Behavioral Ecology Advance Access originally published online on November 28, 2006
Behavioral Ecology 2007 18(1):174-181; doi:10.1093/beheco/arl074
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success
a Biozentrum Grindel, Department of Ethology, University of Hamburg, Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany b Institute of Zoology, Department of Neuroethology, University of Bonn, Germany
Address correspondence to S.H. Nessler. E-mail: stefan.nessler{at}web.de.
Received 2 January 2006; revised 18 August 2006; accepted 17 September 2006.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The morphology of male genitalia often suggests functions besides sperm transfer that may have evolved under natural or sexual selection. In several species of sexually cannibalistic spiders, males damage their paired genitalia during mating, limiting them to one copulation per pedipalp. Using a triple-mating experiment, we tested if genital damage in the orb-web spider Argiope bruennichi increases male fitness either through facilitating his escape from an aggressive female or by obstructing the female's insemination ducts against future copulation attempts from other males. We found no survival advantage for males damaging their pedipalps; however, copulations into a previously used insemination duct were significantly shorter when the previous male had left parts of his genitalia inside the insemination duct. Because copulation duration determines paternity in this species, our result suggests that male genital damage in A. bruennichi is sexually selected. By breaking off parts of their intromittent organs inside a virgin female, males can reduce sperm competition and thereby increase their paternity success.
Key words: mating plug, sexual cannibalism, sexual conflict, sexual selection, sperm competition.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Sperm competition results in strong postmating sexual selection favoring male defense and offense strategies that increase a male's relative paternity success (Parker 1970
; Simmons 2001). So-called mating plugs are well-known features often associated with a defense function. Plugs are mostly secretory, amorphous structures that are applied by the male into or over the female's genital opening after sperm transfer (Parker 1970; Elgar 1998). Although several functions of secretory plugs have been identified (Lange and Loughton 1985; Matsumoto and Suzuki 1992; Andersson et al. 2000), the most obvious function is that they act as a physical barrier against remating (Shine et al. 1999; Polak et al. 2001).
Plugs might also be formed by copulatory organs that partly or completely break off during copulation and remain in the insemination duct of the female (Wiehle 1967; Levi 1968; Berendonck and Greven 2002). Little attention has been paid to the understanding of the adaptive value of such plugs, even though by damaging their genitalia, males usually forfeit their future mating opportunities. Hence, we expect a large advantage in sexual selection to balance out the costs. Indeed, several studies on different insect taxa suggest that males can successfully protect their sperm against future rivals by blocking female insemination ducts with their own genitalia (Monnin and Peeters 1998; Strassmann 2001; Kamimura 2003).
Males of several spider species have been reported to damage their genitalia during copulation (Wiehle 1967; Foelix 1996; Schneider et al. 2001), but in contrast to the majority of insects, male entelegyne spiders have paired secondary copulatory organs, the pedipalps (Figure 1B). Female genitalia are equally paired with 2 independent insemination ducts leading to 2 independent spermathecae (Figure 1C). Importantly, in species that are known to damage their genitalia males generally use only one pedipalp during any copulatory bout limiting potential plugging to one insemination duct at a time.
|
Whereas one observational (Knoflach and van Harten 2001
) and one experimental study support a plug function (Snow et al. 2006), others are less conclusive. Some studies found genital parts of several males in a single insemination duct (Wiehle 1967; Berendonck and Greven 2002), and results of a sperm competition experiment in the spider Nephila plumipes did not provide evidence for a plug function (Schneider et al. 2001). As an alternative functional explanation, the authors suggested that breakage of the tip of the male pedipalp may facilitate male survival from the regular female cannibalistic attacks. Sexual cannibalism is expected to exert a strong selective force on males (reviewed by Elgar and Schneider 2005; Prenter et al. 2006) although to date only few studies identified male strategies that prevent a successful female attack (Moya-Laraño et al. 2004; Fromhage and Schneider 2005a; Bilde et al. 2006). A possible function of genital damage in the context of avoidance of sexual cannibalism is further implied by the dual function of male genitalia in spiders. Besides serving sperm transfer, pedipalps have several appendices that facilitate genital coupling. These male structures have to match corresponding structures of the females for copulation to be successful. In sexually cannibalistic species, a trade-off may exist between optimizing sperm transfer through firm genital coupling and escaping when the female attacks. Ectomizing a part of the pedipalp may allow the male to quickly jump off the female. Interestingly, genital damage is found in many of the notoriously cannibalistic spider genera, such as Latrodectus, Nephila, and Argiope. Current knowledge suggests that in these species, males use each of their pedipalps only once and thus have low mating rates (Herberstein et al. 2005; Fromhage and Schneider 2006). However, a direct causal connection between genital damage and low mating rates has not been established yet (Schneider et al. 2006). Regardless of the direct cause of low mating rates, selection should act strongly on males to maximize paternity success with the single female with which they are likely to mate.
