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Immune Function Reflected in Calling Song Characteristics in a Natural ANIMAL BEHAVIOUR, 2005, 69, 1235–1241 doi:10.1016/j.anbehav.2004.09.011 Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus LEIGH W. SIMMONS*,MARLENEZUK† &JOHNT.ROTENBERRY† *Evolutionary Biology Research Group, School of Animal Biology (M092), The University of Western Australia yDepartment of Biology, University of California, Riverside (Received 9 February 2004; initial acceptance 30 March 2004; final acceptance 24 September 2004; published online 17 February 2005; MS. number: 7999R) Secondary sexual traits have been suggested to provide reliable signals of a male’s ability to resist infection by agents of disease. The immunocompetence handicap hypothesis provides a potential mechanism for reliable signalling in the form of a trade-off between expenditure on trait expression and expenditure on immunity. Thus, males resistant to disease can spend more resources on their sexual signals. Examination of calling song parameters in a natural population of the cricket Teleogryllus commodus revealed that males scoring higher on the third principal component for song had significantly lower ability to encapsulate a foreign object. This component of immune function was associated with syllables of longer duration in both the trill and chirp elements of the song. Males with longer syllables in their song had a lower encapsulation ability. Syllable duration is known to influence phonotaxis by female T. commodus. Although the effect was only weak, our data suggest that females may base their choice of mate on reliable information contained within the temporal properties of male calls. Our study thus demonstrates a connection between sexual signalling and immune function in a natural population of insects and lends support to the immunocompetence handicap hypothesis. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Theory suggests that male secondary sexual traits can between testosterone and immune response is weak become condition dependent, and that females can gain (Roberts et al. 2004). indirect genetic benefits for their offspring by using Insects possess a less complex immune system than secondary sexual traits to choose mates of high quality vertebrates, but none the less may demonstrate both (Andersson 1994). Secondary sexual traits are assumed to condition dependence of secondary sexual traits and a cost carry a cost to their bearer, so that males of low condition of mounting and maintaining an immune response (Rolff cannot invest in trait development (Kotiaho 2001). A par- 2002). Juvenile hormone has a dualistic effect on sexual ticularly compelling aspect of condition is resistance to signalling and immunosuppression suggesting that it may disease, and several recent studies have found that be the hormonal analogue to testosterone that maintains secondary sexual traits are both costly to produce and honesty in insect sexual signalling (Rantala et al. 2003b). reflect either parasite infection or immune function (e.g. Insects are increasingly popular subjects for studies in Blount et al. 2003; Faivre et al. 2003). In vertebrates, the ecological immunology (Rolff & Siva-Jothy 2003). An causal link underlying honest signalling is thought to be advantage to using insects is that they lack a well- the dualistic effect of testosterone on secondary sexual developed immunological memory (Vass & Nappi 2001), trait expression and immunosuppression; only males able so that there is less risk of confusing prior exposure with to resist disease can afford to downregulate their immune resistance; individuals that exhibit a strong response to an systems and develop exaggerated sexual traits (Folstad & antigen cannot merely be indicating a past exposure to Karter 1992). While these arguments are compelling, the agent. Secondary sexual traits such as wing pigmen- a recent meta-analysis suggests that in general the link tation in damselflies (Siva-Jothy 1999, 2000; Rantala et al. 2000), courtship song in field crickets, G. bimaculatus Correspondence: L. W. Simmons, Evolutionary Biology Research Group, (Rantala & Kortet 2003), calling song in house crickets, School of Animal Biology (M092), The University of Western Australia, Acheta domesticus (Ryder & Siva-Jothy 2000), and pher- Nedlands 6009, Australia (email: [email protected]). omones of mealworm beetles, Tenebrio molitor (Rantala M. Zuk and J. T. Rotenberry are at the Department of Biology, et al. 2003a), all show correlations with female preference University of California, Riverside, CA 92521, U.S.A. and male immune function. Furthermore, in scorpionflies, 1235 0003–3472/04/$30.00/0 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 1236 ANIMAL BEHAVIOUR, 69, 6 Panorpa vulgaris, males producing more salivary masses body cavity through the wound. The surface of the during courtship are preferred by females and have a monofilament was roughened with sandpaper before use higher immune function that is inherited by their off- to enhance the likelihood that haemocytes would stick to spring (Kurtz & Sauer 1999). the implant. After implantation each cricket was housed Although studies of damselflies and dragonflies have individually in a 130-ml plastic vial with dry cat food and assessed immune function in natural populations (Rantala water ad libitum. All crickets recovered from the cold et al. 2000; Siva-Jothy 2000; Rolff 2001), studies of anaesthesia and continued to feed and behave normally. immunity and sexual signalling in crickets have been There was no mortality associated with the procedure. confined to laboratory populations that are highly un- Crickets were frozen 36 h after implantation. likely to be exposed to the types of parasites and diseases The implant was dissected from the body cavity and normally encountered in nature. Thus, it is not clear cleaned with 70% ethanol. It was then placed in a cavity whether laboratory findings can be extrapolated to natural slide, fixed with mounting medium (Eukitt) and covered populations. We examined immune function in a field with a cover slip. To measure the degree of encapsulation, population of Teleogryllus commodus, a common field we photographed each implant with a digital camera cricket of southern Australia that is subject to numerous attached to a microscope and analysed the photograph micro- and macroparasites, ranging from fungi to parasit- using NIH Image software (http://rsb.info.nih.gov/nih- oid wasps (Reinganum et al. 1981). Like other crickets, image/). The program provides a measurement of the T. commodus produces a calling song to attract females mean grey scale of the pixels contained in a designated (Evans 1983, 1988), and laboratory studies have charac- area, with 0 being completely white and 256 being terized the qualities of the male song that elicit the completely dark. To control for variation in the colour of strongest female response (Hennig & Weber 1997). To the mounting medium, we compared the outlined area of measure immune response in the field, we assayed the implant with an identical area in the same slide next encapsulation ability (Nappi & Vass 1993; Gillespie et al. to the implant. The measurement used was the mean 1997) by quantifying the degree to which implants of darkness of the implant minus the mean darkness of the nylon monofilament were encapsulated with melanized control area. Melanization is closely linked to disease haemocytes. This is a standard technique for examining resistance and immunity in insects (Nappi & Vass 1993; insect immunity (Ko¨nig & Schmid-Hempel 1995; Stolen Barnes & Siva-Jothy 2000; Wilson et al. 2001). Further- et al. 1995; Rantala et al. 2000, 2003a; Doums et al. 2002; more, the degree of melanization of encapsulating hae- Rantala & Kortet 2003). It mimics the effects of a parasitoid mocytes is positively correlated with other measures of or other foreign object that is introduced into the body immune function, such as the density of circulating cavity, but because the implant is inert, it does not have haemocytes (Rantala et al. 2000) and phenoloxidase any pathogenic effects itself. By recording songs of males activity (Rantala et al. 2002). in the field and then immediately assessing immune During dissection, the body cavity and gut were response, we were able to determine whether songs could checked thoroughly for the presence of macroparasites. reflect immunity under natural conditions and hence be None were found. used by females as an indication of disease resistance. Correlations with Other Immune Parameters METHODS To confirm that the degree of melanization of encapsu- Cricket Collection and Song Recording lating haemocytes was a reliable measure of general Crickets were collected in March 2001 near Walpole in immune function in T. commodus, we collected a random south Western Australia. Calling males were localized by ear sample of 39 male and 29 female crickets in April 2004 and recorded using a Sony Professional Walkman. Record and returned them to the laboratory for immune function levels were standardized at C3 dB peak with the micro- assays. For each individual we measured the encapsulation phone held 10 cm from the calling male. We obtained response as described above. At the time of monofilament several minutes of continuous calling from each male, and implant, a 2-ml sample of haemolymph was withdrawn recorded the temperature at the time of recording by and placed directly into 18 ml of anticoagulant (Mead et al. m placing a thermometer in the grass within 1–2 cm of the 1986) and mixed. A sample of 8 l of haemolymph was calling cricket. Crickets were collected immediately after then placed on to each side of a Neubauer haemocytom- recording and used for immune assays. eter and left to settle for 5 min. Haemocytes were counted in five nonadjacent squares under 200! magnification. Total counts were multiplied to find the number of cells Melanization Assay of Encapsulation Response per ml of haemolymph. We also assayed levels of lysozyme-like activity of Crickets were cold anaesthetized by placing them in samples of haemolymph. An autoclaved agar solution a freezer for 2 min.
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