Behavioral Ecology Advance Access originally published online on December 12, 2007
Behavioral Ecology 2008 19(2):285-291; doi:10.1093/beheco/arm126
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Male insemination decisions and sperm quality influence paternity in the golden orb–weaving spider
Department of Zoology, The University of Melbourne, Victoria 3010, Australia
Address correspondence to T. A. Jones. E-mail: theresa{at}unimelb.edu.au.
Received 24 October 2006; revised 29 October 2007; accepted 30 October 2007.
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ABSTRACT |
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In polyandrous species, paternity may be influenced by the timing and frequency of mating. Female spiders possess 2 genital openings that lead to separate sperm-storage structures. Thus, even when mating with a previously mated female, a male may reduce direct sperm competition by inseminating the opposite opening to her first mate. Such morphology may provide females with greater control over paternity. We examined simultaneously whether males avoided already inseminated female genital openings and whether this behavior varied with the time between successive matings. To explore these questions, we mated female golden orb weaver spiders, Nephila edulis, each to 2 males and manipulated the timing of their second mating. We documented male insemination patterns and explored the influence of male mating decisions on paternity success using the irradiated male technique. We found that 60% of males avoided sperm competition by discriminating against inseminated genital openings. Moreover, male mating behavior had a dramatic impact on the paternity success of irradiated males. When males inseminated the same genital opening, the competitive ability of the irradiated male's sperm was dramatically reduced resulting in lower paternity success. In contrast, when the 2 males inseminated opposite genital openings both males sired equal proportions of offspring regardless of their radiation status. There was no evidence that the timing of the second mating affected patterns of paternity. Our data suggest that differences in sperm quality may influence paternity success of N. edulis males under a sperm-competitive scenario. In contrast, females appear to have limited postmating control over paternity.
Key words: cryptic female choice, insemination, polyandry, sperm competition, sperm quality.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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The mechanisms determining paternity success in polyandrous species have created considerable debate but remain largely unresolved (Parker 1970
, 1984; Birkhead 1995; Birkhead and Møller 1998 and references therein; Simmons 2001). Males may enhance their reproductive fitness by successfully detecting whether a female is nonvirgin prior to copulation and adjusting their mating behavior or copulatory investment accordingly (Engqvist and Reinhold 2006; Friberg 2006; Galeotti et al. 2007). Such behavior may result in males of some species avoiding sperm competition by discriminating against nonvirgin females (Ting et al. 2000) or by mechanically removing the sperm of a rival male before commencing sperm transfer themselves (Fincke et al. 1997; Simmons and Siva-Jothy 1998). However, the ability of males to detect female mating status is generally limited, and, for the majority of polyandrous species, sperm from multiple males are forced to compete within a female's reproductive tract. Subsequent variation in paternity success may arise through quantitative or qualitative differences in sperm or associated seminal products that are transferred during mating and may be driven by male (sperm competition—Parker 1970; Birkhead 1995; Simmons 2001) or female (cryptic female choice—Eberhard 1996) processes. Assessing the relative importance of the male and female role presents arguably the greatest current challenge within the field.
The ability of a male to detect and potentially discriminate against mated females ultimately restricts her number of future partners creating potential conflict between the sexes (Arnqvist and Rowe 2005). From a female perspective, this conflict may be resolved in part if the efficacy of the cue used by males in detection declines over time as is frequently the case with pheromone-based cues (Andersson et al. 2000; O'Donnell et al. 2004; Wedell 2005; Johansson and Jones 2007). Similarly, females gain greater control over the direction of paternity if patterns of paternity vary with the time between successive matings then (Suzuki et al. 1996; Arnaud et al. 2001; Iwata et al. 2005). The time between successive mating events may be particularly influential for those species where females remain sexually receptive for extended periods as is the case for many polyandrous spiders (Elgar 1998).
Spiders provide a unique opportunity to study the relative importance of male and female effects on paternity (Eberhard et al. 1993; Eberhard 2004). Females possess 2 bilaterally symmetrical genital openings that lead to separate sperm-storage structures (spermathecae); thus, males mating with a once-mated female can minimize direct sperm competition by inseminating the opposite genital opening to the first mating male (Bukowski and Christenson 2000; Snow and Andrade 2005). Such morphology may also provide females with greater control over subsequent fertilization success, although whether they can regulate sperm release from individual spermatheca is unclear (Brown 1985; Uhl and Vollrath 1998a; Uhl 2000; Elgar et al. 2003; Eberhard 2004; Berendonck and Greven 2005). Male spiders may reduce the reproductive success of future mates if they introduce physical impediments, such as a mating plug or part of their copulatory organ, into a female's reproductive tract during mating (Elgar 1998; Nessler et al. 2007). However, females may also exert some influence on paternity outcomes by regulating the frequency or duration of copulation (Elgar et al. 2003; Schneider and Elgar 2005; Elgar and Jones 2008). Whether patterns of paternity also vary with the timing of subsequent matings has not been explored explicitly in spiders, although indirect evidence suggests that this has little effect on precopulatory reproductive behavior (Schaefer and Uhl 2003; Norton and Uetz 2005).