In the highly cannibalistic spider genus Argiope, genital damage is reported from several species (Levi 1968, 1975, 1983), but the adaptive value is unclear. In this paper, we use Argiope bruennichi to test 2 alternative adaptive explanations for genital damage: the "mating plug hypothesis" requires that genital damage helps to avoid sperm competition, whereas the "survival hypothesis" requires that genital damage facilitates survival under female attack. A. bruennichi females are polyandrous and have not been observed to reject a courting male. However, immediately after the onset of copulation, females attack the copulating male. Males with no prior mating experience will generally try to survive their first copulation but only 20% of males succeed (Fromhage et al. 2003; Schneider et al. 2005b). Usually, males never survive a second copulation. In most cases, second copulations are longer than first copulations, and copulation duration is positively linked to sperm transfer and relative paternity success (Schneider et al. 2006). Because males use each pedipalp only once, it is plausible that a male will achieve maximal fitness if he can empty both of his palps. Consequently, he will suffer severe fitness costs if he cannot escape a first, usually brief insertion. If genital damage evolved in this context, the survival hypothesis predicts that the frequency of genital damage should be high during a first insertion and low during the second insertion when males do not attempt to escape.
Alternatively or additionally, genital damage may function as a mating plug to avoid sperm competition. Previous investigations showed that in A. bruennichi copulations in used insemination ducts were shorter than copulations in unused ducts (Fromhage and Schneider 2005b). The mating plug hypothesis predicts that pedipalp fragments either prevent subsequent males from copulating into the previously used insemination duct or at least shorten the male's copulation duration.
|
MATERIAL AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Study animals
Subadult males and females of the araneid spider A. bruennichi (Scopoli 1772) were collected in June and July 2004 from their webs from different meadows near Bonn, Germany. In the laboratory, the animals were housed in plastic cups (5 x 10 cm in diameter and height) and were fed every second day on a diet of Drosophila and watered twice per day on 6 days per week. After the final molt, females were transferred to perspex frames (30 x 30 x 6 cm) where they built their typical orb webs. Adult males remained in plastic cups until the start of the mating experiment. Age is given as days elapsed from the final molt until the day of the experiment.
Because males mature earlier than females, they were significantly older (mean ± standard error [SE] 18.51 ± 0.71 days, n = 146) than females (9.75 ± 1.16 days, n = 53; Mann–Whitney U test: z = –5.80, P < 0.0001) when they were used for the experiments.
Male and female body size was measured under a microscope as the length of tibia plus patella of the first leg. Females were weighed after copulation and males the day before or on the day of the first mating trial on a mechanical balance (accuracy 0.01 mg).
Experimental protocol
General protocol
Matings were staged by placing a male in an upper corner of the female's web. Females usually swung in the hub as soon as they detected a male on their web and males almost immediately approached the female and began courtship. In 90% (148 out of 165) of all observed cases, courtship was followed by a copulation that always ended with the females' attacking with or without the result of cannibalism (79%, Ncannibalized = 117, Nsurvived = 31). Because males were removed from the female for investigating the state of their genitalia, cannibalism is here defined as the capture but not the consumption of the male.
We recorded which pedipalp the male used, which insemination duct he inserted into (left or right), and whether cannibalism occurred or not.
Copulation duration was defined as the time period between insertion and removal of the pedipalp. Schneider et al. (2006) have shown that in A. bruennichi paternity success depends on copulation duration: if 2 males mate with the same female, the one that mates the longest fertilizes most eggs. We took advantage of this established relationship and measured the duration of copulation as proxy of relative paternity success. In this study, the average copulation duration was 16.9 s (median = 8, mean ± SE = 16.9 ± 2 s, N = 146; range = 1–160 s).
All males and females were killed by hypothermia and fixed in 70% ethanol immediately after the end of the trial and investigated under a stereomicroscope. We removed the used pedipalps and inspected them for possible damage. The females' genitalia were macerated with NaOH to become translucent, which allowed us to detect pedipalp fragments inside the insemination ducts (Figure 1).
