The Colony is a Single Entity
The superorganism model describes how social insects like bees, ants, wasps and termites behave as single, coordinated parts within a whole (the colony). Each part (or worker) partakes in division of labour, communication, and decision-making processing analogous to the cells of our body. Our cells are too specialised to survive on their own. When sufficient groups of cells get together, they make up tissues and then organs. A few extra steps and these organs make the organism.
A worker insect can survive on its own. When joined with other workers, it become part of a social group that cooperates for the survival of themselves, and their groupmates. When enough groups get together, they from one larger group (colony). Each individual works for betterment of the colony, treating it as something greater than itself. This gives rise to superorganism, an entity formed from many organisms.
This is a theory-heavy article that delves into how we describe the social insect structures and how these insects care for themselves. It concludes with implications for the beekeeper (Hint: there are no implications for the beekeeper).
Explaining Superorganisms Using a Human Body Analogy
The colony is analogous to our body. Just as the body is composed of multiple cell types working together, a colony is made up of individual insects that function as parts of a larger whole. The colony works as a single unit, with different individuals performing specific tasks that help it colony survive, thrive and ultimately reproduce- much like how the cells in our body contribute to our survival, function and reproduction.
Our bodies are made up of somatic and reproductive cells – the latter are the sperm and ova, the former is everything else – muscles, bone, kidneys or your burst appendix. Somatic cells are like the workers – they are “sterile”1 and only reproduce via cloning (cell division). Workers perform the essential tasks – repair, protection, maintenance, resource foraging, brood rearing and so on.
The reproductive system is allocated to the queens and the males (e.g. drones, alates or gynes). The queen lays eggs of the next generation to continue the colony’s growth. Many of those eggs will become workers, some into drones and few into queens. The sterile workers present support the queen and the developing larvae, much like how our somatic cells support and protect the reproductive cells in a body.
The nervous system represents communication – in social insects it is through pheromones, sounds and touch, whereas in our bodies it’s through electrical impulses in response to a variety of stimulation. Communication determines when it’s time to fight, take flight, ventilate (sweat) or shiver (cluster). The brain is complex in higher organisms and that’s no different in superorganisms. Individual workers have limited decision-making capabilities on their own, but when interacting with nestmates, complex decisions are made for the benefit of the colony. Likewise, our neurons do not function alone, but when the individuals come together, they make decisions for the body.
Evolution of the Superorganism
In the beginning, all insects were solitary. Over time and environmental pressures, some started nesting close to one another in groups, perhaps for a survival or brood-care advantage. For example, the mostly-solitary carpenter bees Xylocopa sonoria nest in small groups during the winter (Ostwald et al., 2022). Bees that nested together were more likely to survive the cold than those who remained alone, producing an advantageous adaptation. Over time and additional pressures (e.g. need to share resources), this nesting arrangement would become more permanent, forming communal nesting.
Gregarious species are a step above the solitary species, in that groups of females share the nesting space (e.g. a cliff face or a woody tree) and stock food for the hatchlings. They do not participate in brood care or further feeding of the larvae, nor do they establish a hierarchy as to who forages and who nurses. Communal nesting is seen in multiple bee families, from mining bees to leafcutter & sweat bees.
Transitioning from Communities to Colonies
Is it in these nesting communities that the jump from solitary to social was made? We could hypothesize that random changes in communications or nesting biology drove these adaptations. “Intraspecific communication” refers to signals and cues used in locating and recognising potential mates. This can be achieved through pheromones, cuticular hydrocarbons or acoustics.
Another is adaptation is the provision of alloparental care, where one individual helps care for another’s offspring. This improves the survival rate of larvae in their vulnerable stages, and over time, could have produced cooperation among related individuals (Chenoweth et al., 2007).
Species that nest together must exchange information on matters like laying status, food availability and reproductive dominance. Leonhardt and colleagues suggest these signals are passed on by cuticular hydrocarbon profiles and ovarian activity (Leonhardt et al., 2016). The presence and absence of the respective compounds informs both the competitors and “helpers” about the reproductive potential of each female. The most mighty can use this to her advantage and induce helping behaviour in her subordinates.
As nest size increased over time, the dominance signals and division of labour become more apparent, giving rise to higher forms of social nesting like the bee hives, termite mounds and ant colonies we see today.
Social Immunity at the Individual & Colony Level
The review by Pull & McMahon suggest that a “social immune system” is what makes superorganisms viable (Pull & McMahon, 2020). The biological individual is linked to its immune system, and in order for one to be considered an “individual”, they must:
- Suppress the independent evolution of their parts, so that growth and development occur at a controlled rate.
- When this system fails, it results in cancers, the uncontrolled growth of cells.
- In colonies, the suppression is on the reproductive capabilities of workers, preventing them from laying eggs.
- Develop a clear delineation of the “self” that makes them biologically unique, and
- These are the surface markers on our cells that distinguishes between cells of the “self” and “non-self” cells (e.g. cells from pathogens or organ transplants).
