Molecular underpinnings of division of labour among workers in a socially complex termite

Abstract

Division of labour characterizes all major evolutionary transitions, such as the evolution of eukaryotic cells or multicellular organisms. Social insects are characterized by reproductive division of labour, with one or a few reproducing individuals (queens) and many non-reproducing nestmates (workers) forming a colony. Among the workers, further division of labour can occur with different individuals performing different tasks such as foraging, brood care or building. While mechanisms underlying task division are intensively studied in social Hymenoptera, less is known for termites, which independently evolved eusociality. We investigated molecular mechanisms underlying task division in termite workers to test for communality with social Hymenoptera. We compared similar-aged foraging workers with builders of the fungus-growing termite Macrotermes bellicosus using transcriptomes, endocrine measures and estimators of physiological condition. Based on results for social Hymenoptera and theory, we tested the hypotheses that (i) foragers are in worse physiological conditions than builders, (ii) builders are more similar in their gene expression profile to queens than foragers are, and (iii) builders invest more in anti-ageing mechanism than foragers. Our results support all three hypotheses. We found storage proteins to underlie task division of these similar-aged termite workers and these genes also characterize reproductive division of labour between queens and workers. This implies a co-option of nutrient-based pathways to regulate division of labour across lineages of termites and social Hymenoptera, which are separated by more than 133 million years.

Resource sharing is sufficient for the emergence of division of labour

“…Several studies have proposed that division of labour in social insects is associated with nutritional differences between foragers and nurses 16 – 22 , 38 – 40 . In our model, division of labour leads to a situation where nutrition levels of nurses are higher than those of foragers, and division of labour is enhanced when the metabolic rate while foraging is higher than the metabolic rate while nursing.…”

Evolution and functionalization of vitellogenin genes in the termite Reticulitermes speratus

“…Further analysis is required to determine whether the RsVg1−3 genes have different subfunctions for vitellogenesis in termites. Recently, Elsner et al (2021) discovered that three queen‐biased Vgs were highly expressed in builders compared to foragers (all females) of the fungus‐growing termite Macrotermes bellicosus . To clarify the caste, sex, and age specificity of termite Vg1−3 gene expressions should also be clarified in the future.…”

Resource sharing leads to the emergence of division of labour

“…Our model is based on two general and plausible assumptions. Several studies have proposed that division of labour in social insects are associated with nutritional differences between foragers and nurses [16][17][18][19][20][21][22][34][35][36] . In our model, (a) division of labour leads to a situation where nutrient levels of nurses are higher than those of foragers, and (b) that division of labour is enhanced when the metabolic rate while foraging is higher than the metabolic rate while nursing.…”