Cordyceps: master of the zombie apocalypse?

Ben – Year 12 Student

Editor’s Note: Year 12 student Ben has submitted this fascinating essay to the Peterhouse College, Cambridge, annual Kelvin Science Prize essay competition. Ben’s chosen topic is the Cordyceps fungus, a genus so truly remarkable in its modus operandi that it really does have to be seen to be believed; therefore, I have also shared here a clip from the BBC’s Planet Earth series in which Sir David Attenborough describes what I believe to be one of the most chilling wildlife sequences ever recorded. Don’t read or watch this alone after dark… CPD

Cordyceps: attack of the killer fungi – Planet Earth, BBC Studios

The zombie ant fugus, Cordyceps, manipulates ants by taking control of their brains. Can the ants evolve a response to this or are they locked into a zombie apocalypse forever?

Cordyceps, a grotesque parasitic fungus which infects ants and takes control of their brains to further its own propagation, is a disease which has been persistent drain on ant colonies for over 48 million years [1]. Despite ants being one of the most genetically diverse species on the planet, they seem to lack any resistance to infection from Cordyceps [2]. This lack of resistance to infection in any species of ant is just one of the reasons why it appears that ants will forever be subjected to losing members of their colonies to the grisly fate of succumbing to death in a zombie-like state.

For millions of years, ant species and the Cordyceps fungus have been competing in what is described as an evolutionary arms race. Being living organisms, both species evolve to gain an advantage over the other, with ants evolving more advanced antimicrobial practices and the Cordyceps fungus adapting more effective infection methods to evade the ants’ defences. Despite the arms race, Cordyceps has come out more the victor [3]. It continues to plague ant colonies of every species. Ants are at an inherent disadvantage in the evolutionary arms race against Cordyceps since they reproduce at a lower rate than the fungus, therefore they naturally have a lower rate of mutation than Cordyceps, resulting in ants evolving at a slower pace. This reduced rate of evolution hinders the prospects of ants being able to evolve a counter measure against Cordyceps infections, making it more likely that ants are locked into their fate of suffering with the zombie ant fungus forever. One of the pivotal reasons for the macabre fungus’ success stems from the fact that Cordyceps fungi are incredibly specialised to infecting particular species of ants, which gives them the edge since they can become much better adapted to evolving specialised infection practices which are highly effective against the particular species they infect. Ants, on the other hand, are disadvantaged by the fact that they must evolve to cope with the threat of numerous different infections. When the Cordyceps fungus infects an ant, current understanding suggests that it enacts its manipulation of the ant’s behaviour through secreting bioactive compounds which facilitate its control over the ant; the ant’s brain is left untouched by fungal growth whilst it remains alive. The bioactive compounds which the fungus uses to manipulate its host seem to be largely unique to each species of Cordyceps, with few compounds being common between species [4]. This shows how specialised each species of Cordyceps is to infecting its specific host species of ant and how the chemicals employed by the fungus to enact its behavioural manipulation of the ants vary dramatically. Both factors increase the difficulties ants face when it comes to evolving a resistance to the fungus enormously.

