David P. Hughes

Fellowships and Prizes

• 2008-2011 Marie Curie International Outgoing Fellowship (Harvard & Exeter)
• 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.

Fig 1. The death grip. (a) shows a live ant and (b) & (c) show post-mortem ants with the fungus in the asexual and sexual states respectively. The spore body is the large ‘ball’ in (c).

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.

Most recently I have begun to look at this interaction across the globe. I have begun field work in Brazil (Atlantic Rainforests), USA (South Carolinian deciduous woods) and China (Yunnan Province). In the coming months I will aim to conduct further field collections in Ecuador, Japan, Australia and Honduras. This field work is in very close contact with Dr Harry Evans of CABI, UK who is the foremost authority on the ecology of Cordyceps (in the broad sense) in tropical forests. In addition I am building links with local scientists in Colombia, Guyana, Brazil, Peru, Malaysia, Papua New Guinea and Australia to promote coordinated surveys of ant-parasites across the globe.

Current and future directions

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

• The genomics and transcriptomics of behavioral manipulation.
• 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?
• What is the plant response to biting ants?
• How do natural enemies of O. unilateralis (and there are lots of them) impact disease dynamics?
• How do ants within the colony react to chimeras in the nest (ants + fungi) given that conflicts exist?
• How does a fungal disease spread in a tropical forest and how can individual and colony (superorganism) level behavior respond?

I will shortly develop these ideas further on lab website. I will also detail my previous work on Strepsiptera-manipulating wasp and ant behavior and the collaborative work on hairworm manipulation of crickets (with the excellent Fred Thomas and his team at Montpellier, France).

Applied research at Penn State

Ants pose a significant threat to agriculture because of their mutualism with phloem feeding insects such as hemipterans. Much of the disease incidence and spread of diseases on plants is due to the hundreds of thousands of ants that protect plant-feeding insects that vector disease. Ants farm these sucking insects and ‘milk’ them for the by-product sugar they excrete.  This is a strong mutualism and ant protection increases the populations of plant feeding insects, and in turn, this greatly increases the rate of disease spread between plants as the bugs transmit viral and bacterial infections and the hundreds of thousands of ant legs and mandibles introduce fungi and psuedo-fungi (oomycetes) into leaf tissue.  Reflecting the successful integration found at Penn State I am interested in bringing diverse approaches to study agricultural diseases. We are working now on ants on small holder Cassava and Cocoa farms in Ghana. You see further details on my approach to plant pathology in my recent lecture.

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.

Working with Conrad Labandeira (Smithsonian) and Torsten Wappler  (Steinmann Institute) we uncovered a 48 mya old fossil leaf showing the antiquity of fungal manipulation of ant behavior. This also captured media attention in specialist journals (e.g.Nature, Science), general science periodicals (e.g.New Scientist) and print media (e.g.New York Times, Telegraph, Guardian) and becoming an exhibition at the America Museum of Natural History. It also received attention in blogs (e.g.Loom) and on-line media outlets (e.g.MSNBC).

Publications

* = senior author
** = MSc student

Andersen SB, Ferrari M, Evans HC, Elliot SL, Boomsma JJ, and D.P. Hughes (2012) Disease Dynamics in a Specialized Parasite of Ant Societies. PLoS ONE 7(5): e36352. doi:10.1371/journal.pone.0036352 (PDF)

Andersen SB and D.P. Hughes (2012) Host specificity of parasite manipulation –zombie ant death location in Thailand vs. Brazil Communicative & Integrative Biology 5:2, 1–3; March/April (PDF)

Harry C. Evans, Simon L. Elliot and David P. Hughes (2011) Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests? Communicative & Integrative Biology 4:5, 598-602 (Link)

Hoover, K., M. Grove, M. Gardner, D.P. Hughes, J. McNeil and J. Slavicek. 2011. A gene for an extended phenotype. Science 333: 1401. This paper has been designated a Faculty of 1000 Must Read Factor 8 (PDF)

Hughes, D.P., Andersen, S.* Hywel-Jones, N.L. , Himaman, W., Bilen, J and J.J. Boomsma. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection BMC Ecology 2011, 11:13doi:10.1186/1472-6785-11-1 (Link) (PDF)

Evans, H.E., Elliot, S.L, and D.P. Hughes (2011) Hidden diversity behind the Zombie-Ant fungus Ophiocordyceps unilateralis: Four new species described from  Carpenter ants in Minas Gerais, Brazil PloS One. 2nd March 2011

Semenova, T,** Hughes, D.P. Boomsma, J.J. & Schioett (2011) Evolutionary patterns of proteinase activity in attine ant fungus gardens BMC Microbiology. BMC Microbiology  11:15 (PDF)

D.P. Hughes (2011) Recent developments in sociobiology and the scientific method Trends in Ecology and Evolution Vol 26 (2) 57-8 (PDF)

D.P. Hughes, Wappler, T, & C. C. Labandeira  (2010) Ancient death-grip leaf scars reveal ant fungal parasitism Biology Letters 18th August doi:10.1098/rsbl.2010.0521 (PDF)

D.P. Hughes (2010) A philosophical view of biology Trends in Ecology and Evolution  Vol 25 (7) 384-385 (PDF)

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.

Host Manipulation by Parasites
Edited by David P. Hughes, Jacques Brodeur, and Frédéric Thomas
Preface by Richard Dawkins, University of Oxford, UK

Footnotes

[1] Dawkins, R. (1982). The Extended Phenotype. OUP, Oxford.
[2] Hölldobler B. & E.O. Wilson (1990). The Ants. Harvard University Press, Cambridge.
[3] Evans, H. (1990) Entomopathogenic fungi in tropical forests: an appraisal.
[4] Hughes, D.P., N.E. Pierce & J.J. Boomsma, 2008. Social insect symbionts: evoluion in homeostatic fortresses. Trends in Ecology and Evolution 23(12): 672–677
[5] Andersen, S.B., 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.