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Dr Joanne Cable  -  PhD


We work on several host-parasite systems, combining experimental approaches in the field and lab with microscopy and molecular biology, to assess the factors controlling disease transmission. Much of our current research is focused on fish pathogens, utilising model systems: Gyrodactylus species infecting guppies or sticklebacks. For further details see www.cripescardiff.co.uk

Host factors influencing parasite transmission

Genetic diversity of hosts significantly impacts on parasite resistance (e.g. Ellison et al. 2011); therefore we have invested considerable time in documenting the diversity of wild guppy populations (Barson et al. 2009; Willing et al. 2010) in relation to their parasite fauna (reviewed by Cable 2011). Specifically, we know that host immunity influences all aspects of host-parasite dynamics (Cable & van Oosterhout 2007a). In vertebrates, the Major Histocompatibility Complex (MHC) plays a crucial role in the immune defence against parasites. Low variation of MHC in both captive and natural fish populations has been associated with increased disease susceptibility (Blais et al. 2007). In guppies increased gyrodactylid burdens have been shown to reduce survival of individuals (van Oosterhout et al. 2007; Faria et al. 2010) and this selection may alter MHC allele frequencies both spatially and temporally. MHC also influences host mating preferences, so we are currently investigating how parasitism, and the interaction between visual and olfaction responses in fish affects mate choice. In a new collaboration with Dr Joe Jackson, we are investigating how other aspects of the fish’s immune response are influenced by temperature in the presence of parasites.

Female petshop guppy with clamped fins characteristic of a heavy gyrodactylid infection

Phenotypic variation in hosts is also important for disease dynamics. Host behavioural traits have been shown to affect transmission of infectious diseases in lab (e.g. Richards et al. 2010; Johnson et al. 2011) and field studies (e.g. Croft et al. 2011). We are currently taking this a stage further by investigating disease transmission in artificial flumes. In collaboration with the School of Engineering at Cardiff, we are assessing the trade-offs between fish swimming behaviour in complex environments vs. the risk of infection. In addition, a Marie Curie Fellow in the lab is investigating how fish temperament impacts on the transfer of directly transmitted pathogens.

Parasite traits influencing transmission

Parasite

Most life history traits of parasites will impact on their transmission potential (Viney and Cable 2011); for Gyrodactylus species, an overriding factor is their unusual reproductive mode. These ectoparasitic worms are more akin to microparasites (such as viruses, bacteria and protozoans) rather than typical helminth macroparasites. Adult worms contain several generations of embryos boxed one inside another (like "Russian Dolls"). Each parasite gives birth to a fully grown worm which attaches to the host alongside its parent and this can lead to exponential population growth. The reproductive biology of Gyrodactylus is further complicated as different modes of reproduction (asexual, parthenogenesis and sexual) can all be involved in the life cycle. Schelkle et al. (2012a) have recently shown the importance of hybridization in mixed infections of gyrodactylids using novel microsatellite markers (Faria et al. 2010), which demonstrates, for the first time the occurrence of sexual recombination and hybrid vigour in monogeneans. Transmission between hosts is also influenced by host availability and the degree of parasite specialization (King and Cable 2007; King et al. 2008, 2009).

Environmental factors driving transmission

Photo in the field

Since 2003, we have been conducting fieldwork in Trinidad and Tobago on the interactions between guppies and their parasites (Cable 2011). In extreme environments, such as the hydrocarbon rich conditions of the Pitch Lake, Trinidad, we have investigated how guppies avoid some gyrodactylid infections (Schelkle et al. 2012b). We have also shown how flooding can negatively impact upon the most heavily infected hosts (van Oosterhout et al. 2007). This is being tested further in the Cardiff labs using artificial flumes to precisely assess how water flow rates and turbulence might influence transmission of fish parasites. However, perhaps the most important factor affecting epidemics in managed host populations is the application of anti-parasitic treatments (e.g. Millet et al. 2010; Schelkle et al. 2009, 2010). We are particularly interested in finding alternative chemotherapeutics against the diplomonad protozoan, Spironucleus vortens (see review by Williams et al. 2012).