Social immunity, the principle defence ants utilise in protecting their colonies from rampant disease [5], fails them when it comes to Cordyceps fungi. It consists of two primary approaches which combine to protect ant colonies overall from most pathogens: avoidance and resistance [6]. The avoidance strategy of social immunity aims to mitigate infection of individuals; ants achieve this by avoiding areas and food contaminated with pathogens. However, Cordyceps cannot be easily avoided by ant colonies. When the fungus enacts its manipulation of its host, causing the ant to bite down on a leaf vein before it dies, Cordyceps forces the ant to climb up a plant which is situated on a foraging route used by worker ants. The fungus then sprouts from the dead ant’s body and matures before raining down spores onto the foraging route below, resulting in any ants out foraging becoming contaminated with the pathogen and potentially succumbing to infection. Avoidance strategy also involves the inclusion of materials with natural antifungal properties within ant nests to try and reduce any spread of fungal infections in the populous: wood ants, for example, collect resin with antimicrobial properties from trees and incorporate it into their nests to protect the colony from disease [7]. Here too, ants’ avoidance strategy fails to protect them from Cordyceps; since the fungus propagates its spread outside of ant nests, the antimicrobial protection within the nest is inutile as a defence mechanism. The second key component of social immunity is resistance strategy, which aims to deal with infected individuals to minimise the transmission of any disease onto the rest of the colony. As part of resistance strategy, individuals infected with fungi are groomed by non-infected ants to remove fungal growths from the infected ants’ bodies, thus preventing further infection. Grooming practices are not effective against Cordyceps since the fungus grows internally, first as single cells in the infected ant’s bloodstream, then, as the fungus matures, as connected fibres spanning throughout the ant’s muscular tissues [8]. Another aspect of resistance strategy is that ants infected with fatal fungal diseases self-exclude from the colony, leaving and dying away from the nest to avoid infecting other ants, which is usually an effective measure against the spread of fungi. However, the bioactive compounds secreted by Cordyceps whilst it enacts its control over its host prevent infected ants from excluding themselves from the colony and moving far away before dying to prevent further infection. The fungus thereby evades another of the ants’ evolved anti-fungal behaviours. Whilst most of the social immunity practices that usually protect ants from a variety of pathogens prove to be ineffective against Cordyceps, there is one procedure that ants carry out which does assist in preventing its spread. Ants locate the corpses of individuals infected with Cordyceps on plants nearby their colony, remove the bodies from the leaves and dispose of them [9]. This prevents the fungus inside the bodies of dead infected ants from reaching maturity and producing more fungal spores which would rain down from the leaf onto any ants on a foraging path below. Destroying the cadavers of the infected is the only evidence that ants are capable of evolving social immunity defence strategies to protect themselves against Cordyceps.

Cordyceps infections are persistent drains on ant colonies, however, they do not seem to pose a serious threat to colony stability. In a twenty-month period, a study investigating the effect of a Cordyceps fungus on the ant species Camponotus rufipes found that one hundred per cent of the colonies within a surveyed area had members of their colony infected with the fungus and no colonies cleared the infection within the time frame [9]. However, the study noted that none of the colonies collapsed due to the fungus and a mean measurement of the fatalities due to Cordyceps was 14.5 ants per colony per month. Considering that mature Camponotus rufipes colonies consist of around 3,000 ants, the loss of ants from a colony to Cordyceps infections is relatively negligible. Thus, the fungus does not pose a serious threat to the survival of ant colonies and deaths due to Cordyceps are a manageable drain on a colony. Without Cordyceps being a major threat to colony survival, it does not constitute a selection pressure, therefore evolution of defence practices to mitigate infection via natural selection would be slow, reducing the likelihood that ants will be able to win their evolutionary arms race against the fungus. The model of temporal polyethism also contributes significantly to how Cordyceps does not pose a significant enough threat to ant colonies to constitute a selection pressure. Temporal polyethism is the principle that underpins the division of labour within ant colonies; younger workers spend their time within the nest carrying out tasks, whereas the older workers conduct foraging outside the nest [10]. Foraging for food outside of the nest puts workers at significant risk which is why the older workers are the ones who venture out of the nest to forage; these are the workers which are most likely to be weak and vulnerable within the colony and are therefore the most expendable. Consequently, it is the older workers within a colony which encounter Cordyceps spores when they are out foraging, become infected with the fungus, eventually dying and further contributing to the disease’s spread. Since these workers are likely to be nearing the end of their lifespan, it is of little concern to the colony’s vitality if they are killed by Cordyceps as they will simply be replaced by other workers. The fungus cannot kill too many of the foraging workers since if it did it would run out of hosts. In truth, Cordyceps infecting and killing a relatively small proportion of the old, vulnerable workers which forage outside of the nest may be advantageous to colonies overall; it is a practice that ensures that a colony mainly consists of strong individuals, which is beneficial to ant colonies since competition between neighbouring colonies is rife. Therefore, it could likely be detrimental for ants to develop a response to Cordyceps. They may benefit from its chronic infection.

