Articles Female spotted cucumber beetles use own cuticular hydrocarbon signature to choose immunocompatible mates Jared G.Ali a , * , Douglas W.Tallamy b, 1 a Department of Entomology & Nematology, University of Florida b Department of Entomology & Wildlife Ecology, University of Delaware a r t i c l e i n f o Article history: Received 4 May 2009 Initial acceptance 22 June 2009 Final acceptance 12 March 2010 Available online 21 April 2010 MS. number: A09-00286 Keywords: Chrysomelidae cuticular hydrocarbon Diabrotica female choice immunocompetence immunocompatibility spotted cucumber beetle Using spotted cucumber beetles and their epicuticular hydrocarbon signatures,we examined two hypotheses about how females may use signals that describe a potential mate’s immune system to identify high-quality males. Females may find males to be acceptable mates when (1) a male’s immune system complements or matches the immune system of the receptive female (immunocompatibility), or (2) a male successfully signals that it has a strong immune system (immunocompetence). The first experiment used gas chromatography to compare the epicuticular hydrocarbon signature of a female beetle with that of a male she rejected and a male she accepted as a mate. We also compared the hydrocarbon signatures ofa male and two fertilized females,one that had voluntarily accepted his spermatophore and one that was forced to accept the spermatophore. In both experiments the immune response to an implant inserted in the insect’s abdomen was compared in males and their offspring. The hydrocarbon signature of males accepted as mates in the first experiment differed more from that of their female partners than did the hydrocarbon signature of rejected males. There was no significant difference in the immune response of accepted and rejected males. Offspring from forced matings had significantly lower immune responses than offspring from voluntary matings. This study suggests that females use immunocompatibility rather than immunocompetence as a trait to identify quality mates, which fosters stronger immune systems in offspring. Female choice ofmates in this species may be self-referenced using the cuticular hydrocarbon signature of the female as a standard. Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Many insects use volatile or contact pheromones(odours), typically composed of long-chain fatty acid derivatives located on the surface of the insect’s cuticle, in several forms of communication (Tregenza & Wedell 1997; Ginzel et al. 2003; Howard & Blomquist 2005). Male cuticular hydrocarbons can serve as cues that communicatestatus, symmetry, parasite/pathogen load,mate recognition,and the quality of a male’s immune system (Howard 1993; Blomquist et al. 1996; Fukaya et al. 1996, 1997, 2000; Wang 1998; Ginzel et al. 2002, 2003), while hydrocarbons found on a female’s cuticle can be responsible for inducing male courtship behaviour (Ginzel et al. 2003). Many male insects exhibit traits that have been correlated with the quality of the immune system, including wing pigmentation in damselflies (Siva-Jothy 2000; Rantala et al. 2000), courtship song in field crickets, Gryllus bimaculatus (Rantala & Kortet 2003) and house crickets, Acheta domesticus (Ryder & Siva-Jothy 2000), pheromones of mealworm beetles, Tenebrio molitor (Rantala et al. 2003), and salivary mass in the scorpionfly, Panorpa vulgaris (Kurtz & Sauer 1999). There are two hypotheses that describe the role of the immune system in mate choice (Jennions & Petrie 2000). To be an acceptable mate, (1) males must complement or match the immune system of the female (immunocompatibility; Zeh & Zeh 1996; Jennions & Petrie 2000) or (2) males must demonstrate that they have a strong immune system (‘good genes’), regardless o how their immune system compares to that of the female (immunocompetence; Andersson 1994; Jennions & Petrie 2000). Female discrimination in spotted cucumber beetle, Diabrotica undecimpunctatahowardi Barber (Coleoptera: Chrysomelidae) begins after intromission. Behavioural observations and dissections of beetles flash-frozen during copulation reveal that a male in copula will stroke the female with his antennae until the female relaxes her vaginal duct muscles, allowing the male’s aedeagus to penetrate into the female’s bursa copulatrix (Tallamy et al. 2002, 2003).Once the male gains access to the bursa, he immediately stops antennal stroking, and angles his antennae posteriorly over his elytra. He then begins to pulsate his abdomen slowly as he transfers his spermatophore. Spermatophore transfer only occurs * Correspondence: J. G. Ali, Departmentof Entomology & Nematology, Citrus Research and Education Center, University of Florida, 700 Experiment Station Road, Lake Alfred,FL 33850-2299, U.S.A. E-mail address: jgali@ufl.edu (J.G. Ali). 1 D. W. Tallamy is at the Department of Entomology & Wildlife Ecology, University of Delaware, 250 Townsend Hall Newark, DE 19716-2160, U.S.A. Contents lists available at ScienceDirect Animal Behaviour j o u r n a l homepage: w w w . e l s e v i e r . c o m / l o c a t e / a n b e h a v 0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.03.014 Animal Behaviour 80 (2010) 9e12