Behavioral Ecology Advance Access originally published online on May 25, 2005
Behavioral Ecology 2005 16(4):794-799; doi:10.1093/beheco/ari056
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Sexually transmitted parasites and host mating behavior in the decorated cricket
a Department of Entomology, and b Department of Nematology, University of California, Davis One Shields Avenue, Davis, CA 95616, USA
Address correspondence to L.T. Luong, who is now at the Department of Biological Sciences, University of Cincinnati, OH 45221, USA. E-mail: luongl{at}email.uc.edu.
Received 11 August 2004; revised 14 April 2005; accepted 19 April 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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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.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexually transmitted diseases (STDs) play a potentially important role in the ecology and evolution of host 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 female's 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, females that mate with infected males are expected to receive a smaller spermatophylax than females that mate with nematode-free males. A smaller spermatophylax should result in reduced spermatophylax feeding duration and hence early ampulla removal (Sakaluk, 1984). In other orthopteran species (Tettigoniidae), the duration of ampulla attachment is correlated with female intercopulatory interval (Gwynne, 1986; Wedell, 1994; Wedell and Arak, 1989). In the present study, we expect that females mated to parasitized males will exhibit a shorter intercopulatory interval than females mated to uninfected males.
However, if this were a host-driven system, we would expect the female cricket to avoid mating with infected males to avoid either infection or the cost of mating with a genetically susceptible male (Able, 1996; Loehle, 1997). This may be important if she can distinguish between infected and uninfected males. Female choice can manifest itself in two ways: females might (1) avoid copulating with infected males or (2) copulate indiscriminately with regard to male infection status but exercise "cryptic" choice postcopulation (Sakaluk and Eggert, 1996). That is, the female may preferentially remove the spermatophylax and ampulla of infected males prior to complete insemination. Alternatively, the female may immediately mate with another male to "dilute" the sperm from the undesirable mate. Incomplete insemination can reduce the numerical competitiveness of a male's ejaculate (Parker, 1970; 1984; Sakaluk, 1986).
Evolution for parasite-mediated female choice, however, may be weak in this system because mate avoidance has the potential to reduce parasite fitness. Given that sexually transmitted parasites rely on host mating success for transmission, we would expect the parasite to favor reduced disease detection by mates. Theoretical models have suggested that evolution of female choice may be weak where STDs are involved (Knell, 1999). This alternative hypothesis predicts no female preference with regard to male infection status.
Alternatively, females may preferentially mate with infected males as an adaptive strategy. Because the nematode is sexually transmitted, males with a high parasite load are likely to have been successful at mating. By mating with an infected male, the female potentially acquires those genes associated with high mating success for her offspring. This hypothesis (as suggested by the reviewer) predicts that females would actually prefer to mate with infected males.
Our aim was to investigate the relationship between male infection status and female mating behavior in the decorated cricket. We used laboratory experiments to determine whether the nematode infection in male crickets had an effect on the fate of the spermatophore and female latency to remate. We also examined the female's willingness to mate and mating preference with respect to nematode infection in males.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1
Adult decorated crickets, G. sigillatus, were collected from the campus of the University of California, Davis. The prevalence of infection with M. alii nematodes among adult males in this population is approximately 69% (cf. 68%, Luong et al., 2000
). Nymphs were reared in separate containers to ensure nematode-free conditions. Late-instar males and females were separated to ensure virginity. All crickets were maintained in shoebox-size (30 cm x 11 cm x 16 cm) plastic containers at 28°C and 30% relative humidity. All crickets were kept under a reversed 12:12 h light:dark photoperiod cycle. Crickets were provisioned with water and cat food (Purina Cat Chow, St. Louis, MO) ad libitum. Experimental crickets were dissected in 0.1 M NaCl (saline), and their degree of nematode infection was measured by counting the number of mature nematodes in the hindgut under a dissecting microscope.
Male crickets were naturally infected by housing a single naive (unmated, nematode-free) male with three adult females and three adult males collected from the field. Experimental males were approximately 1–2 weeks posteclosion. The size of the males was controlled by selecting individuals of similar size by sight. Because field-caught crickets are likely to be infected with the nematode, this setup allowed for nematode transmission to take place under seminatural conditions. Previous attempts at establishing infections using only field-caught females yielded low infection rates (see Luong and Kaya, 2005). Because there was no way to determine a priori if a male would actually acquire the nematode infection, excess males (n = 44) were set up for infection. Uninfected males (n = 32) were established in a similar manner, except a naive male that was housed with nematode-free, nonvirgin males and females. Both uninfected and putatively infected males were marked with spots of either white or green "liquid paper" (Paper-Mate, Oak Brook, IL) on the pronotum for identification.