The Australian female golden orb weaver spider Nephila edulis builds semipermanent webs in the drier woodlands of eastern Australia, from Victoria to Queensland. Females are rarely sexually cannibalistic during copulation (Uhl and Vollrath 1998b; Schneider et al. 2000). Mature males weigh between 0.002 and 0.200 g, which is between 1% and 80% of the typical weight of a mature virgin female. Numerous males of varying size reside on the webs of penultimate and sexually mature females (Austin and Anderson 1978; Elgar et al. 2003). Both sexes mate multiply, but, although individual males mature at various times during a female's reproductive season, a male is unlikely to be able to monopolize access to females for the duration of his adult life as male life expectancy is shorter than for females (Elgar 1998). Laboratory trials indicate that mature N. edulis females remain and mate on the web for a 3- to 4-week period prior to commencing egg laying (Schneider et al. 2000; Elgar et al. 2003; Schneider and Elgar 2005); thus, it is likely that females engage in multiple matings that occur at different times during their reproductive cycle. Moreover, as a single female can lay up to 5 egg sacs in one season (mean ± standard error [SE] number of egg sacs = 3.11 ± 0.13, N = 47 females), the patterns of paternity may vary across successive egg sacs depending on when and how frequently a female mates.
The female reproductive tract of N. edulis, like all entelygne spiders, is bilateral with 2 genital pores. Each pore is connected to a separate sperm duct and receptacula seminis where the seminal fluid is stored. Males use secondary structures (pedipalps) for mating, which are filled with sperm and then inserted into the female genital opening. When mating, a male always inserts the left pedipalp into the left genital opening and right pedipalp into the right genital opening, providing an easy assessment of the insemination side of any given male. In contrast to the congener Nephila plumipes (Schneider et al. 2001), N. edulis males do not leave the tip of their copulatory organs as a potential mating plug in a female's reproductive tract during mating, but males mating with nonvirgin females may derive paternity benefits from detecting and discriminating against previously inseminated genital openings. Whether males are capable of doing this, and the potential consequences of such patterns of behavior have not been investigated. Moreover, whereas copulation frequency and male size are important factors promoting paternity success in N. edulis (Schneider et al., 2000; Elgar et al., 2003; Schneider and Elgar, 2005), the influence of the timing of successive copulations on paternity success is unknown.
In this study, we mated female N. edulis to 2 males and manipulated the timing of the second mating. For each mating, we documented whether the second male inseminated the same or opposite genital opening to a female's first mate and then explored the influence of the timing of the second mating on patterns of insemination and subsequent paternity success. We predicted that if males can detect previous insemination events, the second male would avoid mating in the same genital opening and thus potentially maximize his mating success. However, a male's ability to detect a female's previous mating event may decline with the time since she last mated thus providing females with greater control over fertilization.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Subadult and juvenile female and male N. edulis were collected in January and February 2005 from a large population in northern Victoria, Australia (36°45'S, 145°34’E). Females were housed in individual cups until subadult, then transferred to separate Perspex frames (58 x 58 x 15 cm), where they built typical orb webs. Females were watered and fed around 8 blowflies Lucilia cuprina at least 3 times per week. Males were maintained in the laboratory in individual cups (250 ml) until adult and were watered and fed a diet of Drosophila and blowflies at least 3 times per week.
To assess simultaneously the influence of the timing of mating on patterns of male insemination and subsequent fecundity and paternity success, 78 virgin females were allocated to one of 3 mating treatments that varied in the time between the first and second mating (0, 10, 20 day, N = 26 females per mating treatment). They were then mated once with each of 2 males. The 3 mating treatments corresponded respectively to the likely minimum time between 2 matings, the midpoint between a first mating and a female laying an egg batch, and the minimum time after a first mating to a female laying an egg batch. We staged matings by placing a single male in the lower edge of a female's web using a small paintbrush. Typically, the male then traversed the web rapidly toward the hub and commenced copulating after a short period. After mating, the male was removed; females were provided with food as above and left on their webs for 1 h (0-day females), 10 days (10-day females), or 20 days (20-day females) prior to the introduction of a second male. A second male was then introduced to the web and permitted to mate as above. For each male, we noted the duration of copulation and the pedipalp used to transfer sperm in order to determine whether the second male inseminated the same or opposite genital opening as the first male. Males did not always mate on the first day of introduction (each male was given ca. 5 h to mate on any given day). If this occurred, the male was removed and reintroduced to the web the following day for a maximum of 3 days. The mean ± SE number of days between matings for the 3 treatment groups was 0.73 ± 0.16 days (0-day females), 10.34 ± 0.45 days (10-day females), and 21.06 ± 0.39 days (20-day females).
