Behavioral Ecology Advance Access originally published online on May 11, 2006
Behavioral Ecology 2006 17(4):656-663; doi:10.1093/beheco/ark013
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Influence of body and genital morphology on relative male fertilization success in oriental beetle
Department of Plant, Soil & Insect Sciences, Fernald Hall, University of Massachusetts Amherst, 270 Stockbridge Road, Amherst, MA 01003, USA
Address correspondence to A.L. Averill. E-mail: aaverill{at}ent.umass.edu
Received 11 December 2005; revised 21 March 2006; accepted 7 April 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Although the frequently large variance in relative male fertilization success when females are mated by more than 1 male has been appreciated for some time, the factors that influence relative paternity are still poorly understood. Recently, experimental evidence that morphology of male genitalia influences fertilization success has been documented in 2 water striders, a dung beetle, and a leaf beetle. We explored the role of male genital morphology in postcopulatory sexual selection in the oriental beetle. We mated females to 2 males in succession and assessed relative paternity by the sterile male technique. Morphology of the male genitalia was found to strongly influence relative paternity but only for the first male to mate. Male body size influenced relative fertilization success as well, but again, only for the first male; surprisingly, smaller males achieved higher paternity when mating first. We also found suggestive evidence that copula duration of both the first and second male to mate influenced paternity. Other factors, including female size and degree of asymmetry of hind tibiae length of males had no effect on relative fertilization success. Our results for the oriental beetle are novel among sperm precedence studies for 2 reasons: 1) traits of the first male appear to be more important in influencing paternity than those of the second, and 2) smaller, not larger, males achieved greater relative paternity. Our results also contribute to the growing body of empirical evidence in support of the hypothesis that male genitalia evolve by postcopulatory sexual selection.
Key words: evolution of genitalia, first male priority, genital morphology, sexual selection, sperm precedence.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Following Parker's (1970)
seminal review, the study of sperm precedence (i.e., the relative fertilization success among males in successive matings of the same female) has received considerable attention. That male mating success does not necessarily correlate directly with reproductive fitness when females mate multiply is apparent from the large variance in sperm precedence found in many insect species (Simmons 2001). The significance of this variance has long been appreciated (e.g., Lewis and Austad 1990; Simmons and Parker 1992; Cook et al. 1997; Harvey and Parker 2000; García-González 2004), but the factors that influence relative paternity are still poorly understood. The determination of what kinds of male traits are favored by postmating sexual selection is still a crucial issue in sexual selection theory.
Of the traits that influence sperm precedence in insects, the 2 most widely documented are copula duration and male body size (reviewed by Simmons 2001). Longer copulation might facilitate: 1) transfer of more sperm (e.g., Dickinson 1986; Simmons and Parker 1992; Arnqvist and Danielsson 1999b), 2) transfer of more accessory gland products (Parker 1970; Wing 1985), 3) removal of more sperm of prior males (e.g., Siva-Jothy 1987), or 4) more stimulation to the female to induce any number of responses, including mobilization of sperm (that of the current or of prior males) or inhibition of remating (Eberhard 1996). Similarly, larger males may be better competitors for fertilization because they may produce larger ejaculates (e.g., Fox et al. 1995; Bissoondath and Wiklund 1996; Schlüns et al. 2003). Given the general advantage of larger males with respect to precopulatory female choice and intrasexual competition for females (Andersson 1994), it is tempting to assume that postcopulatory sexual selection reinforces the action of precopulatory sexual selection (i.e., traits that are favored under premating sexual selection are also favored by postcoupling processes like sperm competition and cryptic female choice). Some species fit the expected pattern (e.g., larger Dryomyza anilis flies are favored by both pre- [Otronen 1984] and postcopulatory [Otronen 1994] selection), but more direct tests with 2 model systems—water striders (Arnqvist and Danielsson 1999b) and Drosophila melanogaster (Brown et al. 2004; but see Bangham et al. 2002)—do not support the congruence of premating and postmating sexual selection. For species in which females lack direct precopulatory mate choice, postcopulatory sexual selection might be clearer because of the reduction in potentially counteractive forces of sexual selection in operation before coupling (see Danielsson 2001; Sih et al. 2002).