After a period of 7 days, all field-caught males were removed to ensure that any remaining dauers in the females would be transmitted to the experimental male. All field-caught females were removed on the 12th day. On day 14, uninfected and putatively infected males were each allowed access to a virgin female (2–3 weeks posteclosion), without food or water. Thus, there were two sets of females, those mated to uninfected males and those mated to putatively infected males. Behavioral observations were conducted 4 h into the dark photoperiod and lasted 6 h. A shaded window dimly lighted the observation room.
We compared the effect of nematode infection on (1) female's willingness to mate (time elapsed from onset of courtship to copulation), (2) the duration of copulation, and (3) the fate of the spermatophylax and ampulla. Once the first successful mating was complete and the female had removed the ampulla, the experimental male was replaced with a virgin male (1–2 weeks posteclosion). The virgin male was checked for presence of a spermatophore (indication of readiness to mate) before introducing him into the arena with the female. Once the second male initiated courtship calling, the time elapsed for the female to select and mate with the male was recorded as the female intercopulatory interval.
Experiment 2
Treatment (n = 30) and uninfected (n = 30) males were established in the manner described above. Given that parasitism affected spermatophylax size more in small males than in larger males (Luong and Kaya, 2005), small males (<300 mg) were selected to improve the probability of detecting a treatment effect. On the 14th day, both an infected (putative) and an uninfected male were placed in an observation arena with a randomly selected, previously mated female (1–2 posteclosion). Previously mated females were used instead of virgin females to account for the possible effects of mating history on the level of mate discrimination. No assumptions were made about how females assess males.
A male was deemed the preferred mate once the female mounted and initiated copulation with him. Males that failed to initiate courtship were excluded from the test. Female willingness to mate and duration of spermatophylax consumption and ampulla attachment were also recorded. The males were held until the next day, at which time the spermatophylax of each male was extracted and weighed on a Mettler AE50 balance, with an accuracy of ±0.2 mg. This is a reliable method of estimating spermatophylax size at the time of mating because spermatophylax mass shows significant repeatability within males (Sakaluk, 1985).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1
In the first experiment, 30 of the 44 treatment males became infected with the nematode, herein referred to as "infected" males. Treatment males that failed to acquire the nematode infection were excluded from analysis. The mean intensity of infection was 14.3 ± 16.9 adult nematodes/male. All the 32 uninfected males were confirmed to be nematode free. Both uninfected males (68.8%) and infected males (83.3%) mated successfully with a female (Table 1). This difference in mating success was not statistically significant (Fisher's Exact test, p = .24).
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Successful mating attempts (Table 1) resulted in one of three possible outcomes for the spermatophylax. In some instances, the spermatophylax was immediately removed and subsequently fully consumed by the female (females mated with uninfected males = 21.9%, females mated with infected males = 36.7%). Sometimes, the female only ate part of the spermatophylax before abandoning the remains (uninfected = 40.6%, infected = 36.7%). In a few cases, the female dislodged the spermatophylax without eating any part of it (uninfected = 6.3%; infected = 10%).
Failure to mate successfully occurred for various reasons. (1) The female mounted the male but aborted the mating prior to spermatophore transfer (uninfected males = 3.1%, infected males = 10%). (2) The spermatophore failed to attach properly to the female postcopulation (uninfected males = 12.5%, infected males = 6.7%). (3) The ampulla was removed simultaneously with the spermatophylax (uninfected males = 15.6%, infected males = 0%). Note that a failed mating event does not necessarily translate into failure to transmit the nematode. Nematode transmission occurs only during copulation, specifically, when the male phallus hooks onto the female subgenital plate, the initial phase in spermatophore transfer (Luong et al., 2000). So, even if the spermatophore itself failed to transfer, nematode transmission may still have taken place.
The duration of spermatophylax consumption was significantly correlated with the ampulla attachment time for both females paired with uninfected (r = .463, p = .03, Figure 1a) and infected males (r = .540, p = .004, Figure 1b). However, the duration of spermatophylax consumption by the female was not significantly correlated with female intercopulatory interval for either uninfected (r = –.095, p = .67) or infected (r = .009, p = .96) males. There was no significant association between the duration of ampulla attachment and female intercopulatory interval for either the uninfected (r = –.055, p = .80) or infected (r = –.139, p = .51) group.