In terrestrial hosts, we are studying the effects of climate and habitat variables on parasite distributions of (i) rodents, collaboration with Dr Sarah Perkins, (ii) otters, joint study with Dr Liz Chadwick of the Cardiff University Otter Project, and (iii) primates, collaborations with Prof Mike Bruford and Dr Benoît Goossens.

Interplay between biotic and abiotic factors driving host-parasite dynamics

A range of empirical studies from Dr Cable’s lab has illustrated the importance of host, parasite and environmental factors influencing host-parasite dynamics (e.g. Cable & van Oosterhout 2007b). These data have been used to develop an agent based model for gyrodactylids (van Oosterhout et al. 2008), which is currently being expanded in collaboration with colleagues at McGill University to assess the interplay between parasite infrapopulation growth and host immunity. However, all these advances in understanding the ecology and evolution of these pathogens has only become possible in the last decade due to advances in taxonomy of this specious family (e.g. Harris et al. 2008; Paladini et al. 2009, 2010; Schelkle et al. 2011; Shinn et al. 2010). These ectoparasitic monogenean worms are ubiquitous on teleost fish. Over 400 species have been described, but it is estimated that this number may exceed 20,000. With intensifying aquacultural practices, the unique colonization abilities and pathogenicity of gyrodactylids has resulted in major disease epidemics. One species alone, Gyrodactylus salaris, cost the Norwegian Salmon Industry >500 million € in the first 25 years since its introduction from the Baltic.

In collaboration with the Environment Agency and Natural Resources Wales, we are assessing the impact of native and invasive pathogens on both native (e.g. European eels) and invasive fish species (pumpkinseed; Hockley et al. 2011). For eels, this involves looking at multi-species interactions between Pseudodactylogyrus spp. and Anguillicoloides crassus. For otters, we are focussing on the potentially invasive digenean species parasites Pseudamphistomum truncatum and Metorchis albidus, but also trying to identify their intermediate hosts in cyprinid fishes and snails using molecular methods. Finally, we have recently started working on the interactions between native and invasive crayfish species, and their branchiobdellid symbionts.

Current members of the Research Group

Dr Gabrielle Archard - Personality, stress and parasitism.
Dr Alberto Maceda Veiga - The interaction between parasites and nitrates on fish hosts.
Dr Raquel Xavier - Molecular ecology of fish pathogens, particularly the spill over of parasites between farmed and wild fish.
Emma Gillingham- Global climate change affects on host-parasite interactions.
Frances Hockley - Parasite transmission in aquatic ecosystems.
Jo James - Distribution of native and invasive crayfish.
Alex Stewart - Thermal variation and immunity in ectothermic vertebrates.
Jessica Stephenson - Sensory ecology, parasites and mate choice in the guppy, Poecilia reticulata.

Photograph of international visitor

We host a range of international visitors and, each summer, train Erasmus, Nuffield and IAESTE (The International Association for the Exchange of Students for Technical Experience) students; currently MSc students Kate Davidson and Rhidian Thomas.

We are always happy to discuss possibilities for PhD projects, postdoctoral work and collaborations. Possible funding routes include applying for fellowships, e.g. EU Marie Curie or Royal Society fellowships, or grant applications with you as a named postdoc.

