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Writer's pictureNeil Sardesai

Cordyceps: The zombie ant fungus

Updated: Nov 8, 2020

Hello everyone and welcome to this week's blog post. In this article, I will answer the question 'Can ants evolve a response to the zombie ant fungus?'.


“One general law, leading to the advancement of all organic beings, namely, multiply, vary, let the strongest live and the weakest die” (Darwin, 1859) underlines the struggle for life that define all species today. With this statement comes the assumption that any one species will tend to evolve to increase its chances of survival in the environment in which it is found. This explanation has enormous implications in the battle fought between the zombie ant fungus, Ophiocordyceps unilateralis, and the ant species that it infects.


On examination of this conflict for survival between Ophiocordyceps unilateralis and ants, one can see it is unlikely that ants will be able to evolve a response to this threat. Despite the fact that mutations can occur and will be selected for due to natural selection, the reproduction cycle of ants reduces the effectiveness of the adaptations. Likewise, the fact that the fungus can also adapt only exacerbates this problem. Moreover, the ant’s use of pheromones and its interaction with its microbiome also influence the extent to which it can evolve a response.


Ophiocordyceps unilateralis, an entomopathogenic fungus which infects ants in tropical forests, manipulates the ants to kill themselves so that the next stage of the life cycle of the fungus can begin [1]. A spore of the fungus, having been stepped on by an ant, sticks to the ant and a single fungal cell infiltrates its exoskeleton before multiplying inside it, eventually forming almost 50% of the ant’s body mass. Researchers from Pennsylvania State University have proven that this growth is not random in nature, but incredibly precise, as the fungus forms tubular scaffolds that both penetrate and surround the ant’s muscle bundles [2]. This allows the fungus to take control of the ant’s muscles, forcing them to contract without stimulation from the brain. Simultaneously, the fungus secretes chemicals that travel to the ant’s brain and compel the insect to climb up a plant, bite into a leaf, lock its jaw and wait for death. Eventually, the fungus grows a sprout through the head of the ant, from which spores are released which coat the ground below, ready to infect the next ant which passes.

A picture of an ant killed by Ophiocordyceps unilateralis

It makes sense to suggest that ants would adapt a response to this fungal attack, as the fungus provides no benefit to the ant, in stark contrast to other fungal infections such as the symbiosis between ruminating animals, such as cattle, and Neocallimastigomycota fungi, in which both species benefit [3]. This means that there will be no selection in favour of infection.


A population always has genetic variability between individual organisms. This is due to two reasons. Firstly, when DNA replication occurs during meiosis, random mutations can occur, where the sequence of genes in the copied DNA is slightly different, thus causing the offspring to have unique genes and thus unique characteristics. Secondly, genes that make an organism better suited to an environment can be passed on to its offspring. Since these better-suited organisms are more likely to survive to reproduce, the better genes are more likely to prevail after many generations.


Considering that infection by Ophiocordyceps unilateralis results in the death of the ant, any genetic mutation that increases its resistance to the fungus helps it survive. For example, as ants have an immune system which can mount a response to the fungus [4], any mutation which augments the effectiveness of the immune system against the fungus increases the chance of the ant surviving and having offspring. Meanwhile, any mutation which reduces resistance to the disease increases the likelihood that the ant is infected and killed. As such, over many generations, the ant population is likely to evolve resistance to the fungus.


The main issue, however, is that the fungus is also likely to mutate to respond to the changing resistance of the ant population. For instance, when the fungus began spreading towards the poles, it could not force infected ants to bite onto leaves, as trees would shed their leaves in autumn. Instead, the fungus was able to adapt quickly, causing infected ants to hug twigs instead [5].


Additionally, while carpenter ants generally reproduce once every year, Ophiocordyceps unilateralis sexually reproduces much more frequently [6]. This means that mutations can occur much more rapidly in the fungus, suggesting that the fungus can adapt more quickly than the ant and thus mitigating any beneficial mutations which may exist in the ant population.


