Evidence for a conserved queen‐worker genetic toolkit across slave‐making ants and their ant hosts

Abstract

The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste exhibits highly specialized morphology, behaviour, and life‐history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave‐making ants. Here, we investigate whether gene expression varies in parallel ways between lifestyles (slave‐making versus host ants) across five independent origins of ant slavery in the “Formicoxenus‐group” of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave‐making ants than in nonparasitic ants, we also compare caste‐specific gene expression patterns between lifestyles. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste‐associated modules of coexpressed genes with strong connectivity. However, several genes and one gene module are linked to slave‐making across the independent origins of this parasitic lifestyle, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences in gene expression remain consistent even when species switch to a parasitic lifestyle. Our findings strongly support the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, as proposed by the “genetic toolkit” hypothesis.

Co-expression Gene Networks and Machine-learning Algorithms Unveil a Core Genetic Toolkit for Reproductive Division of Labour in Rudimentary Insect Societies

“…Lastly, we see genes related to reproduction (e.g., yolk protein vitellogenin) and gene functions related to metabolism (e.g., carbohydrate and lipid metabolism), which have been consistently implicated as key players in a conserved genetic toolkit for sociality ( Toth and Robinson 2007 ; Amsalem et al 2014 ; Berens et al 2015 ; Morandin et al 2019 ). These results—71 core genes—are within the same range as other studies on conserved expressed genes between: ant slave-making species and host species ( n = 62 genes shared across 162 Ma of divergence [ Feldmeyer et al 2022 ]); animal behavior after social challenge ( n = 6 genes shared across 680 Ma of divergence [ Saul et al 2019 ]). Overall, the emerging picture from our and these studies is that there are conserved gene modules recruited during eusocial evolution for the regulation of convergent social traits (e.g., castes), but few genes are individually predictive of a given trait.…”

The diverse roles of insulin signaling in insect behavior

“…Other social species also show caste differences in brain IIS, but patterns vary. Reproductives have higher brain IIS compared to workers in a wasp ( Polistes candensis 99 ), termite ( Cavitermes tuberosus 100 ), earwig ( Forficula Auricularia 101 ), and many ant species ( 20 , 89 , 102 – 106 ). IIS could be linked to different, specific functional outcomes in these diverse social species, for example, species-specific trade-offs among egg production, queen behavior, and lifespan ( 87 ).…”