Survival hypothesis: genital damage facilitates survival
To test the survival hypothesis, we mated 28 virgin males and 26 mated males (males with a previous mating experience—hence only one functional pedipalp) to one virgin female each (Figure 2). Males and females were randomly assigned to the treatment groups. Females did not differ in size, mass, and age between the 2 treatments (Table 1).
|
|
Mated males were produced by allowing the male a single insertion with a virgin female. To prevent cannibalism of the male, copulations were interrupted after about 3 s with a jet of water from a hand sprayer. From previous studies, we know that a mating of 3 s was sufficient to cause sterility of the used pedipalp (Fromhage and Schneider 2005b
). After at least 5 min of convalescence, mated males were introduced to the web of the virgin female for the test. In the field, males usually climb back and initiate a second mating immediately after their first copulation. They thus do not seem to require longer periods of convalescence. Five minutes does also realistically mimic the time required to encounter a new female. Densities are very high with about 3 webs per m2 (Crome W and Crome I 1961; Nessler SH, personal observation). Virgin and mated males were restricted to a single insertion into one of 2 insemination ducts of the female. The survival hypothesis predicts that genital damage should predominantly occur in matings with virgin males but not in matings with previously mated males. This is because virgin males benefit from another mating opportunity whereas mated males have already used one pedipalp and only benefit from copulating as long as possible during their final, second copulation.
Mating plug hypothesis: genital damage as mating plugs
To test the mating plug hypothesis, we mated each of the 54 females of the previous experiment with 2 additional virgin males in succession (Figure 3A,B). We forced males to insert into the used insemination duct of the females from the previous experiment (Figure 3A, second matings) and subsequent males to insert into the unused side (Figure 3B, third matings). With our experimental design, we can distinguish between the effects of insemination duct status (unused/used) and female status (virgin/mated) on the copulation duration of males. Further, we can compare copulation durations of males that mated in unused ducts of both virgin and mated females.
|
Due to the fixed ipsilateral copulation scheme, right pedipalps can only be inserted into the right insemination duct and left pedipalps only into the left side. Selectively amputating a palp thus allowed us to determine into which of the insemination ducts a male will introduce his remaining pedipalp. Pedipalps were removed by squeezing the femur with tweezers until the male autotomized the appendage without losing hemolymph. Males were not noticeably affected by the treatment as was shown for a lycosid spider previously (Rovner 1967
). Males were mated after at least 5 min of convalescence. We consider it highly unlikely that the fixed order of males that mated into used (second male, Figure 3A) or unused sides (third male, Figure 3B) had an effect on copulation duration, cannibalism, damage, and plugging frequency as the dependent variables because the 2 males used different, independent insemination ducts. In addition, copulations mostly occurred within hours of the same day (see below), and we have no indication that second and third males behaved differently. Nevertheless, we cannot exclude the possibility that some of the observed differences between males that mated into used or unused ducts of mated females were attributed to the mating order.
We could not in all cases identify which pedipalp was used by the first male; hence 3 mating trials deviated from our mating protocol such that the second male mated into an unused and the third male into a used insemination duct.
In contrast to males paired to virgin females, not all second and third males copulated. If the second copulation (Figure 3A) did not occur within 30 min of placing a male with a female, we used a maximum of 2 replacement males. If none of the 3 males mated within 30 min each, we scored the trial as "no remating in used side" (N = 7) and proceeded to introduce the third male that had to mate into the unused side (Figure 3B). Again we used a maximum of 2 replacement males that were observed for 30 min each and scored the trial as "no remating in unused side of mated female" (N = 10) if no copulation took place.
We tried to achieve all 3 matings per female within a single day (day 1). However, we did not succeed in 6 cases: 1 second and 5 third males were mated between 1 and 13 days after the first mating (6.17 ± 2.23, N = 6). In order to control for possible influences of the interval between matings on our dependent variables, we compared third males that mated on day 1 (N = 40) with third males that mated on a day after day 1 (N = 5). We found no significant differences in copulation duration (linear regression t = 0.29, P = 0.77), frequency of genital damage (logistic fit 
2 = 0.11, P = 0.74), and probability of cannibalism (logistic fit 2 = 0.30, P = 0.58) between these 2 groups of males.
Data analyses were carried out with JMP 4.0.2. and SPSS 10.0.7. All statistical tests are 2-tailed (
= 0.05). Sample sizes may differ between analyses because not all data were available for each mating trial. Descriptive statistics are given as mean ± SE. We were not able to obtain a normal distribution with equal variances for copulation duration as the dependent variable. Although the requirements for parametric statistics are not fulfilled, we nevertheless performed analyses of variance using Box-Cox transformed data, and we checked the robustness of the result with additional nonparametric tests.
One male copulated for 406s that is extraordinarily longer than is usual in A. bruennichi. We excluded this extreme outlier in tests that involve copulation duration.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Survival hypothesis: damaged pedipalps facilitate survival
Although virgin and mated males did not differ in mass and size, mated males were significantly older than virgin males (Table 1). Hence, any comparison between virgin and mated males is confounded by age. Consequently, we need to take age into account when analyzing the effects of our treatment.