One male trait that may evolve primarily via postcopulatory sexual selection and is unlikely to be driven directly by precopulatory selection is the morphology of the genitalia (Eberhard 1985, 1994, 1996). Three major hypotheses to explain the rapid and divergent evolution (Eberhard 1985) of male genitalia have been advanced: 1) the lock-and-key hypothesis, which suggests that genitalia evolve via selection for preinsemination reproductive isolation (reviewed by Shapiro and Porter 1989), 2) the pleiotropy hypothesis (Mayr 1963), which states that genitalia evolve not by direct selection but via selection on nonsexual but genetically correlated traits, and 3) the sexual selection hypothesis. Three major models of sexual selection have been proposed: sperm competition (competition among sperm from different males for the fertilization of a set of ova; Parker 1970), cryptic female choice (paternity biasing resulting from female morphology, physiology, or behavior that occurs after coupling; Eberhard 1985, 1996; Pitnick and Brown 2000), and conflict between the sexes over control of reproduction (Lloyd 1979; Alexander et al. 1997; Arnqvist and Rowe 2002). Although the lock-and-key (Shapiro and Porter 1989) and pleiotropy (Arnqvist and Thornhill 1998) hypotheses may continue to possess some utility, evidence against these 2 hypotheses (Eberhard 2004a; Eberhard and Ramirez 2004) and in support of the sexual selection hypothesis (reviewed by Hosken and Stockley 2004) is mounting. In particular, evolution of genital morphology across most arthropods may be better explained by the sperm competition and cryptic female choice models of sexual selection rather than the model of sexual conflict (Eberhard 2004b); however, it should be noted that the 3 models are often not mutually exclusive.
The complexity and diversity of insect genitalia are unlikely to have arisen merely for the relatively simple process of sperm transfer (Hosken and Stockley 2004). Genital morphology might be shaped by selection for other functions, including copulatory courtship (e.g., Eberhard 1992, 1993a, 1993b; Otronen 1998) and removal of previous males' sperm either directly (e.g., Waage 1979; Yokoi 1990; Haubruge et al. 1999) or indirectly (e.g., Córdoba-Aguilar 1999). The possible influence of male genitalia on sperm precedence may be independent of male size, which is often a poor predictor of genital size (Eberhard 1996; Eberhard et al. 1998; Schmitz et al. 2000). Further, although larger body size might be shaped by both natural selection and sexual selection (both pre- and postcopulatory), evolution of male genital morphology is more compatible with the model of postcopulatory sexual selection; therefore, the influence of genital morphology on male reproductive success, including relative paternity, might be particularly important. The significance of the effects of genital morphology on sperm precedence has been appreciated only recently (Arnqvist and Danielsson 1999a; Danielsson and Askenmo 1999; House and Simmons 2003; Rodriquez et al. 2004; see also Otronen 1998) and, therefore, this phenomenon might be more pervasive than current data suggest.
Among sperm precedence studies with 2 males, most insects exhibit on average either strong second male precedence or roughly equal paternity, with a slight bias toward the second male (see Table 2.3 in Simmons 2001). Characters of the second male to mate are usually most influential on relative paternity; although relative characters between the first and second male may also be important, traits of the first male alone rarely impact paternity. This pattern might be explained, in part, by the ability of the second male to adjust his mating strategy according to the risk or intensity of sperm competition when mating with a nonvirgin female (e.g., Wedell and Cook 1999; García-González and Gomendio 2004). Although "defensive" adaptations in males to protect against future competitors for a female's ova exist as well (Clark et al. 1995; Arnqvist and Danielsson 1999a; House and Simmons 2003), assessing the risk of possible future competition is likely more difficult than assessing more immediate risks to a male's reproductive success.
The oriental beetle Anomala orientalis (Waterhouse) (Coleoptera: Scarabaeidae) is an important pest of turf, ornamentals, and some food crops (Vittum et al. 1999); Facundo et al. (1999) characterized the emergence, mating, and postmating behaviors of the oriental beetle but did not examine sperm precedence in this species. Adult virgin females begin calling (i.e., raising the abdomen and releasing sex pheromone) immediately on emergence from the soil (Facundo et al. 1999). The first male to reach a female mates with her, with no overt precopulatory courtship behavior. In the laboratory, females burrow into soil immediately after mating and do not surface until most if not all of their eggs have been laid (Bianchi 1935; EJ Wenninger, unpublished data). If a second male attempts to mate with the female immediately after the first mating, she vigorously waves her hind legs, which appears to function to inhibit the male's ability to mount her, though most rejection attempts are unsuccessful (Facundo 1997) and the female eventually acquiesces. The rate of polyandry in the field is unknown but it almost certainly occurs to some extent given that swarms of males may be seen competing for individual females in the field (Bianchi 1935; Facundo 1997). We predicted that the lack of direct precopulatory female choice and overt precopulatory courtship behavior could contribute to strong postcopulatory sexual selection.
