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

Roy-Zokan EM, Cunningham CB, Hebb LE, McKinney EC, Moore AJ - Proc. Biol. Sci. (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, GA 30602, USA.

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.

No MeSH data available.


vitellogenin expression in head tissue of adult female and adult male N. vespilloides across five behavioural states. (a) vg1 expression and (b) vg2 expression significantly decreases during active care of larvae in females. (c) vg1 expression and (d) vg2 expression decreases in males during care of larvae but the reduction in expression is only statistically significant for vg1. Bars represent mean relative quantity and error bars represent±1 s.e.m. Bars with different letters are statistically significantly different in pairwise comparisons. Expression was measured from whole heads using 10 individuals per behavioural state.
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RSPB20150787F2: vitellogenin expression in head tissue of adult female and adult male N. vespilloides across five behavioural states. (a) vg1 expression and (b) vg2 expression significantly decreases during active care of larvae in females. (c) vg1 expression and (d) vg2 expression decreases in males during care of larvae but the reduction in expression is only statistically significant for vg1. Bars represent mean relative quantity and error bars represent±1 s.e.m. Bars with different letters are statistically significantly different in pairwise comparisons. Expression was measured from whole heads using 10 individuals per behavioural state.

Mentions: We found that the expression pattern of vg1 and vg2 in head tissue changed across the five social conditions examined and that the patterns for vg1 and vg2 were nearly identical. There was a statistically significant association between vg1 gene expression and social condition (figure 2a; F4,45 = 29.490, p < 0.0001) in females. There were statistically significantly lower expressions in caring females than in virgin, mated without a mouse, mated with a mouse and post-caring females (all p < 0.0001). There was also a statistically significantly lower expression in mated without a mouse and mated with a mouse (p = 0.0004) and post-caring (p = 0.0010). Mated with a mouse (p = 0.0152) and post-caring (p = 0.0299) were statistically significantly lower than virgin female expression. No other pairwise comparisons were statistically significant.Figure 2.


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

Roy-Zokan EM, Cunningham CB, Hebb LE, McKinney EC, Moore AJ - Proc. Biol. Sci. (2015)

vitellogenin expression in head tissue of adult female and adult male N. vespilloides across five behavioural states. (a) vg1 expression and (b) vg2 expression significantly decreases during active care of larvae in females. (c) vg1 expression and (d) vg2 expression decreases in males during care of larvae but the reduction in expression is only statistically significant for vg1. Bars represent mean relative quantity and error bars represent±1 s.e.m. Bars with different letters are statistically significantly different in pairwise comparisons. Expression was measured from whole heads using 10 individuals per behavioural state.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4590458&req=5

RSPB20150787F2: vitellogenin expression in head tissue of adult female and adult male N. vespilloides across five behavioural states. (a) vg1 expression and (b) vg2 expression significantly decreases during active care of larvae in females. (c) vg1 expression and (d) vg2 expression decreases in males during care of larvae but the reduction in expression is only statistically significant for vg1. Bars represent mean relative quantity and error bars represent±1 s.e.m. Bars with different letters are statistically significantly different in pairwise comparisons. Expression was measured from whole heads using 10 individuals per behavioural state.
Mentions: We found that the expression pattern of vg1 and vg2 in head tissue changed across the five social conditions examined and that the patterns for vg1 and vg2 were nearly identical. There was a statistically significant association between vg1 gene expression and social condition (figure 2a; F4,45 = 29.490, p < 0.0001) in females. There were statistically significantly lower expressions in caring females than in virgin, mated without a mouse, mated with a mouse and post-caring females (all p < 0.0001). There was also a statistically significantly lower expression in mated without a mouse and mated with a mouse (p = 0.0004) and post-caring (p = 0.0010). Mated with a mouse (p = 0.0152) and post-caring (p = 0.0299) were statistically significantly lower than virgin female expression. No other pairwise comparisons were statistically significant.Figure 2.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetics, University of Georgia, Athens, GA 30602, USA.

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.

No MeSH data available.