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General News Biocontrol News and Information 35(1), 1N–8N www.cabi.org/BNI General News 5 Reminded that it is a hundred years since the term of the imported cabbageworm . Since then, research ‘parasitoid’ was coined, we start 2014 with a ‘feature’ by on parasitoids has thrived, broadening from the ini- tial focus on agricultural applications to now include Apostolos Kapranas and Ian Hardy of the University of a vast array of topics within genetics, physiology, Nottingham: a concise history of key areas of parasitoid behaviour, ecology and evolutionary biology. The research and a bibliography of key references. They first comprehensive review of parasitoid biology was highlight that although pure research uses parasitoids provided by Curtis Clausen in his classic Ento- 6 5 because they are good model insects, many results have mophagous Insects . Later, Paul DeBach’s book Biological Control of Pests and Weeds and DeBach been useful in developing better biological control. The and Rosen’s7 Biological Control by Natural Enemies remainder of the issue includes our usual mix of news but gave full descriptions of biocontrol programmes is weighted towards the use of parasitoids in biological using parasitoids and a wealth of information on control and we thank all our contributors for making this their general biology. possible. The first models of population dynamics of animals with discrete generations were put forward by Thomson8 in the 1920s and by Nicholson9 in the One Hundred Years of Parasitoids 1930s, both were entomologists working on parasi- toids. Extensions to basic models proposed by The phenomenon of insect parasitism was first Nicholson, working with V.A. Bailey, a physicist, described around a thousand years ago by Lu Dian continued throughout the rest of the century10,11 (China, 1042–1102) based on observations of the life 1 indicating new areas of exploration including how cycle of tachinid flies . Further descriptions of para- parasitoid behaviour could affect influential model sitism by insects are credited to European 16th and parameters, such as searching time. Meanwhile, 17th century naturalists, including Jan Jacob George Salt’s physiological and behavioural studies, Swammerdam (assisted by a painter, Otto Mar- from the early 1930s, set the stage for further silius), and the better known work of Antoni van 2 advances on numerous topics such as superpara- Leeuwenhoek . It was not, however, until one hun- sitism and within-host competition, host selection dred years ago that the term ‘parasitoid’ was coined: and the immunological and biochemical effects of German entomologist Odo Morannal Reuter intro- 12,13 3 hosts on parasitoid development and vice versa . duced it in his book on insect habits and life Towards the end of the century, the discovery that histories, Lebensgewohnheiten und Instinkte der parasitoids search for hosts using chemical cues Insekten. He used the term ‘parasitoidea’ (parasitoid emanating directly from the host14 and host-feeding predators) to distinguish insects that live in close induced plant volatiles15 generated a comprehensive association with their host as immatures, killing it research programme on the chemical ecology of host– during their development and living freely as adults, parasitoid interactions, which is ongoing today16. from ‘parasites’ (true parasites) in which both adult and immature stages feed on the host. In defining During the decades that parasitoids were increas- parasitoids, Reuter had particularly in mind mem- ingly deployed as biocontrol agents, important bers of the Hymenoptera, such as ichneumonoid and advances were also occurring in the fields of behav- chalcidoid wasps, and these also form our focus here. ioural and evolutionary ecology. Ideas originating in In reviewing Reuter’s book, American entomologist studies on avian clutch size by David Lack17, that 4 William M. Wheeler mostly downplayed the utility selection maximizes the number of young produced of the term although his criticisms were tempered per nest, were adopted for parasitoids by Klomp and due to the fact that Reuter has been blind for several Teerink18 generating many productive extensions to years beforehand. Despite Wheeler’s critique, the clutch size theory and, more generally, optimal for- term has now become very widely used, especially in aging theory19–21. Many further advances in the last 30–40 years, and today a Web of Science evolutionary ecology can readily be traced back to search on ‘parasitoid’ returns well over 66,000 arti- W.D. Hamilton’s 1960s’ insights into how genetic cles. We have not been able to cite let alone read all relatedness influences the evolution of social behav- of these! Rather, we here provide a narrative over- iour and how sex ratios are influenced