Cleptoparasites, Social Parasites and a Common Host: Chemical

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Cleptoparasites, Social Parasites and a Common Host: Chemical Journal of Insect Physiology 58 (2012) 1259–1264 Contents lists available at SciVerse ScienceDirect Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys Cleptoparasites, social parasites and a common host: Chemical insignificance for visiting host nests, chemical mimicry for living in ⇑ Alessia Uboni a,1, Anne-Geneviève Bagnères b, Jean-Philippe Christidès b, Maria Cristina Lorenzi a, a Dept. of Life Sciences and Systems Biology, University of Turin, via Accademia Albertina 13, 10123 Torino, Italy b I.R.B.I., UMR CNRS 7261, Université de Tours, Faculté des Sciences, Parc Grandmont, 37200 Tours, France article info abstract Article history: Social insect colonies contain attractive resources for many organisms. Cleptoparasites sneak into their Received 2 December 2011 nests and steal food resources. Social parasites sneak into their social organisations and exploit them Received in revised form 20 June 2012 for reproduction. Both cleptoparasites and social parasites overcome the ability of social insects to detect Accepted 23 June 2012 intruders, which is mainly based on chemoreception. Here we compared the chemical strategies of social Available online 30 June 2012 parasites and cleptoparasites that target the same host and analyse the implication of the results for the understanding of nestmate recognition mechanisms. The social parasitic wasp Polistes atrimandibularis Keywords: (Hymenoptera: Vespidae), and the cleptoparasitic velvet ant Mutilla europaea (Hymenoptera: Mutillidae), Brood parasite both target the colonies of the paper wasp Polistes biglumis (Hymenoptera: Vespidae). There is no chem- Paper wasp Semiochemical ical mimicry with hosts in the cuticular chemical profiles of velvet ants and pre-invasion social parasites, Cuticular hydrocarbon but both have lower concentrations of recognition cues (chemical insignificance) and lower proportions Branched alkanes of branched alkanes than their hosts. Additionally, they both have larger proportions of alkenes than their Selective pressure hosts. In contrast, post-invasion obligate social parasites have proportions of branched hydrocarbons as large as those of their hosts and their overall cuticular profiles resemble those of their hosts. These results suggest that the chemical strategies for evading host detection vary according to the lifestyles of the par- asites. Cleptoparasites and pre-invasion social parasites that sneak into host colonies limit host overag- gression by having few recognition cues, whereas post-invasion social parasites that sneak into their host social structure facilitate social integration by chemical mimicry with colony members. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction colonies in the quality and quantity of their components, resulting in colony-specific chemical profiles (Bagnères and Wicker-Thomas, Social insect colonies contain attractive resources for many 2010; van Zweden and d’Ettorre, 2010) although hydrocarbons also organisms. They contain food stores and immature brood that can convey information that is not colony specific (e.g., Endler et al., be used as food and sophisticated nest architectures that can be 2004). Generally, colony residents tolerate individuals whose used as shelters or nests. Finally there are complex social structures chemical profiles match their own (i.e., that have no undesirable that can be exploited to get a workforce. Therefore it is not surpris- cues) and reject those with poor matching (i.e., that have undesir- ing that social insect colonies attract many different kinds of able cues). However, residents occasionally fail to identify enemies. exploiters. For example, social parasites invade host colonies and This happens because the recognition processes are not error free enslave hosts to rear parasite brood (Wilson, 1971) and cleptopar- and also because there are enemies, such as parasites, that have asites loot social insect colonies of food resources (Evans and West- evolved special adaptations to circumvent host detection. For Eberhard, 1970; Schmid-Hempel, 1998; Nash and Boomsma, 2008). example, obligate social parasites overcome host detection by Social insects have evolved defences that protect their colonies chemical insignificance (i.e., low concentration of recognition cues) against all these intruders. The first line of defence consists in iden- and/or mimicry of the cuticular chemical profiles of their hosts tifying enemies. This occurs by means of olfactory cues on the cuti- (Lenoir et al., 2001; Bagnères and Lorenzi, 2010). These findings cle (Gamboa, 2004; Howard and Blomquist, 2005). The cuticle is indirectly confirm that social insects detect intruders