In addition, the way ants reproduce has a detrimental impact on the likelihood of beneficial mutations occurring. Queen ants only mate once during their 10-year lifespan. They then lay eggs twice a year, the first time using fertilised eggs producing sterile female workers, and the second producing winged females from fertilised eggs and males from unfertilised eggs [7] [8]. This reduces genetic variation as the males only receive a single set of chromosomes, solely from the queen, so this prevents them receiving any inherited genes that confer resistance from the male that originally mated with the queen. Additionally, the winged females are only exposed to the fungus for a short amount of time. After mating, they immediately lay eggs in a safe space and stay there for the rest of their lives to form their colonies. Unless the winged females and males interact with the fungus before the queen forms its colony, which is very unlikely, only the sterile female workers are routinely exposed to the fungus.

A picture of a winged carpenter ant

Evolution can still occur because, if enough fungus is present in the environment to completely wipe out a significant proportion of the female worker ants, the colony will not receive enough food and will starve, preventing the queen’s genes from being passed on to future generations. Nonetheless, because only a small minority of the population is capable of breeding, evolution will occur at a much slower rate.


The ants’ use of pheromones also has an impact on how they can evolve to protect themselves from fungal infection. When ants move outside the colony, they rely heavily on the use of trail pheromones [9]. When the first ant leaves the colony, as it travels, it secretes pheromones to mark the path it takes. Each subsequent ant can detect these pheromones and follow them, laying down its own pheromone path as they do so, which helps strengthen the original path.


This behaviour has both advantages and disadvantages for the ant population. Due to repeated contact with the fungus in the past, ants have evolved to recognise whether other ants they encounter have been infected by the fungus. If they have, the ant carries the infected ant far away from its colony to reduce the threat of the spores infecting more members [10]. Since the ants follow the trail of pheromones, they are more likely to come into contact with each other away from the main colony, where the infected ant could be safely disposed of without contaminating a large section of the population, thus protecting the other ants.


On the other hand, the fungus has evolved to maximise the number of ants it infects by manipulating ants to climb up plants before they die, causing spores to be spread over a large area of the pheromone trail. That means even if an ant lays down a safe trail, it may later become unsafe and lead to the death of ants who follow the trail, resulting in the starvation of the colony.


Overall, the presence of pheromones has a negative impact on the ability of the ant population to adapt to the fungal presence. Ants always return to their colony, either to bring back food or to rest. Thus, if an ant is infected, the likelihood is high that it will bring the infection back to the colony, potentially decimating it in its entirety. Pheromone trails increase the chance that an ant can be disposed of before it returns to the colony, as ants could evolve to be able to detect fungal infections in other ants even earlier. Nonetheless, this is outweighed by the showering of fungal spores over the trail, which significantly increases the number of ants that are infected. Furthermore, ants are unable to evolve to stop secreting pheromones as they are an essential part of foraging and finding food.


It has been established in this essay that genetic mutations are unlikely to be passed on to future generations of ants, so it is improbable that ants can evolve a genetic response to the fungal infection. Nevertheless, the ants’ microbiome may be able to protect the insect from infection.


According to Joshua Lederberg, a microbiome is ‘a characteristic microbial community occupying a reasonably well-defined habitat’. Most species, including ants, have both an internal and external microbiome [11]. These microbes form an intrinsic part of the organism, assisting it with various functions ranging from digesting nutrients to bolstering its native immune system.


While the specific makeup of a single organism’s microbiome is partially affected by its species, the environment the organism is exposed to has a much more significant impact on the microbiome’s composition. This is because the microbes can be passed from insect to insect by contact, meaning that ants which live in the same colony are likely to have similar microbiomes.


The implication of this is far-reaching. Many ants have antifungal bacteria on their exoskeleton to prevent fungal infections, like Ophiocordyceps unilateralis, from taking hold. For example, Attine ants can acquire PseudonocardiaI bacteria on their cuticle. This group of bacteria has antifungal properties and can excrete chemicals that prevent the microfungal parasite called Escovopsis from infecting the insect [12].


It is reasonable to assume that a single ant will eventually come into contact with a bacterium that is able to repel Ophiocordyceps unilaterali. Moreover, once the bacterium becomes part of the ant’s microbiome, the ant will pass this bacterium on to all the other ants in the colony. Not only does this mean that the entire colony of ants will have resistance to the fungus and be able to collect food, allowing the resistant colony to thrive, but the mating ants produced by the colony also have a chance of picking up this bacterium and passing it on to the new colonies they form.


