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Nasonia: a Jewel Among Wasps Heredity (2010) 104, 235–236 & 2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00 www.nature.com/hdy EDITORIAL Nasonia: a jewel among wasps New World, but a further three closely related species (including one described for the first time in this issue) are found in bird nests in North America, where they specialize in Protocalliphora flies. Heredity (2010) 104, 235–236; doi:10.1038/hdy.2010.3 Houseflies and their relatives are straightforward, though smelly, to maintain in culture and hence entomologists interested in parasitoids quickly found This issue contains a collection of papers on the Nasonia to be a useful model system to study in the parasitoid wasp Nasonia vitripennis, many of which were laboratory. The first wave of research on Nasonia was in prompted by the publication of its genome sequence as the 1940s–1960s (the genus was then called Mormoniella) well as that of two closely related congeners (The Nasonia and was largely genetical, making use of eye-colour Genome Consortia Werren et al., 2010). This issue focuses mutants to study linkage and similar phenomena on the evolutionary aspects of Nasonia research, whereas (Whiting, 1967). Like all Hymenoptera, Nasonia is a special volume of Insect Molecular Biology presents haplodiploid (females are diploid and develop from recent work on the molecular findings of the Nasonia fertilized eggs, whereas haploid male eggs are not Genome Project. This short essay explores why people fertilized), which simplifies some aspects of genotype are interested in this tiny insect—the back story—and scoring, an advantage that has again recently been then briefly asks how the genome sequence will affect exploited. Other early studies explored the mating future research using the wasp. behaviour of Nasonia, as well as its responses to different First, some taxonomic and natural history context. The insecticides. Hymenoptera—the ants, bees and wasps—are one of the The second wave of Nasonia research began in around four great mega-diverse orders of insects, the other three 1980 and was at least initially prompted by evolutionary being beetles, moths and flies. The Hymenoptera are rather than genetic questions. As Nasonia is haplodiploid, divided into three main divisions, and the charismatic with sex determined by the fact of whether an egg is ants, bees and wasps, which attract the most general fertilized or not, natural selection can act on female attention and include the social species, are all found in behaviour to produce sex ratios that are adapted to the Aculeata. There is a basal group of plant-eating local conditions. Indeed, when Hamilton (1967) formu- sawflies (Symphyta), which includes several major pests, lated his theory of local mate competition, he listed a but the largest division by far is the Parasitica, containing number of examples of species, including N. vitripennis, perhaps a million species, the vast majority of which are with high frequencies of sibmating and notably female- parasitoids. Parasitoid larvae develop on or in the body biased sex ratios to support his argument (Hamilton of other animals, normally insects, eventually killing chose a picture of this wasp to adorn the front cover them. A single host provides all the resources that the of the first volume of his collected papers). Sibmating developing larva needs to mature, and hence the frequencies are high in Nasonia because wasps from one parasitoid life cycle is somewhat intermediate between brood emerge together and mate on the surface of the that of a predator and a true parasite (Godfray, 1994). The host puparium before dispersal. When sibmating is Parasitica contain a diverse array of insects, which are absolute, natural selection should favour the parent generally referred to as parasitoid wasps. Some of these producing just enough sons reliably to fertilize all her are quite large in size, such as many ichneumon wasps, daughters. However, when more than one family is but there are many tiny species, often only a few involved (in the case of Nasonia because more than one millimetres in length, which are sometimes collectively wasp lay their eggs in the same hosts, or because the referred to as microhymenoptera. N. vitripennis is one wasps from several hosts emerge in close proximity), such insect, 2–3 mm long; it is a chalcid wasp, a member a sex ratio intermediate between this and equality of the huge and diverse superfamily Chalcidoidea, is favoured. Research, in particular by Werren and which are characterized by a short antenna and highly colleagues, has shown that females adjust their sex reduced wing venation. The name chalcid comes from ratio as predicted by theory, which is one of the most the Greek word for copper and the majority of chalcids, impressive quantitative tests of sex allocation theory including Nasonia, have a metallic green colouration. The (Werren, 1980). beauty of some chalcids has led to them sometimes