Considering the Longevity of Eusocial Insect Queens
Eusocial species are characterized by reproductive and non-reproductive castes, such as the familiar division of queens and workers in common insect species. Eusociality is more common in insects and less so in other classes of life, although there are a few eusocial mammals, such as the naked mole-rat. For researchers who investigate the comparative biology of aging, one of the more interesting aspects of eusociality is that queens live longer than workers, many times longer in some species, while being genetically identical. Why is this?
Comparing very similar species with divergent life spans is a desirable starting point if trying to reverse engineer the relationship between metabolism and longevity. In principle divergence within the same species should be an even better option, further narrowing the search for relevant mechanisms.
These days the comparative biology of aging is becoming ever less an abstract field of pure scientific inquiry. Practical applications for human medicine likely lie ahead. Determining how any specific aspect of cellular biochemistry contributes to species longevity, or other desirable traits such as the ability to regenerate organs, might deliver the basis for human therapies. Or it might not; it is hard to say in advance whether any specific set of mechanisms could be ported over into our species, or even has any great relevance to our biochemistry.
How Can Ant and Termite Queens Live So Long?
A view of the animal world suggests that because reproduction and maintenance are both costly, animals simply can't maximize both. So the more energy and nutrients an individual invests in producing offspring, the faster it will probably age, and the shorter its life will be. Yet in social insects such as termites, ants, bees, and wasps, the queens appear to have found a way to have their cake and eat it. In many colonies, queens that lay hundreds of eggs every day can stay alive for years or even decades, while workers that never lay a single egg in their life will die after a few months.
Differences in the genetic code can't explain the unusual longevity of queens compared to workers. All workers are daughters of the queen and, in many cases, any of those daughters could have grown up to become queens themselves had they received the appropriate royal treatment when they were larvae. Since the queen is the only one in a colony laying eggs, colonies with long-lived queens are likely to grow larger and send forth more young queens to start new nests, as well as males to fertilize them. In other words, many scientists reason, there must have been strong selective pressure to keep the queen alive for as long as possible by evolving delayed aging.
To try to learn more about what enables the long life of queens in social insects, a team of researchers decided to compare the activity levels of various genes in termites, ants and bees - two species of each. In all, they studied 157 individuals, including insects of different ages as well as different castes. Unsurprisingly, the team found that genes that are known to play crucial roles in reproduction showed different activity patterns in queens than they did in sterile workers. Some of these genes, which carry instructions for making proteins called vitellogenins, were active in queens of all species.
The main role of vitellogenins is to support the production of yolk for the eggs. But some scientists suspect that vitellogenins may be doing more than that: In honeybees, at least, research has found that vitellogenins also function as antioxidants. If vitellogenins do the same thing in other social insects, they might contribute to the resistance of queens to oxidation. The team also found differences in the activity of genes involved in the prevention of oxidative damage or the repair of such damage, between queens and egg-laying workers compared with sterile workers. But the precise genes involved differed strongly from one species to another. Apparently, each species has evolved its own way of keeping its queens alive longer.
This somewhat bewildering variety across species reveals an important lesson about the nature of aging: There isn't one button or switch that allows a species to invest more, or less, in maintenance or reproduction, but a whole dashboard of them that is set up slightly differently in each species.
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.