Termites and other social insects as emerging model organisms of ageing research: how to achieve a long lifespan and a high fecundity

Social insects (termites, ants and some bees and wasps) are emerging model organisms of ageing research. In this Commentary, I outline which advantages they offer compared with other organisms. These include the co-occurrence of extraordinarily long-lived, highly fecund queens together with short-lived workers within colonies that share the same genetic background. I then summarize which new insights have been gained so far from social insect studies. Research on social insects has led to the development of a universal mechanistic framework underlying the regulation of ageing and other life-history trade-offs in insects: the TI-J-LiFe network (short for TOR/IIS-juvenile hormone-lifespan/fecundity). Because of its conservative nature, this network can be extended to also incorporate vertebrates. Current data for social insect models suggest that molecular re-wirings along the I-J-Fe (IIS-juvenile hormone-fecundity) axis of the network can explain the concurrent long lifespans and high fecundity of queens. During social evolution, pathways that foster a high fecundity have apparently been uncoupled from mechanisms that shorten lifespan in solitary insects. Thus, fecundity-related vitellogenesis is uncoupled from life-shortening high juvenile hormone (JH)-titres in the honeybee and from insulin/insulin-like growth factor signalling (IIS) activity in ants. In termites, similarly, vitellogenesis seems tissue-specifically unlinked from JH signalling and IIS activity might have lost life-shortening consequences. However, as in solitary animals, the downstream processes (Li of the TI-J-LiFe network) that cause actual ageing (e.g. oxidative stress, transposable element activity, telomere attrition) seem to differ between species and environments. These results show how apparently hard-wired mechanisms underlying life-history trade-offs can be overcome during evolution.