Economists since Adam Smith have puzzled over a central paradox in capitalism: that selfish behaviour by individuals can lead to an economy capable of provisioning society as a whole. Smith's analysis, in The Wealth of Nations, identified division of labour as the key. By breaking large jobs down into multiple small ones, workers become specialized and thereby vastly more productive. In biology, the most spectacular instances of division of labour occur in social Hymenoptera – wasps, bees and ants. How and why have different divisions of labour evolved?
In a fascinating paper, Giray et al. test two hypotheses about the role of juvenile hormone (JH) in the evolution of division of labour during transitions from primitive to advanced eusociality. Primitively eusocial insects exhibit behavioural but not morphological distinction between queens and workers. In addition, colony workers sometimes perform age-specific tasks(age polyethism), with older workers taking on riskier jobs. By contrast,highly eusocial insects show behavioural and morphological differences between castes, and workers exhibit strong age polyethism. In all insects, JH plays a central role in the development of both morphology and behaviour, so it's a good bet that changes in JH action underlie evolutionary changes in sociality.
One idea, the `single function hypothesis', is that JH evolved from having a purely reproductive role in primitively eusocial species to a purely behavioural role in highly eusocial species – a change possible only with the advent of non-reproductive workers, thereby freeing JH to take on new roles. An alternative, the `split function hypothesis', states that JH played both reproductive and behavioural roles in ancestral solitary species. Upon the evolution of specialized reproductives (queens) and brood caregivers(workers), the roles of JH divided – with JH controlling reproductive maturation of queens and behavioural maturation (age polyethism) of workers. In this hypothesis, JH maintains a dual role throughout the evolution of different permutations in social structure.
Giray and colleagues test the two hypotheses on a primitively eusocial wasp, Polistes canadensis. They first established the reality of worker age polyethism by monitoring the behaviour of paint-marked individuals. Young workers, less than 4 days old, spent much of their time tending larvae and avoiding conflict with non-nestmates. From day 3, however, workers showed a distinct shift to riskier behaviours – foraging and guarding. To find out if JH controls this age polyethism, Giray et al. applied methoprene, a commonly used analogue of JH, to freshly emerged workers. Compared with controls, workers receiving the analogue showed precocious onset of guarding behaviour and were generally more aggressive. But what about JH and reproductive maturation of queens? Giray et al. found that queens have much higher JH levels than workers and that, among queens, ovarian development and JH levels are strongly correlated. Though correlative, the data, together with the known reproductive effects of JH in other Hymenoptera, strongly suggest causation.
Giray et al. interpret their findings in support of the split-function hypothesis – JH clearly functions in both reproduction and behaviour in a primitively eusocial wasp. This outcome, they suggest, represents the evolutionary redistribution among a queen and her workers of functions originally contained in single individuals of ancestral solitary species. Clearly, future studies are needed to explain how something as multifaceted and pervasive as JH can show such evolutionary flexibility. Such studies might illuminate insect diversity as a whole.
