Experimental Parasite Infection Causes Genome-Wide Changes in DNA Methylation.

Parasites are arguably among the strongest drivers of natural selection, constraining hosts to evolve resistance and tolerance mechanisms. Although, the genetic basis of adaptation to parasite infection has been widely studied, little is known about how epigenetic changes contribute to parasite resistance and eventually, adaptation. Here, we investigated the role of host DNA methylation modifications to respond to parasite infections. In a controlled infection experiment, we used the three-spined stickleback fish, a model species for host-parasite studies, and their nematode parasite Camallanus lacustris. We showed that the levels of DNA methylation are higher in infected fish. Results furthermore suggest correlations between DNA methylation and shifts in key fitness and immune traits between infected and control fish, including respiratory burst and functional trans-generational traits such as the concentration of motile sperm. We revealed that genes associated with metabolic, developmental, and regulatory processes (cell death and apoptosis) were differentially methylated between infected and control fish. Interestingly, genes such as the neuropeptide FF receptor 2 and the integrin alpha 1 as well as molecular pathways including the Th1 and Th2 cell differentiation were hypermethylated in infected fish, suggesting parasite-mediated repression mechanisms of immune responses. Altogether, we demonstrate that parasite infection contributes to genome-wide DNA methylation modifications. Our study brings novel insights into the evolution of vertebrate immunity and suggests that epigenetic mechanisms are complementary to genetic responses against parasite-mediated selection.

Inter- and intraspecific conflicts between parasites over host manipulation.

Host manipulation is a common strategy by which parasites alter the behaviour of their host to enhance their own fitness. In nature, hosts are usually infected by multiple parasites. This can result in a conflict over host manipulation. Studies of such a conflict in experimentally infected hosts are rare. The cestode Schistocephalus solidus (S) and the nematode Camallanus lacustris (C) use copepods as their first intermediate host. They need to grow for some time inside this host before they are infective and ready to be trophically transmitted to their subsequent fish host. Accordingly, not yet infective parasites manipulate to suppress predation. Infective ones manipulate to enhance predation. We experimentally infected laboratory-bred copepods in a manner that resulted in copepods harbouring (i) an infective C plus a not yet infective C or S, or (ii) an infective S plus a not yet infective C. An infective C completely sabotaged host manipulation by any not yet infective parasite. An infective S partially reduced host manipulation by a not yet infective C. We hence show experimentally that a parasite can reduce or even sabotage host manipulation exerted by a parasite from a different species.

The development and morphogenesis of Camallanus cotti Fujita, 1927 (Nematoda: Camallanidae), with notes on its phylogeny and definitive host range.

The freshwater fish nematode Camallanus cotti Fujita, 1927 (Spirurida: Camallanidae) is naturally distributed in East, South and Southeast Asia. During the past three or four decades the species has been disseminated to Europe, North America, Australia and Hawaii, mainly due to the extensive ornamental fish trade. In the present study, its development and larval morphogenesis is described. Newborn first-stage larvae are ingested by copepods and within hours reach the haemocoel, where the worms moult twice. At 22 degrees C ambient temperature, fully-developed third-stage larvae appear on day 11 p.i. After transmission into the fish intestine two further moults occur before the adult stage is reached. At 23 degrees C water temperature, the final moult is initiated around day 33 p.i. in males and between 34 and 42 days p.i. in females. Morphologically the young and older adults are similar, but the buccal capsule of both young males and young females is not yet fully sclerotised. Based on the close similarity in the development and adult morphology of the buccal capsule in C. cotti and three congeners from Europe and North America, we suggest, in general agreement with earlier workers, that the Camallanus Railliet & Henry, 1915 originated in tropical Asia and subsequently radiated to species when adapting to new climatic and/or host-related conditions in the Old World and the New World. C. cotti may thus represent a lineage of speciation which did not apparently involve extensive changes in relation to their natural geographical distribution or definitive host range.

Selection pressure towards monoxeny in Camallanus cotti (Nematoda, Camallanidac) facing an intermediate host bottleneck situation.

This paper describes the ability of the Asian fish nematode Camallanus cotti to carry out both heteroxeny, i.e. an indirect life-cycle using copepods as intermediate host, and monoxeny, i.e. direct infection and development in the definitive fish host. C. cotti occurs naturally in various freshwater teleosts in Asia. During the past decades it has been disseminated into closed or semi-closed aquaculture systems and aquaria around the world, mainly due to the ornamental fish trade. Under such conditions the species may frequently face a bottleneck situation with regard to the availability of copepods. It is known that C. cotti may reproduce and persist in copepod-free aquaria for several months. In order to investigate whether C. cotti has selected towards monoxeny in water systems lacking copepods, in contrast to the opposite selection pressure when copepods are present, 2 separate infection trials were run. It was shown that the parasite can infect the fish host both indirectly via copepods, and directly. However, C. cotti has significantly higher fitness, expressed as survival to maturity, when transmitted indirectly compared to the direct transmission mode. We suggest that the ability of aquarium populations of C. cotti to carry out a direct life-cycle is favoured by selection in order to avoid extinction whenever copepods are absent. It still remains unknown, however, whether the parasite shows the same characteristics in the wild.