being This work on Nasonia sex ratio also produced a series called jewel wasps. of surprises. Various strains produced highly biased sex Nasonia species are gregarious pupal endoparasitoids ratios that were not predicted by theory, and research of cyclorrhaphan Diptera. In other words, the parent lays over the years has discovered a zoo of non-Mendelian a clutch of eggs into the pupae of a group of fly species inherited elements, each with its own optimum sex ratio. that are broadly related to the housefly (Musca). The The first discovered element, psr, caused a male-biased larvae feed together inside the fly pupa (technically a sex ratio and is now known to be a B-chromosome that puparia), where they form their own pupae, the adults can be transmitted through sons but not daughters emerging through little round holes drilled through the (Werren et al., 1981). The nature of msr, which causes a host puparial wall. A typical habitat in which to find female-biased sex ratio, is still not known, but it is Nasonia is in bird nests, where they attack flies that suck preferentially transmitted through females (Skinner, blood from young nestlings or feed on dead birds. The 1982). Interestingly, models showed that in populations most well-known species is N. vitripennis, which is found with local mate competition, msr can persist only in the in the northern hemispheres of both the Old and the presence of psr (Werren and Beukeboom, 1993). Another Editorial 236 strain also produced highly female-biased sex ratios and to single-nucleotide polymorphism and microsatellite was initially called sk (for son killer) as males died in libraries—are available or are under development for early development (Skinner, 1985). The causative agent Nasonia. In addition to further studies on speciation, turned out to be a maternally transmitted bacterium that much of the rich biology of Nasonia that has been was named, after the wasp, Arsenophonus nasoniae (Gherna explored by evolutionary ecologists—sex ratio, clutch et al., 1991). The sequence of this bacterium is reported in size, host finding and mating behaviour—will increas- companion papers to the Nasonia genome (Darby et al., ingly become amenable to genetic analysis. The com- 2010; Wilkes et al., 2010). By selectively killing males, pleted genome sequence and the increasing importance the bacteria reduce within-host competition and hence of Nasonia is due to the work of many laboratories, but is increase the fitness of the females that will transmit also a personal triumph for Jack Werren of the University Arsenophonus. Although non-Mendelian elements such as of Rochester, who has championed the work on this these are widespread, it is still remarkable to find so many species for over 30 years. As someone who has spent in one species, and to be able to study how they interact. much of his career studying parasitoids other than There is yet another external element involved in the Nasonia, I fear this wasp is bent on world domination! Nasonia story. It was discovered in the 1960s that there were mating barriers between some strains of Nasonia, and then in the 1980s it was shown that this was due to cytoplasmic incompatibility caused by the bacterium Conflict of interest Wolbachia (Breeuwer and Werren, 1990). This micro- The author declares no conflict of interest. organism is very widespread in insects and often spreads by disadvantaging uninfected females through modify- HCJ Godfray ing sperm in such a way that they can be used only by Department of Zoology, University of Oxford, Oxford, UK females carrying Wolbachia. The three closely related E-mail: [email protected] species of Nasonia carry incompatible Wolbachia, which acts as the main isolating mechanism. It also appears that the psr B-chromosome arose after a hybridization event References between two closely related wasp species with different Wolbachia strains. Breeuwer JAJ, Werren JH (1990). Microorganisms associated The latest phase of Nasonia research has seen the wasp with chromosome destruction and reproductive isolation emerge as a model system for speciation research and the between two insect species. Nature 346: 558–560. present volume provides fine examples of this work. Darby AC, Choi J-H, Wilkes T, Hughes MA, Werren JH, Hurst Wolbachia GDD et al. (2010). Characteristics of the Arsenophonus nasoniae Once the have been removed, the three species genome; son-killer bacterium of the wasp Nasonia. Ins Mol can be crossed and the factors affecting hybrid fitness Biol 19(S1): 75–89. and the morphological differences between the species Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, can be mapped. In this regard, the availability of the Mandelco L et al. (1991). Arsenophonus nasoniae gen. nov., sp. genome sequence will become increasingly useful and nov., the causative agent of the son-killer trait in the parasitic Nasonia’s haplodiploid genetics allows a more straight- wasp Nasonia vitripennis.
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