Behavioral Ecology Advance Access originally published online on January 22, 2008
Behavioral Ecology 2008 19(2):433-440; doi:10.1093/beheco/arm153
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Paternity costs from polyandry compensated by increased fecundity in the hide beetle
Department of Zoology, University of Melbourne, Victoria 3010, Australia
Address correspondence to T.M. Jones. E-mail: theresa{at}unimelb.edu.au.
Received 18 July 2006; revised 31 August 2007; accepted 11 December 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Polyandry-induced sperm competition is assumed to impose costs on males through reduced per capita paternity success. In contrast, studies focusing on the consequences of polyandry for females report increased oviposition rates and fertility. For these species, there is potential for the increased female fecundity associated with polyandry to offset the costs to males of shared paternity. We tested this hypothesis by comparing the proportion and number of offspring sired by males mated with monandrous and polyandrous females in the hide beetle, Dermestes maculates, both for males mating with different females and for males remating with the same female. In 4 mating treatments, monandrous females mated either once or twice with the same male and polyandrous females mated either twice with 2 different males or thrice with 2 males (where 1 male mated twice). Polyandrous and twice-mating monandrous females displayed greater fecundity and fertility than singly mating monandrous females. Moreover, males remated to the same female had greater paternity regardless of whether that female mated with another male. In both polyandrous treatments, male mating order did not affect paternity success. Finally, although the proportion of eggs sired decreased if a male mated with a polyandrous female, multiply mating females or females that remated with a previous mate laid significantly more eggs and thus the actual number of eggs sired was comparable. Thus, males do not necessarily accrue a net fitness loss when mating with polyandrous females. This may explain the absence of any obvious defensive paternity-protection traits in hide beetles and other species.
Key words: monandry, polyandry, remating, sexual conflict, sperm competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Polyandry is typically thought to impose costs on males. This view is derived primarily from studies of sperm competition that focus on the shared and, therefore, reduced per capita paternity success of competing males (Birkhead and Møller 1998
; Simmons 2001). In contrast, studies that consider the consequences of polyandry for females report increased oviposition rates and enhanced fertilization success (Chapman et al. 1995; Rice 1996; Eady et al. 2000; Worden and Parker 2001). For these species, increased female fecundity associated with polyandry has the potential to offset the costs to males of shared paternity, with males mating with monandrous and polyandrous females siring a similar number of offspring. Surprisingly, studies of sperm competition typically do not consider whether the absolute paternity of a male, an equally important measure of reproductive success, increases when mating with polyandrous females. Thus, although the costs and benefits of polyandry have been clearly identified for males and females, respectively, the potential for an increase in female fecundity to ameliorate the fertilization costs to males has not been examined.
Sperm competition has been selected for the development of a variety of behavioral, physiological, and morphological traits in males that serve to maximize reproductive success (Simmons 2001). However, the underlying mechanisms that determine sperm utilization patterns remain poorly understood (Simmons 2001). Several factors are thought to be important in determining paternity patterns. Among invertebrates, mating order is frequently influential, with a mating advantage favoring the second male due to the partitioning of ejaculates within the female's reproductive tract (Simmons 2001). Alternatively, males may use defensive strategies to prevent their partner from mating again through either mechanical (Crudgington and Siva-Jothy 2000) or chemical inhibition (Rice 1996). Males may also engage in offensive strategies, such as increasing the quantity of ejaculate transferred to a female (Parker 1970; Dickinson 1986) by copulating repeatedly with the same female and/or by delivering larger ejaculates (Pitnick and Markow 1994; Schneider et al. 2000).
Surprisingly, few studies have quantified explicitly the benefits of remating with the same partner for male invertebrates. Those that have been carried out contain potentially confounding factors such as male paternal investment (Smith 1979; Simmons 1987; Müller and Eggert 1989) or reveal a positive relationship between copulation duration and paternity success such that the effect of mating frequency and total duration of copulation cannot be easily separated (Schneider et al. 2000).