- In colonies, the recognition of self is done by the guards, who identify the incoming workers based on their cuticular hydrocarbons.
- Prevent exploitation by infectious diseases.
Once the immune system is established, the individual organism is established, and when multiple cooperative groups fuse to form a colony, the superorganism is established. Consider that in a nest full of closely-related kin, there is little disadvantage to aiding your nestmate in an “I scratch my back you scratch mine” approach (literally, as grooming is one such example). This access to additional resources and workers benefits the individual in times of disease, for they can take a step back from hive duties and recover while the nestmates absorb their workload.
Worker Policing to Prevent Conflicts and Maintain Harmony
One expression of superorganism immunity is in worker policing. Policing is performed by other workers, who will remove worker-laid eggs when a queen is present, or herd small hive beetles into the nooks and crannies of the hive and prevent their egg laying.
Remember, the hive is a rich resource, and any rogue worker (“social cheater”) aims to take advantage of these resources for her own young. When a rogue lays eggs, her nestmates rapidly remove the abnormal eggs, presumably being identifiable due to a lack of queen-marking pheromones. Under normal conditions, Her Majesty herself inhibits worker reproduction by emitting pheromones that signal her presence and fertility.
Pull & McMahon liken reproductive workers to cancers, as their selfish replication is costly to the superorganism- perhaps due to the effort required in removing eggs, and combating the laying workers to restore order; when worker-laid eggs occur, it’s rarely just one worker producing these eggs (Pull & McMahon, 2020).
Undertaking is Analogous to Damaged Cell Death
The removal of dead nestmates is like the body’s removal of damaged cells via apoptosis or autophagy. If these cells are not removed by the white blood cells, they release noxious chemicals and cause inflammation. Likewise, the dead insects left in the colony can harbour pathogens and reduce organism survival.
The presence of oleic acid triggers undertaking behaviour in honey bees. Oleic acid and beta-ocimene (“β-ocimene”) are released from freeze-killed brood, with the former serving as the actual death cue (McAfee et al., 2018). Oleic acid is known to be a death pheromone in many insects. In A. mellifera, it is the combination of oleic acid and β-ocimene that triggers undertaking and hygienic behaviour. This removal of dead and/or diseased individuals after sensing oleic acid is one way to maintain social immunity and colony hygiene (Yao et al., 2009).
Self-removal of Infected Individuals: Self-undertaking?
Rueppel & colleagues found that in order to reduce the spread of disease, infected bees will leave the hive (Rueppel et al., 2010). This voluntary self‐removal of diseased or parasitised individuals decreases the risk of infection for their healthy kin. In their study, artificially weakening or infecting bees caused them to leave hives more often, with a knock-on effect of having younger bees commence foraging earlier.
This adaption can backfire – if high numbers of individuals are infected, whether by pesticides or other disease, then a large number of adults may leave the colony, causing colony collapse. Nonetheless, this shows that in addition to recognizing the need to remove dead nestmates, the infected individual bee can remove herself from the hive to reduce the prevalence of disease.
Nestmate Recognition & Superorganism Uniqueness
Pheromones on the insect exoskeleton are used in nestmate recognition, and this signature distinguishes nestmates from non-nestmates. Nestmates will have the same cuticular hydrocarbon “smell” as the hive, informing the guards that she is a friendly. In honey bees, Signorotti and colleagues describe this as a “label” and “template”– the scent of incoming bee (“label”) is matched against the colony odour (“template”; reviewed in Signorotti et al., 2015). Guards develop their template from the wax comb (which is an extension of the queen and brood pheromones) and compare incoming workers against it.
Newly-emergent bees produce their own cuticular hydrocarbons based on their genetics (Signorotti et al., 2015). As they spend time in the hive, they pick up the “hive scent”; by the time they commence foraging, they can recognise and be recognised by guard bees. Along with policing, the screening of incoming visitors another way the superorganism establishes itself as “unique”. All parts of the colony bear the same markers, much like how our cells have surface markers that classify them as belonging to our own body. This makes for easier removal of harmful entities- pests and pathogens.
Mistakes in Nestmate Recognition Can be Costly
Guards can make mistakes. Usually, this is not an issue. It is when the mistake is due to deliberate evasion by the intruder that problems arise (be it a cancer cell or cuckoo bumble bee or Varroa mite). The cuckoo bumble bees (subgenus Psithyrus; reviewed in Lhomme & Hines, 2019). These parasites invade the nests of other bumble bees to lay eggs, whereby the host colony unknowingly rears the bee’s offspring. The larvae grow and consumes the host’s resource, including the larvae, leading to eventual colony collapse.
Likewise, Varroa jacobsoni, the less destructive cousin of V. destructor, has a cuticular hydrocarbon profile similar to its host Apis mellifera bees (Nation et al., 1992). These mites obtain chemical camouflage either passively from close contact with adults and larvae, or actively via feeding on bee fat body tissue (Ramsey et al., 2019). A total of 91 compounds were shared between V. jacobsoni and A. mellifera, with mites having slight differences in their proportions (Martin et al., 2001). This imperfection could be why bees can detect and remove V. jacobsoni more readily, and why it is (relatively) less harmful than V. destructor.
