
THEY fight, punish, reward and coerce their friends. They are promiscuous, selfish, altruistic, deceptive and manipulative. They are farmers, predators and scavengers. They dispense law and order. Eusocial insects – bees, wasps, ants and termites – are the soap opera stars of the non-human animal kingdom.
Much of that behaviour centres around an extreme division of labour, with individuals becoming queens, workers and sometimes soldiers. Once it starts, this process is usually irreversible – much as embryonic stem cells have no alternative but to become part of a kidney or cartilage once the biological “switch” is thrown.
Recent research into honeybees and other social insects is painting a fascinating picture of the mechanisms that underlie those processes in both insects and cells. This will help us build a better model of how cells and insects lose and gain plasticity. Needless to say, one of the big goals is a better understanding of those cells humans prize most – stem cells.
Advertisement
First things, first, though. Let’s look closely at the insect colonies. Every day, millions of colony-mates settle conflicts or fall victim to coercion in order to coordinate the countless interactions required for a colony to function at all. Alongside that collective behaviour, each individual also strives to cash in as best as they can on their own personal investment. Queens do the reproducing, workers help raise the brood, to whom they are usually related, and, in some species, soldiers defend the colony.
So the evolution of “castes” is the secret to eusocial insects’ success. In highly social species such as honeybees and most ants, queen and worker castes can differ so profoundly in physiology, morphology and behaviour that they can easily be mistaken for a different species. Queens can be orders of magnitude larger than workers, and may lack the enormous mandibles some workers have for foraging or defence. In many species, such differences arise during brood development, usually in response to environmental cues. For example, only honeybee larvae fed royal jelly develop into queens, the rest become workers.
The process behind eusocial insect castes is one of the most amazing examples of how a single genome can give rise to individuals that differ dramatically in behaviour, morphology, and/or physiology. Recent research has shown that castes usually arise through different levels of expression of the genes they share, and common sets of genes seem to be associated with queen and worker behaviours across different species.
This society-level functioning is not unique to social insects: it pervades all levels of biological organisation – from cells to organisms to societies, including human ones. For example, your body is your own personal society made up of cells committed to performing specialised functions essential for the “society” called “you”. Uncommitted, or totipotent, cells are programmed to perform specific tasks through cell differentiation, which amounts to a coordinated division of labour. Such a division must be perfectly coordinated to ensure the successful working of the society that is your body.
We now wonder if the evolution of cellular society and eusocial insect society can be explained by the same theoretical framework: group living, whether as a multicellular organism or insect colony, evolves if the benefits and degree of relatedness of group members outweigh the costs of living as a group. Could this framework mean that the same processes control the division of labour in both cells and insect colonies?
The notion of commonalities between cells and societies is not as surprising as it may seem at first. For decades, ethologists and cellular biologists have used the same terminology. Social insect biologists describe a larva as “totipotent” while it can still become queen, worker or, in some species, soldier. Similarly, for cellular biologists a totipotent cell is one yet to embark on any of several different pathways to specialisation.
More broadly, early ethologists talked about an animal’s behaviour being “programmed” or “reset” in response to the creature’s changing internal or external environment. The defining feature of insect castes and differentiated cells, then, is that they are programmed to “commit” to their fate in response to some environmental trigger and subsequently may lose the ability to be reprogrammed. The same key phases of development – reprogramming and commitment – describe development at the cellular and at the colony level.
But the commonalities run deeper. Like social insect castes, cell differentiation is an example of plasticity in the phenotype. The same genome allows for different cell functions through differential expression of shared genes. We know quite a lot about cell differentiation: a key process is the chemical (epigenetic) “tagging” of a creature’s DNA that does not affect its sequence, but helps control both reprogramming and cell commitment. The question is whether the processes before, during and after the “switch” at both the cellular and colony levels of biological organisation are controlled by similar epigenetic mechanisms.
Epigenetic modifications are ancient mechanisms found in fungi, plants and animals, controlling fundamental biological functions such as cell differentiation. Recently, a DNA methylation system (the addition or removal of methyl “tags” on specific genes) was identified in the honeybee. These epigenetic changes appear to control the cell differentiation that turns larvae into queens or workers. This is the latest piece of research in social insects tying the machinery of methylation to caste differentiation.
So the potential building blocks are there, and early evidence suggests epigenetic processes are involved in caste regulation. But how far can we push the analogy of cell and caste differentiation? The best data comes from mammalian cell development. There, totipotent zygotes turn out to have a specific epigenetic profile that allows them to produce any kind of cell, much like the totipotent insect larva. Big changes occur after fertilisation when the zygote sheds methyl groups from its DNA as epigenetic programs from the previous generation are erased in preparation for creating a new individual.
“How far can we push the analogy of cell and caste differentiation?”
This epigenetic “clean slate” is short-lived, however. The early embryo’s cells soon lose their totipotent ability and begin to differentiate into many different types of cells with specialised functions. As cells commit to their new function, they also acquire specific patterns of DNA methylation throughout their genome. These unique epigenetic signatures help define the identity and physiological function of specific cell lineages and organs in the developing embryo.
A similar point of divergence must occur in social insects, when the totipotent insect receives a specific nutritional or social cue that sets it on its developmental pathway. And, like humans cells, that pathway is likely to involve a reorganisation of methylation on specific genes. Once these epigenetic profiles are set, caste and cell lineage (and therefore phenotype) is fixed and there is rarely an opportunity for future change.
But one of the great things about studying eusocial insects is that we can see clearly how different species represent different stages in eusocial evolution, with different degrees of caste differentiation and commitment. Take the polistine paper wasps. This subfamily includes species that range from the small colonies of the primitively eusocial Polistes paper wasps, which represent an early stage of social evolution where individuals seem able to reprogram throughout adulthood, to the large, socially complex colonies of highly eusocial and swarm-forming paper wasps, which have roles fixed during development.
Two new and powerful ideas make these exciting times for sociobiologists. The first is that the dynamic epigenetic landscape controlling caste differentiation may well be the same as that which controls cell differentiation. The second is that the same ancient molecular regulatory processes have been co-opted to produce the fascinating array of social complexities in both insects and cells.
Using the comparatively simple insects as models, where there are few “lineages” compared with cells, we may have the technical means to test the idea of a unified framework across levels of biological organisation. Looks like our soap opera may be heading for an uncharacteristically happy ending.
Profile
This essay is based on a recent in Current Opinion in Cell Biology by Solenn Patalano, Timothy A. Hore, Wolf Reik, and Seirian Sumner (). Sumner is at the Institute of Zoology, London, and Patalano is based at the Babraham Institute, Cambridge, UK