Should genital damage facilitate escape, its probability should be higher in virgin than in mated males. Virgin males escaped the female's attack with higher probability (9/28) than mated males (1/26; 2 = 7.15, Nvirgin = 28, Nmated = 26, P = 0.0075; Figure 4A), but neither male mating history (G test2,53 = 1.95, P = 0.16) nor male age (G test2,53 = 1.09, P = 0.30; full model: G test2,53 = 4.11, r2 = 0.09, P = 0.13) had an effect on frequency of genital damage (virgin males 26/28; mated males 20/26, respectively; Figure 4A). Males with damaged genitalia did not survive with a higher probability than males with intact genitalia regardless of their mating status (G test1,54 = 0.23, Ncannibalized = 46, Nescaped = 8, P = 0.63).
|
Mated males copulated significantly longer (40 ± 8.16 s, N = 26) than virgin males (8.67 ± 1.49 s, N = 27; U test: z = –4.49, P < 0.0001; Figure 4B), and copulation duration was not correlated with age neither in mated males (spearman correlation: rs = 0.15, N = 26, P = 0.48) nor in virgin males (rs = 0.11, N = 27, P = 0.59). In addition to the nonparametric tests, we performed an analysis of covariance (ANCOVA) investigating the effect of the treatment corrected for age on the duration of copulation even though we could not achieve a normal distribution of the dependent variable. The analysis suggests that male mating history is a stronger predictor of copulation duration than male age (F2,49 = 14.82, r2 = 0.38, P < 0.0001; Fmale mating history = 18.22, P
0.0001; Fmale age = 3.38, P = 0.07). Thus, even though virgin males survived with higher probability and had shorter copulations, genital damage did not seem to be related neither to the mating history of the male nor to the sexual cannibalism directly.
Mating plug hypothesis: damaged pedipalps as mating plugs
The mating plug hypothesis predicts that copulations into plugged insemination ducts should be impossible or at least shortened.
Copulations into used sides (second males: 9.46 ± 1.71 s, N = 48) were significantly shorter than copulations into unused sides (third males: 16.02 ± 2.34 s, N = 43; Wilcoxon matched-pair test: z = –2.37, N = 40, P = 0.018; Figure 5A). These 2 groups did not differ in age, weight, and size (Table 2B).
|
|
In order to investigate whether mating plugs were responsible for the differences, we compared copulation durations of second males that mated into used ducts that did or did not contain a plug. We found that copulations into insemination ducts that contained a plug were significantly shorter (7.06 ± 1.82 s, N = 33) than copulations into used ducts not containing a plug (15.33 ± 3.89 s, N = 9; U test: z = 2.15, P = 0.031; Figure 5B).
However, by chance those 9 males that had used unplugged insemination ducts were significantly older (23.22 ± 2.45 days, N = 9) than the males that had mated into plugged sides (16.91 ± 1.36 days, N = 33; U test: z = 2.28, P = 0.02). A previous study found that older males were more likely to be cannibalized and thus had longer copulation durations (Schneider et al. 2006). If we compare the copulation duration of all cannibalized second males that used unplugged (N = 9) or plugged ducts (N = 24), the difference is no longer significant (U test: z = 1.56, P = 0.12). With this particular data set, it is hence not possible to decide whether age or the presence of a plug explained the difference in copulation duration. This may be due to the low sample size in the group of males that mated into unplugged ducts.
Therefore, in order to statistically control for the potential confounding effect of age, we combined the second males that copulated into unplugged sides with the third males that also copulated into unplugged sides of mated females. Both groups did not differ in copulation duration (U tests: z = 0.11, Nsecond = 9, Nthird = 42, P = 0.91), in age (z = 1.26, Nsecond males = 9, Nthird males = 42, P = 0.21), or in frequency of cannibalism (Nsecond males = 9/9, Nthird males = 35/42, 83%; 2 = 1.98, P = 0.16). In this way, we increased the sample size of males that mated into insemination ducts that had no obstruction for an ANCOVA with age as covariate. The analysis revealed that only the condition of the insemination duct (plugged/unplugged) had an effect on copulation duration (F = 16.65, P = 0.0001) but not age (F = 0.05, P = 0.83; full model: F2,82 = 8.87, r2 = 0.18, P = 0.0003).
Our experimental design allowed us to test the effect of female mating history (virgin/mated) on the copulation duration of males. We found that copulations into unused ducts of mated females were significantly longer (third males: 17.95 ± 3.27, N = 21) than copulations into unused ducts of virgin females (first virgin males: 8.67 ± 1.49, N = 27; Wilcoxon matched-pair test: z = –2.86, N = 20, P = 0.004). The 2 groups of males did not differ in age, weight, size (Table 2), and cannibalism frequency (Nfirst males = 19/28, 68%; Nthird males = 35/44, 80%; 2 = 1.25, P = 0.26).
