By Alison Campbell 22/10/2019


Back in 2010, I wrote about the strange tale of the zombie ants, which do the bidding of their fungal overlords. (They’re not an isolated example; a range of parasites change their hosts’ behaviour. See here and here for example – though as you’ll find, the toxoplasmosis story may be even more complex than first thought.)

There’s been quite a lot more work done on this relationship since that tale was published. For example, it seems that the fungus may be achieving its ends by manipulating gene expression in its hosts.

And it also appears that past changes in climate may have driven evolutionary changes in how the fungus makes its hosts act: specifically, whether they do their death-bite on a twig, or the midrib of a leaf. NB this manipulation of host behaviour, in a way that’s ‘visible’ to natural selection, could be seen as part of the extended phenotype of the parasitic fungus (Loreto, Araujo, Kepler et al., 2018).

Loreto & his colleagues had previously found that the behaviour of carpenter ants parasitised by fungi in the genus Ophiocordyceps differed depending on the environment. In the tropics, the great majority of ants bit onto leaves, while in temperate forests they bit onto (& wrapped their legs around) twigs. One obvious difference between tropical and temperate forests is that the former are evergreen, while in temperate regions trees shed their leaves in autumn. In that light, the researchers hypothesised that a fungus whose zombie ants bite onto twigs prior to death will have an extended window for raining spores down onto other ants on the ground – this could have a positive effect on the evolutionary fitness of that particular fungal strain.

In order to test their hypothesis, the team took a three-pronged approach. They:

  • looked at global distribution of the Ophiocordyceps unilateralis species complex, to see if there were indeed geographic differences in ants’ biting choices;
  • studied the development of one species from that complex in a temperate forest, to determine if twig-biting did give an adaptive advantage over leaf-biting in that environment;
  • and tested the idea that manipulating ants to chose a different substrate was convergent across fungi in different temperate regions. They did this by “inferred the phylogenetic relationships and conducted ancestral state reconstruction (ASR) between different species of fungi within the O. unilateralis complex that manipulate the host to bite leaves and those that manipulate their hosts to bite twigs, in both Old and New World temperate and tropical forests”.

They found that the Ophiocordyceps species complex has quite a broad latitudinal range, from 47o North (deciduous forests in Canada) to 27o South (tropical forests in Brazil). Leaf-biting predominated in the tropics, while in things were more variable in the temperate forests of the US, Canada, & Japan. However, the US and Japanese observations of leaf-biting came from evergreen forests. This allowed the team to conclude that the type of biting substrate (twigs vs leaves) is correlated to latitude.

When they looked at fungal development in ants parasitised in a deciduous temperate forest, Loreto et al. discovered that the fungal stalk & sporangium (the bit sticking out from the ant’s head in the photo at the top of this page) didn’t happen until the year after the ants died. They also found that the majoring of ants had not only bitten onto a twig, but had also wrapped their legs around the twig prior to death, a behaviour that would maximise the odds of the ant remaining suspended into the following year.

Finally, the team’s phylogenetic analysis found that the Ophiocordyceps complex is a monophyletic group, with two major subclades (or branches). One subclade was of species from Asia & Oceania, while the other comprised American species (with the exception of one species from Japan). As a result of their analysis, the researchers concluded that leaf-biting is the ancestral trait in Ophiocordycep‘s extended phenotype, and that the shift to making ants bite onto stems happened 4 times in the fungal group’s evolutionary history:

based on past climate and forest type distribution, fossil evidence of leaf biting and our ancestral state character reconstruction, there are grounds to suggest that the species in the O. unilateralis clade originally manipulated ants to bite leaves and subsequently experienced independent convergent evolution to twig biting by different fungal parasites in response to global climate change and the emergence of the deciduous forests in different areas of the globe. The emergence of the additional twig grasping presumably came later as it may increase the likelihood that the host cadaver, which the fungus requires for reproduction, stays in position over extended periods of time.

What were the likely global climate change events that might have driven this convergent evolution? It’s quite possible that the changes during the Eocene, which saw the development of drier, cooler deciduous forests around 49 million years ago, had something to do with it.

And how does it all happen? That’s a question for future research.

Although it remains to be discovered how a microbe inside the body of its host can affect such precise choices in its manipulated host, our data suggest that the infected manipulated ants have a behavior, the extended phenotype, which is encoded by the fungus and results in the optimal selection of the plant tissue (leaf versus twig) to bite before being killed by the parasite.

 

The post zombie ants, updated appeared first on BioBlog. Featured image: Ophiocordyceps unilateralis and Camponotus leonardi, Wikimedia Commons.