Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers

Abstract

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialization from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole‐body gene expression. A total of 3,644 genes were associated with behavioural specialization which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characterized by an upregulation of three Vitellogenin (Vg) genes, one of which, Vg‐like A, was the most differentially expressed gene that was recently shown experimentally to control the switch from brood to worker care. The expression of Conventional Vg was unlinked to behavioural specialization, age or fertility, which contrasts to studies on bees and some ants. Diversity in Vg/Vg‐like copy number and expression bias across ants supports subfunctionalization of Vg genes and indicates that some regulatory mechanisms of division of labour diverged in different ant lineages. Simulations revealed that our experimental dissociation of co‐varying factors reduced transcriptomic noise, suggesting that confounding factors could potentially explain inconsistencies across transcriptomic studies of behavioural specialization in ants. Thus, our study reveals that worker gene expression is mainly linked to the worker's function for the colony and provides novel insights into the evolution of sociality in ants.

A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee

“…Indeed, it is not only oviposition and aggression that reside under the strict definition of a behavioral change but also the expression levels of vg. While vg, a gene typically encoding the yolk protein invested in female ovaries, is regulated by JH in most insects, it was suggested to decouple from JH in the transition to advanced eusociality and to regulate aggressive behavior in B. terrestris (Amsalem et al, 2014b), B. impatiens (Padilla et al, 2016) and Themnothorax ants (Kohlmeier et al, 2019(Kohlmeier et al, , 2018. In the latter, vg was duplicated and its ortholog was associated with behavioral maturation.…”

Expressions of conventional vitellogenin and vitellogenin‐like A in worker brains are associated with a nursing task in a ponerine ant

“…The molecular mechanisms regulating such worker division of labour has been investigated for recent decades (Smith et al, 2008). Although the worker ages strongly affect expressions of various genes in an ant (Lucas et al, 2017), such "task reversion" enabled us to show that First published online 12 November 2020. the gene expressions were more strongly associated with behaviours rather than ages in a honeybee and an ant (Kohlmeier et al, 2019;Whitfield et al, 2003).…”

“…However, workers maintain behavioural flexibility and can respond to disruption of colony demography by switching between tasks independent of age (Beshers and Fewell, 2001). For example, if the nursing workers at younger ages are removed from a colony, some older foragers can switch their task into nursing to meet colony demands for nursing (Kohlmeier et al, 2018;Robinson, 1992;Shimoji et al, 2020). The molecular mechanisms regulating such worker division of labour has been investigated for recent decades (Smith et al, 2008).…”

“…Early in the insect evolution, ancestral Vg had duplicated into conventional Vg (CVg), Vg-like A and Vg-like B, and then Vg-like C is also originated from the Hymenopteraspecific duplication (Kohlmeier et al, 2018;Morandin et al, 2014). Moreover, the CVg underwent multiple duplication events in several insect lineages, including ants (Kohlmeier et al, 2018;Morandin et al, 2014;Okada et al, 2017).…”

Transcriptomic basis and evolution of the ant nurse-larval social interactome

“…Transcriptomic studies are often used to identify sets of genes underlying the expression of particular traits by performing RNA-sequencing on individuals that vary in the expression of such traits. For example, in social insects, recent studies have compared the transcriptomes of workers that perform nursing versus foraging tasks [37–39], or nurses feeding larvae of different stages or castes [35,40]. However, given the phenotypic co-regulation known to occur between interacting social partners (here, nurses and larvae), it is likely that genes expressed in one social partner affect the expression of genes in the other social partner, and vice-versa, such that interacting social partners are connected by “social” gene regulatory networks [14,32,41,42].…”