There was no difference in the age of females at first mating (mean ± SE age of females in the 0-day treatment = 21.8 ± 0.50, 10-day treatment = 22.2 ± 0.85, 20-day treatment = 24.2 ± 2.14, F2,65 = 1.12, P = 0.33). Males used in the trials were not standardized for size (mean ± SE male leg length = 13.41 ± 0.49 mm, range = 5.53–29.06 mm). The difference in leg length between the 2 males used in a trial was on average 5.73 ± 0.43 mm (range = 0.13–21.13 mm). The difference in leg length was initially included as a covariate in all models but was dropped if it did not significantly explain variation in the y variable.
Patterns of paternity were determined using standard double-mating trials (following Boorman and Parker 1976). Mature males were randomly assigned to either normal (N) or irradiated (R) treatments; males in the latter were irradiated with a dosage of 10 krad from a cobalt-
-emitter. In both treatments, one of the 2 males was irradiated to allow allocation of paternity. The order of introduction to the web (first or second) of the irradiated male was randomly assigned throughout the experiment. The proportion of developed eggs was then used to calculate the proportion of eggs fertilized by the normal male. To estimate paternity of N males, we controlled for the proportion of eggs remaining unfertilized after double NN matings (=0.947) and RR matings (=0.00003), respectively (see Boorman and Parker 1976 for calculation of paternity; Schneider and Elgar 2005 for proportions fertilized in double NN and RR trials).
After 2 matings, females were transferred to individual, clear plastic cups, where they were watered and fed around 8 blowflies at least 3 times per week. On average, mated females laid a first egg sac 28.1 ± 1.29 days after their first mating and a second egg sac 38.6 ± 1.14 days later. All egg sacs were removed and placed in a separate sterile plastic vial with a perforated lid in an incubator (25 °C) for about 1 month or until the spiderlings began to hatch (typically indicated when the egg sac felt soft). After this time, the eggs were preserved in alcohol. The hatchlings and undeveloped eggs in the first and second clutch were subsequently counted under the microscope. Paternity was scored in each egg sacs to assess whether there was any temporal variation in paternity success between the first and second clutches across the 3 mating treatments. At the end of the experiment, males and females were frozen and the length of the tibia–patella of the first leg was measured using digital calipers (to the nearest 0.02 mm).
Data analyses
Analyses were performed using JMP (version 4.0.2 [academic], SAS Institute Inc, Cary, NC). Data were inspected for normality, transformed where appropriate, and analyzed using analysis of covariance if the response variable was continuous or a nominal logistic model if the response variable was categorical. Where transformation to normality was not possible, nonparametric statistics were used. All presented averages are means ± SEs unless otherwise stated.
The number of days between the first and second mating (0, 10, 20 day), the insemination side (same, opposite), and male irradiated status (N, R) were added as categorical variables, and percentage of total time spent in copula by the second male was added as a continuous variable in all analyses of paternity. As copulation duration varies with male size (Schneider et al. 2000) and we were interested in the relative investment of the second male when compared with the first male, the percent (rather than absolute) time spent copulating was used for analysis of copulation duration. However, it should be noted that the results were qualitatively identical when the absolute values were used.
Sample sizes vary for a number of reasons. A number of trials were discarded from the main analyses of fecundity and fertilization success. Nine females in the 20-day treatment were discarded as they laid eggs prior to a second mating. This reduced the sample size for this group but confirmed the appropriateness of the chosen minimum time period between the first mating and a female commencing laying her eggs. Additionally, a 20-day female was discarded because the insemination side of her first mate was not determined. Finally, several females died prior to commencing egg laying (1 = 0-day female), laid a first egg sac but died before laying a second egg sac (1 = 0-day female, 4 = 10-day females), or laid a first egg sac that desiccated prior to measurement (1 = 0-day female, 2 = 10-day females). Thus, in total, 69 females mated with 2 males prior to laying their first egg sac; the pattern of insemination by males was assessed for 68 of these females.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Copulation behavior
The second male to mate with a female was more likely to inseminate the opposite genital opening than the same genital opening as the first male (nominal logistic model:
= 4.65, N = 68, P = 0.03; Figure 1). However, the proportion of second males inseminating the opposite genital opening was unrelated to the time between the first and second matings (nominal logistic model: 
= 2.04, P = 0.36) or the time the first male spent in copula ( = 0.04, P = 0.84). Two males mating second inserted their pedipalp into one genital opening but then switched pedipalp and genital opening prior to commencing delivery of sperm. On both occasions, this behavior resulted in the male placing his sperm in the opposite genital opening to the first male. No first mating male switched sides after his initial choice.