Further, if ants could hypothetically evolve a response to this fungus and thus increase their prevalence in tropical rainforests, their increased abundance may actually be to the species’ detriment, due to the effect that would have on the food web. Tropical rainforests are incredibly diverse regions, with highly interconnected food webs [13]. This means that most species are dependent on others. As such, if the fungus is no longer able to restrict the population size of the ants and their population size increases, the food the ants require will also increase accordingly. By depleting these food supplies, the ants could potentially decimate the rest of the intricate food web, possibly rendering the rainforest unsuitable for ants to thrive, thus negatively impacting the ant population.


In conclusion, it is unlikely that ants will be able to evolve a response to the fungus Ophiocordyceps unilateralis. While the microbiome may provide some defence against fungal infection, the chance that an ant comes into contact with an antifungal bacterium is slim. Even if this occurs, the ant still has to return to the nest and spread its bacterium, something which is not a given. Moreover, the process by which ants reproduce further reduces the extent to which the ants can evolve, as it slows down the speed at which the ants can evolve, potentially allowing the fungus to adapt faster. Further, not only could an adaptation prove fatal for the species as a whole due to its effect on the ecosystem, but any adaptations to do with pheromones, for example by getting rid of them (so ants are less likely to encounter the fungus) would not be possible due to their necessity for the survival of ants.

Sources:

[1]H. Evans, S. Elliot and D. Hughes, "Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?," Communicative and Integrative Biology, vol. 4, no. 5, pp. 598-602, 2011.[2]National Geographic, "How a parasitic fungus turns ants into 'zombies'," 18 April 2019. [Online]. Available: https://www.nationalgeographic.com/animals/2019/04/cordyceps-zombie-fungus-takes-over-ants/. [Accessed 11 March 20].[3]A. Kameshwar and W. Qin, "Genome Wide Analysis Reveals the Extrinsic Cellulolytic and Biohydrogen Generating Abilities of Neocallimastigomycota Fungi," Journal of Genomics, vol. 6, pp. 74-87, 2018.[4]H. Schluns and R. Crozier, "Molecular and chemical immune defenses in ants (Hymenoptera: Formicidae)," Myrmecological News, vol. 12, pp. 237-249, 2009.[5]C. Zimmer, "After This Fungus Turns Ants Into Zombies, Their Bodies Explode," The New York Times, 24 October 2019. [Online]. Available: https://www.nytimes.com/2019/10/24/science/ant-zombies-fungus.html. [Accessed 1 April 2020].[6]K. Hirata, "The Zombie Ant: Parasitic Fungi and Behavior Manipulation," 2014. [Online]. Available: https://www.reed.edu/biology/courses/BIO342/2014_syllabus_old/2014_WEBSITES/khsite/ontogeny.html. [Accessed 12 March 2020].[7]E. Hauschteck-Jungen and H. Jungen, "ANT CHROMOSOMES II, KARYOTYPES OF WESTERN PALEARCTIC SPECIES," Insectes Sociaux, Paris, vol. 30, no. 2, pp. 149-164, 1982.[8]Science Encyclopedia, "Ants Mating, Reproduction, And Life Span," [Online]. Available: https://science.jrank.org/pages/447/Ants-Mating-reproduction-life-span.html. [Accessed 20 March 2020].[9]A. Renyard, S. Alamsetti, R. Gries, A. Munoz and G. Gries, "Identification of the Trail Pheromone of the Carpenter Ant Camponotus modoc.," Journal of Chemical Ecology, vol. 45, no. 11-12, pp. 901-913, 2019.[10]D. Attenborough, Director, Cordyceps: attack of the killer fungi - Planet Earth Attenborough BBC wildlife. [Film]. UK: BBC Earth, 2008.[11]M. Ramalho, O. Bueno and C. Moreau, "Species-specific signatures of the microbiome from Camponotus and Colobopsis ants across developmental stages," PLOS ONE, vol. 12, no. 11, 2017.[12]K.-O. Chua, S.-L. Song, H.-S. Yong, W.-S. See-Too, W.-F. Yin and K.-G. Chan, "Microbial Community Composition Reveals Spatial Variation and Distinctive Core Microbiome of the Weaver Ant Oecophylla smaragdina in Malaysia," Scientific Reports, vol. 8, no. 10777, 2018.[13]R. Pennington, M. Hughes and P. Moonlight, "The Origins of Tropical Rainforest Hyperdiversity," Trends in Plant Science, vol. 20, no. 11, pp. 693-695, 2015.

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