Research

Overview pictures of one of our field sites in Central Florida

Parasitic manipulation of animal behavior

The battle between parasites and their hosts is ever-ongoing. As such, certain parasite-host interactions have already been taking place for millions of years. This close co-evolution between parasite and host can result in complex phenotypes. The adaptive parasitic manipulation of host behavior is a widespread example of this. Here, parasites have evolved intricate strategies to manipulate the output of their host’s brain such that this benefits their own life cycle and, eventually, transmission. For many of these parasite-host interactions, their captivating natural history has been rather well-described. Our current knowledge about the molecular mechanisms in play, however, only scratches the surface. Our research aims to bring us to the level of a deeper mechanistic understanding. In general, we ask the question how parasites are able to manipulate the animal brain. This coincides with learning how certain behaviors are regulated and how pathological behaviors develop.

 

Model System: Behavior manipulating fungi (BMF) and their ant hosts

One of the most pronounced examples of parasites changing host behavior is that of Ophiocordyceps fungi infecting and manipulating Carpenter ants. Fungal spores infect ants while they forage for food. During the course of infection, the fungus gradually changes the behavior of its ant host, and ultimately makes her leave the nest. The ant climbs up  the vegetation where she latches on with her mandibles. This manipulated biting is not part of the regular behavior as observed in healthy ants. It is a novel behavior induced by the fungus. This so-called “death grip” keeps the ant in position as death sets in. The parasite then uses the ant’s tissues as a carbon source to grow a fruiting body from between the ant’s thorax and head, which releases infective ascospores for transmission [1,2].

   

Camponotus castaneus infected with Ophiocordyceps kimflemingiae (left) and Camponotus floridanus infected with Ophiocordyceps camponoti-floridani (right)

 

We mainly work with fungal insect parasites (entomopathogens) of the genus Ophiocordyceps to learn how certain microbes are able to control animal behavior. More specifically, we focus on Ophiocordyceps unilateralis s.l. species isolated from Carpenter ants collected in South Carolina and Florida.

These parasite-host interactions represent excellent model system for studies into parasitic manipulation of host behavior since:

A) the manipulation is very apparent
B) the manipulation is clearly adaptive to the parasite
C) the parasite is cultivable and the host is easy to keep in the lab
D) this allows for reproducible, controlled infection studies

Carpenter ants (left) and Ophiocordyceps unilateralis s.l. isolates (middle) are used to perform controlled infection studies (right)

 

Recent and ongoing research

Infection studies combined with behavioral observations and metabolomics analyses of the fungal secretome suggest that fungal manipulation of the ant brain is rather species-specific [3].

We have sequenced the Ophiocordyceps genome [4], which is publicly available through NCBI and the Fungal Genomics Group at Utrecht University.

We have also produced a transcriptomics dataset, which compares gene expression before infection with gene expression during and after manipulated biting. This study, together with the above mentioned metabolomic analyses, have led to the reporting of the very first candidate genes, compounds and pathways that could be involved in the fungal manipulation of ant behavior [3,4].

Moreover, they suggest that biological clocks might play an important role in the altered behaviors that we observe [5].

 

Having established these recent advances we now use an interdisciplinary approach to ask a variety of research questions, including:

  1. How has the parasitic ability to control the insect brain evolved?
  2. Which fungal genes are essential to establish behavioral manipulation and what is their function?
  3. How could circadian rhythms be involved in the parasite-host interactions that lead to altered behavioral outputs?

 

References

  1. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J et al. (2009) The life of a dead ant: The expression of an adaptive extended phenotype. American Naturalist 174: 424-33
  2. Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC ecology 11:13
  3. de Bekker C, Quevillon LE, Smith PB, Fleming KR, Ghosh D, Patterson AD et al. (2014) Species-specific ant brain manipulation by a specialized fungal parasite. BMC evolutionary biology 14:166
  4. de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, Merrow M et al. (2015) Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC genomics 16:620
  5. de Bekker C, Merrow M, Hughes DP. (2014) From behavior to mechanisms: An integrative approach to the manipulation by a parasitic fungus (Ophiocordyceps unilateralis s.l.) of its host ants (Camponotus spp.). Integrative and Comparative Biology 54(2), 166-176