A key prediction of the evolution by sexual selection model regarding male genitalia is that relative male fertilization success is linked with genital morphology (Eberhard 1985). We tested this hypothesis in the oriental beetle by evaluating the influence of male genital morphology on relative paternity in twice-mated females. We also investigated the importance of other potential sources of variation in sperm precedence, including male body size, copula duration, and male body symmetry.
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METHODS |
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Collection and rearing
We collected third instar larvae from turf at Bay Pointe Country Club golf course, Onset, MA on 18 May 2004, placed them in plastic containers with soil, and then took them back to the laboratory where they were placed individually into clear plastic cups (30 ml) that were filled with prepared soil and fitted with a lid. The soil mixture was comprised of 2 parts screened sand with 1 part screened peat moss (1.18 mm sieve). We sterilized the soil in an autoclave (123°C, 1 kg/cm2 for 60 min), allowed it to cool, and then added sterilized, deionized water to moisten the mixture to about 12% water by weight. A heavy pinch of grass seed (Pennington® mix comprised of 63% shining star perennial ryegrass, 15% boreal red fescue, 9% kenblue Kentucky bluegrass, 9% blue bonnet Kentucky bluegrass, 2% inert matter, 1.9% other crop seed, and 0.1% weed seeds) was placed on top of the soil in each cup to provide food. We placed cups on 30-cup capacity clear plastic trays and placed each tray into a clear 9.46-l plastic, resealable bag with a damp sponge to reduce moisture loss from cups. Larvae were held in a rearing chamber on a 16:8 h light:dark cycle at 10°C to slow development until needed for experiments.
About 1 month before adult beetles were needed, we placed trays in a rearing chamber on a 16:8 h light:dark cycle at 25°C; adult eclosion began after about 3–4 weeks under these conditions. We checked each cup weekly for pupae and checked pupae daily for adult eclosion in order to establish adult age. Adults were sexed (based on size of antennal lamellae) and held in their rearing cups until needed for mating experiments.
Sperm precedence after double mating
Beetles were mated in the laboratory under conditions that simulated dusk—the period of peak female sexual receptivity (Facundo et al. 1994) and peak male responsiveness to pheromone (Facundo et al. 1994; EJ Wenninger, unpublished data). We moved beetles to a room held at about 60% humidity and maintained on a 16:8 h light:dark cycle (as above for rearing chambers), but at 25–27°C during photophase and 21–22°C during scotophase and the last 1 h of photophase. Light intensity during photophase was held at approximately 150 lux, except during the first and last 2 h of photophase when it was held at 15 lux. We paired beetles within the last 2 h of photophase.
We held virgin females for 5–8 days after eclosion before pairing with 4- to 9-day old virgin males; females reach sexual maturity by the age of 5 days, and males age 4–9 days display peak response to female sex pheromone (Zhang et al. 1994). To establish mating pairs, we placed a female in a plastic, 30-ml cup with a layer of soil approximately 0.5 cm deep. Females typically begin calling within 2 min of being placed on soil under simulated dusk conditions (EJ Wenninger, personal observation). We introduced a male after the female began calling; males promptly mounted calling females in the laboratory (EJ Wenninger, personal observation).
Males were sterilized 3–6 h before use in mating experiments by exposure to gamma radiation (80 Gy at ca. 7.5 Gy/min) using a cobalt-60 source housed in a Gammacell 220 irradiator (previous results showed that a dose of 80 Gy resulted in >95% sterility of ova, with no apparent effect on male fertilizing capacity; EJ Wenninger, unpublished data). Each female was paired with 1 normal male (N) and 1 irradiated male (R); females were paired first with either an irradiated male (RN; n = 17) or a normal male (NR; n = 16), with treatments randomly assigned to each female. The second male was introduced immediately after the first pair separated (<1 min after copulation ended). Additional females were paired with 2 normal males (NN; n = 19) or 2 irradiated males (RR; n = 6).
