Lovesick: Immunological Costs of Mating of Male Sagebrush Crickets

A growing body of evidence suggests that resources invested in sexual signals and other reproductive traits often come at the expense of the ability to mount an immune response. Male sagebrush crickets, Cyphoderris strepitans, offer an unusual nuptial food gift to females during mating: females chew on the tips of males' fleshy hind wings and ingest hemolymph seeping from the wounds they inflict. Previous research has shown that once a male has mated, his probability of obtaining an additional copulation is reduced relative to that of a virgin male seeking his first mating. One hypothesis to account for this effect is that wing wounding triggers an energetically costly immune response, such that nonvirgin males are unable to sustain the costly acoustical signaling needed to attract additional females. To test this hypothesis, we injected virgin males with lipopolysaccharides (LPS), a non-living component of bacterial cell walls that leads to upregulation of the insect immune system. Males were released in the field and recaptured over the course of the breeding season to monitor their mating success. Over two breeding seasons, LPS-injected males took significantly longer to secure matings than sham-injected virgin males. An encapsulation rate assay showed no difference in the encapsulation response of males of different mating status, but virgin males had significantly higher levels of phenol oxidase than non-virgin males. These results suggest that males trade off investment in reproduction and investment in immunity. INTRODUCTION The sagebrush cricket, Cyphoderris strepitans, is one of only seven extant species of a relatively unknown orthopteran family, the hump-winged grigs (Haglidae) (Kumala et al. 2005). C. strepitans occurs exclusively in high-altitude sagebrush meadows in mountainous areas of Colorado and Wyoming (Morris and Gwynne 1978). Mating occurs in the late spring after the snow melts. Males climb into sagebrush or lodgepole pine shortly after sunset to secure a perch, from where they emit acoustical signals that function to attract females (Snedden and Irazuzta 1994) and appear to be the primary means of pair formation (Snedden and Sakaluk 1992). Copulation is initiated when a female climbs onto the dorsum of the male, at which time he attempts to transfer a spermatophore, a small gelatinous packet containing sperm. During copulation, the female feeds on the male's fleshy hind wings and the hemolymph that oozes from the wounds she inflicts. After the spermatophore has been transferred, the male actively pulls away from the female, terminating wing feeding (Eggert and Sakaluk 1994). Virgin males secure more matings than their relative abundance in the population would predict, a population wide pattern that has been described as the "virgin-male mating advantage" (Morris et al. 1989; Snedden 1996). Mating appears to be costly to males: not only do they lose a significant portion of their hind wing tissue and hemolymph, they must also produce another spermatophore if they are to mate again. Previous work has shown that non-virgin male calling time is reduced relative to virgin males (Sakaluk et al. 198 7; Sakaluk and Snedden 1990). Given the importance of calling in pair formation and the marked 1 Lehman et al.: Lovesick: Immunological Costs of Mating of Male Sagebrush Cricket Published by Wyoming Scholars Repository, 2008