From a female perspective, the consequences of a polyandrous mating strategy have been debated widely (Hosken and Blanckenhorn 1999; Arnqvist and Nilsson 2000; Jennions and Petrie 2000; Simmons 2001; Andersson 2005). A range of studies report that polyandrous females gain genetic (Newcomer et al. 1999; Bernasconi and Keller 2001; Pai and Yan 2002; Tregenza and Wedell 2002; Tarpy 2003; Garcia-Gonzalez and Simmons 2005; Ivy and Sakaluk 2005) and/or direct benefits (Eady et al. 2000; Konior et al. 2001; Marshall and Evans 2005; Uller and Olsson 2005) through mating with several males, but they may also suffer substantial fitness costs (Chapman et al. 1995; Radwan and Rysinksa 1999; Crudgington and Siva-Jothy 2000). A recent meta-analysis found that 30–70% of the average fitness gains accrued by polyandrous female insects arise from direct benefits (Arnqvist and Nilsson 2000); however, such benefits may also be acquired by monandrous females if they mate repeatedly with the same male (Brown et al. 2004; Kamimura 2005). Remating with a previous mate may provide the best strategy to optimize reproductive success in species where the sexes are patchily distributed in time and space, and access to mating partners may be limited.
The hide beetle, Dermestes maculatus DeGeer (Coleoptera: Dermestidae), is a small carrion-feeding insect that forms aggregations on spatially and temporally patchy resources where individuals feed and mate (Archer and Elgar 1998). Male hide beetles possess a pheromone gland on the base of their abdomen that elicits an aggregation response in both sexes (Abdel-Kader and Barak 1979; Rakowski and Cymborowski 1986), and pheromone-based signaling may facilitate female mate choice (Jones and Elgar 2004; Jones et al. 2006). Natural aggregations vary in size depending on the food source, but, on a small carrion source, they typically range from 1 to 13 adults (mean ± standard error = 2.37 ± 0.5, n = 6 carcasses; Archer MS, unpublished data). To date, there are no field observations of mating behavior in the hide beetle; however, in the laboratory, both sexes mate multiply and will remate readily with a previous partner (McNamara et al. 2004). Moreover, in laboratory trials when females were presented with the opportunity to mate with 5 males, they typically mated only once or twice (mean number of matings = 1.7 ± 0.31) although some mated up to 7 times (Jones et al. 2006). There is no pattern of sperm precedence (Archer and Elgar 1999), and neither copulation duration nor male size predicts variation in fertilization success (Archer and Elgar 1999; Jones and Elgar 2004).
Our study has 3 aims. First, we assess the consequences of variation in female mating frequency and the number of mating partners on the probability of commencing oviposition and on overall fecundity. Second, we explore explicitly the effects of male mating frequency and mating order on male reproductive success when males mate with monandrous or polyandrous females. Finally, we examine the degree to which males that engage in sperm competition incur the predicted costs of polyandry through loss of paternity.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Culturing
Adult beetles were obtained from a large (between 200 and 400 adults) laboratory population that had been maintained for 15 generations at the University of Melbourne. Individuals were reared and maintained at 27 °C on a 12:12 h day:night cycle. Larvae and adults were fed an ad libitum diet of dried bonemeal and water. Pupae were isolated in individual tubes to ensure virginity at emergence. Experimental adults were kept individually in small plastic containers (diameter = 6.8 cm, height = 2.8 cm) with ad libitum bonemeal where they can live for up to 6 months in the laboratory environment (Archer and Elgar 1999
). Beetles were aged between 4 and 6 weeks (mean ± standard error for female age = 37.94 ± 0.32 days; male age = 42.21 ± 0.31 days) and were virgin when they commenced their trial. All beetles were weighed 24 h prior to being used in an experiment.
Mating trials
To quantify the effects of mating frequency and mating strategy (monandry or polyandry) on male and female reproductive success, we assigned females to 1 of 4 mating treatments: monandrous, single-mating (M1, n = 61 females); monandrous, double-mating with the same male (M2, n = 40 females); polyandrous, 2 single matings with 2 different males (P2, n = 48 females); and polyandrous, a single mating with one male and a double mating with another male (P3, n = 132 females). Sample sizes differ across groups as we attempted to obtain similar numbers of ovipositing M1, M2, and P2 females, and we also required a larger sample size of P3 females to test simultaneously the effects of mating order and frequency. Depending on their treatment group, experimental males mated either once or twice with a single female, whereas females mated between 1 and 3 times. Paired P2 and P3 males were matched closely for age and weight (mean ± standard error difference in weight between competing males = 1.4 x 10–6 ± 0.8 x 10–6 g).