Disease Control by the Superorganism Level: Hygienic Behaviour
In honey bees, disease and pest control come down to colony strength and hygienic behaviour. Infested or infected brood removal is a hallmark of hygienic behaviour. Another is the uncapping of suspect cells for inspection, followed by recapping if deemed fit for survival.
This behaviour is a general hygienic approach to other diseases- when workers open a cell for inspection, they disturb the internal environment, interrupting the lifecycle of the pathogen (e.g. reproduction of V. destructor or proliferation of Chalkbrood-causing Ascosphaera apis). The infested brood is either removed by way of cannibalisation, or entombed with propolis and sealed off from the rest of the colony.
Superorganism Resilience: Tolerating Loss
In social insects, there is task allocation within castes. The queen monopolises reproduction, drones mate with Her Majesty and the workers tend to everything else. If one or one hundred workers were to disappear from a honey bee colony in spring, the impacts would be minimal – the queen continues laying eggs and the workers buffer the loss to continue working. Just consider that a colony of 10,000 bees may lose half that amount to reproductive swarming, and yet both colonies (usually) survive, re-establishing themselves to repeat the process next season.
In a solitary insect or small-sized colonies (e.g. the founding colony by an overwintered hornet queen), any damage or loss would impact the subsequent fitness of the colony – a solitary bee is the only reproductive unit, and damage or death would “end her bloodline”. Returning to the workers as somatic cells analogy above, the basis of superorganism resilience is the tolerance to worker losses and subsequent buffering to establish a new equilibrium in the colony – maybe some middle-aged bees will revert to nursing duties, or accelerate their development into foragers (Johnson, 2010).
Not all buffers are created equal – losing 100 bees in spring is not the same as 100 bees in winter. In the latter situation the entire colony may collapse due to insufficient workers for temperature control. In general, the bigger the colony, the better it can tolerate the loss. Losing 10% of workers from a paper wasp colony (~40 members) will have a higher impact than losing 10% of workers from a leafcutter ant colony (millions of members).
An example in honey bees is that larger colonies are better able to withstand Deformed Wing Virus infections from Varroa mites than smaller ones (Dainat & Neumann, 2013). Colony size was found to be superior to mite treatments (oxalic and formic acid in this study) for overwintering survival. When viewed from a superorganism perspective, it is evident that larger colony can withstand the losses from mites and DWV, as well as the additional stressors from the chemical treatments.
Queens are the Weak Point of Superorganisms
Disturbances and damages to worker honey bees are of no consequence, since they live for ~40 days. Under natural conditions, their queen can live for several years, and this puts her at risk of repeated stressor exposure, namely pesticides. It is known that honey bee colonies chronically exposed to pesticides performed more supersedures to replace their failing queens (Sandrock et al., 2014).
The ability to replace dead or diseased queens makes chemical exposure a relatively minor disturbance. However, some insect colonies cannot replace their queens after a loss, leading to its collapse. For example, colonies of leafcutter ants Atta die shortly after queen loss, as a result of dwindling foraging and colony maintenance and the same is true of the fungus-growing ants, Acromyrmex (Sousa-Souto & Souza, 2006). In situations where queen replacement is not possible, it becomes advantageous to produce colonies with multiple laying queens, as in the Argentine ants Linepithema humile.
From these findings, the social insect species with both multiple queens and multiple nesting sites (“polydomous” – literally “multiple houses”) are expected to have the best opportunities to buffer against various stressors- should one nest fall, the colony migrates to another location and continue activities. Solitary insects are exposed to every stressor and have no buffer beyond what their bodies can offer – if the stressor is too greater, she dies and can no longer pass her genes to the next generation.
Implications of the Superorganism Structure for Beekeepers, Antkeepers and Wasp Watchers
Knowledge of the superorganism model will not directly make you a better ant or bee keeper. Nor will it change the way you approach pest control. If anything, this should give you an appreciation for the order inside colonies and how they respond to various stressors. If you’re (un)fortunate enough to find laying worker bees due to queenlessness or otherwise, you could view this from the colony’s perspective as their response to the loss of reproductive dominance, and the ensuing struggle by the worker bees for the task of being the “head of the colony”.
Diving down the rabbit hole (ant-mound?) of social insects and theories for their evolution is convoluted and contested – we have a good idea of what gave rise to these behaviours, but not a firm “this is the key moment” for their evolution. Maybe you can say thanks to your queen at your next inspection, for she is maintaining order and harmony over her tens of thousands of sterile daughters.
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Footnotes
- The analogy breaks down in the South African Cape honey bees, Apis mellifera capensis, whose workers can produce fertile offspring without mating, through parthenogenesis. ↩︎