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The time the second male spent copulating relative to the first male varied with the number of days between the first and second matings (F1,60 = 4.70, P = 0.01): males mating 20 days after the first mating copulated for relatively longer (mean relative copulation time = 0.61 ± 0.06 min) than males mating 0 days (0.41 ± 0.05 min) or 10 days (0.41 ± 0.04 min) after the first mating (Student's t-tests; both comparisons P < 0.05). There was no difference in the relative duration of copulation between the first and second males in the 0- and 10-day treatments (P > 0.05). The relative copulation duration of the second male was unrelated to male size (F1,60 = 0.60, P = 0.44), the radiation status of the second male (F1,60 = 0.23, P = 0.63), or whether he mated in the same or opposite opening to the first male (mean relative time spent copulating by second mating males inseminating the same genital opening = 0.41 ± 0.05; opposite genital opening = 0.49 ± 0.04; F1,60 = 3.34, P = 0.07).
Fecundity
There was a positive correlation between the number of eggs laid in the first and second egg sacs (rs = 0.26, P = 0.046), but the number laid in the first egg sac was significantly higher than the number laid in the second egg sac (matched pairs t-test: t = 2.06, P = 0.04; Table 1).
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First egg sac
The number of eggs laid by a female in her first egg sac was unrelated to the time between matings (F2,59 = 0.49, P = 0.61; Table 1), her size (F1,59 = 0.54, P = 0.47), the total time she spent copulating (F1,59 = 0.10, P = 0.75), or whether the 2 males inseminated the same or opposite genital openings (F1,59 = 0.30, P = 0.58).
Second egg sac
The number of eggs laid by a female in her second egg sac was also unrelated to the time between mating (F2,55 = 0.79, P = 0.46; Table 1), the total time spent copulating (F1,55 = 2.11, P = 0.15), and whether males inseminated the same or opposite genital openings (F1,55 = 0.003, P = 0.96). However, there was a positive relationship between female size and the number of eggs laid (F1,55 = 4.09, β [SE] = 12.24 [6. 05], P = 0.05).
Paternity success
First egg sac
Paternity success varied between 0% and 100%. When both males inseminated the same genital opening 30% of eggs sacs were sired by a single male; when the second male inseminated the opposite genital openings 56% were sired by a single male (nominal logistic model: = 3.54, P = 0.06). However, the number of sires within an egg sac was unrelated to the number of days between first and second matings ( = 0.02, P = 0.99), or the interaction between the number of days between the first and second matings and insemination side ( = 1.42, P = 0.49). There was no mating order effect with respect to the radiation treatment regardless of whether the second male inseminated the same (Kruskal–Wallis test: = 2.54, P = 0.11) or the opposite genital opening to the first male (Kruskal–Wallis test: 1 = 0.69, P = 0.41).
The proportion of eggs sired by the second male (P2) varied with male radiation status and whether he inseminated the same or opposite genital opening (Kruskal–Wallis test: 
= 8.66, P = 0.03; Figure 2a). Post hoc comparisons of the least square means revealed that when males inseminated the same genital opening, the irradiated male sired a lower proportion of eggs than the nonirradiated male (Tukey test: P = 0.02). In contrast, when males inseminated the opposite genital openings there was no advantage for the nonirradiated male (Tukey test: P = 0.60). P2 was positively related to the relative time the second male spent in copulation irrespective of whether the 2 males inseminated the same or opposite genital openings (same opening: rs = 0.62, P < 0.0001; opposite opening: rs = 0.30, P = 0.008). However, it was unrelated to the number of days between the first and second matings (Kruskal–Wallis test: = 3.44, P = 0.18; Figure 2b).
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Second egg sac
Paternity success in the second egg sac also varied between 0% and 100%. When both males inseminated the same genital opening 40% of eggs sacs were sired by a single male; when the second male inseminated the opposite genital openings 57% were sired by a single male (nominal logistic model:
= 2.16, P = 0.14). The number of sires was unrelated to the number of days between the first and second matings ( = 0.28, P = 0.87) or the interaction between the number of days between the first and second matings and insemination side ( = 2.55, P = 0.28). There was no mating order effect with respect to the radiation treatment regardless of whether the second male inseminated the same (Kruskal–Wallis test: = 2.21, P = 0.14) or the opposite genital opening to the first male (Kruskal–Wallis test: = 0.36, P = 0.55).
