DNA methylation and expression of the egfr gene are associated with worker size in monomorphic ants (original) (raw)

The reproductive division of labour is a hallmark of eusocial Hymenoptera. Females are either reproductive queens or non-reproductive workers. In ants, workers often display further task specialisation that is associated with variation in size and/or morphology. Because female polyphenism is typically under environmental control, it is thought epigenetic mechanisms (such as DNA methylation) play a central role since they mediate gene-by-environment interactions. Methylation of the growth-promoting gene epidermal growth factor receptor (egfr) was indeed shown to control worker size in a highly polymorphic ant. However, it remains unknown if egfr methylation could also regulate worker size in monomorphic species. By combining experimental pharmacology and molecular biology, we show that worker size is associated with egfr methylation in two monomorphic ants. Furthermore, we functionally demonstrate that EGFR signalling affects worker size. These results indicate that worker size regulation by egfr methylation has been mechanistically conserved in ants but remains unexploited in monomorphic species. Phenotypic plasticity occurs when a single genotype encodes multiple, diverse phenotypes 1. Common in all living organisms, it is often highly adaptive. By altering their phenotypes in response to external cues, organisms can react to environmental changes, boosting survival and reproduction. Some of the most remarkable forms of phenotypic plasticity are found in social Hymenoptera (bees, wasps, and ants) where the same genotype can lead to morphologically, physiologically, and behaviourally distinct female castes: large, fertile queens that specialise in reproduction, and smaller, usually sterile workers that ensure colony maintenance 2. Whether a female larva develops into a reproductive queen or a non-reproductive worker typically results from environmental (e.g., food quantity or quality) or social (e.g., queen and brood presence/absence) cues, which cause the baseline genome to express itself along different developmental lines 3-5. Unlike bees and wasps, numerous ant species exhibit a high degree of worker polymorphism, i.e. a colony's workers can vary in size and/or morphology 6,7. Worker size variation exists along a spectrum, ranging from monomorphism, where there are slight isometric differences, to dimorphism, where there are multiple, distinct worker subcastes that display marked, non-proportional differences in body features. Worker polymorphism has appeared repeatedly in Formicidae, suggesting that size-dependent division of labour in workers promotes colony fitness 8-10. Decades of research have been devoted to understanding the evolution and maintenance of worker polymorphism in ants. Yet, its genetic and developmental origins are only beginning to be deciphered. At the molecular level, body size is regulated by evolutionarily conserved growth-regulating pathways, such as the insulin/ insulin-like growth factor signalling (IIS) 11 , target of rapamycin (TOR) 12 , and epidermal growth factor receptor (EGFR) signalling 13. The pathways are triggered by dietary cues, causing cell-signalling cascades that promote cell growth, proliferation, and differentiation 14. In insects, the result is the production of the growth-regulating hormones ecdysone 15 and juvenile hormone (JH) 11,13,16. However, it remains unknown how these pathways have become fine-tuned to generate worker size variation from the same genotype. Recently, it has been hypothesised that epigenetic mechanisms, such as DNA methylation, are at play because they mediate gene-by-environment interactions, translating environmental signals into long-lasting changes in gene expression without modifying the DNA itself 17-19. Numerous studies have investigated whether DNA methylation influences queen-worker