Abstract
The exceptional longevity of social insect queens despite their lifelong high fecundity remains poorly understood in ageing biology. To gain insights into the mechanisms that might underlie ageing in social insects, we compared gene expression patterns between young and old castes (both queens and workers) across different lineages of social insects (two termite, two bee and two ant species). After global analyses, we paid particular attention to genes of the insulin/insulin-like growth factor 1 signalling (IIS)/target of rapamycin (TOR)/juvenile hormone (JH) network, which is well known to regulate lifespan and the trade-off between reproduction and somatic maintenance in solitary insects. Our results reveal a major role of the downstream components and target genes of this network (e.g. JH signalling, vitellogenins, major royal jelly proteins and immune genes) in affecting ageing and the caste-specific physiology of social insects, but an apparently lesser role of the upstream IIS/TOR signalling components. Together with a growing appreciation of the importance of such downstream targets, this leads us to propose the TI–J–LiFe (TOR/IIS–JH–Lifespan and Fecundity) network as a conceptual framework for understanding the mechanisms of ageing and fecundity in social insects and beyond.This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’
Highlights
Why do organisms age? This is a major question in evolutionary biology, given that an unlimited lifespan associated with continuous reproduction would increase fitness and should be favoured
The absence of an age signal in T. rugatulus and the weak trend in A. mellifera capensis might be explained by the fact that age could not be very reliably determined in the former and that age differences and sample sizes were small in the latter
Among the genes positively associated with old age, we found several genes related to immunity, reproductive physiology, Juvenile Hormone (JH) biosynthesis and three genes involved in chemical communication
Summary
Why do organisms age? This is a major question in evolutionary biology, given that an unlimited lifespan associated with continuous reproduction would. We collected gene expression data from transcriptomes of young and old individuals of reproducing castes (queens, pseudoqueens, reproducing workers and, for termites, kings) as well as non-reproducing workers from recently published studies of our So-Long consortium for two termites (C. secundus and M. bellicosus), two bees (E. viridissima and A. mellifera capensis) and the ant T. rugatulus (see [30,42,45,46], and [36] and details therein). We first determined how many homologues of these 123 candidate genes from D. melanogaster occurred in each study species by performing BLAST searches using the corresponding D. melanogaster genes as query either against the official gene sets from available genomes that had been used to map the raw sequence reads (i.e. termites and bees) or against the de novo assemblies (for the ants) (see electronic supplementary material, §S1.7 and table S21, and archive S6 in Dryad [48]). We inferred a maximum-likelihood gene tree that included all identified Vgs or Vg-like sequences from our six study species as well as data from the termite Z. nevadensis, the cockroach Blattella germanica and a subset of species used in Kohlmeier et al [63] (see electronic supplementary material, tables S23 and S24; details are described in the electronic supplementary material, §S1.9 and in archive S8 in Dryad [48])
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