P2 in the second egg sac similarly varied with male radiation status and whether he mated in the same or opposite genital opening (Kruskal–Wallis test: = 8.14, P = 0.04; Figure 2c). Post hoc comparisons of the least square means revealed that when males inseminated the same genital opening, the irradiated male sired a lower proportion of eggs than the nonirradiated male (Tukey test: P = 0.02) In contrast, when males inseminated the opposite genital openings there was no advantage for the nonirradiated male (Tukey test: P = 0.30). P2 in the second egg sac was positively correlated with the relative time the second male spent in copulation when the 2 males inseminated the same, but not the opposite genital openings (same opening: rs = 0.33, P = 0.03; opposite opening: rs = 0.15, P = 0.21), and was also unrelated to the number of days between matings (Kruskal–Wallis test: = 2.22, P = 0.33; Figure 2d). Finally, a comparison between the first and second egg sacs revealed a positive correlation between P2 in the first and second egg sacs (rs = 0.66, P < 0.0001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Provided with a choice, 60% of N. edulis males avoided inseminating a previously mated genital opening and thus reduced the time that their sperm were in direct competition with that of their rival's. The observed variation in male precopulatory behavior has several consequences for paternity success. Perhaps most significantly, the second male's paternity success was related to his radiation status and whether he inseminated the same or opposite genital opening as the first male. When the 2 males inseminated the same genital opening, the competitive ability of the irradiated male's sperm was dramatically reduced resulting in a lower paternity success compared with his nonirradiated rival. In contrast, when the 2 males inseminated opposite genital openings both males sired equal proportions of offspring regardless of their radiation status. We found no evidence that the timing of the second mating had any influence over paternity success.
The observed variation in paternity is not driven by the quantity of sperm transferred during mating because the amount of time invested in copulation was comparable for irradiated and nonirradiated males and was also unrelated to whether the second male inseminated the same or opposite opening as the first male. Moreover, although paternity share in N. edulis is positively correlated with both copulation frequency and duration (Schneider et al. 2000; Elgar et al. 2003; Schneider and Elgar 2005), all males in this study obtained a single copulation only. Instead, we propose that a qualitative difference between competing sperm of irradiated and nonirradiated males is the most parsimonious explanation for the superior fertilization success of nonirradiated males. Moreover, because irradiated males fared well when their sperm were not competing, such a qualitative difference probably arose because of a reduction in fertilization capability or impaired movement of sperm to the site of fertilization rather than the irradiation process having killed the sperm. These data provide direct evidence that qualitative differences in sperm can have a substantial influence on paternity success in a polyandrous spider and suggest that females may gain direct and indirect benefits from mating multiply (sensu Radwan 2003). This result also highlights the effect of the irradiated technique on sperm quality in this species and indeed may explain why previous studies that did not control for patterns of insemination have reported effects of the irradiation technique (Schneider and Elgar 2005; Elgar and Jones 2008). However, our data also allow us to speculate that, assuming males are able to assess their own sperm quality, they should adapt their behavior accordingly. Thus, males with lower quality sperm should avoid mating in previously inseminated genital openings; conversely, males with higher quality sperm may secure increased paternity success by mating in a previously inseminated opening and outcompeting their rival.
Our study suggests that N. edulis males are capable of exerting precopulatory choice, but it is unclear how they detect a previously inseminated genital opening. While chemical cues form the basis of mate detection (Dodson and Beck 1993; Evans and York-Main 1993; Papke et al. 2001) and assessment of female reproductive status (Gaskett et al. 2004) in male spiders, males lack the necessary sensilla on their pedipalps to detect such cues once mating has commenced (Eberhard 2004 and references therein). In addition, males of N. edulis do not leave the tip of their embolus within the female reproductive tract after copulation unlike other spiders (Schneider et al. 2001; Schneider et al. 2005; Snow et al. 2006). However, they do perform a characteristic drumming display with their pedipalps on a female's abdomen prior to insemination. This drumming behavior may provide the male with an indication of which side has been previously mated prior to inserting his pedipalp. Anecdotal evidence from our experiment—2 males switched pedipalps prior to sperm release and in both cases inseminated a previously unmated genital opening—suggests that N. edulis males may indeed be capable of adapting their behavior even after their initial insertion.
Detection and avoidance of previously inseminated genital openings was much less likely for N. edulis males compared with that reported for the Australian redback spider, Lactrodectus hasselti, where 95% (N = 20) of males avoided mating in a previously inseminated opening (Snow and Andrade 2005). This difference may derive in part by the extreme cost of mating for L. hasselti males: 12% are cannibalized during their first mating attempt and all males are functionally sterile after 2 matings (Andrade and Banta 2002). In contrast, rates of cannibalism are much lower for N. edulis; the vast majority of males have a second mating opportunity and can mate with up to 4 females without suffering functional sterility (Jones TM, Elgar MA, unpublished data). Additionally, mature female N. edulis are frequently found with several males on their web (Austin and Anderson 1978; Elgar et al. 2003), and they remain sexually receptive even after mating suggesting that natural mating rates during the period prior to oviposition may be high (Elgar et al. 2003; Schneider and Elgar 2005). Thus, as the season progresses, the probability of a male encountering an unmated female or a female with an unmated genital opening is low thereby reducing the selective pressure for males to detect the inseminated status of a female's reproductive tract. Nonetheless, when female mating rates and/or the density of males in the population is low, the benefits of detecting previous insemination events may be sufficient for maintenance of this male trait.