Damage probability and plugging success
Pedipalp fragments that broke off did not always remain inside the female ducts, suggesting that some males were unsuccessful in plugging the female. We compared the frequencies of genital damage and successful plugging between males that mated with virgin females into unused ducts (first virgin and mated males) and males that copulated with mated females into either used (second males) or unused ducts (third males; Figure 6). In 7 cases, we could not assign the pedipalp fragments to one of the 2 males that mated into the same duct because both males had damaged pedipalps. These cases were excluded from the analysis.
|
Damage frequency was 85% when males copulated into unused ducts of virgin females (46 of 54), 22% when males copulated into used ducts (11 of 49), and 73% when males copulated into unused insemination ducts of mated females (32 of 44; Figure 6). A multiple logistic regression revealed that damage frequency was mainly explained by the condition of the insemination duct (previously used or not), less so by female mating history, and not by male mating history (G test3,147 = 50.00, r2 = 0.25, P < 0.0001; condition of insemination duct: G = 25.15, regression coefficient r = –1.12, P = 0.0001; female mating history: G = 4.1, r = 0.66, P = 0.04; male mating history: G = 1.86, r = 0.5, P = 0.17). Post hoc tests showed that damage frequency was significantly lower when the insemination duct was previously used, while we found no difference in the probability of breakage when males copulated into unused ducts of either virgin or mated females (statistical tests in Figure 6). Therefore, it seems unlikely that female mating history had an effect on damage frequency.
In order to determine plugging success, we tested how many of the ectomized pedipalp fragments remained stuck in the female's insemination duct depending on the condition of the duct. The proportion of successful plugging was 97% when males copulated in an unused insemination duct of either virgin (38 out of 39) or mated (31 out of 32,) females and 75% when males copulated in used ducts (3 out of 4). Plugging success did not differ statistically between the treatments (G test2,75 = 4.87, P = 0.09). Due to the low sample size in the latter group, these results should be interpreted with caution.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
In A. bruennichi, males mate twice in their lifetime because they use each of their pedipalps only once. During mating, pedipalps are damaged, and we asked whether genital damage has a function of facilitating rapid detachment of genitalia after a female attack or whether it is a strategy that reduces sperm competition by blocking the female genital system. We found that mated males mated for longer and were cannibalized with higher probability than virgin males. However, the frequency of genital damage was similar between groups. We found strong evidence for the mating plug hypothesis because genital damage shortened copulations of males that copulated into plugged ducts. Not all males were equally successful in plugging the female. Of all males that mated with a virgin female, 15% did not break their genitalia and 3% did not place the broken off piece into the female insemination duct. Hence, almost 20% of the males that copulated with a virgin female failed to decrease sperm competition.
Prolonged copulations are commonly associated with increased paternity shares (Saul et al. 1988; Wolf et al. 1989) and of fundamental importance for postcopulatory sexual selection in many invertebrates (Simmons 2001), including many spiders (Elgar 1998). In the highly cannibalistic species A. bruennichi, previous experiments showed that a positive relationship between copulation duration and paternity arises through time-dependent sperm transfer (Schneider et al. 2006).
Following a suggestion for the function of genital damage in N. plumipes (Schneider et al. 2001), we hypothesized that genital damage could be a means to survive the attack of a female. Although death after the second copulation may not have a strong impact on male fitness because 2 copulations are the maximum a male can achieve, surviving the first insertion is likely extremely relevant. Indeed, virgin males survived with a higher probability than mated males. However, in opposition to the prediction of the survival hypothesis, they did not damage their genitalia more often. Unfortunately, the effect of male mating status was confounded by male age such that mated males were significantly older than virgin males. In A. bruennichi, older males are cannibalized with a higher probability than younger males, and cannibalized males have longer copulation durations (Schneider et al. 2006). However, we did not find a correlation between male age and copulation duration within the virgin and mated samples of males in this study so that an effect, if present, may not be very large.
Alternatively, we hypothesized that the function of genital damage is to reduce sperm competition and our results clearly support this idea. Parts of male genitalia can obstruct the insemination duct of a female (Figure 1 C,D) such that subsequent copulations are significantly impaired. Again, the results are confounded by an unplanned bias in male age. Males that happened to mate into a used insemination duct that the previous male did not successfully plug mated longer but were also older than males that used a successfully plugged duct. Therefore, copulations of the first group of males may have been longer because older males were more often cannibalized (Schneider et al. 2006). Perhaps due to the small number of males that mated into unplugged sides, any comparisons within the group of second males did not allow a confident exclusion of a confounding age effect. As an additional test, we compared the copulations of males that mated into plugged ducts with all second and third males that mated into unplugged ducts and included age as a factor in the model. In the model, age was not a significant covariate, whereas the condition status of the insemination duct (plugged/not plugged) was, suggesting that age had no effect on copulation duration. Additionally, recent experiments that independently controlled for effects of age no longer support an influence of time since maturity per se (Nessler SH and Schneider JM, unpublished observations).