For all matings, a female was placed initially in a small plastic vial (diameter = 2.5 cm; height = 5 cm) prior to the introduction of a male. The pair was left for 20 min (sufficient time for 85% of females to copulate; Jones and Elgar 2004) or until they copulated. The duration of copulation was recorded and, once complete, the male was removed and discarded. Females that were scheduled to mate more than once were given a 40-min rest period (sufficient time for sperm to reach the female's spermatheca; Featherston R, unpublished data) prior to each subsequent mating. Once a female had completed her total number of matings, she was transferred to a fresh plastic container (diameter = 6.8 cm, height = 2.8 cm) to oviposit for 6 days. Any female that failed to complete her designated number of matings was discarded (number of discarded M1 females = 10/61, M2 females = 2/40, P2 females = 7/48, P3 females = 49/132).
For P3 females, a reciprocal mating design was used such that approximately half the sample of females mated twice with their first mate and once with their second mate (n = 39 females); the rest mated once with their first mate and twice with their second mate (n = 44 females).
The standard sterile male technique was used to infer patterns of paternity in P2 and P3 females (Boorman and Parker 1976). This technique has been applied successfully in D. maculatus. Females mated to 2 irradiated males lay only 0.1% eggs that develop eyespots (a sign of embryo development), whereas 97% of eggs laid by females mated to 2 non-irradiated males develop eyespots and there is no evidence of an irradiation effect on fertilization success (Archer and Elgar 1999). Twenty-four hours prior to the commencement of a trial, half of the males assigned to the P2 (n = 41 males) and P3 (n = 83 males) treatment groups were subjected to a sublethal dose of radiation (3.5 krad from a Cobalt-60 source) that renders sperm capable of fertilization but prevents embryo development. A balanced reciprocal design was used to control for the potential effects of irradiation. In the P2 treatment, IN females (n = 20) mated with the irradiated (I) male first and the normal (N) male second; NI females (n = 21) mated with the normal male first and the irradiated male second. In the P3 treatment, IIN females (n = 19) mated twice with an irradiated male and then once with a normal male; INN females (n = 23) mated once with an irradiated male and then twice with a normal male; NII females (n = 21) mated once with a normal male and then twice with an irradiated male; and NNI females (n = 20) mated twice with a normal male and then once with an irradiated male. There was no effect of the radiation treatment on the duration of copulation for radiated and non-irradiated males (paired t-test comparing the average copulation duration of the irradiated and non-irradiated males when mating with the same P2 female: t = 1.03, N = 41 females, P = 0.16; P3 female: t = 0.64, N = 42 females, P = 0.26).
Assessment of fecundity and fertilization success
To assess fecundity and fertilization success, mated females were provided with a water-soaked sponge (1 x 1 cm), a piece of ox liver (0.5 x 0.5 cm), and a square (3 x 3 cm) of synthetic fur, a fabric suitable as an oviposition substrate (Archer and Elgar 1999), on which to lay eggs. Food, water, and fur were replenished every 1–3 days. At 25 °C, egg viability can be determined by embryo pigmentation 48 h after oviposition (after; Archer and Elgar 1999). For M1 and M2 females, fertilized eggs were determined by the presence of characteristic eyespots and opaque eggs were categorized as infertile. For P2 and P3 females, eggs that developed eyespots were assigned to the non-irradiated male and eggs that remained opaque were assigned to the irradiated male. The balanced reciprocal design ensured that any biases in paternity were detected.
For all females, we recorded the presence and total number of eggs laid over a 6-day period (see also, Jones and Elgar 2004; Jones et al. 2006). For M1 and M2 females, the total number of fertilized eggs produced was noted. For P2 and P3 females, the total number of eggs sired by the irradiated and non-irradiated males was assigned as above.
The experiment was carried out over 3 time blocks. Time block was added as an additional variable in all analyses but was then dropped as the amount of variation it explained was, in all cases, nonsignificant.
