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The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus

Centre for Applied Entomology and Parasitology, School of Life Sciences, Huxley Building, Keele University, Staffordshire ST5 5BG, UK, ¹ Inserm U547, Institut Pasteur, rue du Professeur A Calmette, 59019-Lille, France and ² USM 0401, UMR 5178 CNRS/MNHN/UPMC Biologie des Organismes Marins et Ecosystemes, DMPA, Muséum National d’Histoire Naturelle, 7 rue Cuvier, 75231 Paris cedex 05, France

Correspondence should be addressed to D Hoole; Email: d.hoole{at}biol.keele.ac.uk

The tapeworm Ligula intestinalis occurs in the body cavity of its cyprinid second intermediate host, in this study the roach Rutilus rutilus, and inhibits host gonadal development. The mechanism by which infected fish are prevented from reproducing is unknown. Comparison of parameters, such as body length and weight, and condition factor and age, between infected and uninfected individuals, indicated only minor effects of parasitism on growth and condition. In contrast, seasonal gonadal development, as observed in uninfected fish, did not occur in infected fish, and gonads remained small and blocked at the primary oocyte stage in female roach. As immature ovaries and testes are still present, the parasite is presumed to act upon the brain–pituitary–gonadal axis of the fish to inhibit further development of reproductive organs. We investigated the Ligula/fish interaction at the level of the pituitary gland by determination of gonadotrophin (LH) content using a heterologous RIA for carp (Cyprinus carpio) LHß subunit. The results indicated that the pituitary glands of infected roach contained approximately 50% less LH than non-infected fish. After the cloning and sequencing of roach LHß subunit, we measured roach LHß mRNA levels by real-time RT-PCR. A corresponding 50% reduction in LHß mRNA pituitary levels was determined. These results reflect a significant and measurable effect of parasitism on the pituitary gland, and lend support to the hypothesis that excretory/secretory products released from the parasite interact with the brain–pituitary–gonadal axis of the fish host and thus inhibit gonadal development.