A second shortcoming is that the order of males that mated into the used and unused duct of a mated female was fixed in most cases. Hence, we cannot unambiguously distinguish whether differences between second and third males are due to the order of mating or to the condition of the spermatheca. However, we consider the former possibility unlikely to be of high relevance for several reasons: 1) most copulations happened in quick succession so that no changes to the web occurred (Gaskett et al. 2004); 2) males did not obviously behave differently; 3) males mated into different insemination ducts, and as their second pedipalp was removed, they had no means to probe the other side; moreover, males usually proceeded immediately to copulation without appearing to sample information about the female; and 4) males never attempted to use the stump of the amputated pedipalp.
Although males could not prevent rivals from mating into the same insemination duct, it is unclear whether sperm transfer occurred during these copulations. Preliminary morphological examinations indicate that sperm transfer by males copulating into plugged ducts may be unlikely because the pedipalp fragment tightly obstructs the insemination duct. Further investigations are necessary that quantify sperm transfer rates and paternity success under such circumstances. Interestingly, males do not seem to notice before actual mating whether a duct is obstructed or not.
Genital damage has been described for many spider species (Wiehle 1967; Levi 1975; Schneider et al. 2001; Berendonck and Greven 2002); however, its adaptive function has rarely been tested experimentally (Snow et al. 2006). Recently, it was observed for the cannibalistic Nephila fenestrata that genital damage reduces the chance of female remating (Fromhage and Schneider 2006). In the congener Nephila madagscariensis, Schneider et al. (2005a) suggested that pedipalp fragments obstructing the female's insemination duct may prevent subsequent males from copulating or at least hinder further copulations. In the species Tidarren argo, males even show a more bizarre behavior: males leave the whole pedipalp attached to the female's genital organ and it is discussed that it acts as a temporary mating plug (Knoflach and van Harten 2001).
Interestingly, genital damage can often be found in sexually cannibalistic species, suggesting a causal connection. Under the most common circumstances, genital damage seems a very drastic means to prevent sperm competition because males thereby forfeit all future mating opportunities in most (Berendonck and Greven 2002; Herberstein et al. 2005; Fromhage and Schneider 2006) but not all species (Breene and Sweet 1985). However, especially in species with monogynous males and polyandrous females the evolution of such traits may be favored if it increases the relative paternity share of males (Fromhage et al. 2005).
The function of genital damage in other invertebrate taxa is ambiguous. In honeybees, it is discussed that genital damage prevents semen from flowing out of the female's insemination duct immediately after mating (review by Strassmann 2001). Melo et al. (2001) reported that in the stingless bee Melipona quadrifasciata, queens' ovarian activation is triggered by stimulation of a genital fragment that remains in the genital chamber after mating, but it has not been tested yet whether genital damage may also function as mating plug. Only in the ant Dinoponera quadriceps, where the female cuts off the abdomen of the male during copulation, Monnin and Peeters (1998) found strong evidence for genital damage effectively preventing remating.
Although in A. bruennichi plugged insemination ducts lead to shorter copulations, males that copulated into the unused duct of a mated female had longer copulations than males that mated with a virgin female. It is known for many species (Simmons 2001) that males adjust their copulation duration to the female mating history. This is in accordance with Parker's (1998) sperm competition risk model, which states that males should increase their ejaculate expenditure when mating with a female that has already mated. In several species, copulation duration is associated with higher paternity success because males flush out and replace sperm of previous males (Siva-Jothy 1987; Siva-Jothy and Tsubaki 1989) or, when sperm mixes randomly, males with longer copulations are more likely to fertilize more eggs (Simmons and Siva-Jothy 1998). However, in the present study, males copulated into an unused, independent spermatheca, and thus males cannot remove or displace rival sperm, and sperm of different males did not get into direct contact. Still, fertilization success under sperm competition in A. bruennichi is a function of the relative duration of copulation and transferred sperm numbers (Schneider et al. 2006). How the females organize sperm usage for fertilization from their 2 independent spermathecae is unknown.