There is little evidence that the timing of the second mating had any influence on patterns of male insemination or subsequent paternity success in N. edulis. There are a number of probable explanations. First, mature females are fertile for a long period prior to laying their first egg sac; they do not appear to enter a refractory period or display overt signs of reluctance to mate again and are therefore likely to mate many times prior to oviposition (Elgar et al. 2003; Schneider and Elgar 2005). Second, males can similarly mate frequently with either the same or other females (Jones TM, Elgar MA, unpublished data). Moreover, the rate of cannibalism per mating attempt is relatively low compared with the congener N. plumipes (Schneider and Elgar 2001). Males can either guard their current female or seek further matings (Bateman 1948; Trivers 1972). In the absence of fail-safe paternity protection (Fromhage et al. 2005), the latter strategy seems most appropriate. Finally, once inside a female's reproductive tract, sperm are encapsulated into discrete packages by proteinaceous secretions that render them nonmotile until the encapsulation layer is dissolved and they become flagellate (Boissin 1973). This mechanism potentially provides females with a greater control overfertilization and enables sperm to be stored until oviposition (Uhl 1996; Burger et al. 2006). However, the time taken for encapsulated sperm to become motile once inside a female's reproductive tract and the subsequent time to oviposition may increase with female age, as for the closely related Nephila clavipes (Brown 1985). If this is the case, then sperm from later second matings may simply become motile more rapidly thus reducing any potential influence a female may have over subsequent patterns of paternity. Given the potential physiological and behavioral constraints, there maybe little advantage to either sex for influencing paternity consistently with respect to the timing of oviposition.
Our results suggest that despite having 2 separate genital openings, N. edulis females probably have limited direct postcopulatory control over paternity. When the 2 males mated in opposite openings, paternity was on average evenly distributed, suggesting that sperm are released equally from the 2 spermathecae rather than females preferentially releasing sperm from one side (sensu Uhl and Vollrath 1998a; Uhl 2000). A female may be able to move encapsulated sperm to a specific location prior to fertilization to increase the paternity success of a preferred male (Eberhard 2004), but whether this is possible or indeed has any influence on fertilization success in N. edulis is unknown. Instead, polyandrous females produce the highest quality offspring by remaining sexually receptive over a long period, thereby facilitating sperm competition within both of their seminal recepticles. This mechanism contrasts with the more dramatic, but taxonomically less widespread, mechanism of terminating copulation attempts by attempted or actual cannibalism (Elgar et al. 2000; Elgar and Schneider 2004; Snow and Andrade 2004; Snow et al. 2006).
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Funding |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Australian Research Council (DP0558265 to T.M.J.)
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ACKNOWLEDGEMENTS |
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We thank Kathryn McNamara for commenting on the manuscript and for help maintaining the spiders.
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REFERENCES |
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Andrade MCB, Banta EM. Value of male re-mating and functional sterility in redback spiders. Anim Behav (2002) 63:857–870.[CrossRef][Web of Science]
Arnaud L, Gage MJG, Haubruge E. The dynamics of second- and third-male fertilization precedence in Tribolium castaneum. Entomol Experi Appl (2001) 99:55–64.[CrossRef]
Arnqvist G, Rowe L. Sexual conflict. (2005) Princeton (NJ): Princeton University Press.
Austin AD, Anderson DT. Reproduction and development of the spider Nephila edulis (Koch) (Araneidae: Araneae). Aus J Zool (1978) 26:501–518.[CrossRef]
Bateman AJ. Intra-sexual selection in Drosophila. Heredity (1948) 2:349–368.[Web of Science][Medline]
Berendonck B, Greven H. Genital structures in the entelegyne widow spider Latrodectus revivensis (Arachnida; Araneae; Theridiidae) indicate a low ability for cryptic female choice by sperm manipulation. J Morphol (2005) 263:118–132.[CrossRef][Web of Science][Medline]
Birkhead TR. Sperm competition: evolutionary causes and consequences. Repro Fert Devel (1995) 7:755–775.[CrossRef]
Birkhead TR, Møller AP. Sperm competition and sexual selection. (1998) London: Academic Press.
Boissin L. Étude ultrastructurale de la spermiogenèse de Meta bourneti Simon (Arachnides, Aranéides, Metinae). C.R. 2e Réunion Arachnol. Expr. Francaise, Montpellier (1973) 7–22.