Statistics
We employed 4 comparisons to explore the individual and simultaneous effects of mating frequency and mating order on fecundity and fertilization success. First, to assess explicitly the effect of mating frequency on female mating success, we compared the number of females ovipositing, the total number of eggs laid, and the proportion of eggs that were fertilized by M1 and M2 males. Second, the main effect of mating order on paternity success was explored by comparing the number and proportion of eggs sired by the first and second males in the P2 treatment group. Third, to examine the combined effects of mating frequency and mating order on paternity success, we compared the number and proportion of eggs sired by the first and second males who mated either once or twice in the P3 treatment group. There was no effect of the irradiation treatment on the number of eggs sired by P2 males (NI vs. IN females—first male: F1,37 = 0.08, P = 0.77; second male: F1,37 = 1.12, P = 0.30) or the proportion of eggs sired by the second male (Kruskal–Wallis test comparing NI vs. IN females: 
12 = 0.02, P = 0.90). Similarly, for P3 males there was no effect of the irradiation treatment on the number of eggs sired (NNI vs. IIN females—first male: F1,68 = 0.003, P = 0.96; second male: F1,68 = 0.63, P = 0.43; NII vs. INN females—first male: F1,68 = 0.82, P = 0.37; second male: F1,68 = 2.00, P = 0.16) or the proportion of eggs sired by the second male (Kruskal–Wallis test comparing NNI vs. IIN females: 12 = 0.02, P = 0.90; NII vs. INN females: 12 = 2.13, P = 0.14). For both P2 and P3 comparisons, the non-irradiated male only was used in analyses of fertilization success. Finally, to explore the relative importance of a female's mating strategy (monandrous or polyandrous) and male remating behavior on male reproductive success, we compared the fertilization success of the first male to mate in each of the 4 female mating treatments. Using the data from the first males only was a valid measure as mating order had no effect on any of the reproductive parameters measured (see Results). This resulted in 5 groups of males: monandrous, single mating (M1-1); monandrous, double mating (M2-2); P2 polyandrous, single mating (P2-1); P3 polyandrous, single mating (P3-1), and P3 polyandrous, double mating (P3-2).
Analyses of the variation in fecundity and fertilization success were performed using general linear models in MLwiN 1.2 (Rasbash et al. 2000). Fecundity data (excluding the proportion of fertilized eggs) were transformed to achieve normality and then analyzed using response models that assumed a normal error distribution. Variation in the proportion of fertilized eggs was assessed assuming a binomial error distribution with a logit link function. This model included the total number of eggs laid as a denominator, thus accommodating the large amount of variation observed in the number of eggs laid across females. The exception to this was the final analysis comparing the proportion of fertilized eggs sired. For this analysis, the proportion of eggs sired by M1-1 and M2-2 males was set to 1.0 (variance = 0.0); our data violated the assumptions of both parametric and binomial models and thus we used nonparametric analyses.
All models carried out in MLwiN 1.2 incorporated female identity as a random term in the model. Although female weight has never influenced fecundity or fertilization measures (Archer and Elgar 1999; Jones and Elgar 2004; Jones et al. 2006), in this study it varied across the 4 treatment groups (mean weight ± standard error of M1 females = 0.026 ± 0.001; M2 females = 0.030 ± 0.001; P2 females = 0.031 ± 0.001; P3 females = 0.026 ± 0.0003; F3,446 = 26.36, P < 0.0001) and was therefore included as a parameter in all models. Male weight also varied across the 4 treatment groups (mean weight ± standard error of M1 males = 0.026 ± 0.001; M2 males = 0.028 ± 0.001; P2 males = 0.026 ± 0.001; P3 males = 0.022 ± 0.0003; F3,446 = 31.22, P < 0.0001) and was initially included in all models but was then dropped as it had no significant effect on the measured patterns of fecundity and fertility. Female weight was retained in the models because it was found to be positively correlated with fecundity in some (but not all) of our trials. For models with an assumed normal error distribution, the significance of explanatory variables was determined by calculating the change in model deviance (which approximates the 2 distribution) as each term (or treatment) was eliminated from the full model. For binomial models, significance levels were determined using Wald chi-square tests.
Two P2 females were dropped from analyses exploring variation in fecundity and fertilization success due to missing values for female body weight. Raw data (medians and interquartile ranges) are presented in tables and figures for ease of comparison.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Consequences of imposed female mating strategy and frequency on oviposition and fecundity
Treatment groups showed considerable variation in the probability that a mated female laid eggs (nominal logistic regression:
32 = 19.73, P = 0.0002; Figure 1a). Post hoc comparisons revealed that polyandrous females were more likely to lay eggs than monandrous females (M1 and M2 females vs. P2 and P3 females: 12 = 28.36, P < 0.0001). The probability of oviposition was not related to female weight (12 = 1.81, P = 0.18). Non-ovipositing females were discarded from further analyses.
