Gene expression and variation in social aggression by queens of the harvester ant Pogonomyrmex californicus

Abstract

A key requirement for social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behaviour and head gene expression profiles. A proportion of queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to perform aggressive acts, and conflict escalated more frequently in pairs of haplometrotic queens. Whole-head RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate differentiation in overall transcriptional profile, suggesting that genetic differences underlie the two founding strategies. The largest detected difference, however, was associated with aggression, regardless of queen founding type. Several modules of coregulated genes, involved in metabolism, immune system and neuronal function, were found to be upregulated in highly aggressive queens. Conversely, nonaggressive queens exhibited a striking pattern of upregulation in chemosensory genes. Our results highlight that the social phenotypes of cooperative vs. solitary nest founding tap into a set of gene regulatory networks that seem to govern aggression level. We also present a number of highly connected hub genes associated with aggression, providing opportunity to further study the genetic underpinnings of social conflict and tolerance.

Adaptations to thermal stress in social insects: recent advances and future directions

“…the number of genes that are differentially expressed) differences in responses to environmental pressures in a variety of organisms, including plants, insects, molluscs, crustaceans, and fish (Ye et al ., 2014; Zhao et al ., 2014; Cañas et al ., 2015; Faddeeva et al ., 2015; Cheng, Hui, & Sha, 2019; Jesus et al ., 2019). In recent years, DGE studies in social insects have highlighted a number of genes that are involved in colony organisation and adaptation to environmental constraints (Ferreira et al ., 2013; Helmkampf et al ., 2016; Lucas, Romiguier, & Keller, 2017; Willot et al ., 2018; Holman et al ., 2019). However, such studies remain fairly rare, and many taxa are currently ignored.…”

Transcriptomic changes during caste development through social interactions in the termite Zootermopsis nevadensis

“…Several transcriptome analyses have been performed during caste differentiation in hymenopteran species, all of which suggested that social cues were crucial modulators of gene expression changes (Toth & Rehan, ). For example, huge transcriptomic differences were observed among different social contexts in the ants Pogonomyrmex californicus and Cardiocondyla obscurior (Helmkampf, Mikheyev, Kang, Fewell, & Gadau, ; Schrader, Simola, Heinze, & Oettler, ). Moreover, the expression levels of nutrition‐sensitive genes involved in caste determination changed in different conditions with/without reproductive castes in the ant Diacamma sp.…”

Candidate genes for cooperation and aggression in the social wasp Polistes dominula

“…We focused on two previously published studies on the transcriptomic basis for nest founding behaviour in paper wasps and fire ants. These were the only studies available at the time when we designed the experiment that explored global changes of gene expression associated with dominance behaviour in foundresses of social insects (but see Helmkampf et al 2016 for another more recent study on the transcriptomics of ant foundresses). The first study (study “A”, Toth et al 2014 ) investigated the global patterns of gene expression associated with dominance hierarchies in Polistes metricus , a paper wasp closely related to P. dominula .…”