Ecology, Epidemiology, and Evolution of Parasitism in Daphnia
In 1990, I was working on my PhD on the life-history evolution of Daphnia at the Zoological Institute of the University of Basel when Bill Hamilton came for a visit there. Being deeply interested in the evolution of parasites, he did not wait long before asking me about parasites in Daphnia. To my embarrassment, I had to answer that I had never seen a parasite in Daphnia and that I believed they may not be very important. Of course Bill was not convinced by my obviously rather superficial and uninformed statement, and after some discussion I agreed that I would collect some field samples the next day and screen them with him for parasites. Except for a few individual Daphnia carrying some algae epibionts, we did not find anything. Bill was convinced, however, that there was more to discover, and a month later he sent me a copy of Green's 1974 paper on "Parasites and Epibionts of Cladocera." Green lists numerous symbionts living on and in Daphnia and other Cladocerans—too many to be ignored.
At the same time, Paul Schmid-Hempel’s group was working at the Zoological Institute in Basel, establishing bumblebees as a new model system to study host–parasite interactions. On the basis of many interactions with Paul and his students, mainly Jacqui Shykoff and Christine Müller, I started to develop an interest in host–parasite evolution and eventually decided that this may be a good topic for a postdoc. Interestingly, other PhD students in our group pursued the same direction.
Being an experimentalist at heart, I decided that I would like to start working with a rather simple host–parasite system that would allow me to do sophisticated experiments. I asked Bill Hamilton to host me in Oxford. Bill was enthusiastic, but we were undecided about what system would be good. Bill suggested Daphnia, but I was not so sure, because I still had not seen parasites in Daphnia. The advantage with Daphnia, however, was that I already had experience with them and that they seemed, indeed, like a good system: easy to maintain, reproducing clonally, short generation time, and small size, to name just a few. Nonetheless, before I settled on Daphnia, I did an intensive literature search (back in the early nineties, this was still a time-consuming enterprise) and came up with three host systems I wanted to check out: the Indian meal moth (Plodia interpunctella), Tribolium, and Daphnia. The two earlier systems are genetically more tractable than Daphnia, because genetic crosses of Daphnia clones are still not very easy. In the end, one factor swayed my decision to work with Daphnia: How could one control airborne pathogens during experiments in which controls and infected replicates are standing side by side? With waterborne pathogens, I reasoned, this would be much less of a problem. It turned out to be correct.
My initial field surveys around Oxford were not very successful: plenty of Daphnia, but no parasites. After several months, I decided to contact Jim Green, who was still working in London but was about to retire. He invited me to bring him the samples in which I wanted to find parasites. It took him 10 minutes to find the first parasites, and over the next two hours a few more species turned up as well. What I did not know was that it is essential to use phase-contrast microscopy, because microsporidian parasites, in particular, are barely visible without it. Despite his enthusiasm, Jim was rather pessimistic about the possibilities of culturing Daphnia parasites and conducting controlled experiments. However, back in Oxford I checked all of my cultures and realized that I had already cultured one species for several months together with the D. magna clone it lived in. Within 2 weeks I worked out a method for controlled culturing of Glugoides intestinalis (formerly Pleistophora intestinalis) and 3 months later submitted the first paper on it. Since then, my lab has developed culturing methods for more than 10 species of parasites.
This work with the Daphnia parasites has absorbed my attention since then, and together with my research group, I have spent many exciting hours in the laboratory and in the field finding out more about Daphnia parasites, and about parasites in general. The Daphnia–microparasite system has proved to be a powerful model for many questions in basic epidemiology, ecology, and evolution. The upcoming genome data will extend this into the “Narrow Roads of Gene Land“ (the title of Bill Hamilton’s second book with many parts on the evolution of host–parasite interactions, 2001) and will hopefully open up a pluralistic approach to understanding host–parasite coevolution.
This book would not have been possible without the collaboration of the marvelous people working with me in Oxford, Silwood, Basel, and Fribourg, and also collaborators from around the world who shared my enthusiasm for host–parasite interactions. I want to thank the people in and around my group (in roughly chronological order): Valentino Lee, Katrina Mangin, Heide Stirnadel, Sven Krackow, Judy Wearing-Wilde (Oxford), Dermot McKee (Silwood Park), Christine Zschokke-Rohringer, Hans-Jochaim Carius, Tom Little, Daniel Fels, Marc Capaul, Myriam Riek, Patrick Mucklow, Pia Salathé, Katja Pulkkinen (Basel), Christoph Haag, Dominik Refardt, Dita Vizoso, Olga Sakwinska (Basel and Fribourg), Lusia Sygnarski, Sandra Lass, Marc Zbinden, Knut Helge Jensen, Raffael Aye, Florian Altermatt, Holly Ganz (Fribourg and Basel), and Thomas Zumbrunn (Basel). Special thanks to Jürgen Hottinger, who became over the years not only a close friend but also the irreplaceable center of the group. Numerous collaborators, many of whom are theoreticians, helped open my eyes when I was blinded by the beauty of Daphnia symbionts: Sebastian Bonhoeffer, Marc Lipsitch, Martin Nowak, Wolfgang Weisser, Richard Lenski, Bill Hamilton, Paul Rainey, Mitja Scholz, Martin Embley, Janne Bengtsson, Liz Canning, Steve Stearns, Ilmari Pajunen, Roland Regoes, Ronny Larsson, Kerstin Bittner, Ellen Decaestecker, and Paul Schmid-Hempel. Florian Altermatt, Holly Ganz, Sandra Lass, Dominik Refardt, Marc Zbinden and Thomas Zumbrunn read most of the book in earlier drafts and helped me to polish style and content. Dita Vizoso produced several figures to illustrate important aspects of life cycles and transmission. Dita Vizoso and Frida Ben-Ami are thanked for contributing photographs. I thank my son Gleb for help with producing some of the figures. Suzanne Zweizig improved the style and readability of the language throughout the book. Rita Gunasekera helped me with the formatting of the various files. Jo McEntyre and Laura Dean were of great help in all aspects of publishing this book. Thanks to their work, the book can be made available to a wide audience via the Internet. Finally, I want to thank my friends and family for their support and the encouragement to write this book.
November 2005, Dieter Ebert