J. Parasitol., 89(3), 2003, pp. 516–521 q American Society of Parasitologists 2003
EFFECTS OF TAPEWORM INFECTION ON MALE REPRODUCTIVE SUCCESS AND MATING VIGOR IN THE RED FLOUR BEETLE, TRIBOLIUM CASTANEUM Aditi Pai and Guiyun Yan Department of Biological Sciences, State University of New York at Buffalo, Buffalo, New York 14260. e-mail:
[email protected] ABSTRACT: Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male–male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14–22% even when male–male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.
Parasites are ubiquitous in nature and exert negative effects on host survivorship and reproductive success. Infected hosts often exhibit reduced fecundity (Yan et al., 1994; Yan and Stevens, 1995; Thomas, Gente et al., 1999; Hurd et al., 2001), poor body condition (smaller pectoral fin size in male three-spined stickle back [Bakker and Mundwiler, 1999], lower mass and comb size in male junglefowl [Zuk et al., 1998]), and reduced male competitiveness (Thomas, Oget et al., 1999). Because of such effects, they are thought to have an important role in sexual selection (Hamilton and Zuk, 1982). The effects of parasites on individual hosts can be reverberated to population dynamics and community structure (Hudson et al., 1992; Jaenike, 1992). The effects of parasites on populations depend on the magnitude of negative fitness consequences of parasites on both female and male hosts. The effects of parasites on female host fitness can be determined simply by measuring fecundity and are well documented (for example, Yan and Stevens, 1995; Thomas, Gente et al., 1999). However, the effects of parasites on the fitness of males and particularly the underlying mechanisms that lead to change in reproductive success of male hosts are not well understood. The present study used the rat tapeworm (Hymenolepis diminuta) and the red flour beetle (Tribolium castaneum) as a model system to determine the consequences of parasite infection on male reproductive success. Tribolium castaneum is an intermediate host of H. diminuta. In nature, the adult parasite lives in the lumen of the small intestine of rats, where the eggs are produced and passed out with the host’s feces. Cysticercoid development takes place when the eggs are ingested by intermediate hosts, often grain-infesting species such as Tribolium and Tenebrio. Thus, this parasite cannot be horizontally or vertically transmitted. Tapeworm infection reduces female fecundity by 11–17% (Yan et al., 1994; Yan and Stevens, 1995) and male sperm precedence by up to 13% (Yan and Stevens, 1995). However, it is not clear whether the reduction in male sperm precedence is caused by reduced male reproductive vigor, reduced attrac-
tiveness of infected males to females before copulation, reduced sperm competitiveness or by differential use of sperm by females after copulation. Adult beetles infected with tapeworms exhibited a 2- to 22fold increase in the secretion of defensive compounds but no significant reduction in aggregation pheromone (Yan and Phillips, 1996). Parasite-induced alterations in the production of the defensive compounds may have significant consequences for host mating behavior because female beetles exercise precopulatory mate choice based on male pheromone (Boake, 1985, 1986; Lewis and Austad, 1994). In addition, female red flour beetles show postcopulatory mate choice (Lewis and Austad, 1994; Edvardsson and Arnqvist, 2000). Edvardsson and Arnqvist (2000) demonstrated that females manipulate paternity of offspring based on their perception of male quality as determined by the vigor of male copulatory courtship. Thus, infection may have important consequences for sexual selection if females discriminate against infected males before copulation (based on pheromone cue) or after copulation (based on vigor of copulatory courtship). Yan and Stevens (1995) demonstrated that tapeworm infection reduced male reproductive success by 43% under the condition of high intraspecific competition. Reduction in male fitness could be caused by the direct effects of parasite infection and intrasexual competition (before or after copulation), intersexual selection (female choice against infected individuals), or both. The aim of the present research is to discern the underlying mechanisms of fitness effects of tapeworm infection on male T. castaneum. We examined the fitness effect of parasite infection on male red flour beetles in the absence of sperm competition by comparing reproductive success (measured by offspring production) and reproductive vigor (measured by number of females inseminated and offspring production) of infected and uninfected males. Also, we determined whether infection reduces attractiveness of the male to females by measuring the response to male pheromone and by observing copulatory courtship of infected and uninfected males. These data allow us to determine whether female choice plays a role in reducing infected males’ fitness.
