Host resistance and within-host competition between leaf-cutting ant parasites with opposing transmission strategies

Lead Research Organisation: University of Leeds
Department Name: Inst of Integrative & Comparative Biolog

Abstract

Parasites have significant effects on host biology. Most research has focussed on infections by single, virulent parasites that cause obvious disease. However, infections frequently involve more than one parasite, many of which may appear relatively avirulent and thus hard to detect. Although their effects may be more subtle, these cryptic parasites can nevertheless have important effects on host fitness. Furthermore, they may influence the infection success of other, perhaps more virulent, parasites either by reducing the host's immune response or by directly inhibiting the infection of the other parasite. This project will investigate the interactions between hosts and parasites in leaf-cutting ants infected by a virulent fungal pathogen and/or an avirulent bacterial parasite. It will examine if host genotypes and phenotypes differ in resistance to the avirulent parasite and if the same hosts are also resistant to the virulent pathogen. It will also establish if infection by the apparently avirulent parasite reduces host immunity. Finally it will determine the infection success of the virulent pathogen in hosts that are either infected by, or free from, the avirulent parasite. Together these results will shed important light on the role of more cryptic parasites in the biology both of hosts, and other more obvious pathogens.

Publications

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Frost C.L. (2008) One gene or five? Wolbachia in the fungus-growing ant tribe Attini in Winter Meeting of the North-western European Section of the International Union for the Study of Social Insects

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Lorenzo Santorelli (Author) (2008) Genetic resistance to the cryptic parasite Wolbachia in the leaf-cutter ant Acromyrmex echinatior in 4th European Meeting of the International Union for the Study of Social Insects

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Scully J. (2010) The effects of within-host competition on parasite evolution in Royal Entomological Society Postgraduate Forum

 
Description Evolutionary theory predicts that hosts will often exhibit genetic variation in resistance to parasites. Here we investigated whether the leaf-cutting ant Acromyrmex echinatior shows such genetic variation in resistance to the avirulent bacterial parasite Wolbachia by comparing the infection of patrilines within colonies. We genotyped 96 workers from each of five colonies of A. echinatior at three microsatellite loci to determine their patriline. We then screened all of these individuals for Wolbachia infection by amplifying the Wolbachia-specific wsp genetic marker. Unexpectedly, we found very little variation between patrilines in infection with Wolbachia. Possibly this relates to the fitness effects of Wolbachia infections on ant workers. As ant workers are sterile, they represent a reproductive dead-end for Wolbachia so there is no advantage to the symbiont in expressing virulence. During the project we also discovered unexpectedly high frequencies of Wolbachia infection in A. echinatior. Previous studies with Wolbachia in the same population of species found that approximately 50% of A. echinatior workers were infected with the parasite (van Borm et al. 2001 J Evol Biol; 2003 Mol Phyl Evol). Similarly infection prevalences have also been found in other ants (Wenseleers et al. 2002 Proc R Soc Lond B). In this project, however, we combined a more rigorous protocol with a larger sample size and found that at least 80% of A. echinatior workers were infected with Wolbachia. Indeed many colonies even showed 100% infection. Previous reports of lower infection frequencies therefore appear to be in error, most likely due to failed PCR amplification or DNA extraction. The extremely high infection frequencies we found further suggest that Wolbachia has little or no negative impact on the fitness of host ant workers. The combined results of the project all suggest that, in contrast to previous literature (van Borm et al. 2001; 2003; Wenseleers et al. 200), Wolbachia has little affect on the fitness of A. echinatior workers. The extremely high infection frequencies further raise the possibility that Wolbachia may benefit from these infections via horizontal transmission. To examine this we have incorporated the results of the project in a phylogenetic analysis and this confirms that horizontal transmission is commonplace amongst these ants.
Exploitation Route Fundamental research with no potential near-term application. However study species is a major agricultural pest and work contributes to a better understanding of their biology, thereby informing potential control strategies in the future No direct exploitation routes
Sectors Agriculture, Food and Drink

 
Description The work was used in a Discovery Zone exhibit for school children.
First Year Of Impact 2007
Sector Education
Impact Types Societal

 
Description EC FP6 Marie Curie Fellowship
Amount € 181,350 (EUR)
Organisation European Commission 
Sector Public
Country European Union (EU)
Start  
 
Description International collaboration with Copenhagen 
Organisation University of Copenhagen
Country Denmark 
Sector Academic/University 
PI Contribution We contributed expertise and resources to the collaboration, and provided training to researchers at the partner organisation
Collaborator Contribution The partner contributed expertise and resources, and provided training to members of my research team.
Impact Nehring, V., Evison, S.E.F., Santorelli, L.A., D'Ettorre, P. & Hughes, W.O.H. 2011. Kin-informative recognition cues in ants. Proc R Soc Lond B 278:1942-1948. Frost, C.L., Fernandez-Marin, H., Smith, J.E. & Hughes, W.O.H. 2010. Multiple gains and losses of Wolbachia symbionts across a tribe of fungus-growing ants. Mol Ecol 19:4077-4085
Start Year 2007
 
Description International collaboration with Dr Fernandez-Marin 
Organisation Smithsonian Institution
Department Smithsonian Tropical Research Institute
Country Panama 
Sector Academic/University 
PI Contribution We led the development of this collaboration, contributed expertise and resources, and provided training to partner researchers
Collaborator Contribution The partner contributed expertise and resources, and provided training to members of my research team.
Impact Frost et al. 2010 Mol Ecol paper
Start Year 2008
 
Description Discovery Zone exhibit 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Discovery Zone exhibit

None
Year(s) Of Engagement Activity 2009