Boorman E, Parker GA. Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecol Entomol (1976) 1:145–455.
Brown SG. Mating behaviour of the golden orb-weaving spider, Nephila clavipes: II. Sperm capacitation, sperm competition and fecundity. J Comp Psych (1985) 99:167–175.[CrossRef]
Bukowski TC, Christenson TE. Determinants of mating frequency in the spiny orb weaving spider, Micrathena gracilis (Araneae: Araneidae). J Insect Behav (2000) 13:331–352.[CrossRef]
Burger M, Michalik P, Graber W, Jacob A, Nentwig W, Kropf C. Complex genital system of a haplogyne spider (Arachnida, Araneae, Tetrablemmidae) indicates internal fertilization and full female control over transferred sperm. J Morphol (2006) 267:166–186.[CrossRef][Web of Science][Medline]
Dodson GN, Beck MW. Pre-copulatory guarding of penultimate females by male crab spiders, Misumenoides formosipes. Anim Behav (1993) 46:951–959.[CrossRef][Web of Science]
Eberhard WG. Female control: sexual selection by cryptic female choice. (1996) Princeton (NJ): Princeton University Press.
Eberhard WG. Why study spider sex: special traits of spiders facilitate studies of sperm competition and cryptic female choice. J Arachnol (2004) 32:545–556.[CrossRef]
Eberhard WG, Guzmangomez S, Catley KM. Correlation between spermathecal morphology and mating systems in spiders. Biol J Linn Soc (1993) 50:197–209.[CrossRef][Web of Science]
Elgar MA. Sperm competition and sexual selection in spiders and other arachnids. In: Sperm competition and sexual selection—Birkhead TR, Moller AP, eds. (1998) 1 ed. San Diego (CA): Academic Press. 307–339.
Elgar MA, Champion de Crespigny FE, Ramamurthy S. Male copulation behaviour and the risk of sperm competition. Anim Behav (2003) 66:211–216.[CrossRef][Web of Science]
Elgar MA, Jones TM, Forthcoming. Size dependent mating strategies and the risk of cannibalism. Biol J Linn Soc. (2008).
Elgar MA, Schneider JM. The evolutionary significance of sexual cannibalism. Ad Study Behav (2004) 34:135–163.[CrossRef]
Elgar MA, Schneider JM, Herberstein ME. Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc R Soc Lond B (2000) 267:2439–2443.[Medline]
Engqvist L, Reinhold K. Theoretical influence of female mating status and remating propensity on male sperm allocation patterns. J Evol Biol (2006) 19:1448–1458.[CrossRef][Web of Science][Medline]
Evans TA, York-Main B. Attraction between social crab spiders: silk pheromones in Diaea socialis. Behav Ecol (1993) 4:99–105.
Fincke OM, Waage JK, Koenig W. Natural and sexual selection components of odonate mating patterns. In: The evolution of mating systems in insects and arachnids—Crespi JCaB, ed. (1997) Cambridge (UK): Cambridge University Press. 58–74.
Fisher DO, Double MC, Moore BD. Number of mates and timing of mating affect offspring growth in the small marsupial Antechinus agilis. Anim Behav (2006) 71:289–297.[CrossRef][Web of Science]
Friberg U. Male perception of female mating status: its effect on copulation duration, sperm defence and female fitness. Anim Behav (2006) 72:1259–1268.[CrossRef][Web of Science]
Fromhage L, Elgar MA, Schneider JM. Faithful without care: the evolution of monogyny. Evolution (2005) 59:1400–1405.[CrossRef][Web of Science][Medline]
Galeotti P, Pupin F, Rubolini D, Sacchi R, Nardi PA, Fasola M. Effects of female mating status on copulation behaviour and sperm expenditure in the freshwater crayfish Austropotamobius italicus. Behav Ecol Sociobiol (2007) 61:711–718.[CrossRef][Web of Science]
Gaskett AC, Herberstein ME, Downes BJ, Elgar MA. Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae: Araneidae). Behaviour (2004) 141:1197–1210.[CrossRef]
Ginsberg JR, Huck UW. Sperm competition in mammals. Trends Ecol Evol (1989) 4:74–79.[CrossRef]
Iwata Y, Munehara H, Sakurai Y. Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Mar Ecol (2005) 298:219–228.
Johansson B, Jones TM. The role of chemical signals in sexual selection. Biol Rev Cam Soc (2007) 82:265–289.[CrossRef]
Nessler SH, Uhl G, Schneider JM. Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success. Behav Ecol (2007) 18:174–181.