by comparing covered by blends of hydrocarbons that differ among species and the cues in the chemical profiles of the intruders with those of their own colonies. However, we are still far from deciphering how the recognition process works. For example, we do not know which ⇑ Corresponding author. cues are informative, how important cue concentration is and when E-mail address: [email protected] (M.C. Lorenzi). it pays off to be chemically insignificant rather than chemically mi- 1 Current address: School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive Houghton, MI 49931, USA. metic (Bagnères and Lorenzi, 2010). Deciphering the code through 0022-1910/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jinsphys.2012.06.013 1260 A. Uboni et al. / Journal of Insect Physiology 58 (2012) 1259–1264 separate functional analysis of the compounds would be endless previous data on 14 free-living P. biglumis foundresses (collected since the cuticular blends are composed of up to hundreds of com- in Montgenèvre, N = 6 in 1991, N = 8 in 1997) and 5 P. atrimandib- pounds (Blomquist, 2010; Hefetz et al., 2010). However, some stud- ularis social parasites (Montgenèvre, of which 2 ‘‘pre-invasion so- ies have identified the importance of quality and quantity of cial parasites’’ collected before they invaded host nests and 3 cuticular hydrocarbons by separating them into three classes: lin- ‘‘post-invasion social parasites’’ collected 1 month after they in- ear alkanes, branched alkanes, and alkenes. Bonavita-Cougourdan vaded host nests, i.e., when host brood emerge) (Bagnères et al., et al. (1991) and Dani et al. (1996, 2001) found that linear alkanes 1996; Lorenzi and Bagnères, unpublished data). on nest visitors do not provoke a defensive reaction in nest hosts, while branched alkanes and alkenes do. Moreover, the higher the 2.2. Chemical analyses quantity of these complex hydrocarbons is, the stronger the defen- sive reaction of the hosts becomes (Cini et al., 2009). Cuticular compounds of hosts and velvet ants were extracted by The annual colonies of the paper wasp Polistes biglumis Linnaeus separately dipping insects in 1-ml pentane for 60 s. An internal (Hymenoptera: Vespidae) are targeted by cleptoparasites and so- standard (800 ng of n-C20) was added to each extract to quantify cial parasites. Velvet ants Mutilla europaea Linnaeus (Hymenop- compounds. Two microlitres of each extract were analysed by gas- tera: Mutillidae) visit Polistes colonies as cleptoparasites chromatography (GC), using a Delsi Nermag DN200 gas-chromato- (Brothers et al., 2000). In these colonies, velvet ants either eat graph with a flame ionisation detector and a Chrompack CPSIL5 the honey stored in the nest or suck saliva from wasp larvae, and WCOT CB nonpolar capillary-column (25 m  0.25 mm  0.12 lm) P. biglumis larvae are still alive after parasite visits (Uboni, unpub- (15-s splitless injection). Helium was the carrier gas (1 bar). Oven lished data). Velvet ants are parasitoids of Bombus bumblebees temperature increased from 70 to 150 °C (rate: 30°/min). After (Brothers et al., 2000). Female velvet ants enter bumblebee nests, 5 min at 150 °C, oven temperature increased again up to 320 °C lay eggs on host pupae and leave the nests, usually unharmed. (rate: 5°/min) (Galaxie software). Velvet ant compounds were iden- The only residents of bumblebee nests that attempt to stop them tified by GC–MS analysis using a Hewlett-Packard 5890 GC system are the guardians, while the other bumblebees usually ignore vel- coupled with a 5989A Mass Spectrometer (HP chemstation soft- vet ants (Hoffer, 1886). Polistes atrimandibularis Zimmermann ware). Pools of extracts were injected into the GC–MS (temperature (Hymenoptera: Vespidae) invades P. biglumis colonies as a rare, program as above) and compounds were identified by their mass workerless, obligate social parasite (Lorenzi and Thompson, spectra. Each peak corresponded to a compound or a mixture of 2011). It enslaves hosts without fighting and exploits them for compounds. The compounds in the profiles of hosts and social para- rearing its own brood (Cervo et al., 1990). These social parasites sites were determined in previous work (Bagnères et al., 1996; Lore- are initially chemically insignificant and subsequently become nzi et al., 1997). chemically indistinguishable from their hosts. More specifically, The area of each peak was converted to its proportional contri- parasites lose all the alkenes in their cuticular profiles and start bution to total peak area in that sample. This resulted in a matrix of matching their host profiles by producing their same branched al- the relative amounts of 74 peaks that included the chemical pro- kanes. The matching process is reached just before the host brood files of velvet
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