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The total number of eggs laid by ovipositing females varied significantly across the 4 treatment groups (
32 = 5.95, P < 0.0001; Figure 1b); M1 females laid significantly fewer eggs than females from any other treatment group (all P < 0.05); all other comparisons between females were nonsignificant. The number of eggs laid was positively correlated with female weight (12 = 5.95, P = 0.01).
Effect of mating frequency and mating order on fertilization success
Mating frequency: M1 and M2 treatments
The probability of producing an infertile clutch was significantly greater for M1 (7/30) than M2 (1/27) females (Fisher's Exact test: P = 0.054), thus we carried out 2 sets of analyses, one including and the other excluding females that laid completely infertile clutches.
Including all ovipositing females, the average number of eggs sired by M2 males was 100% greater than that for M1 males (12 = 6.48, P = 0.02; Figure 2a), but this was not influenced by female weight (12 = 0.27, P = 0.60). The median proportion of fertilized eggs sired by M1 and M2 males was comparable (12 = 0.31, P = 0.58; Figure 2b) and did not vary with female weight (12 = 1.16, P = 0.28).
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Excluding females that produced completely infertile clutches, the above patterns remain the same. The median number of eggs fertilized by M2 males was considerably higher than that for M1 males (
12 = 5.56, P = 0.02) and was not related to female weight (12 = 0.86, P = 0.39). The median proportion of eggs fertilized was comparable for M1 and M2 males (12 = 0.27, P = 0.62) and was not related to female weight (12 = 1.75, P = 0.19).
Mating order: P2 treatment
Thirty (76.9%) ovipositing P2 females produced egg batches that comprised eggs sired by both males. Of the remaining clutches, I and N males were equally likely to be the single sire (N males = 4 clutches; I males = 5 clutches). The total number of eggs produced was comparable for ovipositing NI and IN females (12 = 1.62, P = 0.20; Table 1) but was positively related to female weight (12 = 13.3, P = 0.0003).
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The number of eggs sired by the non-irradiated P2 male was not influenced by the order in which he mated with the female (
12 = 0.42, P = 0.52; Table 1). Similarly, the proportion of eggs sired by the non-irradiated male was also not related to the order in which he was mated to a female (12 = 0.03, P = 0.86; Table 1).
The interaction between mating order and mating frequency: P3 treatment
Fifty-four (75%) ovipositing P3 females produced egg batches that comprised eggs sired by both males. Of the remaining clutches, I and N males were equally likely to be the single sire (N males = 9 clutches; I males = 9 clutches). The total number of eggs produced was comparable for all 4 female groups (32 = 2.76, P = 0.43; Table 2) and was not related to female weight (12 = 0.01, P = 0.75).
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The total number of eggs sired by non-irradiated twice-mating P3 males tended to be higher than that for single-mating P3 males (
12 = 2.84, N = 83 females, P = 0.08; Table 2). The number of eggs sired was also not related to the order in which a male was mated to a female (12 = 1.37, P = 0.74) or the interaction between mating order and mating frequency (12 = 2.18, P = 0.14).
The proportion of eggs sired by non-irradiated P3 males was significantly higher for males that mated twice compared with males that mated once with a P3 female (12 = 5.83, N = 83 females, P = 0.02; Table 2) but was not related to the order in which a male was mated to a female (12 = 0.69, P = 0.40) or the interaction between mating order and mating frequency (12 = 2.07, P = 0.15).
Consequences for males of imposed female mating strategy and male mating frequency
There was significant variation in the number of eggs sired across the 5 groups of males mating first with a female (41 = 14.91, P = 0.005; Figure 3a). Controlling for mating frequency, there was no effect of the imposed female mating strategy on the number of eggs sired. Post hoc comparisons revealed that a male who mated once with a polyandrous female sired a similar number of eggs to a male who mated once with a monandrous female (M1-1 = P2-1 = P3-1 males; All P > 0.05). Similarly, a male who mated twice with a polyandrous female sired a similar number of eggs to a male who mated twice with a monandrous female (M2-2 = P3-2 males; P > 0.05). However, M2-2 males sired a larger number of eggs than males permitted a single-mating opportunity (M1-1, P2-1, and P3-1 males) (Post hoc comparisons: all P < 0.03); P3-2 males also sired a larger number of eggs than M1-1 and P3-1 males (both P < 0.03) but sired a comparable number of eggs to P2-1 males (P = 0.24).