Norton S, Uetz GW. Mating frequency in Schizocosa ocreata (Hentz) wolf spiders: evidence for a mating system with female monandry and male polygyny. J Arachnol (2005) 33:16–24.[CrossRef]
Papke MD, Riechert SE, Schulz S. An airborne female pheromone associated with male attraction and courtship in a desert spider. Anim Behav (2001) 61:877–886.[CrossRef][Web of Science]
Parker GA. Sperm competition and its evolutionary consequences in the insects. Biol Rev Cam Phil Soc (1970) 45:525–567.
Parker GA. Sperm competition and the evolution of animal mating strategies. In: Sperm competition and the evolution of animal mating strategies—Smith RL, ed. (1984) London: Academic Press. 2–60.
Parker GA. Sperm competition games—raffles and roles. Proc R Soc Lond B (1990) 242:120–126.
Preston BT, Stevenson IR, Wilson K. Soay rams target reproductive activity towards promiscuous females' optimal insemination period. Proc R Soc Lond B (2003) 270:2073–2078.[Medline]
Radwan J. Male age, germline mutations and the benefits of polyandry. Ecol Lett (2003) 6:581–586.[CrossRef][Web of Science]
Schaefer D, Uhl G. Male competition over access to females in a spider with last-male sperm precedence. Ethology (2003) 109:385–400.[CrossRef][Web of Science]
Schneider JM, Elgar MA. Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes (Araneoidea): female and male perspectives. Behav Ecol (2001) 12:547–552.
Schneider JM, Elgar MA. The combined effects of pre- and post-insemination sexual selection on extreme variation in male body size. Evol Ecol (2005) 19:419–433.[CrossRef]
Schneider JM, Fromhage L, Uhl G. Copulation patterns in the golden orb-web spider Nephila madagascariensis. J Ethol (2005) 23:51–55.[CrossRef]
Schneider JM, Herberstein ME, De Crespigny FC, Ramamurthy S, Elgar MA. Sperm competition and small size advantage for males of the golden orb-web spider Nephila edulis. J Evol Biol (2000) 13:939–946.[CrossRef][Web of Science]
Schneider JM, Thomas ML, Elgar MA. Ectomised conductors in the golden orb-web spider, Nephila plumipes (Araneoidea): a male adaptation to sexual conflict? Behav Ecol Sociobiol (2001) 49:410–415.[CrossRef][Web of Science]
Sheldon BC. Timing and use of paternity guards by male chaffinches. Behaviour (1994) 129:79–97.
Simmons LW. Sperm competition and its evolutionary consequences in the insects. (2001) Princeton (NJ): Princeton University Press.
Simmons LW, Siva-Jothy MT. Sperm competition in insects: mechanisms and the potential for selection. In: Sperm competition and sexual selection—Birkhead TR, Møller AP, eds. (1998) London: Academic Press. 341–434.
Siva-Jothy MT, Blake DE, Thompson J, Ryder JJ. Short- and long term sperm precedence in the beetle Tenebrio molitor: a test of the ‘adaptive sperm removal’ hypothesis. Physiol Entomol (1996) 21:313–316.[CrossRef]
Snow LSE, Abdel-Mesih A, Andrade MCB. Broken copulatory organs are low-cost adaptations to sperm competition in redback spiders. Ethology (2006) 112:379–389.[CrossRef][Web of Science]
Snow LSE, Andrade MCB. Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice. Behav Ecol (2004) 15:785–792.
Snow LSE, Andrade MCB. Multiple sperm storage organs facilitate female control of paternity. Proc R Soc Lond B (2005) 272:1139–1144.[Medline]
Suzuki N, Okuda T, Shinbo H. Sperm precendence and sperm movement under different copulation intervals in the silkworm Bombyx mori. J Insect Physiol (1996) 42:199–204.[CrossRef][Web of Science]
Trivers RL. Parental investment and sexual selection. In: Sexual selection and the descent of man, 1871–1971—Campbell B, ed. (1972) Chicago: Aldine-Atherton.
Uhl G. Sperm storage secretion of female cellar spiders (Pholcus phalangioides; Araneae): a gel-electrophoretic analysis. J Zool (1996) 240:153–161.[Web of Science]
Uhl G. Female genital morphology and sperm priority patterns in spiders (Araneae). In: Proceedings of the 19th European Colloquium of Arachnology—Toft S, Scharff N, eds. (2000) Aarhus (Denmark): Aarhus University Press. 145–156.
Uhl G, Vollrath F. Genital morphology of Nephila edulis: implications for sperm competition in spiders. Can J Zool (1998a) 76:39–47.[CrossRef]
Uhl G, Vollrath F. Little evidence for size-selective sexual cannibalism in two species of Nephila (Araneae). Zool Anal Complex Syst (1998b) 101:101–106.
Wysocki D, Halupka K, Wedell 2005. The frequency and timing of courtship and copulation in blackbirds, Turdus merula, reflect sperm competition and sexual conflict. Behaviour (2004) 141:501–512.[CrossRef]
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