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Nasonia Wasp Behavior Genetics This article was originally published in the Encyclopedia of Animal Behavior published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Watt R. and Shuker D.M. (2010) Nasonia Wasp Behavior Genetics. In: Breed M.D. and Moore J., (eds.) Encyclopedia of Animal Behavior, volume 2, pp. 513- 519 Oxford: Academic Press. © 2010 Elsevier Ltd. All rights reserved. Author's personal copy Nasonia Wasp Behavior Genetics R. Watt, University of Edinburgh, Edinburgh, Scotland, UK D. M. Shuker, University of St. Andrews, St. Andrews, Fife, Scotland, UK ã 2010 Elsevier Ltd. All rights reserved. Introduction organism with complex behavior and ecology. Moreover, haplodiploidy facilitates powerful quantitative genetic and Nasonia is a genus of parasitoid wasp that attacks the crossing designs (Figure 2), which can be important given pupae of many large fly species (across families such the low heritability of many behavioral traits. as the Muscidae, Sarcophagidae, and Calliphoridae; The study of the behavior and genetics of Nasonia Figure 1(a) and 1(b)). As a parasitoid, Nasonia kill the wasps has a long history. As a genetic study organism, pupae they attack, being as much predatory as they are Nasonia played an important role in early studies of muta- parasitic (Godfray, 1994). In common with many other tion (Figure 1(d)), but it is perhaps best known for its parasitoids, Nasonia can influence the population density behavior, in particular its sex ratio behavior and for the of the host species they parasitize and may act as presence of sex ratio distorting endosymbionts. More biological control agents. Also known as ‘jewel wasps,’ generally though, as a parasitoid wasp, Nasonia displays a there are four species in the Nasonia genus. By far the broad array of behaviors, spanning host location and host best known is Nasonia vitripennis, which is distributed choice, through to the reproductive allocation decisions across the whole of the northern Palearctic region, being that females need to make, and their elaborate courtship the only Nasonia species so far found in Europe and Asia. behavior. Our understanding of the genetic basis of many N. vitripennis co-occurs with the other three species in of these behaviors is only just beginning to take shape, but North America. N. longicornis is found predominantly in thanks to the Nasonia Genome Project the arrival of the the west of North America, with N. giraulti and N. oneida full genome sequences of three of the four Nasonia species occurring in the eastern United States. Recent data sug- (vitripennis, giraulti, and longicornis) has resulted in a rich gest that range margins may be changing however, and the new source of genetic and genomic information. We will very recent discovery of N. oneida suggests that further begin with an introduction to the field of insect behavior species may await discovery in both America and across genetics and then review the behavior genetics of Nasonia, Europe and Asia. The four species are reproductively taking the life cycle of the wasp as our guide. isolated from each other both prezygotically by various behaviors associated with mating (discussed later) and also postzygotically due to nuclear–cytoplasmic incom- Insect Behavior Genetics patibilities associated with the endosymbiotic bacteria Wolbachia . Bidirectional cytoplasmic incompatibilities Behavior genetics seeks to characterize the genes and between different Wolbachia strains mean that F1 hybrids genetic networks that control or influence an animal’s usually fail to develop, although antibiotic curing of the behavior. As such, behavior geneticists have to integrate different wasp species of Wolbachia facilitates hybrid for- whole organism phenotypes (the behavior or behaviors mation (albeit with some more ‘conventional’ loss of of interest) with increasing levels of genotypic detail, hybrid fitness). The ability to make these crosses has including the action of individual molecules. Since behav- played an important role in the success of many Nasonia ior is, at its most basic, a motor response to some aspect of genetics projects, as differences between the species are the environment, behavioral genes include those asso- usually more pronounced (and so easier to resolve) than ciated with the development and action of the nervous differences among individuals within a species. system, including the associated sensory systems, as well Another factor in the success of Nasonia genetic studies aspects of physiology and cellular metabolism. Moreover, is haplodiploidy (Figure 1(c)). As with all Hymenoptera since behavior is a key intermediary between an organism (bees, ants, and wasps), Nasonia are haplodiploid. This and its environment, the ecological context of behavior is means that females are diploid with both maternal and also crucial for understanding how genetics shapes behav- paternal chromosomes, developing conventionally from ioral variation and therefore influences evolution. All fertilized eggs. Males on the other hand are haploid, devel- this means that behavior genetics is at the center of an oping parthenogenetically from unfertilized eggs. Males integrated approach to understanding animal behavior, as therefore only contain maternal chromosomes. Haplodi- envisaged by Tinbergen in his ‘four questions.’ Most ploidy combines many of the advantages of haploid genetic obviously, genetics can tell us a lot about the mechanistic analysis (no effects of dominance for example), with an basis of behavior (what neural and physiological systems 513 Encyclopedia of Animal Behavior (2010), vol. 2, pp. 513-519 Author's personal copy 514 Nasonia Wasp Behavior Genetics (a) (b) ϫ (d) (c) Diploid (2n) Haploid (n) Figure 1 Some aspects of Nasonia biology. (a) Blowfly pupae are the host for this parasitoid wasp. (b) A female Nasonia laying eggs on a host: females choose hosts depending on the host species, its size, and whether or not other females have already parasitized the host. (c) As with all Hymenoptera, Nasonia are haplodiploid, with females being diploid (2n), carrying chromosomes from both their mother (pink arrow) and father (blue arrow), while males are haploid (n), carrying chromosomes only from their mother (pink arrow). Inset: Nasonia are gregarious, with multiple wasp pupae developing on one fly pupa, within the host puparium. (d) There are a number of visible mutant markers available, derived from early studies of mutation in Nasonia; shown here is the red-eye mutant STDR, often used in studies of sex ratio in Nasonia. Photographs by David Shuker and Stuart West. Line drawings from Whiting AR (1967) The biology of the parasitic wasp Mormoniella vitripennis. Quarterly Review of Biology 42: 333–406, used with permission from the University of Chicago Press. geneticists tend to either focus on mechanistic, ‘bottom- P L X H up’ approaches to behavior, or on describing patterns of behavioral variation in populations, and from that infer- F1 ring something about the genetics of behavior using quantitative genetic techniques in a more ‘top-down’ approach. F2 Insect behavior genetics, at least from a bottom-up 1 2 N perspective, has been dominated by study of the fruitfly Drosophila melanogaster. Considerable progress has been Backcrosses X X made in indentifying and characterizing the genetic path- 2 H L ways influencing neural patterning (including famous Clonal sibships genes such as fruitless), neurohormones and their recep- n = 10 n = 10 tors, neurotransmitters, and other important cellular sig- Figure 2 Haplodiploid genetics allow powerful breeding naling cascades. In terms of top-down approaches, while designs for genetic analysis. Here is illustrated a ‘clonal-sibship’ Drosophila has again been popular, many more species design for a QTL study. Parents from a ‘high’ and ‘low’ line (for a have been studied, not least because of the array of beha- theoretical trait, such as body size) are first crossed. F1 viors available across species and the evolutionary (as daughters are collected as virgins and given hosts to parasitize, with the (all) male recombinant F2 offspring collected. These F2 opposed to mechanistic) puzzles they represent. However, males can then be backcrossed to high and low parental line most species are without the access to the molecular females for the screening of the phenotypes of the recombinant resources available in Drosophila necessary to link molec- male genotypes in both high and low genetic backgrounds (see ular processes with the biological variation that evolution Velthuis et al., 2005, for an example of this approach). acts upon. One of the major challenges currently facing insect behavior genetics is to link bottom-up and top- influence behavior), but genes can also tell us about how down approaches, and species with both rich behavioral behavior develops, its evolutionary past
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