated in sterility (Duncan, Hyink, & Dearden, ; Ronai, Oldroyd et al, ), caste differentiation (Begna, Han, Feng, Fang, & Li, ; Li et al, ), queen reproductive development (Pang et al, ), worker embryogenesis (Fang et al, ; Zheng et al, ), age‐dependent division of labor (Huo et al, ), and other aspects of social foraging (the proboscis extension reflex; da Silva Menegasso et al, ). Where available, information from these networks should serve to identify hub proteins and other topological features that, similarly to the gene networks, can be used to detail ideas on their origins and activity.…”

“…A comparison of these proteins to corresponding gene sets (e.g., Cardoen et al, 2011;Grozinger et al, 2007;Thompson et al, 2008;Thompson, Kucharski, Maleszka, & Oldroyd, 2006) revealed some overlap. From a gene-level screen, for instance, Thompson et al (2008) were able to infer that the major yolk that mediate sterility are necessary to identify hub proteins implicated in sterility (Duncan, Hyink, & Dearden, 2016;, caste differentiation (Begna, Han, Feng, Fang, & Li, 2012;Li et al, 2010), queen reproductive development (Pang et al, 2017), worker embryogenesis (Fang et al, 2014;Zheng et al, 2011), age-dependent division of labor (Huo et al, 2016), and other aspects of social foraging (the proboscis extension reflex; da Silva Menegasso et al, 2017). Where available, information from these networks should serve to identify hub proteins and other topological features that, similarly to the gene networks, can be used to detail ideas on their origins and activity.…”