After each mating pair separated, we removed the male and froze him for later morphological measurements (see below); after the female's second mating, we transferred her to a clear plastic oviposition cup (diameter: 12 cm, height: 13 cm) with a layer of soil approximately 3-cm deep. Ten days after mating (when most if not all eggs had been laid), we sorted through the soil in oviposition cups and collected all eggs into Petri dishes lined with filter paper moistened with sterilized, deionized water. If the female was still alive, we returned her to the oviposition cup with fresh soil and collected any additional eggs approximately 7 days later. We held eggs until fertility could be assessed; fertile eggs increase in size, become more spherical, maintain their white color, and just before hatching, the orange–brown mandibles of the developing larva are visible through the chorion (EJ Wenninger, personal observation).
We recorded the percent fertility of each female's clutch of eggs and calculated P2 (the portion of eggs laid by a female that was sired by the second male to mate) values based on the formula of Boorman and Parker (1976):
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equation may be greater than 1 or less than 0 when estimates of x are lower than z or higher than p; P2 values were transformed using the formula by Cook et al. (1997) so that the data lay within the range of 0–1.
Mating behavior and morphological measurements
For each mating pair, we recorded (in minutes) copula duration (length of time between intromission and retraction of the aedeagus) and duration of "resistance" (total length of time the female walked and kicked her hind legs at the copulating male).
After use in mating experiments, we measured the dry mass of each male to the nearest 0.1 mg. We also measured the length of the left (L) and right (R) hind tibia of each male to the nearest 0.02 mm using a stereomicroscope equipped with an ocular micrometer; we then calculated unsigned fluctuating asymmetry (FA) of the hind tibiae as the absolute value of the difference between left and right tibia length |L – R|. Increased FA (deviations from perfect symmetry in bilateral morphological traits) may reflect developmental instability in the face of genomic and/or environmental stress (Watson and Thornhill 1994) and correlates negatively with reproductive success in some insects (e.g., Allen and Simmons 1996; Otronen 1998). Finally, we characterized genital morphology of each male using 4 measurements (see Figure 1). To prepare genitalia for measurements, we removed the phallus of each male and macerated it in 10% KOH for 2 h and then in 80% aqueous lactic acid for 10 min before mounting the structures on slides with glycerin. We captured digital images of the genitalia and used ImageJ software (Rasband 1997–2005) to measure the area bound by readily distinguishable landmarks or by traced edges of each sclerite (see Figure 1).
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Data analysis
To avoid including highly correlated variables within the regression model, we first produced a correlation matrix of all the morphological traits of interest (Table 1); although size of the lateral lobe was correlated with several other traits, the magnitude of correlations was small and, thus, no traits were excluded. We used multiple linear regression with P2 value (arcsine transformed to achieve normality) as the dependent variable and the following independent variables (for both the first and second male to mate): male mass, copula duration, |FA| (fluctuating asymmetry) of hind tibiae, and size of the 4 genital sclerites measured (see Figure 1). We also included female size (as estimated by right elytron length) in the regression model as well as duration of female resistance to the second male (cube root transformed to achieve normality). Finally, we included treatment (NR and RN) in the model using dummy variable coding. For each variable, we tested the residuals for normality by Kolmogorov–Smirnov test, and we tested for homogeneity of variance by examining residual plots; tests were repeated on transformed variables. We used hierarchical partitioning with Schwarz Bayesian information criterion to select the best fitting model. All data were analyzed using SAS (version 8.2, SAS Institute, Inc. 1999
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The oriental beetle exhibited mixed paternity after double mating, with sperm precedence ranging from complete first male to complete second male paternity. The mean ± SD P2 value for NR + RN treatments was 0.58 ± 0.38 and did not differ significantly from 0.5 (Wilcoxon signed-rank test, z = 1.16, P = 0.247; however, the power for this test was low: 0.212). Mean ± SD P2 for NR treatments was 0.43 ± 0.30 (range: 0.004–1.05) and for RN treatments was 0.71 ± 0.38 (range: –0.05 to 1.04). Mean ± SD number of eggs laid was 33.9 ± 9.8 for NN treatments, 21.0 ± 7.1 for NR treatments, 28.1 ± 10.6 for RN treatments, and 27.8 ± 15.7 for RR treatments. Mean ± SD percent egg fertility was 94.7 ± 7.0 for NN treatments, 56.8 ± 27.4 for NR treatments, 69.8 ± 36.0 for RN treatments, and 4.6 ± 11.3 for RR treatments. The potential impact of "nonsperm representation" on P2 estimates (see García-González 2004
) is negligible given the near absence of infertile matings in this species (Wenninger 2005).