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The proportion of eggs sired by a male varied significantly across the 5 groups (Kruskal–Wallis test:
42 = 88.79, P < 0.0001; Figure 3b). Post hoc comparisons revealed that monandrous (M1-1 and M2-2) males sired a greater proportion of offspring than polyandrous (P2-1, P3-1, and P3-2) males regardless of their number of matings (all P < 0.01). As above, polyandrous males who mated twice with their mate (P3-2 males) sired a significantly greater proportion of offspring than single-mating (P3-1 males) males (P < 0.05). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Our study of the hide beetle has 3 key findings. First, mating frequency per se had significant consequences for both sexes. Polyandrous and twice-mating monandrous females laid significantly more eggs than monandrous females that mated just once. Twice-mating monandrous females also produced more offspring than single-mating monandrous females, and males that remated with the same female increased their paternity success regardless of whether they were a female's sole mate or whether she mated multiply. Second, after controlling for mating frequency, mating order had little impact on paternity: males that mated with a virgin female sired similar numbers of offspring to males that mated with an already mated female (see also Archer and Elgar 1999
). Finally, the observed positive correlation between fecundity and female mating frequency may balance the potential costs of polyandry to males: although the proportion of eggs sired decreased if a male mated with a polyandrous female, multiply mating females or females that remated with a previous mate laid significantly more eggs and thus the absolute number of eggs sired was comparable.
Polyandry, mating frequency, and male reproductive success
Studies exploring the consequences of polyandry for males have suggested that sperm competition imposes a substantial fitness cost in terms of reduced relative paternity success (Birkhead and Møller 1998; Simmons 2001). This pattern occurs in the hide beetle; on average, males mated with a polyandrous female sired proportionally fewer offspring than when mated with a monandrous female, irrespective of a male's mating frequency. However, our results suggest that the reproductive fitness of male hide beetles is not necessarily compromised by sperm competition: when the absolute number of offspring sired by a male is considered, the reduction in paternity share resulting from multiple mating is compensated by a positive relationship between female mating frequency and fecundity. Clearly, the significance of this effect in natural populations will depend on the average mating frequency of both males and females (Parker 1998).
The lack of congruence between relative and absolute paternity observed in this study is driven in part by the considerable variation in female fecundity. It is also pertinent to note that the observed response ratio (the ratio between the number of eggs produced by a single-mating female and the number produced by a female after multiple matings) (sensu, Arnqvist and Nilsson 2000) was approximately 2.0. This is higher than that has been found in other insects (Arnqvist and Nilsson 2000). Moreover, although the pattern revealed by our experiments may be broadly applicable to other species where there is a positive relationship between female mating frequency and fecundity (Arnqvist and Nilsson 2000), it may only operate at low levels of polyandry, particularly if females are constrained in the number of eggs that they can lay. Finally, although the rate of egg laying declines with age in the hide beetle (Featherston R, unpublished data), patterns of paternity may vary if females were permitted to oviposit for a greater proportion of their lifespan. Nevertheless, absolute values of paternity success should be incorporated into measures of male reproductive fitness in species in which there is high variation in female fecundity. Failure to consider the effect of mating frequency on female fecundity may inflate the impact that sperm competition has on male reproductive success.
Male mating frequency and reproductive success
Whereas the reproductive costs of sperm competition may be partly offset by increases in female fecundity, hide beetle males can also increase their paternity success by increasing the quantity of sperm transferred to a female through increased copulation frequency, a result previously noted for other invertebrates (Schneider et al. 2000). Remating with a previous mate also reduces the variation in the number of eggs laid across females: the coefficient of variation for the number of eggs produced by single-mating monandrous females (CV = 119.15%) was almost double that of twice-mating monandrous females (CV = 64.56%). However, although males gain immediate fitness benefits from a remating strategy, this may be offset against a potential loss of genetic benefits gained through future mating opportunities with additional females. Thus, within a species, the relative prevalence of polygynous and remating strategies may depend on variation in the operational sex ratio and density at the population level.
Polyandry, mating frequency, and female reproductive success
Several lines of evidence suggest that female hide beetles gain direct benefits from mating more than once. Polyandrous and twice-mating monandrous females laid a greater quantity of eggs and produced a larger number of fertilized eggs than monandrous females that mated once only. This pattern is consistent with observations across many studies that have explored the selective advantages of polyandry (Ridley 1988; Arnqvist and Nilsson 2000). Polyandrous female hide beetles were also more likely to commence oviposition than monandrous females. Given that remating reduced the probability of producing a completely infertile clutch of eggs, it is likely that a polyandrous mating strategy may offer similar benefits.