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For the five behavioral parameters we measured (Table 2), there were no statistically significant differences between females that mated with uninfected males and females that mated with infected males. Male infection status was not significantly associated with time to first mating attempt (ANOVA with log10 transformation, F1,56 = 0.40, p = .53). Thus, female willingness to mate was not affected by male infection status. The duration of copulation (ANOVA with log10 transformation, F1,49 = 0.21, p = .65), duration of spermatophylax consumption (ANOVA with square-root transformation, F1,50 = 2.30, p = .14), and duration of ampulla attachment (ANOVA with square-root transformation, F1,49 = 1.87, p = .18) did not differ significantly between the two groups. Female intercopulatory interval (ANOVA with log10 transformation, F1,46 = 1.19, p = .28) was also not influenced by male infection status.
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The intensity of infection (including uninfected males: 0 nematodes) was not significantly correlated with duration of spermatophylax consumption (Spearman rank test, r = .199, p = .16), duration of ampulla attachment (r = .152, p = .29), or female intercopulatory interval (r = .027, p = .86).
Experiment 2
All uninfected males were confirmed to be nematode free. Eighteen of the 30 treatment males acquired the nematode infection. In these males, the mean intensity of infection was 10.8 ± 13.9 nematodes/male (range: 1–55). The mean weight for uninfected males was 273.3 ± 29.5 mg and 293.6 ± 36.9 mg for infected males. This difference in mean body weight was not statistically significant (F1,10 = 1.11, p = .32). Infected males produced a significantly smaller spermatophylax than uninfected males (uninfected = 5.99 ± 0.58, infected = 5.07 ± 0.90 mg; F1,20 = 8.43, p = .009; cf. Luong and Kaya, 2005).
Female willingness to mate was not significantly different for females paired with either uninfected or infected males (ANOVA with log10 transformation, F1,16 = 0.16, p = .69). The mean (back-transformed) time to mate of females paired with uninfected (n = 8) and infected (n = 10) males was 3.77 min (95% confidence interval [CI]: 1.30–10.89) and 4.86 min (95% CI: 1.83–12.85), respectively (the CIs have also been back-transformed to the original scale). The probability of a successful mating outcome did not differ significantly between the two groups (females paired with uninfected males = 50%, females paired with infected males = 60%, Fisher's Exact test, p = 1.00).
The observed reduction in spermatophylax size did not influence the duration of spermatophylax consumption, which was not significantly different between females paired with uninfected (48.6 ± 41.0 min, n = 4) and infected (39.8 ± 28.6 min, n = 5) males (F1,7 = 0.15, p = .71). The 95% CI for females paired with uninfected males ranges from –16.6 to 113.8, and for females paired with infected males it ranges from 4.24 to 75.4, reflecting the large variability in spermatophylax consumption times. The mean duration of ampulla attachment (uninfected = 58.9 ± 44.6, n = 4, CI = –8.3–156.62; infected = 48.2 ± 27.4, n = 5, CI = 15.8–84.7) was not significantly different for the two groups (F1,7 = 0.20, p = .67). These results are consistent with those observed in Experiment 1. In some cases, data on spermatophylax consumption and ampulla attachment were absent due to failure of spermatophore transfer during copulation, as in Experiment 1.
We observed no female mate preference with regard to male infection status. We excluded those trials in which the treatment male failed to acquire the nematode. Of the 18 trials in which the treatment male was infected, the female chose to mate with the uninfected male on 8 occasions and with the infected male on 10 occasions. Thus, females were just as likely to mate with an uninfected male as with an infected male (binomial test, p = .81). The 95% CI for the proportion of females preferring uninfected males is 0.22–0.69 and 0.l3–0.78 for females preferring infected males. Thus, there was no detectable difference in preference for either uninfected or infected males.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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While the durations of spermatophylax consumption and ampulla attachment were positively correlated, we found no association between either of these variables and female intercopulatory interval. Parasitism in males had no effect on female (1) spermatophylax consumption time, (2) ampulla attachment time, or (3) intercopulatory interval. We also found no significant effect of male infection status on male mating success or female willingness to mate. There was no evidence of female mate preference for uninfected versus infected males. As a result of the high degree of variability in the intercopulatory intervals, the CIs in this experiment were very wide. Overall, however, there was no suggestion of a consistent trend towards a difference between infected and uninfected males. Interestingly, the mean duration of spermatophylax consumption and ampulla attachment were both higher for females paired with infected than uninfected males (Table 2), which is in the opposite direction than initially predicted.
The positive correlation between spermatophylax consumption and ampulla attachment time, for both uninfected and infected males, is consistent with those reported by Sakaluk (1984). In most cases, the spermatophylax apparently served to deter the female from removing the ampulla prematurely. However, on many occasions, the female did not fully consume the spermatophylax. Sakaluk (1984, 1985, 1987) found that females do not fully consume the spermatophylax approximately 50% of the time. Furthermore, the dropped spermatophylaxes were generally larger than those fully consumed (Sakaluk, 1985). Kodrick-Brown and Brown (1984) suggested that female crickets may be able to assess males based on the quality rather than quantity of the nuptial gift; thus, females may be able to assess the quality of the spermatophylax without consuming it entirely. Alternatively, females may simply have been satiated, as the case may be in this experiment because females had access to food on days prior to observation.
