School of Biosciences

G. salaris Photo courtesy of T.A. Bakke

I work on several host-parasite systems combining experimental approaches with microscopy and molecular biology. Much of my current research is focused on the biology of Gyrodactylus species. 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. Much of our work in Cardiff is based on model systems (G. turnbulli infecting guppies and G. gasterostei infecting sticklebacks) but, through collaboration with Norwegian colleagues, comparative studies are being performed on the economically-important G. salaris which infects salmonids.

Parasite reproduction

Gyrodactylus species have an unusual mode of reproduction more akin to that of microparasites (such as viruses, bacteria and protozoans) rather than typical helminth macroparasites. Adult worms contain several generations of embryos boxed one inside another and are often referred to as "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) may be involved in the life cycle of an individual worm.

In Figure 1, a-h represent the different stages of a newborn parasite. When this parasite (shown in red) is born it already contains a developing F1 embryo (green) in utero and as the parasite matures an F2 embryo (purple) is visible developing within the F1. After birth of the 1 st born daughter (green), an oocyte (yellow) enters the uterus and development of the 2 nd born daughter begins. The 1st born daughter can only develop asexually as development begins before birth of its mother, but 2 nd and subsequent daughters may develop parthenogenetically or sexually.

Fig.1. Different developmental stages of a newborn Gyrodactylus sp. (a-h) and its offspring.

Light and electron microscopy are being used to examine gyrodactylid reproduction, particularly the adaptations for viviparity. After birth, a large oocyte moves from the Egg Cell Forming Region (ECFR) into the uterus via the posterior cap cell region (Fig. 2). Embryology is unusual, characterised by duet, rather than quartet, cleavage and extreme regulative development (“blastomere-anarchy”). Unlike most monogeneans, which release encapsulated embryos nourished by vitelline cells, Gyrodactylus embryos are nourished in utero. The embryo is separated from the parental gastrodermis by a metabolically-active uterus lining, which appears to form a “placental-type” role. The F2 embryo (not shown in Fig. 2) derives its nutrients directly from the F1 embryo.

Fig. 2. Structures involved in Gyrodactylus reproduction. F1 embryo in the central uterus flanked by anterior (acc) and posterior cap cells (pcc) in close proximity to the parental uterus (Ul) and gastrodermis (ga). The ECFR serves as both ovary and sperm storage chamber.

We are also investigating the role of sex in gyrodactylid strain evolution, and the potential of these organisms for genetic change using a battery of molecular techniques. Recently, we have provided the first conclusive evidence that sexual reproduction does occur in Gyrodactylus, and that under laboratory conditions cross-fertilization of worms is common.

The effects of host population structure on parasite diversity

The guppy, Poecilia reticulata, is a classic model for studies on microevolution, and yet the impact of parasitism on this host in the wild remains relatively unexplored. We are conducting the first field studies in Trinidad and Tobago to examine parasite diversity and assess their potential impact on poeciliid sexual- and shoaling behaviour. We are screening guppies and their associated parasites with species-specific microsatellite loci to assess genetic diversity at different geographical and population levels (between rivers, within rivers and within shoals). Uniquely, this study will assess the relative importance of parasites, particularly gyrodactylids, in relation to other natural- and sexual selection pressures on the host. In a parallel study, we are assessing the impact of parasites on speciation of Lake Malawi cichlids.

Parasite transmission

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

The guppy and its common gyrodactylid parasites, Gyrodactylus turnbulli and G. bullatarudis, are ideal species with which to test the influence of fish behaviour on parasite transmission. Female guppies not only school more than males but also show a greater preference for associating with their familiar schoolmates. Males, on the other hand, seem to move between schools in search of mating opportunities (Griffiths & Magurran 1998). The higher schooling tendency of female compared to male guppies has until now been explained by the higher cost of reproduction and thus increased investment in anti-predator behaviour for females. However, school fidelity may also be a defence against parasite infection as individual risk of infection is reduced by joining a school. We are currently testing whether female guppies experience low parasite load compared to males, and if males, by their increased mobility, contribute disproportionately to parasite transmission. We also plan to examine sex-differences in the cost of parasite infection. Testing such predictions will have important evolutionary consequences. Furthermore, comparative studies with Norwegian colleagues on G. salaris infected salmonids are revealing unpredicted transmission strategies that could have significant management and conservation implications for disease control. In collaboration with computer scientists, we are developing software to model gyrodactylid infra- and metapopulations.