Received 10 August 2002; revised 26 December 2002; accepted 26 December 2002. 516
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MATERIALS AND METHODS Beetle rearing The cSM strain of T. castaneum was used for all experiments (see Wade, 1977 for strain origin). Male and female pupae were sexed to ensure virginity of adults. Beetles were raised in 8-dram shell vials containing 5 g standard medium (95% by weight fine, sifted whole wheat flour and 5% yeast). Vials were maintained in a dark incubator regulated at 29 C and 70% relative humidity. Black female and red male beetles were used in all experiments to facilitate distinguishing male and female beetles (Pai and Yan, 2002a). Tapeworm infection Beetle infections followed the method described in Yan et al. (1994). Briefly, beetles at the age of 1 wk postemergence were starved for 1 wk and exposed to a thin layer of rat feces infested with tapeworm eggs on a 35-mm-diameter filter paper for 24 hr. Tapeworm-infected rat feces were acquired from Carolina Biological Supplies (Burlington, North Carolina). The filter paper was then removed, and beetles were exposed to a new filter paper with fresh tapeworm-infested rat feces for 24 hr. The experiments described below used beetles 3 wk after infection. Infection and male reproductive success in the absence of sperm competition and female mate choice This experiment was conducted to test whether tapeworm infection reduces male ability to sire progeny when a single female was exposed to only 1 male for 24 hr in an 8-dram vial with 5 g of flour medium. The male beetle was then transferred into a vial with a virgin female for another 24 hr. This process was repeated for 5 days; thus, each male was exposed to a total of 5 females in 5 days. Males were immediately dissected to determine infection intensity (the number of parasites in a beetle). Females were allowed to lay eggs for 5 wk, and F1 adults and pupae in the vials were counted. Sample sizes were 40 infected individuals and 10 uninfected individuals as control. Infection and male reproductive vigor Male reproductive vigor, defined as the willingness to mate, or the ability to sire offspring, or both, was measured by the ability of a male to inseminate available females within a short period of time. Here, male reproductive vigor is determined by multiple factors, including motivation to mate; ability to locate, attract, and mount females; and ability to produce or transfer sperm. A male was exposed to a virgin black female in an 8-dram vial with 2 g of flour medium for 1 hr. The small amount of flour improved the probability of male–female encounter. The male was then transferred into another vial with another virgin female and fresh flour medium for 1 hr. In this manner, a male was exposed to a total of 24 females within a 24-hr period. Because the females used in this study were virgins and thus strongly motivated to copulate, the effect of female choice on copulation and insemination was minimal. The male was then dissected to determine infection intensity. Females were allowed to lay eggs, and the F1 eggs were allowed to grow into adults in a vial with 5 g of flour. Five weeks later, all offspring including pupae and adults were counted. The number of females that produced offspring and the total number of offspring sired by a male serve as an indicator of male reproductive vigor. Twenty infected males and 10 uninfected males were used. Infection and attractiveness of male pheromone To test whether female beetles can distinguish between infected and uninfected males, simultaneous mate choice experiments were conducted following the protocol of Pai and Yan (2002b). The mate choice arena was an 18-cm-diameter petri dish lined with a filter paper and a thin layer of flour. Ten virgin females were exposed to 2 filter-paper disks with male pheromone from an infected male and from an uninfected male. The disks were placed diametrically opposite each other in the arena at random locations along the circumference of the dish. Pheromone collection by the filter-paper disks was as described by Boake (1986). Male beetles were placed into individual 1-dram vials with a 5-mm-diameter Whatman filter-paper disk for 3 wk, and compounds secreted by the male were absorbed by the paper disk. Previous
