David P. Hughes

Education

1999	BSc (Hons) Zoology, University of Glasgow; 1st Class degree with highest grade in my year
2003	DPhil Entomology, University of Oxford

Fellowships and Prizes

2008-2011	Marie Curie International Outgoing Fellowship (Harvard)
2006-2008	Marie Curie Intra-European Fellowship (Copenhagen)
2004	Varley-Gradwell Travelling Fellowship in Insect Ecology (Oxford)
1999-2003	Hope Studentship in Entomology (Oxford)
1999	Graham Kerr Prize in Zoology (Glasgow)

Research Interests

Parasite manipulation of host behavior

Parasites can control hosts turning them into vehicles for parasite genes. To achieve transmission the behavior of the host can become an extended phenotype of the parasite^[1]. Research into extended phenotypes can provide novel insights into parasite-host interactions because it integrates across a number of biological levels of the antagonism: expression of parasite genes leading to parasite phenotypes (e.g. secreted metabolites) that affect host process (CNS and motor-physiology) leading to altered behavior that affects con- and heterospecific responses (e.g. defense and predation respectively). If the altered behavior is non-transient then effects at the ecological level can occur as well. My work explores the integrative nature of parasite manipulation to address general issues in disease dynamics and virulence evolution. I recently developed as a model system one of the most dramatic examples of adaptive parasite manipulation of host behavior, the ‘death grip’ of ants infected by a fungus.

Ants are the dominant fauna of all terrestrial ecosystems and in tropical forests almost 70% of individual insects are ants (yet ants account for <2% of all insect species)^[2]. As such they represent a prime resource for parasites. Fungi are probably the most important group of ant parasites in tropical forests^[3]. The challenge facing fungi infecting ants is that the hygienic behavior of thousands of workers prevents fungal lifecycle completion inside the colony^[4]. The fungus Ophiocordyceps unilateralis solves this problem in a most impressive manner.

Worker ants become infected when foraging in the forest and 3-9 days pass as the fungus develops inside the ant’s body. Once ready to complete its lifecycle, the fungus manipulates the infected worker ant (Camponotus leonardi) to descend from its colony in the dry, hot canopy to the humid understory where the ant selects and bites into a leaf before dying (Fig 1) (Remaining in the nest or in the canopy results in zero fitness^[5]). Leaves on the N-NW side of the plant in a narrow band 25cm above the ground are chosen. Having bitten a leaf the ant is killed and the fungus grows a stalk from its head from which spores are dispersed to infect other ants.

Current and future directions

Currently my focus is progressing this system along a number of lines:

1. The evolutionary genomics of behavioral manipulation
2. How does the finely detailed manipulation we observed in Southern Thailand vary geographically both in Thailand and in other areas where this host-parasite system occurs?
3. What is the plant response to biting ants?
4. How do natural enemies of O. unilateralis (and there are lots of them) impact disease dynamics?
5. How do ants within the colony react to chimeras in the nest (ants + fungi) given that conflicts exist?

I will shortly develop these ideas further on this site. I will also detail my previous work on Strepsiptera-manipulating wasp and ant behavior and the collaborative work I was fortunate to take part in on hairworm manipulation of crickets (Fred Thomas’ team).

Media Coverage

The first two papers to appear from Ophiocordyceps–ant work in Thailand received quite a bit of media attention. At the bottom of this page are a few of the links that I feel serve as very nice general introductions to the system. Particularly noteworthy are the Discovery Magazine Blog piece by expert parasite proponent, Carl Zimmer, the ScienceNews piece by Susan Milius and the Scientific American coverage.

There was also coverage by Science Shots, the BBC, ScienceDaily, MSNBC, the Ecological Society of America, LiveScience and FoxNews.

You can see coverage in other languages as well: German (n-tv.de and pressetext Austria), Finnish, French (lesoir.be and Abstrait Concret), Danish, Chinese, Norwegian, Vietnamese, Italian, Spanish, Portuguese and Russian.

The zombie metaphor used in a number of the above press pieces has been developed in rather interesting ways – for example, see these three articles: one, two and three.

Publications

Articles and book chapters

* = senior author
** = MSc student

Andersen, SB, ** S. Gerritsma, ** K.M. Yusah, D. Mayntz, N.L. Hywel-Jones, J. Billen, J.J. Boomsma & D.P. Hughes* (2009). The life of a dead ant - the expression of an extended phenotype. American Naturalist 174: 424–433 (PDF)

Pontoppidan, M-B, ** W. Himaman, N.L. Hywel-Jones, J.J. Boomsma & D.P. Hughes* (2009). Graveyards on the move: The spatio-temporal distribution of dead Ophiocordyceps infected ants. PloS One 4(3): e4835 doi:10.1371/journal.pone.0004835 (PDF)

Hughes, D.P. (2009). Altruists since life began: the evolution of the superorganism (book review). Trends in Ecology and Evolution 24(8): 417–418 (PDF)

Hughes, D.P., H.C. Evans, N.L. Hywel-Jones, J.J. Boomsma & S.A.O. Armitage (2009). Emerging fungal diseases in complex leaf-cutting ant societies. Ecological Entomology in 34: 214–220 (PDF)

Lefevre, T., S. Adamo, D.G. Biron, D. Misee, *D.P. Hughes & F. Thomas (2009). Invasion of the Body Snatchers: The Diversity and Evolution of Manipulative Strategies in Host–Parasite Interactions. Advances in Parasitology 68: 45–83 (PDF)