Given that premature ampulla removal terminates sperm transfer (Sakaluk, 1984), we also predicted a correlation between spermatophylax consumption (and/or ampulla retention) and female intercopulatory interval. However, we found no association between the duration of spermatophylax feeding or ampulla retention and female intercopulatory interval. Fleischman and Sakaluk (2004) also found no effect of spermatophore (ampulla only) attachment on female remating interval in the house cricket, Acheta domestica. In our study, this was the case for both trials involving uninfected males and trials involving infected males.
The lack of association between spermatophylax retention and female remating interval, along with the lack of an effect of male parasitism on the duration of spermatophylax consumption, has some bearing on our initial prediction. Contrary to our expectations, the female G. sigillatus remating interval did not differ significantly between females that mated with an infected male and females that mated with an uninfected male. Despite previous evidence of parasite-mediated reduction in spermatophylax size (Luong and Kaya, 2005), parasitism in the males had no effect on female latency to remate. Unfortunately, the rationale for this prediction was based on specific assumptions that did not come to bear in this experiment.
In Experiment 1, the effect of parasitism on female postcopulatory behavior may have been masked by male body size. Previous studies have shown that spermatophylax weight is significantly correlated with male body size (Sakaluk and Smith, 1988). Furthermore, the parasite-mediated reduction in spermatophylax size is more apparent in smaller males (Luong and Kaya, 2005). Perhaps a difference in female postcopulatory behavior would have been more evident if we had used only small males in the experiments rather than males of median size. Because the females used in the first experiment were 2- to 3-week-old virgins and hence sperm deprived, they may have been less choosy in selecting their mates. However, the protocol was modified in Experiment 2 to account for the potential influence of male size and female mating history. While these conditions were expected to produce the strongest treatment effect, that is, to maximize the sensitivity of our assay, we still found no effect of parasitism. Therefore, we conclude that there really is no effect of parasitism in this case.
It may be that we were unable to detect any differences in female intercopulatory interval because females in both groups remated much sooner than they would under natural conditions. The experimental setup, in which a virgin female was confined in a small observation arena with two males, may be particularly conducive to reduced latency to remate. Indeed, Calos and Sakaluk (1998) noted that females in nature mate less than once per night. Therefore, future studies on the Gryllodes-Mehdinema system should account for the potential influence of limited female access to males and female mating experience on female latency to remate.
The lack of female mate choice in Experiment 2 may simply be due to an inability to detect or assess male infection status, which may be particularly relevant in the nematode-cricket system because both the dauer and adult stages of the nematode are situated internally. However, STDs are predicted to evolve reduced virulence; at low virulence, parasites are less detectable, and the selective advantage for detection by the female is reduced (Knell, 1999). Moreover, sexually transmitted parasites should select against hosts developing indicators of infection as this would result in avoidance and hence nontransmission (Knell, 1999; Kokko et al., 2002).
Given that females did not discriminate against parasitized males, the cost of parasitism to the male is minimal or perhaps nil. In addition, infected males do not experience increased mortality or reduced progeny production (Luong and Kaya, unpublished data). There may, however, be subtle costs of infection that are undetectable under laboratory conditions. Future studies should consider the impact of parasitism under conditions of stress, such as crowding, starvation, dehydration, and/or costs association with acquiring mates.
One possible explanation for our failure to detect an effect of parasitism on female intercopulatory interval is that the decorated crickets have a highly promiscuous mating system, so there is ample opportunity for nematode transmission. In addition, the dauers can persist for a long period of time in the female (Luong and Kaya, 2002). The outcome is apparently weak selection on the part of the parasite to manipulate host mating behavior, that is, to enhance transmission. The extent to which conflict arises between the host mating behavior and nematode transmission should be minimal.
Because the female crickets serve only as a vector for nematode transmission, there is no direct cost of multiple mating attempts. It is likely that the benefits to females of mating with multiple males, regardless of parasite infection, outweigh any potential costs of mating with a susceptible male. The evolutionary outcome for this system may differ slightly from standard STDs in which both males and females are at risk of infection. Further investigations are needed to fully understand the evolutionary implications of sexually transmitted parasites, particularly among natural populations of invertebrate hosts.
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ACKNOWLEDGEMENTS |
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We would like to thank Ann Hedrick, Jay Rosenheim, the editor, and two anonymous referees for their comments. We also thank Hien Trinh for her assistance in the care and maintenance of the cricket colony.
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