"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

December 17, 2020

Ophiocordyceps sinensis

Ophiocordyceps is a genus of fungi that is probably most well-known for their abilities to usurp and manipulate the behaviour of ants, which gave rise to their more commonly known name - the "zombie ant fungi". But aside from the ant-infecting species, the genus Ophiocordyceps also contains another very well-known insect-zombifying fungus - Ophiocordyceps sinensis, more commonly known as the "caterpillar fungus" - which infects the caterpillars of ghost moths.

Left: O. sinensis fruiting body emerging from a caterpillar, photo by Zhu Liang Yang from here
Right: Ghost moth (top) adult, and (bottom) caterpillar stage, photos from here

While the reputation of the ant-infecting Ophiocordyceps species were built upon their ability to control their host's mind, the roots of O. sinensis' fame is based on the fungus' prized medicinal properties, which has been known and documented for centuries in China where it is known as dōng chóng xià cǎo (冬蟲夏草: which translates into "winter worm, summer grass). It also made an appearance in Moyashimon, a manga (and subsequently, anime) about microbes. Unfortunately, in recent decades, this fungus is currently under threat from a combination of climate change and over-harvesting.

Despite being highly valued and extensively studied for its pharmaceutical potential, the natural ecology of this fungus is not all that well-understood. For example, it is not entirely clear as to how this fungus actually infects its caterpillar host in the first place. Attempts to cultivate the fungus in artificial settings to alleviate harvesting pressure on wild populations have been met with limited success, in terms of producing them on a commercially-viable level.

The host of O. sinensis are ghost moth caterpillars, which live underground munching on the roots of plants. So unlike the ant-infecting zombie fungi that can simply scatter their spores around areas where their ant hosts are likely to walk by, such means of dispersal would be ineffective for reaching caterpillars that spend their entire time underground. Furthermore when scientists examine the soil around fruiting bodies of O. sinensis, the concentration of spores was fairly low, and in any case, they don't seem to disperse very far, with most of the spores found within 20 cm of the fungus fruiting body.

But some of these zombie insect fungi also live a secret double life. When they are not infecting and zombifying or mummifying insects, some of those fungi moonlight as plant symbionts called endophytes. They dwell out of sight within plant tissue, and in some cases providing the plants with various benefits. So perhaps O. sinensis is also leading this double life too? If so, that might be a way through which they are coming into contact with their soil-dwelling caterpillar hosts. 

A group of scientists in China set out to investigate this ecological puzzle at Mount Gongga, in the Sichuan province of China. First of all, they ascertain whether O. sinensis is indeed spending part of its life cycle dwelling as endophytes in the tissue of plants. To do that, they collected plants from areas where the caterpillar fungus was found at the Yanzigous valley, and extracted DNA from the leaves and root tissues of those plants. They then used Quantitative PCR to screen for the presence of O. sinesis. Of the 115 species of plants that were examined, O. sinensis was present in about half of them, across 18 different plant families

Secondly, they also investigated the caterpillars' diet to determine whether they have been eating any of those O.sinesis-positive plants. The scientists collected the caterpillars' gut content, extracted the genetic material they contained, and amplified key sections of DNA that can be used as genetic markers to detect and distinguish different types of plants. From that, they found that those ghost moth caterpillars munched on plants from at least 22 different families, and of the plants that were on the caterpillar's menu, 12 of them had the endophytic stage of O. sinesis in their roots. 

So this might mean that instead of relying upon those spores coming into direct contact with the caterpillars, the way that this fungus completes its life cycle is by using its spores to infect a plant, become established in the plant tissue, then wait for a hungry, hungry caterpillar to come by.

Infecting the host via hiding in their food or prey item (also known as trophic transmission) is a transmission strategy that is usually associated with parasitic worms with complex life-cycles. But here we have a fungus that seem to have convergently evolved this way of reaching its host. While in this case, the hosts (plants and caterpillars) are very different to those that parasitic worms usually infect, functionally it is the same - the hosts become infected through what they eat. Additionally, many of those aforementioned parasitic worms can alter the behaviour and/or appearance of a prey to make it more attractive to a potential host. Can O. sinensis do the same to their host plants to make them more attractive to those soil-dwelling caterpillars?

Given that there are many other fungi which also infect subterraneans insects - this transmission mode might be more common than previously thought, with a wide range of fungi secretly living this double life of being both friends to plants and killers of bugs.