What mechanisms might drive the observed variation in fecundity? In the hide beetle, some females may require more than a single mating to initiate egg production (see also Davey 2007) but this does not explain why more than 50% of single-mated females commenced oviposition, a result comparable with 2 previous studies (Archer and Elgar 1999; Jones and Elgar 2004). It is unlikely that a failed mating attempt explains the observed variation in the probability of oviposition as 96% (N = 28/29) of males (aged 49 days) transfer seminal products to females during a single mating (Hale J, unpublished data). An alternative explanation is that single-mated females have eggs available but are capable of either delaying oviposition or restricting the number that they lay in the short term to increase the chance of obtaining direct fertilization and/or genetic benefits from further matings (Arnqvist and Nilsson 2000; Jennions and Petrie 2000). This is supported by the observation that single-mated monandrous females produced fewer eggs than double-mated monandrous females (this study) and that single-mated females that have not commenced oviposition will do so after a second mating (Archer and Elgar 1999). However, although there is a large increase in the number of eggs laid between the first and second matings, the number of eggs laid does not increase monotonically with female mating frequency. The most parsimonious explanation for this result is that females are physiologically constrained in their egg-laying rate, producing close to their optima after only a few matings. Whether the observed increased fecundity is a "true" benefit to female hide beetles or is traded off against longevity, as has been reported for other insects (Chapman et al. 1995; Rice 1996), remains to be determined. Indeed, the costs associated with polyandry may explain why some hide beetle females mate only once despite the potential benefits that may be accrued from mating more frequently. Moreover, whether such patterns vary with female mating frequency (Arnqvist et al. 2005) or whether females are able to influence patterns of paternity through postcopulatory choice (Eberhard 1996) requires further consideration.
The observation that a female gains direct benefits from remating does not preclude the possibility that she may also accrue genetic benefits from mating with several males. We did not measure whether polyandry confers any fitness advantage to females through increased offspring viability, but 3 lines of evidence suggest that polyandrous females may benefit from mating with multiple males (Yasui 1998; Jennions and Petrie 2000). First, a previous study found that females took longer to remate when presented with the same male rather than a new mate (Archer and Elgar 1999). Second, females mating with 2 males successfully fertilize 97% of their eggs (Archer and Elgar 1999), whereas females that mate twice with the same male achieve only 80% fertilization success (this study). Finally, 75% of polyandrous females in this study produced broods sired by both males. The relative importance of genetic and direct benefits for maintaining polyandry varies across species (Arnqvist and Nilsson 2000; Worden and Parker 2001; Andersson 2005; Kamimura 2005; Marshall and Evans 2005), but it is unlikely that the 2 mechanisms are mutually exclusive.
The absence of male mate-guarding strategies and the maintenance of polyandry
Males of many species have evolved defensive mate-guarding measures to prevent their mate from copulating polyandrously, such as prolonged copulations (Dickinson 1986), mating plugs (Waage 1979; Orr and Rutowski 1991), or the transfer of chemicals that reduce the female's attractiveness (Happ 1969) or receptivity to future mates (Kalb et al. 1993). In contrast, male hide beetles provide ejaculates that induce no obvious refractory period in females, and males do not show any functional form of postcopulatory mate guarding. Male hide beetles do not necessarily accrue a net fitness loss when mating with a female who subsequently copulates with additional males. The absence of such a selection pressure may be one reason for the lack of any obvious defensive paternity-protection traits in this species. This may also be true of other organisms in which there is a dramatic increase in female fecundity and fertilization success with mating frequency. A further possible reason for the absence of male-imposed traits that reduce a female's propensity to mate again is that male hide beetles also accrue direct benefits from remating with a previous partner although these may be less important when access to mates is unlimited. Nevertheless, when resources and mates are patchily distributed, as is likely in the hide beetle, these benefits may be sufficient to constrain the evolution of male-imposed monandry.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The Royal Society (a Travelling Fellowship to T.M.J.) and the Australian Research Council (grant DP0209680).
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ACKNOWLEDGEMENTS |
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We thank Melanie Archer, Leigh Simmons, and Michael Magrath for their useful comments and advice.
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REFERENCES |
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