Sexually transmitted parasites and host mating behavior in the decorated cricket

Lien T. Luong 0 1 3 Harry K. Kaya 0 1 2 0 The Author 2005. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions , please 1 ment of Biological Sciences, University of Cincinnati , OH 45221, USA . Received 11 August 2004; revised 14 April 2005; accepted 19 April 2005 2 Department of Nematology, University of California , Davis One Shields Avenue, Davis, CA 95616, USA 3 Department of Entomology Sexually transmitted diseases play a potentially important role in the ecology and evolution of host mating behavior. Here, we use a sexually transmitted nematode-cricket (Mehdinema alii-Gryllodes sigillatus) system to examine the effects of parasitism on host mating activity and female choice. Previous work has shown that infected male crickets produce a significantly smaller nuptial gift (spermatophylax) than uninfected males. This is expected to result in reduced spermatophylax feeding duration and early ampulla removal. Here, we hypothesize that the parasite-mediated reduction in spermatophylax size will consequently shorten female intercopulatory interval. We predict that females mated to infected males will exhibit a shorter intercopulatory interval than females mated to uninfected males. To test this hypothesis, we experimentally measured the behavioral responses of females mated to uninfected and infected males. We found no significant difference between female handling of the spermatophylax and ampulla from infected versus uninfected males. Although the duration of spermatophylax consumption is positively correlated with the duration of ampulla attachment, neither of these variables is correlated with female intercopulatory interval. Intercopulatory intervals for females previously mated with uninfected versus infected males are not statistically different. We conclude that parasitism in male G. sigillatus does not influence female intercopulatory interval or male mating success. We found no evidence for female mate choice based on male infection status. The lack of female choice is consistent with theoretical predictions involving parasites that are sexually transmitted. [Behav Ecol 16:794-799 (2005)] - Simportant role in the ecology and evolution of host exually transmitted diseases (STDs) play a potentially mating systems (Freeland, 1976; Hamilton, 1990; Loehle, 1995; Sheldon, 1993). Sexually transmitted parasites are transmitted via sexual contact, either horizontally or vertically. In the latter, transmission occurs via the zygote. Vertically transmitted agents include plasmids, mitochondria, and some Wolbachia species (Lockhart et al., 1996). Horizontal transmission results from sexual contact between an infected mate and an uninfected partner. Here, we use STDs to refer specifically to horizontally transmitted infections. Given that STDs rely on host mating success for transmission, there is a potential for tight coevolution between sexually transmitted parasites and host reproduction. Conceptual and theoretical studies suggest that STDs can influence the evolution of host mating structures, mating behavior, and secondary sexual characters (Able, 1996; Boots and Knell, 2002; Kokko et al., 2002; Loehle, 1997; Thrall et al., 1997). More specifically, sexually transmitted parasites are expected to favor an increase in host sexual activity, either by altering host mating behavior or by inducing sterility (Lockhart et al., 1996). The outcome would be repeated attempts at mating and hence increased parasite transmission. In a parasite-driven system, selection should favor an increase in host mating success, but not necessarily host reproductive success (i.e., fertility). There are, however, few empirical studies on the effects of a STD on host sexual behavior. Abbot and Dill (2001) found no evidence of parasite-mediated mate choice in Libidomera clivocollis. Likewise, Webberley et al. (2002) found no effect of parasite infection on Adalia bipunctata mate choice and female willingness to mate. The parasite-host system in our study involves a nematode, Mehdinema alii (Nematoda: Diplogasterida), which occurs in the hindgut of the decorated cricket Gryllodes sigillatus (Orthopera: Gryllidae). This nematode is ovoviviparous and produces infective juveniles called dauerlarvae (dauers). M. alii is exclusively sexually transmitted; females harboring dauers transfer the nematodes to males during copulation and vice versa. The propagative stages of the nematode occur exclusively in adult male crickets; thus adult females crickets are refractory to infection (Luong et al., 2000). While other studies have investigated the effect of parasitism on host sexual behavior (Abbot and Dill, 2001; Hurst et al., 1995; Lehmann GUC and Lehmann AW, 2000a,b), the present study is the first to examine such effects from an infection by a sexually transmitted nematode. Moreover, this nematode-cricket system is different from other STDs in that the females do not become infected with the nematode. The female serves only as a vector for nematode transmission, and the nematodes do not develop in her gut, as they do in the male cricket. Most studies on gender differences in infection rates focus on the mechanism for the sex differences (Poulin, 1996; Sheridan et al., 2000; Zuk and McKean, 1996). The male-specific infection in this study system provides an opportunity to examine the ecological and behavioral implications of a sex bias in parasite infection. As in other insects with STDs, the hosts are highly promiscuous, such that both male and female G. sigillatus mate multiple times in their lifetime. At each mating, the female receives a bipartite spermatophore consisting of a spermatophylax and a sperm-containing ampulla. The ampulla is removed by the female after she has consumed the spermatophylax (Sakaluk, 1984). The duration of spermatophylax consumption is positively correlated with the duration of ampulla attachment, which in turn determines the number of sperm transferred to the female spermatheca (Sakaluk, 1984, 1985, 1987). Premature ampulla removal truncates the time for sperm transfer. If insufficient sperm is transferred to fertilize all of the females eggs, the female may soon seek out new mating opportunities. This may in turn result in a decrease in female intercopulatory interval (Gwynne, 1986; Simmons and Gwynne, 1991). Lehmann GUC and Lehmann AW (2000a,b) showed that in bush crickets (Orthoptera: Tettigoniidae) parasitized by a parasitoid fly, females that mated with parasitized males received a smaller spermatophylax. This resulted in shorter intercopulatory intervals compared to females that mated with unparasitized males. In our nematode-cricket system, we expect the parasite to favor an increase in host mating activity. Luong and Kaya (2005) found that male crickets infected with M. alii produced a significantly smaller spermatophylax than uninfected males. Based on these findings, femal (...truncated)