The multiple regression analysis revealed 2 male characters to be strongly correlated with relative paternity: genital spicule size and body mass, both only of the first male to mate (Table 2). Relative paternity was also influenced by treatment (Table 2), apparently reflecting a slight negative impact of sterilization on the fertilizing capacity of males—an unfortunate, but common side effect of the sterile male technique (e.g., Danielsson and Askenmo 1999; Vermette and Fairbairn 2002; see also Simmons 2001). P2 values were negatively correlated with spicule size and positively correlated with mass of the first male to mate; thus, the larger the spicule and the smaller the first male the greater his relative paternity (Figure 2). Male mass and spicule size were not correlated (see Table 1); thus, their effects on relative paternity were independent. Neither asymmetry of the hind tibiae of males was correlated with relative paternity nor were duration of female resistance behavior, female size, or size of the other 3 genital traits included in the analysis.
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Any effects of copula duration on P2 were not detected in the multiple regression analysis. However, P2 values tended to decline with increasing duration of copulation of the first male, especially for NR treatments (Figure 3A), but the relationship was not significant (full model: F4,32 = 4.61, P = 0.006, r2 = 0.397; partial regression slope: t = 0.30, P = 0.769), owing in part to 2 RN data points that were outliers with respect to the overall pattern (see Figure 3A). Copula duration of the second male appeared not to influence relative paternity, but separate analysis of treatments revealed a positive correlation between copula duration and P2 for the NR treatment (Figure 3B; full model with mass and spicule size of first male: F3,15 = 9.56, P = 0.002, r2 = 0.705; partial regression slope: t = 2.53, P = 0.026). Mean ± SE copula duration of the second male (32.2 ± 1.6) was significantly greater than that of the first (26.3 ± 1.4; paired t-test: t = –2.81, P = 0.012), but only for NN treatments. The difference was not significant for NR (first male: 29.9 ± 1.8, second male: 28.9 ± 1.4; t = 0.37, P = 0.717) or RN (first male: 25.9 ± 1.9, second male: 29.3 ± 2.1; t = –2.81, P = 0.251) treatments.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male genital morphology
For the past 2 decades, Eberhard (1985
, 1993b, 1996, 1997, 2004a, 2004b; Eberhard and Ramirez 2004) has invoked postcopulatory sexual selection as a likely explanation for the complexity and diversity of the genitalia of male insects and other arthropods. However, direct empirical support of this hypothesis has been surprisingly scant given the strong interest in sperm precedence in general. Our data show that size of the spicule on the genitalia of male oriental beetles is correlated with relative fertilization success and, thus provide further support that genital morphology of male insects is shaped by sexual selection.
Lacking data that point to the precise function of the spicule, we can only speculate. Examination of flash-frozen pairs of beetles in copula (EJ Wenninger, personal observation) revealed that the spicule is positioned just inside the vagina where it "hooks" onto the female's last abdominal segment. Therefore, it is possible that a larger spicule contributes to better leverage or stability to facilitate deeper penetration (for depositing sperm closer to storage or fertilization sites) or more effective thrusting of the endophallus. The male might induce the use of his sperm by providing stimulation to the female via his phallus, with a larger spicule perhaps contributing to more effective stimulation; morphology of female genitalia might be important as well. Although mediation of cryptic female choice via specialized stimulation is an intriguing possible function of complex male genitalia, sperm competition and sexual conflict may also contribute. Distinguishing among the 3 models of sexual selection regarding the evolution of genitalia has proved challenging, and complex interactions among these nonmutually exclusive processes may be expected (Eberhard 2000).
Male body size
Our finding that smaller males—when mating first—achieved greater relative paternity appears to be at odds with much of the current theory on pre- and postcopulatory sexual selection (see introduction). A trade-off between male body size and the size (and productivity) of the testes or accessory reproductive glands is possible; in the oriental beetle, adult males feed very little, if at all (Friend 1929; Hallock 1933), and all the biochemical resources available for ejaculate production must be present within the male at eclosion. However, we are aware of no other study that has demonstrated such a trade-off in insects.
It is also possible that males use different mating "strategies" depending on their size. For example, even if larger males produce more sperm or accessory gland products, if they also generally achieve higher mating frequencies (perhaps by outcompeting smaller males for access to females), then they might be selected to invest less of their finite reproductive resources into each mate. Conversely, if smaller males are less likely to mate more than once, they could be selected to invest more reproductive effort into any given mating, which could give them an advantage in sperm competition. Evidence for a similar strategy has recently been found in the black-horned tree cricket Oecanthus nigricornis (Bussière et al. 2005), in which larger males (which are preferred by females) decrease the size of nuptial gifts in response to the perception of more future mating opportunities. Whether a similar situation exists in the oriental beetle remains to be tested. An investigation into the effect of male mating history on female reproductive output (Wenninger 2005) suggested that male body size is indeed positively correlated with lifetime reproductive success. Although this pattern is consistent with the idea that larger males partition resources more evenly among their mates or are otherwise better adapted for multiple mating, more rigorous tests will be needed to clarify the importance of male size to lifetime reproductive success in polyandrous situations.