Cremer, S., L.V. Ugelvig, F.P. Drijfhout, B.C. Schlick-Steiner, F.M. Steiner, B. Seifert, D.P. Hughes, A. Schultz, K.S. Petersen, H. Konrad, C. Stauffer, K. Kiran, X. Espadaler, P. d’Ettorre, N. Aktaç, J. Eilenberg, G.R. Jones, D.R. Nash, J.S. Pedersen, J.J. Boomsma (2008). The Evolution of Invasiveness in Garden Ants. PLoS ONE 3(12): e3838 (PDF)

Hughes, D.P., N.E. Pierce & J.J. Boomsma (2008). Social insect symbionts: evolution in homeostatic fortresses. Trends in Ecology and Evolution. 23(12): 672-677 (PDF)

Hughes, D.P. (2008). The extended phenotype within the colony and how it obscures social communication. (book chapter in Sociobiology of Communication eds. P. d’Ettorre and D.P. Hughes) (PDF)

Hughes, D.P., D.J.C. Kronauer & J. J. Boomsma (2008). Extended Phenotype: Nematodes turn ants into bird-dispersed fruits. Current Biology. 18: R294–R295 (PDF)

Sánchez, M.I., F. Ponton, A. Schmidt-Rhaesa, D.P. Hughes, D. Missé & F. Thomas (2008). Two steps to suicide in insects harbouring hairworms. Animal Behaviour, 75(5): 1621–1624 (PDF)

Sánchez, M.I., F. Ponton, D. Missé, D.P. Hughes & F. Thomas (2007). Hairworm response to notonectid attacks. Animal Behaviour 75(3): 823–826 (PDF)

Hughes, D.P. & S. Cremer (2007). Plasticity in anti-parasite behaviours and its suggested role in invasion biology. Animal Behaviour 74(5): 1593–1599 (PDF)

Lefevre, T., M. Sanchez, D.P. Hughes & F. Thomas (2007). Virulence and resistance in malaria: who drives the outcome of the infection? Trends in Parasitology 23(7): 299–302 (PDF)

Ponton, F., C. Lebarbenchon, T. Lefevre, D.G. Biron, D. Duneau, D.P. Hughes & F. Thomas (2006). Hairworm anti-predator strategy: a study of causes and consequences. Parasitology 133(5): 631–638 (PDF)

Hughes, D.P. & J.J. Boomsma (2006). Muscling out malaria. Trends in Ecology and Evolution 21(10): 533–534 (PDF)

Ponton, F., C. Lebarbenchon, T. Lefevre, D.G. Biron, D. Duneau, *D.P. Hughes & F. Thomas (2006). Parasite survives predation on its host. Nature 440: 756–756 (PDF)

Kathirithamby J. & D.P. Hughes (2006). Description and biological notes of the first species of Xenos (Strepsiptera:Stylopidae) parasitic in Polistes carnifex (Hymenoptera: Vespidae) in Mexico. Zootaxa 1104: 35–45 (PDF)

Hughes, D.P. & J. Kathirithamby (2005). Virulence under low extrinsic mortality: the benefit of parasitizing social insects? Oikos 110: 42–434 (PDF)

Hughes, D.P. (2005). Parasitic Manipulators: a social context. Behavioural Processes 68(3): 263–266 (PDF)

Hughes, D.P., J. Kathirithamby & L. Beani (2004). Prevalence of the parasite Strepsiptera in adult Polistes wasps: field collections and literature overview. Ethology, Ecology and Evolution 16: 363–75 (PDF)

Johnston, S.J., L. Ross, L. Beani, D.P. Hughes & J. Kathirithamby (2004). Tiny genomes and endoreduplication in Strepsiptera. Insect Molecular Biology 13(6): 581–585 (PDF)

Hughes, D.P., J. Kathirithamby, S. Turillazzi & L. Beani (2004). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioural Ecology 15(6): 1037–1043 (PDF)

Hughes, D.P., P. Pamilo & J. Kathirithamby (2004). Horizontal transmission of Wolbachia by strepsipteran endoparasites? A reply to Noda et al. 2001. Molecular Ecology 13(2): 507–9 (PDF)

Hughes, D.P., G. Moya-Raygoza & J. Kathirithamby (2003). The first record among Dolichodernae (Formicidae) of parasitism by Strepsiptera. Insectes Sociaux. 50 (2): 148–150 (PDF)

Hughes, D.P., L. Beani, S. Turillazzi & J. Kathirithamby (2003). Prevalence of the parasite Strepsiptera in Polistes as detected by dissection of immatures. Insectes Sociaux 50(1): 62–68 (PDF)

Hughes, D.P. (2002). The value of a broad mind: some natural history meanderings of W.D. Hamilton. Ethology, Ecology and Evolution 14 (2): 83–89 (PDF)

Kathirithamby, J. & D.P. Hughes (2002). Caenocholax fenyesi Pierce (Strepsiptera: Myrmecolacidae) parasitic in Camponotus planatus Roger (Hymenoptera: Formicidae) in Mexico: is this its original host? Annals of the Entomological Society of America 95 (5): 558–563 (PDF)

Books

P. D’Ettorre & D.P. Hughes (2008). Sociobiology of Communication. Edited book for Oxford University Press.

More information about the book can be found on the Oxford University Press website.

 

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Footnotes