In summary, this study indicates that genital damage in A. bruennichi is not an adaptation to sexual cannibalism, but it rather suggests that sexual selection through sperm competition is the driving force.
|
ACKNOWLEDGEMENTS |
|---|
We thank G. von der Emde and K.-P. Sauer for providing workplace; many thanks to Lutz Fromhage for helpful comments on the manuscript. We thank A. Pauly and U. Sorciere for help with collecting spiders, and U. Grundtner and B. Bauch for their assistance in looking after the spiders; and we thank Rudy Joqué for assistance with digital imaging software. The research was supported by a D.F.G. grant to J.M.S.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson J, Borg-Karlson A-K, Wiklund C. (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B Biol Sci 267:1271–1275.[Medline]
Berendonck B and Greven H. (2002) Morphology of female and male genitalia of Latrodectus revivensis Shulov, 1948 (Araneae, Theridiidae) with regard to sperm priority patterns. In Toft S and Scharff N (Eds.). European arachnology 2000(Aarhus University Press, Aarhus (Denmark)) pp. 157–167.
Bilde T, Tuni C, Elsayed R, Pekar S, Toft S. (2006) Death feigning in the face of sexual cannibalism. Biol Lett 2:23–25.
Breene RG and Sweet MH. (1985) Evidence of insemination of multiple females by the male black widow spider Latrodectus mactans (Araneae, Theridiidae). J Arachnol 13:331–335.
Crome W and Crome I. (1961) Paarung und Eiablage bei Argyope bruennichi (SCOPOLI) auf Grund von Freilandbeobachtungen an zwei Populationen im Spreewald/Mark Brandenburg (Araneae: Araneidae). Mitt Zool Mus Berlin 37:189–254.
Elgar MA. (1998) Sperm competition and sexual selection in spiders and other arachnids. In Birkhead TR and Moeller AP (Eds.). Sperm competition and sexual selection(Academic Press, San Diego (CA)) pp. 307–339.
Elgar MA and Schneider JM. (2005) The evolutionary significance of sexual cannibalism. Adv Stud Behav 34:135–163.
Foelix RF. (1996) Biology of spiders 2nd ed. (Oxford University Press, Oxford).
Fromhage L, Elgar MA, Schneider JM. (2005) Faithful without care: the evolution of monogyny. Evolution 59:1400–1405.[CrossRef][Web of Science][Medline]
Fromhage L and Schneider JM. (2005a) Safer sex with feeding females: sexual conflict in a cannibalistic spider. Behav Ecol 16:377–382.
Fromhage L and Schneider JM. (2005b) No discrimination against previous mates in a sexually cannibalistic spider. Naturwissenschaften 92:423–426.[CrossRef][Web of Science][Medline]
Fromhage L and Schneider JM. (2006) Emasculation to plug up females: the significance of pedipalp damage in Nephila fenestrata. Behav Ecol 17:353–357.
Fromhage L, Uhl G, Schneider JM. (2003) Fitness consequences of sexual cannibalism in female Argiope bruennichi. Behav Ecol Sociobiol 55:60–64.[CrossRef][Web of Science]
Gaskett AC, Herberstein ME, Downes BJ, Elgar MA. (2004) Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae: Araneidae). Behaviour 141:1197–1210.[CrossRef][Web of Science]
Herberstein ME, Gaskett AC, Schneider JM, Vella NGF, Elgar MA. (2005) Limits to male copulation frequency: sexual cannibalism and sterility in St Andrew's cross spiders (Araneae, Araneidae). Ethology 111:1050–1061.[CrossRef][Web of Science]
Kamimura Y. (2003) Effects of broken male intromittent organs on the sperm storage capacity of female earwigs, Euborellia plebeja. J Ethol 21:29–35.
Knoflach B and van Harten A. (2001) Tidarren argo sp. nov. (Araneae: Theridiidae) and its exceptional copulatory behaviour: emasculation, male palpal organ as a mating plug and sexual cannibalism. J Zool 254:449–459.[CrossRef]
Lange AB and Loughton BG. (1985) An oviposition-stimulating factor in the male accessory reproductive gland of the Locust, Locusta migratoria. Gen Comp Endocrinol 57:208–215.[CrossRef][Web of Science][Medline]
Levi HW. (1968) The spider genera Gea and Argiope in America (Araneae: Araneidae). Bull Mus Comp Zool 136:319–351.
Levi HW. (1975) Mating behavior and presence of embolus cap in male Araneidae. In: Proceedings of the 6th International Arachnological Congress 1974. p 4:9–50.
Levi HW. (1983) The orb-weaver genera Argiope, Gea, and Neogea from the Western Pacific Region (Araneae: Araneidae, Argiopinae). Bull Mus Comp Zool 150:247–338.
