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.
Highlights
Division of labour characterizes all major evolutionary transitions, such as the evolution of eukaryotic cells or multicellular organisms
It is established (i) that Vgs play an important role in division of labour (DOL) between termite reproductives and w orkers[11,29,30], (ii) that juvenile hormone (JH) titres and Vg expression are positively associated in termite q ueens[31,32], and (iii) that queens have considerable higher JH titres than w orkers[33,34,35]
Termites have three Vg copies that are upregulated in queens[36,37] and at least in Cryptotermes secundus these three Vg copies are members of a gene coexpression network that characterizes the queen phenotype[30]. These results lead us to hypothesize that Vgs and JH underlie reproductive DOL and regulate task division among termite workers, similar as in social Hymenoptera
Summary
Division of labour characterizes all major evolutionary transitions, such as the evolution of eukaryotic cells or multicellular organisms. As in the social Hymenoptera, age polyethism is common with older workers performing riskier tasks such as foraging or d efence[27,28] It is established (i) that Vgs play an important role in DOL between termite reproductives and w orkers[11,29,30], (ii) that JH titres and Vg expression are positively associated in termite q ueens[31,32], and (iii) that queens have considerable higher JH titres than w orkers[33,34,35]. Termites have three Vg copies that are upregulated in queens[36,37] and at least in Cryptotermes secundus these three Vg copies are members of a gene coexpression network that characterizes the queen phenotype (see “Discussion”)[30] These results lead us to hypothesize that Vgs and JH underlie reproductive DOL and regulate task division among termite workers, similar as in social Hymenoptera
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