Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids Nicolas Desneux a,b, *, Ruth J. Barta a , Camille J. Delebecque a , George E. Heimpel a a Department of Entomology, University of Minnesota, 1980 Folwell Avenue, Saint Paul, MN 55108, USA b Unite ´ de Recherches Inte ´gre ´es en Horticulture, INRA, 400 route des chappes, BP 167, 06903 Sophia-Antipolis, France 1. Introduction The dichotomous hypothesis for parasitoid life-history evolu- tion postulates that variation in life histories can be classified according to two distinct development modes: ectoparasitoids and idiobionts with one suite of traits, and endoparasitoids and koinobionts with a different set of traits (Haeselbarth, 1979; Askew and Shaw, 1986; Mayhew and Blackburn, 1999). The capacity to permanently paralyse hosts is only found in idiobiont parasitoids, while koinobiont endoparasitoids leave their hosts able to develop, move and sometimes reproduce (Pennacchio and Strand, 2006). However, the act of stinging can induce transient host paralysis by some koinobiont endoparasitoids as well (Griffiths, 1961; Calvert and van den Bosch, 1972; Mackauer and Chow, 1990; Moreau et al., 2002). This suggests that these species have retained some ancestral properties of ectoparasitoid venom, as the induction of permanent paralysis appears to be ancestral within the Apocrita (Whitfield, 1998). More subtle effects such as transient paralysis or the redirection of the venom function toward more diverse impacts are thought to have appeared later (Gauld and Bolton, 1988). Aphid parasitoids within the braconid subfamily Aphidiinae contain mostly species that do not induce transient host paralysis along with a few species that do (Griffiths, 1961; Calvert and van den Bosch, 1972; Mackauer and Chow, 1990). Aphidiines known to engage in temporary host paralysis share a number of morpho- logical and behavioural characteristics, including moderately long oviposition times, and the use of appendages (abdominal prongs or forelegs) to grab the host during oviposition (Vo ¨ lkl and Mackauer, 2000). Here, we address two adaptive hypotheses that could explain temporary host paralysis in the koinobiont aphidiine Binodoxys communis Gahan, which uses abdominal prongs to grasp the host (Stary and Schlinger, 1967), and was observed paralysing aphids during laboratory observations (N. Desneux, personal obs.). The first hypothesis is that paralysis may increase oviposition success by interfering with aphid defensive behaviours (Kouame ´ and Mackauer, 1991; Wharton, 1993; Michaud and Mackauer, 1995). The second hypothesis is that paralysis can act as a signal that an individual aphid has been recently parasitized, and thus that it Journal of Insect Physiology 55 (2009) 321–327 ARTICLE INFO Article history: Received 3 November 2008 Received in revised form 16 December 2008 Accepted 17 December 2008 Keywords: Aphid parasitoid Superparasitism Idiobiont Koinobiont Binodoxys communis Soybean aphid Aphis nerii Oviposition ABSTRACT The term ‘idiobiont’ refers to those parasitoid species that permanently paralyse their hosts during parasitism, causing the cessation of host growth and development. This is in contrast to koinobiont parasitoids, which allow their hosts to continue developing after being parasitized. While no koinobiont species induce permanent paralysis in their hosts, a minority of koinobionts induce a temporary paralysis that does not interfere with overall host growth and development. We characterized transient paralysis induction in two koinobiont aphid parasitoids in the genus Binodoxys (Hymenoptera: Aphidiinae). Both Binodoxys species induced transient paralysis in Aphis glycines, with paralysis time ranging between 4.5 and 8 min (depending upon parasitoid species and host instar). In a separate experiment, B. communis was capable of inducing transient paralysis in nine aphid species. We addressed two hypotheses potentially explaining the adaptive value of temporary host paralysis in experiments using A. nerii, which is readily accepted but engages in strong defensive behaviour. The first hypothesis is that paralysis increases oviposition success by interfering with host defences and the second is that it aids in the avoidance of self-superparasitism. Paralysed aphids were more likely to be rejected by B. communis than were aphids that had never been stung or that had recovered from paralysis. This result supports the avoidance-of-self-superparasitism hypothesis and is inconsistent with the hypothesis that transient paralysis increases oviposition success of B. communis. ß 2008 Elsevier Ltd. All rights reserved. * Corresponding author at: Unite ´ de Recherches Inte ´ gre ´ es en Horticulture, INRA, 400 route des chappes, BP 167, 06903 Sophia-Antipolis, France. Tel.: +33 4 92 38 64 27. E-mail address: nicolas.desneux@sophia.inra.fr (N. Desneux). Contents lists available at ScienceDirect Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys 0022-1910/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2008.12.009