Matsumoto K and Suzuki N. (1992) Effectiveness of the mating plug in Atrophaneura alcinous (Lepidoptera: Papilionidae). Behav Ecol Sociobiol 30:157–163.[CrossRef][Web of Science]
Melo G, Buschini MLT, Campos LAO. (2001) Ovarian activation in Melipona quadrifasciata queens triggered by mating plug stimulation (Hymenoptera, Apidae). Apidologie 32:355–361.[CrossRef][Web of Science]
Monnin T and Peeters C. (1998) Monogyny and regulation of worker mating in the queenless ant Dinoponera quadriceps. Anim Behav 55:299–306.[CrossRef][Web of Science][Medline]
Moya-Laraño J, Pacual J, Wise DH. (2004) Approach strategy by which male Mediterranean tarantulas adjust to the cannibalistic behaviour of females. Ethology 110:717–724.[CrossRef][Web of Science]
Parker GA. (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567.[CrossRef]
Parker GA. (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In Birkhead TR and Møller AP (Eds.). Sperm competition and sexual selection(Academic Press, San Diego (CA)) pp. 3–54.
Polak M, Wolf LL, Starmer WT, Barker JSF. (2001) Function of mating plug in Drosophila hibisci Bock. Behav Ecol Sociobiol 49:196–205.[CrossRef][Web of Science]
Prenter J, MacNeil C, Elwood RW. (2006) Sexual cannibalism and mate choice. Anim Behav 71:481–490.[CrossRef][Web of Science]
Rovner J. (1967) Copulation and sperm induction by normal and palpless male Linyphiid spiders. Science 157:835.
Saul SH, Tam SYT, McInnis DO. (1988) Relationship between sperm competition and copulation duration in the Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 81:498–502.[Web of Science]
Schneider JM, Fromhage L, Uhl G. (2005a) Copulation patterns in the golden orb-web spider Nephila madagascariensis. J Ethol 23:51–55.[CrossRef]
Schneider JM, Fromhage L, Uhl G. (2005b) Extremely short copulations do not affect hatching success in Argiope bruennichi SCOPOLI, 1772 (Araneidae). J Arachnol 33:663–669.[CrossRef]
Schneider JM, Gilberg S, Fromhage L, Uhl G. (2006) Sexual conflict over copulation duration in adult cannibalistic spider. Anim Behav 71:781–788.[CrossRef]
Schneider JM, Thomas ML, Elgar MA. (2001) Ectomised conductors in the golden orb-web spider, Nephila plumipes (Araneoidea): a male adaptation to sexual conflict? Behav Ecol Sociobiol 49:410–415.[CrossRef][Web of Science]
Scopoli JA. (1772) Observationes zoologicae. In Annus V (Ed.). Historico-naturalis, Leipzig (Germany) pp. 70–128.
Shine R, Olsson MM, Mason RT. (1999) Chastity belts in gartersnakes: the functional significance of mating plugs. Biol J Linn Soc 70:377–390.
Simmons LW. (2001) Sperm competition and its evolutionary consequences in the insects(Princeton University Press, Princeton (NJ)).
Simmons LW and Siva-Jothy MT. (1998) Sperm competition in insects: mechanisms and the potential for selection. In Birkhead TR and Møller AP (Eds.). Sperm competition and sexual selection(Academic Press, London) pp. 341–434.
Siva-Jothy MT. (1987) Variation in copulation duration and the resultant degree of sperm removal in Orthetrum cancellatum (L.) (Libellulidae: Odonata). Behav Ecol Sociobiol 25:389–394.
Siva-Jothy MT and Tsubaki Y. (1989) Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae). 1. Alternative mate-securing tactics and sperm precedence. Behav Ecol Sociobiol 24:39–45.
Snow LSE, Abdel-Mesih A, Andrade MCB. (2006) Broken copulatory organs are low-cost adaptations to sperm competition in redback spiders. Ethology 111:1–17.[Web of Science]
Strassmann J. (2001) The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc 48:1–13.
Wiehle H. (1967) Steckengebliebene Emboli in den Vulven von Spinnen (Arach, Araneae). Senckenb Biol 48:197–202.
Wolf LL, Waltz EC, Wakeley K, Klockowski D. (1989) Copulation duration and sperm competition in white-faced dragonflies (Leucorrhinia intacta; Odonata: Libellulidae). Behav Ecol Sociobiol 24:63–68.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. M. Schneider and K. Lesmono Courtship raises male fertilization success through post-mating sexual selection in a spider Proc R Soc B, September 7, 2009; 276(1670): 3105 - 3111. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Welke and J. M. Schneider Inbreeding avoidance through cryptic female choice in the cannibalistic orb-web spider Argiope lobata Behav. Ecol., September 1, 2009; 20(5): 1056 - 1062. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. M. Jones and M. A. Elgar Male insemination decisions and sperm quality influence paternity in the golden orb-weaving spider Behav. Ecol., March 1, 2008; 19(2): 285 - 291. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H Nessler, G. Uhl, and J. M Schneider A non-sperm transferring genital trait under sexual selection: an experimental approach Proc R Soc B, September 22, 2007; 274(1623): 2337 - 2341. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||