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studies demonstrated that 1 wk was sufficient for the pheromone deposited on the filter paper to elicit female response (Boake, 1986). Virgin females, 4–6 wk postemergence, were first allowed to habituate under a 3.5-cm-diameter petri dish inside the arena for 5 min; the smaller petri dish was then lifted, and females were allowed to move freely in the arena. Female beetles respond to pheromone by moving toward the pheromone source and attempting to climb it (Obeng-Ofori and Coaker, 1990). We recorded the number of visits each pheromone disk received every 60 sec for 5 min. Twelve replicates were conducted. Males were dissected to determine tapeworm infection intensity. Infection and male copulatory courtship This experiment was conducted to compare copulatory courtship of infected and uninfected males with uninfected virgin females. In T. castaneum, males typically approach the female and mount from the rear (Wojcik, 1969). Copulation lasts from a few seconds to 30 min (Bloch Qazi et al., 1996; Haubruge et al., 1999; Edvardsson and Arnqvist, 2000). While in copula, the male strokes the female elytra with his legs (Wojcik, 1969; Edvardsson and Arnqvist, 2000). This behavior, referred to as copulatory courtship, directly determines the male’s success in fertilization because there is a significant positive correlation between the intensity of male copulatory courtship and the male’s share of paternity (Edvardsson and Arnqvist, 2000). A virgin male and a virgin female were placed in a 3.5-cm clear plastic petri dish, and courtship was observed under a microscope with 2.53 magnification under ambient conditions. The pair was observed until copulation occurred (thus, the observation time varied for pairs). Duration of copulation and the number of strokes produced by the males with their legs on female elytra while in copula were recorded (n 5 12). Females were 6 wk postemergence. Males of 8 wk postexposure to tapeworm eggs were used for this experiment. Control males were of the same age but were not infected. Data analysis Linear regression analyses were used to examine the effect of infection intensity on male offspring production and male reproductive vigor (number of females inseminated) during 24 hr. Number of progeny sired by infected and uninfected males was compared using Students’ t-test (SAS, 1995). Female response to infected and uninfected males’ pheromone was compared using Wilcoxon signed rank test (Sokal and Rohlf, 1995). Comparison of copulatory courtship of infected and uninfected males was also made using t-tests (SAS, 1995).
RESULTS Infection and male reproductive success in the absence of sperm competition and female mate choice Of the 40 males exposed to tapeworm-infected rat feces, 8 died 3 wk after infection, and 7 were not infected with parasites. These uninfected males were pooled with the control group males. Thus, the final sample size for treatment of uninfected males was 17, and for infected males it was 25. Infection intensity of male beetles used in this experiment ranged from 1 to 13 parasites, with an average of 3.6 (SD 5 2.9). During the 5-day experimental period, tapeworm infection reduced male reproductive success by 14% (t40 5 2.9, P 5 0.004; Fig. 1A). Significant reduction in male reproductive success was observed on days 2 and 3 (day 2 5 28.5% reduction; t40 5 2.9, P 5 0.005; day 3 5 22.8% reduction, t40 5 2.4, P 5 0.019). Infection intensity was not significantly correlated with male reproductive success (r2 5 0.04, F1,24 5 1.17, P 5 0.28; power 5 0.18, least significant number 5 84; Fig. 1B). Infection and male reproductive vigor Of the 20 males exposed to rat feces, 2 were not infected. These uninfected males were pooled with the control group;
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0.001; Fig. 2B). Thus, tapeworm infection significantly reduced male reproductive vigor. There was no significant negative correlation between infection intensity and the number of offspring sired by males (r2 5 0.09, F1,17 5 1.7, P 5 0.20; power 5 0.23, least significant number 5 42; Fig. 2C). Infection and attractiveness of male pheromone The infection intensity of the male beetles used in this experiment ranged from 6 to 12, with an average of 7.7 parasites (SD 5 2.16). Female beetles did not exhibit significant difference in response to pheromone disks of infected males in comparison with uninfected males in the simultaneous mate choice tests (Wilcoxon signed rank test, n 5 12, P . 0.05; Table I). Infection and male copulatory courtship The infection intensity of male beetles used in this experiment ranged from 1 to 11 parasites per beetle, with an average of 4.6 parasites (SD 5 3.62). The duration of copulation of infected males was not significantly different from that of uninfected males (t22 5 0.80, P 5 0.42; Table I). The number of strokes produced by infected males was not significantly different from that of uninfected males (t22 5 1.1, P 5 0.25; Table I). Thus, tapeworm infection did not significantly affect male copulatory courtship. DISCUSSION
FIGURE 1. The effect of tapeworm infection on reproductive success of Tribolium castaneum males in 5 days. (A) Average offspring sired per male per day (SD is shown). (B) Average offspring sired by a male as a function of infection intensity.