Ants remain plagued by a fungus which controls their bodies, puppeteering them to aid in its continued propagation, just as they have for millions of years. Whilst this is their current reality, it is possible, in principle, that ants could evolve responses to Cordyceps. If they were to develop the ability to produce compounds which counteracted the effects of the bioactive substances secreted by the fungus, ants may be able to free themselves from the manipulation of Cordyceps, allowing their social immunity practices of self-exclusion of the fatally infected to protect colonies from further contact with the disease. Alternatively, ants could evolve immune systems with more effective antifungal capabilities, to mitigate the growth of Cordyceps within its host. However, the stark reality is that in the world of parasite versus host there are two competitors. Ants are losing their evolutionary arms race against Cordyceps; the fungus has evolved more counter measures to the ants’ defence mechanisms than vice versa. Furthermore, with Cordyceps being a slow, yet continuous, drain on ant colonies it simply does not pose a severe enough threat to colony vitality to constitute a selection pressure, severely limiting the probability that ants will evolve a response to it. With Cordyceps only infecting and killing workers that forage outside of the colony, the older and more vulnerable members, the fungus could even be favourable to colony survival. Systemic infection of a colony with Cordyceps ensures that the older workers who forage outside of the colony, where they are likely to encounter fungal spores, are regularly succumbing to the fungus, keeping the colony’s workforce strong overall. On the colony level, the number of ants lost to Cordyceps infection is relatively negligible, making it ever more unlikely that evolution via natural selection will produce effective defence responses against the fungus.

Ostensibly, ants are condemned to becoming the zombie-like hosts of a macabre fungus forever. Moribund infected individuals are utilised to spread Cordyceps to more ants, creating a steady stream of zombies. Each fallen ant fuels the opportunity to create another, giving rise to a constant zombie apocalypse.

Ben

Bibliography

  • de Bekker, C., Ohm, R.A., Evans, H.C., Brachmann, A., Hughes, D.P., 2017. Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. Sci. Rep. 7 [online]. Available at: https://doi.org/10.1038/s41598-017-12863-w (Accessed: Wednesday 8th April 2020)
  • Andersen, S.B., Ferrari, M., Evans, H.C., Elliot, S.L., Boomsma, J.J., Hughes, D.P., 2012. Disease Dynamics in a Specialized Parasite of Ant Societies. PLoS ONE 7 [online]. Available at: https://doi.org/10.1371/journal.pone.0036352 (Accessed: Wednesday 8th April 2020)
  • Liu, L., Zhao, X.-Y., Tang, Q.-B., Lei, C.-L., Huang, Q.-Y., 2019. The Mechanisms of Social Immunity Against Fungal Infections in Eusocial Insects. Toxins 11 [online]. Available at: https://doi.org/10.3390/toxins11050244 (Accessed: Wednesday 8th April 2020)
  • Bos, N., Kankaanpää-Kukkonen, V., Freitak, D., Stucki, D., Sundström, L., 2019. Comparison of Twelve Ant Species and Their Susceptibility to Fungal Infection. Insects 10 [online]. Available at: https://doi.org/10.3390/insects10090271 (Accessed: Wednesday 8th April 2020)
  • Loreto, R.G., Elliot, S.L., Freitas, M.L.R., Pereira, T.M., Hughes, D.P., 2014. Long-Term Disease Dynamics for a Specialized Parasite of Ant Societies: A Field Study. PLoS ONE 9 [online]. Available at: https://doi.org/10.1371/journal.pone.0103516 (Accessed: Thursday 9th April 2020)
  • Santana Vieira, A., Desidério Fernandes, W., Fernando Antonialli-Junior, W., 2010. Temporal polyethism, life expectancy, and entropy of workers of the ant Ectatomma vizottoi Almeida, 1987 (Formicidae: Ectatomminae). Acta Ethologica 13, 23–31 [online]. Available at:  https://doi.org/10.1007/s10211-010-0069-2 (Accessed: Thursday 9th April 2020)

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