Former members of the Research Group

Post-doctoral

Dr Nicola Barson - Population genetics and behavioural ecology of guppies
Dr Stephen Casey - Genetic diversity of Leucochloridium spp.
Drs Stephen Cummings and Domino Joyce - Guppy MHC and parasite diversity
Dr Patricia J. Faria - Experimental infections and population genetics of gyrodactylid parasites
Dr Mireille Johnson - Morphology and population genetics of gyrodactylid parasites
Dr Marie Le Goff - Population genetics of gyrodactylid parasites
Dr Simon Shayler - Culturing Ichthyophthirius multifilis

Graduate Students

Katherine Dunbar (2003-2006) Gene flow and adaptation in the South frican sea star Patiriella exigua (co-supervised with Prof Mike Bruford).
Farius Jalil (2002-2006) Primate phylogeography and genetic differentiation (co-supervised with Prof Mike Bruford and Benoit Goossens)
Rhys Jones (part-time graduated 2009) British reptile conservation: phylogeography and translocation studies (co-supervised with Prof Mike Bruford)
Tracey King (2004-2008) Local adaptation and host specificity of gyrodactylid parasites
Mark McMullan (2006-2010) Genetic variation at the Major Histocompatibility Complex (MHC) in guppies (Poecilia reticulata) (co-supervised by Dr Cock van Oosterhout, UEA).
Coralie Millet (2005-2009) Host specificity and adaptation to parasitism in Hexamita and Spironucleus species: a phylogenetic analysis of the evolution of biochemical pathways (co-supervised with Prof. David Lloyd).
Joanna Randall (2008-2011) Co-evolution in a multiple-parasite-host system (co-supervised with Dr Jo Lello).
E. Loys Richards (2006-2010) Foraging, personality and parasites: investigations into the behavioural ecology of fishes (co-supervised with Dr Rob Thomas).
Rui Sá (2008-2012) Parasites of Guinea-Bissau Chimpanzees (co-supervised with Prof Mike Bruford and Dr Claudia Sousa, New University of Lisbon).
Milena Salgado-Lynn (2006-2010) Primate viability in a fragmented landscape: genetic diversity and parasite burden of long-tailed macaques and proboscis monkeys in the Lower Kinabatangan Floodplain, Sabah, Malaysia (co-supervised with Prof Mike Bruford and Benoit Goossens)
Bettina Schelkle (2008-2012) Herbal control of gyrodactylid parasites
Ellie Sherrard-Smith (2009-2013) Biotic and abiotic factors influencing the distribution of parasites of Eurasian otters (co-supervised with Dr Liz Chadwick in collaboration with the (Cardiff University Otter Project)
Catrin Williams (2009-2013) Biology of Spironucleus vortens (co-supervised by Prof David Lloyd and Dr Mike Coogan).

Collaborations

In addition to collaborators within Cardiff (parasitologists Jo Lello and Sarah Perkins plus Mike Bruford, Liz Chadwick, Benoit Goossens, Siân Griffiths, David Lloyd, Ian Vaughan and Catherine Wilson), we work with a range of evolutionary biologists and applied scientists:

Profs. Tor Bakke and Phil Harris (Zoological Museum, University of Oslo)
Biology of Gyrodactylus salaris
Prof Christine Dreyer (Max Planck, Tübingen)
Guppy genetic diversity
Dr Joe Jackson (Aberystwyth University)
Thermal variation and immunity in ectothermic vertebrates
Dr Matt Longshaw (Cefas)
Parasite transmission in artificial flumes
Dr Paul Kemp (University of Southampton)
Impact of parasites of fish swimming behaviour
Dr Andy Shinn (University of Stirling)
Gyrodactylid biology
Dr Sonia Consuegra (Swansea University)
Killifish parasites
Dr Cock van Oosterhout (University of East Anglia)
Guppy MHC and parasite resistance; parasite modelling using computational steering; parasite fauna of Trinidadian guppies and Lake Malawi cichlids
Dr Chris Williams and Amy Reading (Environment Agency), Catrin Grimstead and Dr Kyle Young (Natural Resources Wales)
Invasive species and the impact of climate change on aquatic host-parasite systems.

Grants

Environment Agency
European Commission
Fisheries Society of the British Isles (FSBI)
Leverhulme Trust
Natural Environment Research Council (NERC)
Norwegian Research Council (NRC)
Waltham Foundation

We are also grateful to Aquarian and Rolf C. Hagen for the provision of aquarium equipment and consumables.