thus, final sample size for treatment of infected males was 18, and for treatment of uninfected males it was 12. The average infection intensity of male beetles used in this experiment was 6.5 parasites (SD 5 5.9), ranging from 1 to 21. Number of offspring sired by a male declined significantly with time, i.e., number of mating partners, for both infected and uninfected beetles (r2 5 0.22, F1,23 5 6.2, P 5 0.02 for uninfected beetles; r2 5 0.17, F1,23 5 4.7, P 5 0.04 for infected beetles; Fig. 2A). Infected males sired significantly fewer (22%) offspring (mean 5 58.5, SD 5 18.7/hr) than did uninfected males (mean 5 74.9, SD 5 23.6/hr) during the 24-hr period (t28 5 2.1, P 5 0.043; Fig. 2A). The proportion of successful inseminations by infected males (mean 5 0.44, SD 5 0.15) was 30% less than for uninfected males (mean 5 0.18, SD 5 0.10; t28 5 5.1, P ,
In the present study, we have demonstrated that tapeworm infection reduced the reproductive success of T. castaneum males by 14% when females were not given mate choice and when there was little intraspecific competition among offspring. Male reproductive vigor, measured by number of females inseminated in 24 hr, was diminished by tapeworm infection. Infected males inseminated 30% fewer females and sired 22% less offspring than did uninfected males. There was no significant correlation between infection intensity and number of offspring sired by males. We did not detect any effect of tapeworm infection on the attractiveness of male pheromone to female beetles, and male copulatory courtship was not affected by infection. Yan and Stevens (1995) previously demonstrated that tapeworm infection reduced second-male sperm precedence (P2) and also showed reduced male fitness because of tapeworm infection as measured by offspring production when a male was placed in a competitive environment with 7 other males and 8 females. The lower fitness of infected males could be explained by 1 or a combination of the following mechanisms: (1) a disadvantage in male–male competition before or after copulation; (2) female mate choice against infected males; and (3) a direct adverse effect of parasites on male sperm production, the quality of the sperm, or mating vigor. Because tapeworm infection does not change male copulatory courtship or female response to male pheromone, parasite-induced reduction in sperm precedence did not likely result from female choice. Our current experimental design did not involve male–male interactions because a female was mated with a single male. Discrimination against an infected male by females in mate choice is not likely because we found no evidence for pre-
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TABLE I. Effects of tapeworm infection on the attractiveness of male pheromone and male copulatory courtship. Mean values and standard deviations are shown. Infected males Attractiveness of male pheromone Proportion response to pheromone disks 0.55 (0.26) Male copulatory courtship Copulation duration Number of strokes
FIGURE 2. The effect of tapeworm infection on the reproductive vigor of Tribolium castaneum males. (A) Offspring production per male per hour for a period of 24 hr. (B) Proportion of successful inseminations each hour. (C) Number of offspring sired by a male as a function of infection intensity.
