doi:10.1111/j.1420-9101.2010.02049.x REVIEW The evolution of polyembryony in parasitoid wasps M. SEGOLI* ,A.R.HARARIà,J.A.ROSENHEIM ,A.BOUSKILA*&T.KEASAR§ *Department of Life Sciences, Ben Gurion University, Beer Sheva, Israel Department of Entomology, University of California, Davis, CA, USA àDepartment of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel §Department of Science Education – Biology, University of Haifa – Oranim, Tivon, Israel Keywords: Abstract brood size; Polyembryony has evolved independently in four families of parasitoid wasps. egg limitation; We review three main hypotheses for the selective forces favouring this host quality; developmental mode in parasitoids: polyembryony (i) reduces the costs of egg parasitoid wasps; limitation; (ii) reduces the genetic conflict among offspring; and (iii) allows parent–offspring conflict; offspring to adjust their numbers to the quality of the host. Using comparative polyembryony. data and verbal and mathematical arguments, we evaluate the relative importance of the different selective forces through different evolutionary stages and in the different groups of polyembryonic wasps. We conclude that reducing the cost of egg limitation is especially important when large broods are favoured. Reducing genetic conflict may be most important when broods are small, thus might have been important during, or immediately following, the initial transition from monoembryony to polyembryony. Empirical data provide little support for the brood-size adjustment hypothesis, although it is likely to interact with other selective forces favouring polyembryony. each family are monoembryonic, and the families are not Introduction closely related to each other within the Hymenoptera Polyembryony is a unique mode of development that (Strand, 2003; Grbic, 2003). This raises the questions: involves the production of several genetically identical what are the main selective forces favouring polyembry- embryos from a single egg through clonal division. ony in parasitoid wasps, and why has it evolved in some Occasional polyembryony that results in twinning occurs groups but not in others? in almost all animal taxa. By contrast, obligatory poly- In this paper, we attempt to provide a synthetic, embryony (which occurs in every reproductive event) is concise review of several hypotheses for the evolution relatively rare and occurs in fewer taxonomic groups of polyembryony. We start by presenting general (e.g. flatworms, bryozoans, insects, mammals; reviewed information on polyembryonic parasitoids and discuss in Patterson, 1927; Craig et al., 1997). It has been possible preadaptations for this developmental mode. suggested that polyembryony is costly, because it clones We then introduce three nonmutually exclusive an unproven genotype (different from that of the parent) hypotheses for possible selective forces favouring poly- at the expense of genetic diversity within a brood (Craig embryony in this group (Table 1). We evaluate rele- et al., 1995, 1997). In spite of this likely disadvantage, vant empirical data and consider some simple models polyembryony has evolved in at least four families of that explore the plausibility and relative importance of parasitoid wasps (Hymenoptera). One of these polyem- the different hypotheses through different evolutionary bryonic lineages has become highly successful, diversify- stages and in the different groups of polyembryonic ing to include hundreds of species (Guerrieri & Noyes, wasps. 2005). Polyembryony has probably evolved indepen- dently in each of these families, as most species within Polyembryony in parasitoid wasps Correspondence: Michal Segoli, Department of Entomology, Polyembryony is known from the hymenopteran families University of California, 1 Shields Ave, Davis, CA 95616, USA. Platygasteridae, Braconidae, Dryinidae and Encyrtidae Tel.: 530 752 4481; fax: 530 752 1537; e-mail: [email protected] (Craig et al., 1997; Strand, 2003). In the process of ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 1807–1819 JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1807 1808 M. SEGOLI ET AL. Table 1 Main hypotheses for the evolution of polyembryony in parasitoid wasps. Hypothesis Assumptions Predictions Test of predictions Relative importance Reduce the cost of Reproductive success of Polyembryonic wasps can Comparative analysis Important during the initial egg limitation female parasitoids is potentially produce more demonstrates that transition from limited by the number of offspring than monoembryonic polyembryonic encyrtids monoembryony to eggs that they can wasps. Polyembryony is can potentially produce polyembryony, and in produce accompanied by increased more offspring, have larger maintaining and brood