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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 receptor is expressed in heads and isolated brain tissue of adult female and adult male N. vespilloides. (a) vgr expression in females shows a significant change in expression levels across the five behavioural states examined, with levels decreasing when mated on a carcass and while caring. (b) With one outlier removed, a similar pattern of changing expression levels of vgr is seen in males across different social conditions. 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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RSPB20150787F3: vitellogenin receptor is expressed in heads and isolated brain tissue of adult female and adult male N. vespilloides. (a) vgr expression in females shows a significant change in expression levels across the five behavioural states examined, with levels decreasing when mated on a carcass and while caring. (b) With one outlier removed, a similar pattern of changing expression levels of vgr is seen in males across different social conditions. 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 also examined the expression pattern of the receptor responsible for Vg uptake into cells. Examining vgr expression in head tissue of females and males across the five social conditions, we found that vgr was expressed at moderate levels in both females and males. Again, we see the same biological trend of decreasing vgr expression during caring within females (figure 3a; F = 2.765, d.f. = 4,45, p = 0.0390). Expression in females who were mated with a mouse was significantly lower than expression in virgin females (p = 0.0485), females mated without a mouse (p = 0.0063) and post-caring females (p = 0.0265). Expression in females mated without a mouse was also significantly higher than in caring females (p = 0.041). A similar pattern was seen for males, albeit again not as strongly and not reaching statistical significance (F = 2.319, d.f. = 4,44, p = 0.071). However, this appears to be driven by one extreme value in the ‘caring male’ state. If we exclude this value, then we do see a significant reduction in vgr expression during caring in males (figure 3b; F = 3.682, d.f. = 4,43, p = 0.0115). In caring males, expression was statistically significantly lower than in virgin (p = 0.0055), mated without a mouse (p = 0.0041) or post-caring males (p = 0.0017).Figure 3.


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 receptor is expressed in heads and isolated brain tissue of adult female and adult male N. vespilloides. (a) vgr expression in females shows a significant change in expression levels across the five behavioural states examined, with levels decreasing when mated on a carcass and while caring. (b) With one outlier removed, a similar pattern of changing expression levels of vgr is seen in males across different social conditions. 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

RSPB20150787F3: vitellogenin receptor is expressed in heads and isolated brain tissue of adult female and adult male N. vespilloides. (a) vgr expression in females shows a significant change in expression levels across the five behavioural states examined, with levels decreasing when mated on a carcass and while caring. (b) With one outlier removed, a similar pattern of changing expression levels of vgr is seen in males across different social conditions. 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 also examined the expression pattern of the receptor responsible for Vg uptake into cells. Examining vgr expression in head tissue of females and males across the five social conditions, we found that vgr was expressed at moderate levels in both females and males. Again, we see the same biological trend of decreasing vgr expression during caring within females (figure 3a; F = 2.765, d.f. = 4,45, p = 0.0390). Expression in females who were mated with a mouse was significantly lower than expression in virgin females (p = 0.0485), females mated without a mouse (p = 0.0063) and post-caring females (p = 0.0265). Expression in females mated without a mouse was also significantly higher than in caring females (p = 0.041). A similar pattern was seen for males, albeit again not as strongly and not reaching statistical significance (F = 2.319, d.f. = 4,44, p = 0.071). However, this appears to be driven by one extreme value in the ‘caring male’ state. If we exclude this value, then we do see a significant reduction in vgr expression during caring in males (figure 3b; F = 3.682, d.f. = 4,43, p = 0.0115). In caring males, expression was statistically significantly lower than in virgin (p = 0.0055), mated without a mouse (p = 0.0041) or post-caring males (p = 0.0017).Figure 3.

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.