copulatory female choice against infected males in pheromone choice tests, and we also found no difference in copulatory courtship of infected and uninfected males. The results indicating that infected males showed reduced mating vigor and inseminated fewer females than did uninfected males suggest that infection may have altered some aspects of male reproductive biology. In Tenebrio molitor beetles, another natural
54.6 (32.42) 41.3 (32.63)
Uninfected males
0.45 (0.26) 65.4 (31.78) 61.4 (50.32)
host of H. diminuta, although tapeworm infection did not show detectable adverse effects on male spermatogenesis (Carver, 1997), it significantly reduced number of offspring sired by infected males (Worden et al., 2000). In the present study, significant reductions in offspring production of infected males were seen on days 2 and 3 during the 5-day experimental period, suggesting a temporal effect of infection on male reproductive success, a phenomenon also observed by Worden et al. (2000). Although we found that tapeworm infection significantly lowered male fitness, there was no correlation between infection intensity and fitness reduction. The lack of correlation may be caused by the relatively low infection intensity of the beetles used in this study; there may be a threshold level of infection intensity above which the effect of parasitism on fitness is significant (Worden et al., 2000). Yan (1997) did not detect a significant correlation between T. castaneum male fitness and infection intensity even when the range of infection intensity was 1–28 parasites per beetle (mean 5 12.6, SD 5 6.8). Another possibility is that perhaps the sample size used in the correlation analysis was not sufficiently large, as indicated by the power analysis. Reduction in male reproductive effort because of disease has been documented in many species, and the effects of parasite infection on male hosts can be far broader than the effect on mating vigor or the ability to sire offspring. For example, in a chrysomelid beetle (Timarcha maritima), males infected with a protozoan gut parasite are less competitive in obtaining mates than are uninfected males because more infected males than uninfected males were found to be unpaired in the field (Thomas, Gente et al., 1999; Thomas, Oget et al., 1999). Male sedge warblers show reduced song variability and parental care when infected with blood parasites (Nordling et al., 1998; Buchanan et al., 1999), and male kestrels have lower fitness because of infection with hematozoans (Korpimaki et al., 1995). In the three-spined stickleback, parasites cause males to have poor body condition and smaller pectoral fins, which in turn lead to reduced parental care (Bakker and Mundwiler, 1999). Thus, T. castaneum females that mate with infected males could have reduced fitness either directly through reduced offspring production or indirectly through reduced offspring fitness if susceptibility to tapeworm infection is determined genetically. The direct effects of mating with a genetically susceptible male may be less significant for female T. castaneum if females can mate with other males. Infection with the tapeworm leads to an increase in the se-
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cretion of defensive compounds (Yan and Phillips, 1996), which are known to have a repellent effect on conspecifics (Suzuki, 1980). Thus, our original hypothesis was that female red flour beetles would be less attracted to infected males’ pheromone. Odor is an important cue for mate choice in many species, and this may be affected by infection. In mice, for example, females prefer the odor of uninfected males because infection causes male odor to lose its attractiveness (Penn and Potts, 1998; Dawson and Bortolotti, 2001). We found no evidence for precopulatory female choice against infected males in odor-based pheromone choice tests. Thus, defensive compounds in infected male’s pheromone did not appear to repel females. Also, we found no difference in copulatory courtship of infected and uninfected males, which is a very important cue for cryptic female choice (Edvardsson and Arnqvist, 2000). Hence, female choice against infected males appears unlikely, and tapeworm infection does not seem to play a significant role in mate selection for T. castaneum beetles. An absence of female choice against infected males has also been recorded in Drosophila sp. (Kraajeveld et al., 1997) and pied flycatchers (Dale et al., 1996). However, Worden et al. (2000) found that female Tenebrio molitor beetles disliked the odor of tapeworm-infected males compared with the odor of uninfected males. In conclusion, tapeworm infection caused significant fitness reduction in T. castaneum male beetles. Fitness reduction of the male beetles was not caused by female mate choice against infected males. Because male copulatory courtship was not affected by infection, direct effects of infection on sperm production, sperm competitive ability, or some other aspect of male reproductive biology are more plausible explanations for infection-induced fitness reduction in male beetles. ACKNOWLEDGMENTS We are grateful to G. S. Bajwa, C. Ma, M. Park, and A. Niertit for technical assistance. M. Webster, C. Berman, D. Taylor, and M. Coffroth provided useful suggestions in the course of this work. We thank S. Lewis and 2 anonymous reviewers for helpful advice on the article. The research is supported by National Science Foundation grant DEB 0076106.
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