Adaptive sequence variation in MHC of guppies (Poecilia reticulata) and its role in immunocompetence

It has been clearly documented that teleosts respond against monogenean infections, including gyrodactylids, but the mechanisms involved are unclear. In other vertebrates, the Major Histocompatibility Complex (MHC) plays a crucial role in the immune defence against parasites, and such a determinant of host specificity is an important character in the taxonomy of infectious organisms. Low variation of MHC in both captive and natural populations has been associated with increased disease susceptibility. MHC dependent mate-choice and kin-recognition suggests that MHC genes may also be important in sexual selection. The adaptive significance and polymorphism of MHC warrants further study into the use of MHC genes in conservation genetics, ecology and evolution. We are using the guppy as a model organism to test the effects of MHC genotype and haplotype on the fitness of individuals, including disease resistance. Parasite establishment, survival and fecundity on wild and captive guppy populations exposed to parasites are being examined in relation to MHC genotype.

Grants

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

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

Collaborations

Kjetil Olstad.

Aside from collaborators in Cardiff BIOSI (Mike Bruford, Sian Griffiths, Jo Lello, David Lloyd, Sarah Perkins and Rob Thomas), we work closely with a range of parasitologists, evolutionary biologists and applied scientists:

Prof. Tor Bakke and Prof. Lutz Bachmann (Zoological Museum, University of Oslo)
Biology of Gyrodactylus salaris

Dr Mike Coogan (Cardiff Chemistry)
Biochemistry of Spironuclues vortens; water chemical analysis

Prof Christine Dreyer  (Max Planck, Tübingen)
Guppy genetic diversity

Drs Haakon Hansen (National Veterinary Institute, Oslo) 
Biology of Gyrodactylus salaris

Dr Matt Longshaw (Cefas) and Dr Catherine Wilson  (Cardiff ENGIN)
Parasite transmission in artificial flumes

Prof. George Turner  (Bangor University)
Cichlid parasites

Drs Andy Shinn and James Bron (University of Stirling)
Gyrodactylid taxonomy including GyrodB; culturing Ichthyophthirius multifilis

Dr Cock van Oosterhout (University of Hull)
Guppy MHC and parasite resistance; parasite modelling using computational steering; parasite fauna of Trinidadian guppies and Lake Malawi cichlids

(A) Adult slow growing and neotenic Polystoma integerrimum which infect

(B) Rana temporaria, otherwise known as the common frog.

(C) contain unusual crystalline bodies in the gastrodermis

Current Members of the Research Group

I am 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, with me acting as sponsor, or grant applications with you as a named postdoc.

Frances Hockley
Parasite transmission dynamics in aquatic ecosystems

Dr Mireille Johnson-Bawe
Morphology and population genetics of gyrodactylid parasites

Mark McMullan (based at Hull University)
Genetic variation at the Major Histocompatibility Complex (MHC) in guppies (Poecilia reticulata)

Loys Richards
Dietary conservatism in solitary and social fish, and its evolutionary consequences for their prey

Joanna Rumsey
Co-infection biology

Gastro-intestinal parasites in Malaysian Primates

Rui Sa
Parasites of Chimpanzees

Bettina Schelkle
Herbal control of gyrodactylid parasites

Eleanor Sherrard-Smith
Spatial and temporal variation of Otter Lutra lutra) parasites (in collaboration with the Cardiff University Otter Project)

Catrin Williams
Biology of Spironucleus vortens

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 student Rienk Doejtes.

Former members of the Cardiff Research Group

Post-doctoral

Nicky Barson and Cock van Oosterhout.

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 Marie Le Goff Vitry
Morphology and population genetics of gyrodactylid parasites

Dr Simon Shayler
Culturing Ichthyophthirius multifilis

Graduate Students

Farius Jalil (2002-2006)
Primate phylogeography and genetic differentiation

Katherine Dunbar (2003-2006)
Gene flow and adaptation in the South African sea star Patiriella exigua.

Dr Rhys Jones (part-time graduated 2009).
Phylogeography and conservation of British snakes

Dr Tracey King (2004-2008)
Local adaptation and host specificity of gyrodactylid parasites

(2005-2009)
Host specificity and adaptation to parasitism in Hexamita and Spironucleus species: a phylogenetic analysis of the evolution of biochemical pathways