Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology A.D.N. Mabiala-Moundoungou, G. Doury, P. Eslin, A. Cherqui, G. Pre ´ vost * Laboratoire de Biologie des Entomophages, EA 3900 BioPI, Universite ´ de Picardie-Jules Verne, 33 rue Saint Leu, 80039 Amiens cedex, France 1. Introduction The various strategies developed by insect endophagous parasitoids to escape or overcome their host’s immunity defenses, and to regulate the host’s physiology to the benefit of their own development, have been extensively described in many host– parasitoid systems (Beckage and Gelman, 2004; Edwards et al., 2006; Pennacchio and Strand, 2006; Poirie ´ et al., 2009; Suzuki and Tanaka, 2007). To escape the host’s immunity reaction of encapsulation, some species evolved ‘‘passive’’ strategies relying on a ‘‘camouflage’’ such that the parasitoid egg or larva avoids the recognition and/or the attack by the host hemocytes (Asgari et al., 1998; Corley and Strand, 2003; Davies and Vinson, 1986; Zhang et al., 2006). Other species developed ‘‘active’’ strategies resulting in the inhibition or the destruction of the host’s cellular immunity system (Schmidt et al., 2001; Strand and Pech, 1995). Regulation of hosts’ physiology was shown to target the hormones or the hemolymph protein content of the parasitized host (Bae and Kim, 2004; Beckage and Kanost, 1993; Song et al., 2008). In order to regulate their host’s immunity and physiology, parasitoids produce and release active factors in the host hemocoel. These active factors may be synthesized by the female parasitoid (in venom glands or ovaries) and injected along with the parasitoid egg during oviposition, or they may be of embryonic origin (teratocytes). In many species of the ichneumonid and braconid families (Ichneumonoidea), symbiotic polydnaviruses (PDVs) or virus-like particles (VLPs) present in the females’ calyx fluid were shown to infect the host tissues and to be the agents controlling the host’s physiology (Beck and Strand, 2005; Labrosse et al., 2005; Schmidt et al., 2001; Suzuki et al., 2008; Webb and Luckhart, 1994). Venoms from female parasitoids have been reported to cause abnormalities of host development, with modes of action that vary according to the lifestyle of the parasitoid species (Pennacchio and Strand, 2006). Venoms of ectoparasitoids are often paralytic and may cause the developmental arrest of the host that can be beneficial to the externally developing parasite (Doury et al., 1995). In most cases, the role of endoparasitoids’ venoms in suppressing the host’s immune defences has not been clearly established. In some braconid species, however, the venom may contribute to the inhibition of the host’s growth by acting synergistically with the calyx fluid or PDVs (Gupta and Ferkovich, 1998; Jones and Wache, 1998; Tanaka and Vinson, 1991a,b). A limited number of studies suggest that the venom of endoparasitoid species devoid of symbiotic viruses and VLPs (Asgari et al., 2003; Cai et al., 2004) may perturb the host’s immune defences. For example, venom from the pupal parasitoid Pteromalus puparum (Hymenoptera: Pteromali- dae) suppresses the cellular immune responses of its host, Pieris Journal of Insect Physiology 56 (2010) 35–41 ARTICLE INFO Article history: Received 29 June 2009 Received in revised form 10 September 2009 Accepted 10 September 2009 Keywords: Asobara parasitoid Drosophila Venom and ovarian secretions Immuno-suppression Host regulation ABSTRACT Asobara japonica (Braconidae) is an endophagous parasitoid developing in Drosophila larvae. The present study shows that A. japonica was never encapsulated in Drosophila melanogaster, and that it caused an overall inhibition of the host encapsulation reaction since injected foreign bodies were never encapsulated in parasitized hosts. Both the number of circulating hemocytes and the phenoloxidase activity decreased in parasitized larvae, and the hematopoietic organ appeared highly disrupted. We also found that A. japonica venom secretions had atypical effects on hosts compared to other braconid wasps. A. japonica venom secretions induced permanent paralysis followed by death of D. melanogaster larvae, whether injected by the female wasp during an interrupted oviposition, or manually injected into unparasitized larvae. More remarkably, these effects could be reversed by injection of ovarian extracts from female wasps. This is the first report that the venom of an endophagous braconid parasitoid can have a deadly effect on hosts, and moreover, that ovarian extracts can act as an antidote to reverse the effects of the wasp’s venom. These results also demonstrate that A. japonica secretions from both venom gland and ovary are required to regulate synergistically the host physiology for the success of the parasitoid. ß 2009 Elsevier Ltd. All rights reserved. * Corresponding author. Tel.: +33 (0) 322 827 554; fax: +33 (0) 322 827 554. E-mail address: genevieve.prevost@u-picardie.fr (G. Pre ´ vost). Contents lists available at ScienceDirect Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys 0022-1910/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2009.09.001