Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect

Abstract

Complex social behaviour in Hymenoptera has been hypothesized to evolve by co-opting reproductive pathways (the ovarian ground plan hypothesis, OGPH) and gene networks (the reproductive ground plan hypothesis, RGPH). In support of these hypotheses, in eusocial Hymenoptera where there is reproductive division of labour, the yolk precursor protein vitellogenin (Vg) influences the expression of worker social behaviour. We suggest that co-opting genes involved in reproduction may occur more generally than just in the evolution of eusociality; i.e. underlie earlier stages of social evolution such as the evolution of parental care, given that reproduction and parental care rarely overlap. We therefore examined vitellogenin (vg) gene expression associated with parental care in the subsocial beetle Nicrophorus vespilloides. We found a significant reduction in the expression of vg and its receptor, vgr, in head tissue during active parental care, and confirmed that the receptor is expressed in the brains of both sexes. Ours is the first study to show that vgr is expressed in the brain of a non-eusocial insect. Given the association between behaviour and gene expression in both sexes, and the presence of vitellogenin receptors in the brain, we suggest that Vg was co-opted early in the evolution of sociality to have a regulatory function. This extends the association of Vg in parenting to subsocial species and outside of the Hymenoptera, and supports the hypothesis that the OGPH is general and that heterochrony in gene expression is important in the evolution of social behaviour and precedes subsequent evolutionary specialization of social roles.

Modification of feeding circuits in the evolution of social behavior

“…Within colonies, nurses have higher Vg expression and more ovarioles than foragers, indicating that nurse bees performing brood care exhibit a reproductive physiology more similar to that of mothers despite being nonreproductive themselves . In addition, Vg and its interaction with juvenile hormone and insulin signaling regulate maternal effects on caste determination in ants (Libbrecht et al, 2013), and changes in Vg are associated with behavioral transitions to parental care in both male and female burying beetles (Parker et al, 2015;Roy-Zokan et al, 2015). In concert, these studies present evidence that mechanisms mediating maternal care have been selected upon during the evolution of sociality.…”

Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris

“…These are the only tissues with Vg upregulated in comparison with workers. Since Vg expression in the brains of some insects is linked to caste- or reproduction-related behavior and physiology (Corona et al, 2007; Roy-Zokan et al, 2015), it appears likely that this finding could be linked to a queen-specific role of Vg.…”

The role of neuropeptide F in a transition to parental care

“…Primer sequences were generated and validated as in [21]. We ran samples on a Roche LightCycler 480 [21] with tbp as the endogenous control [20]. Analyses were performed with the MCMC.qpcr R package [22] using an 'informed' MCMC qpcr model with default settings and both sex and behavioural state as factors.…”

“…Sample collection (whole heads), RNA extraction and cDNA synthesis are described in [20]. Primer sequences were generated and validated as in [21].…”