(Epi)Genetic Mechanisms Underlying the Evolutionary Success of Eusocial Insects

Abstract

Eusocial insects, such as bees, ants, and wasps of the Hymenoptera and termites of the Blattodea, are able to generate remarkable diversity in morphology and behavior despite being genetically uniform within a colony. Most eusocial insect species display caste structures in which reproductive ability is possessed by a single or a few queens while all other colony members act as workers. However, in some species, caste structure is somewhat plastic, and individuals may switch from one caste or behavioral phenotype to another in response to certain environmental cues. As different castes normally share a common genetic background, it is believed that much of this observed within-colony diversity results from transcriptional differences between individuals. This suggests that epigenetic mechanisms, featured by modified gene expression without changing genes themselves, may play an important role in eusocial insects. Indeed, epigenetic mechanisms such as DNA methylation, histone modifications and non-coding RNAs, have been shown to influence eusocial insects in multiple aspects, along with typical genetic regulation. This review summarizes the most recent findings regarding such mechanisms and their diverse roles in eusocial insects.

Keywords: behavioral plasticity; epigenetics; eusocial insects; evolution.

Figure 1

Epigenetic modifications occur at different points in the A. mellifera life cycle. Embryos hatch into larvae, which may develop into workers or queens. Workers overall possess a higher level of methylation than queens, opposing the case in bumblebees and ants. Honeybee workers also possess decreased expression of JH synthesis genes. As workers age, they switch from a nursing behavioral phenotype (signified by the hive icon) to a foraging behavioral phenotype (signified by the basket icon). This switch is associated with decreased Vg and increased JH production, as well as expression differences in the foraging gene and associated lncRNAs.

Figure 2

A summary of the upregulated genes and structural changes occurring in three different tissue types (the brain, fat body, and ovary) in reproductive and non-reproductive castes. Additionally, genes found to be upregulated in transcriptome analyses of whole insect bodies are also included. Non-reproductive females possess larger brains and inactivated ovaries, while reproductive females generally experience a reduced brain size, but much larger activated ovaries. Representative genes from all major eusocial insect lineages are listed here, including genes from ants [31,32,33,34,37,73,74], bees [75,76,77,78,79,80], social wasps [81,82], and termites [72].

Figure 3

Harpegnathos saltator workers undergo changes in gene expression and tissue structure to become reproductive gamergates. In the absence of queen pheromones, workers will commence dueling, a behavior in which antennal strikes are rapidly exchanged between workers. Victors will become destined reproductive. Changes in gene expression in the brain will trigger gene expression changes in fat bodies and ovaries, eventually resulting in reproductive status. The gamergate state is not permanent and can be reversed following isolation and subsequent introduction to the pheromone of another reproductive. Changes in gene expression and tissue structure undergo reversion, and the gamergate behaves like a regular worker once again. The brain figure is adapted from Smith et al., 2016 [109], and the ovary images are adapted from Gospocic et al., 2017 [32].