Copula duration
Copula duration may be longer for a male mating with a nonvirgin female if the male adjusts his mating strategy based on increased risk or intensity of sperm competition (e.g., Wedell and Cook 1999; Carazo et al. 2004). Such a phenomenon might explain the increased copula duration of second males for NN treatments. Copula duration for NR and RN treatments did not differ between the first and second male; however, our data suggest that longer copula duration enhances a male's relative paternity, especially for the second male to mate. If sterilized males in the RN treatment transferred a smaller or lower quality ejaculate, second (fertile) males might have perceived only weak stimuli to increase their copula duration. This might explain the difference between treatments regarding the effect of copula duration of the second male on relative paternity. However, we caution that more research will be needed to clarify the importance of copula duration to sperm precedence in the oriental beetle.
First versus second male advantage
In a preponderance of studies of sperm precedence in insects, variance in P2 has been attributed to characters of the second male alone; even when traits of the first male matter, those of the second usually have primacy (Simmons 2001). Clearly, the possibility that we failed to measure one or more traits that are important for second male paternity in the oriental beetle cannot be discounted. For example, perhaps another aspect of genital morphology was overlooked. In water striders (Anrqvist and Danielsson 1999a) and dung beetles (House and Simmons 2003), independent traits of the genitalia had "offensive" (contributing to preemption of the sperm of prior males) and defensive (contributing to avoidance of sperm preemption by subsequent males) functions in paternity biasing. Our simple, 2-dimensional measurements of the genitalia undoubtedly underestimated the overall variation in morphology; however, Arnqvist and Thornhill (1998) found that—when comparing patterns of variation in general and genital morphology—simple linear measures yielded essentially the same result as more complex measures of shape. Indeed, our preliminary analyses using linear measures of genital morphology yielded no major difference in the results (data not shown).
Examples in insects in which traits of the first male to mate have primacy in influencing relative paternity are scarce. In Drosophila pseudoobscura, males of certain karyotypes were better able to avoid displacement of their sperm by subsequent males; karyotype of the second male and of the female had no effect on relative paternity (Turner and Anderson 1984). In the southern green stink bug Nezara viridula, P2 was lower when the first male was larger (McLain 1985) or mated longer (McLain 1980). Interestingly, larger males also yielded greater fertility (McLain 1980), and females were more likely to oviposit before remating when the first mating was of sufficient duration (McLain 1981). These patterns in the southern green stink bug are consistent with the idea that traits in male oriental beetles that enhance reproductive output in their mate might also contribute to higher relative paternity when such males mate first (Wenninger 2005). It is noteworthy that increased rate of oviposition after mating with certain males is the context in which the term "cryptic female choice" was first used (Thornhill 1983).
Why characters of the first male should be particularly important in influencing sperm precedence in the oriental beetle is unclear. Perhaps traits that contribute to relative male fertilization success (i.e., spicule size and body size) also function to make a male good at resistance of any subsequent competitors for the female's ova. Possibly, polyandry is relatively uncommon in the field (perhaps because males are generally able to successfully escort females back into the soil before other males can mate with them), resulting in relatively weak selection for means to preempt the sperm of previous mates; however, low levels of polyandry should also impose weak selection on males to avoid preemption of their ejaculate. To clarify these issues, it will be necessary to estimate rates of polyandry in the field and examine how ejaculates are stored within the female as well as the mechanism by which certain males resist preemption of their ejaculate.
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ACKNOWLEDGEMENTS |
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We thank Marty Sylvia for technical assistance and Mike Rocky for allowing grub collection from his golf course. We are grateful to John Buonaccorsi for assistance with data analysis. Our appreciation extends to Joe Elkinton, Elizabeth Jakob, Ben Normark, and several anonymous reviewers for helpful comments on the manuscript. We are indebted to Dave Lance and Natalie Leva for helping us irradiate beetles. E.J.W. was supported by a Lotta Crabtree Fellowship from the University of Massachusetts.
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