by population view of selected highlights of parasitoid research structure22,23 plus John Maynard Smith’s 1970s’ from just prior to Reuter’s terminological advance to developments of game-theoretic thinking, especially the present time. concerning contest behaviour24. Early developments in contest theory had little to do with the study of Parasitoids were intentionally utilized as agents of parasitoids, but numerous species of parasitoids biological pest control before they were so named. In exhibiting aggressive behaviour have since been 1883, Valentine Riley, a US Department of Agricul- used to test and develop contest research25. In con- ture entomologist, directed the first successful trast, parasitoid wasps and other hymenopterans introduction of a parasitoid, the braconid wasp Apan- were central to the stimulation and testing of some of teles glomeratus, from the UK to the USA for control the key developments in social behaviour and sex Are we on your mailing list? Biocontrol News and Information is always pleased to receive news of research, conferences, new products or patents, changes in personnel, collaborative agreements or any other information of interest to other readers. If your organization sends out press releases or newsletters, please let us have a copy. In addition, the editors welcome proposals for review topics. 2N Biocontrol News and Information 35(1) ratio theory: it is no accident that a parasitoid wasp, ticides and, as parasitoids are among the most Nasonia vitripennis, is depicted on the cover of the deployed natural enemies, parasitoid research volume collecting Hamilton’s works from this should be the vanguard of this. Further, parasitoids period26. will assuredly continue to serve as model systems for probing various questions in behavioural, evolu- The extreme female bias of many parasitoid species tionary and population ecology. For instance, they is often explained by Hamilton’s theory of Local Mate remain ideal for researching the evolution of sex Competition23. Around a decade later the tendency ratios, which connects to a number of general issues 31 for parasitoids to lay female eggs in larger (high- in evolutionary biology , and are currently being 42 quality) hosts and male eggs on smaller (lower- developed as genetic model organisms . In conclu- quality) hosts, a phenomenon which had been com- sion, in defining the characteristics of parasitoids monly observed by biological control practitioners27, that mark them as distinct from predators and from was explained by Charnov and co-authors28,29, bor- parasites, Reuter, though blind, was far-sighted. For rowing concepts from mammal-oriented theory. our part, we envisage no reason that research on These theories show how sex ratio bias arises from insect parasitoids will lose its impetus in the century sexually differential returns from parental invest- to come. This is because parasitoids are important ment and, together with R.A. Fisher’s frequency- for both pure and applied biology and for the syner- dependent explanation for unbiased sex ratios, form gistic interplay between the two. the basis for arguably the most detailed and elegant area of understanding within evolutionary biology: Acknowledgements parasitoids have played no small part in this29–31. This potted history inevitably overlooks many impor- Hamilton’s Local Mate Competition paper23 also laid tant details and some research areas entirely: we the foundations for understanding the influence of apologise. We thank our parasitoid research col- symbiotic organisms on the sexual reproduction of leagues, past and present, and in particular those their hosts. Parasitoids have played an important from the University of California Riverside, Silwood role in this, notably the discovery that Wolbachia Park and the University of Leiden. We dedicate this bacteria cause parthenogenesis in Trichogramma 32 article to the memory of Kees Hofker (13 May 1956 to wasps . Today it is established that symbiotic 6 December 2013), a valued Leiden parasitoid organisms, either in hosts or in parasitoids, have research colleague and friend. enormous significance for ecological and evolu- 33–35 tionary interactions . References From the early 1980s parasitoids increasingly cap- 1Cai, W., Yan, Y. and Li, L. (2005) The earliest record tured the interest of evolutionary and population of insect parasitoids in China. Biological Control 32, ecologists due to the many interspecific variations 8–11. around the relatively simple core life history (it often seems possible to find a parasitoid to fit almost any 2van Lenteren, J.C. and Godfray, H.C.J. (2005) Euro- set of modelling assumptions) and to the rather pean science in the enlightenment and the discovery direct fitness and population dynamic consequences
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