size per host, increased broods and lower accelerating the degree of host size ⁄ quality and reduced fecundities than polyembryony in species fecundity monoembryonic species* with large broods: e.g. Gregarious ancestor genus Copidosoma Reduce genetic Parent–offspring conflict High cooperation between Evolution of a soldier caste Important during, or conflict between depends on relatedness offspring of polyembryonic in encyrtid species. immediately following, the offspring among offspring compared to monoembryonic Soldiers attack according initial transition from species to relatedness monoembryony to Cooperation according to polyembryony, and in relatedness species with small broods, Solitary ancestor e.g. genus Platygaster Adjust brood size to Large variation in hosts’ Offspring adjust their numbers Weak evidence for Likely to interact with the host carrying capacity final carrying capacity according to host size ⁄ quality adjustment of primary other selective forces cannot be foreseen by clone sizeà when secondary rather the mother but may be than primary brood sizes perceived by the offspring are adjusted during their development *Current paper, Box 1. Giron et al. (2004) for Copidosoma floridanum, Segoli et al. (2009b) for Copidosoma koehleri. àSaeki et al. (2009) for Copidosoma bakeri, Segoli et al. (2010) for C. koehleri. polyembryonic development, a primary cell mass (mor- soldier larvae with slim bodies and large mandibles. ula) divides into a mass of developing embryos (poly- Soldiers attack intra- and inter-specific competitors inside morula). Embryos develop into larvae that actively feed the host and never pupate or emerge from the host as on the host tissues before they pupate (Grbic et al., 1998). adults (Cruz, 1981, 1986; Giron et al., 2004; Segoli et al., The number of embryos developing from a single egg 2009b). The large clone sizes and the development of a through polyembryony varies substantially among spe- soldier caste suggest that in this family, polyembryony has cies. In platygasterids that parasitize eggs of gall-midges reached its most specialized form. (Diptera), clone size is small, with 2 to approximately 10 individuals developing from each egg (Leiby & Hill, 1923, Common life history features of 1924; Leiby, 1929). In the species Platygaster hiemalis, polyembryonic wasps some eggs are monoembryonic, whereas others develop into two embryos. This was suggested to represent the Parasitoid life histories can be divided into several most primitive form of polyembryony (Leiby & Hill, categories. One distinction is between endoparasitoids 1923). In polyembryonic braconids that parasitize moth that develop within the body of their hosts, feeding from larvae (Lepidoptera), clone size ranges from 2 to 50, the inside, and ectoparasitoids that feed on the host depending on species (Daniel, 1932; Parker, 1931; Orr externally. Another important distinction is between et al., 1994; White & Andow, 2008). In polyembryonic koinobiont parasitoids that allow their hosts to continue dryinids that parasitize nymphs of leafhoppers (Hemipter- developing after parasitism (for example egg-larval par- a), clone size reaches 60 (Kornhauser, 1919). In polyem- asitoids that parasitize the host egg, with their offspring bryonic encyrtids that parasitize eggs of Lepidoptera and emerging out of the host larva) and idiobionts that arrest some Hymenoptera, clone sizes vary from 2 (e.g. Ageniaspis host development. Finally, in gregarious parasitoids citricola, Zappala` & Hoy, 2004) to several dozens (e.g. several larvae can complete their development on the Ageniaspis fuscicollis, Kuhlmann et al., 1998; Copidosoma body of a single host, whereas in solitary parasitoids only koehleri, Segoli et al., 2009a), and up to hundreds or even one larva survives (Godfray, 1994). thousands of individuals (e.g. Copidosoma floridanum, Interestingly, all polyembryonic wasps fall into the Strand, 1989; Ode & Strand, 1995; Copidosoma bakeri, same category: they are relatively small in size (adult Saeki et al., 2009). In some encyrtid parasitoids, a subset of body size usually £ 1 mm), endoparasitoids and the embryos from a single egg develops into specialized koinobionts (mostly egg-larval parasitoids). Because ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 1807–1819 JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY The evolution of polyembryony 1809 Box 1: Potential number of offspring for ily, suggesting that once polyembryony is established, it may polyembryonic vs. monoembryonic wasps allow females to reduce their costs of egg production. However, this result should be treated with caution, as the difference is Polyembryony may reduce the cost of egg limitation by not large, and data were not corrected