Vitellogenin and vitellogenin-like gene expression patterns in relation to caste and task in the ant Formica fusca

A. Hietala,C. Morandin,H. Helanterä

doi:10.1007/s00040-019-00725-9

A. Hietala, C. Morandin + Show 1 more

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https://doi.org/10.1007/s00040-019-00725-9

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Abstract

Social insect colonies are characterized by division of labour, and extensive morphological, physiological and behavioural differences between queens and workers. The storage protein vitellogenin (Vg) affects multiple aspects of social insect life histories, and has been suggested as a key player for caste differentiation and maintenance. Recently, three genes homologous to Vg have been described in the ant Formica exsecta. Their role is currently unclear but their structural variation suggests variable functions. We examined the expression patterns of the conventional Vg and the three Vg-like genes using qRT-PCR in the common black ant Formica fusca between queens and workers, between nurse and foragers workers, and across social contexts (queenless vs. queenright nests), and sampling time. As expected, we found a significant queen caste and nurse task-related increase for the conventional Vg, while Vg-like-C displayed a consistent forager-biased expression pattern. Task (forager vs. nurse) was the only factor that explained expression variation among workers in any of the studied genes. The removal of the queen did not affect expression, although the proportion of fertile nurses increased in queenless nests. The observed expression biases suggest that in Formica fusca, the ancestral duplication has led to alternative social functions for Vg-like genes across castes and tasks. To get a broader picture of the role of gene duplications in social evolution and the roles of Vg-like genes in caste differentiation and maintenance, how these genes achieve these roles at a molecular level need to be investigated further.

Highlights

The societies of ants, social bees and wasps with morphologically separated castes are remarkable examples of evolution of reproductive altruism (Hamilton 1964, 1972; Boomsma and Gawne 2018), where the reproductive queens and the non-reproductive workers arise from the same1 3 Vol.:(0123456789)Despite long standing research investigating the molecular pathways and genes involved in division of labour, the precise mechanisms remain relatively unknown (but see e.g., Chandra et al (2018) for recent developments)
Two different analyses were done separately for each Vg copy: (1) we compared the expression levels in foragers, nurses and queens in the queenright nests, while taking into account the effect of caste and time of sampling, using a generalized linear mixed model (GLMM). ∆Cq values were set as a response variable, while day and caste were set as fixed explanatory variables, and colony as
Considering the generally low but worker-biased expression compared to the conventional Vg, it is unlikely that Vg-like genes B and C would work as storage proteins in egg yolk formation

Summary

Introduction

The societies of ants, social bees and wasps with morphologically separated castes are remarkable examples of evolution of reproductive altruism (Hamilton 1964, 1972; Boomsma and Gawne 2018), where the reproductive queens and the non-reproductive workers arise from the same1 3 Vol.:(0123456789)Despite long standing research investigating the molecular pathways and genes involved in division of labour, the precise mechanisms remain relatively unknown (but see e.g., Chandra et al (2018) for recent developments). Because of its primary role in egg formation, in social insects the conventional Vg is commonly upregulated in queens compared to workers (Piulachs et al 2003; Weil et al 2009; Wurm et al 2011; Corona et al 2013), and is one of the most studied genes involved in division of labour (Amdam and Omholt 2003; Corona et al 2007, 2013; Morandin et al 2014; Salmela et al 2016). Examples include ageing and queen longevity (Excels 1974; Corona et al 2007), temporal worker division of labour (Guidugli et al 2005b; Nelson et al 2007; Münch and Amdam 2010; Bloch and Grozinger 2011), and royal jelly production (Amdam et al 2003). In addition to its multiple social roles, Vg has been shown to be involved in antioxidation to enhance stress resistance (Seehuus et al 2006; Münch and Amdam 2010; Havukainen et al 2013), defence against inflammation, and transgenerational immune priming (Salmela et al 2015)

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