Behavioral Ecology Advance Access originally published online on November 28, 2006
Behavioral Ecology 2007 18(1):251-258; doi:10.1093/beheco/arl077
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Age-related sperm transfer and sperm competitive ability in the male hide beetle
a Department of Zoology, The University of Melbourne, 3010 Victoria, Australia b Institute of Biomedical and Life Sciences, University of Glasgow, UK
Address correspondence to T.M. Jones. E-mail: theresa{at}unimelb.edu.au.
Received 26 June 2006; revised 12 October 2006; accepted 18 October 2006.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The influence of male age on reproductive success after a single mating has been explored widely; however, few studies have investigated whether quantitative or qualitative differences in male sperm are responsible for the observed patterns. Moreover, the role of male age on sperm competitive ability has been largely ignored. We examined the importance of male age on the probability and amount of sperm transferred during a single mating and explored whether sperm competitive ability varies with male age in the hide beetle Dermestes maculatus, a species where sperm viability does not vary with male age. We also investigated whether sperm transfer rates varied with female age. We found that the probability of sperm transfer and the amount of sperm transferred varied with male, but not female, age. All males performed behaviorally successful copulations, but intermediate-age and old males were more likely to transfer sperm successfully and also transferred a greater quantity of sperm than young males. Old males were less likely to transfer sperm than intermediate-age males, but if they did transfer sperm successfully, they transferred comparable amounts. Sperm competitive ability varied with male age and reflected the quantity of sperm transferred. On average, intermediate-age males achieved greater fertilization success when competing against young or old males than when competing against other intermediate-age males. Old males were poor competitors against intermediate-age males, but they achieved significantly higher rates of fertilization when competing against young males. Our findings suggest that quantitative differences in the amount of sperm transferred determine male success in sperm competition in the hide beetle.
Key words: female age, male age, sperm competition, sperm transfer.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
In theory, female preference for males of particular ages is thought to be maintained largely through the benefits accrued by choosy females (Manning 1985
; Hansen and Price 1995; Kokko 1998; Beck and Powell 2000; Proulx et al. 2002). For example, female sand flies Lutzomyia longipalpis preferentially mate with intermediate-age males and derive direct fertilization benefits from their choice (Jones et al. 2000). Such fertilization differences may have arisen through quantitative or qualitative variation in male sperm, yet few studies attempt to discriminate between these potential factors, which in insects may include age-related variation in sperm length (Green 2003), sperm quantity (Hayashi 1999), and sperm storage (Taylor et al. 2001). Moreover, by focusing on the consequences of female mating preferences, the relative importance of female age and the opportunity for sperm competition to influence the outcome of reproductive events has been largely ignored.
Most studies that explore age-related variation in male mating success use a single mating attempt to determine the reproductive potential of males in specific age classes (e.g., Delisle 1995; Fox et al. 1995; Rogers and Marti 1997; Jones et al. 2000; Jones and Elgar 2004; Wedell and Ritchie 2004). Although this may be appropriate for monandrous species, it reveals little about the reproductive success of males of different age classes in polyandrous species. This may be particularly pertinent if polyandry biases paternity toward the most competitive and highest quality males (Tregenza and Wedell 2002). Studies that have explored variation in sperm competitive ability report a range of outcomes. The likelihood of being cuckolded decreases with male age in the brown thornbill Acanthiza pusilla (Green et al. 2002), and second male sperm precedence is more prevalent in the noctuid moth Heliothis virescens if the second male to mate is older than the first (LaMunyon 2001). In contrast, old male cellar spiders Pholcus phalangioides have reduced fertilization success if they are the second to mate (Schafer and Uhl 2002), and young male bulb mites Rhizoglyphus robini outcompete their older rivals in sperm competition trials (Radwan et al. 2005). Selection experiments have also revealed evidence of senescent decline in sperm competitive ability in the fruit fly Drosophila melanogaster (Service and Fales 1993). However, these studies cannot determine whether the variation in success in sperm competition arises through qualitative or quantitative differences in the sperm transferred. In the only study to hold sperm quantity constant, Hoysak et al. (2004) found no evidence that sperm competitive ability of sockeye salmon Oncorhynchus nerka varied with male age or mating position. Nevertheless, it is unclear whether fertilization success in this species actually varies with male age (Hoysak and Liley 2001).
Female age may also influence the probability of copulation or subsequent patterns of fertilization. Female mating success in the oblique-banded leaf roller Choristoneura rosaceana declines with age (Delisle 1995). In contrast, the number of cloacal contacts and male mounting rates in the common tern Sterna hirundo were positively associated with female age (Gonzalez-Solis and Becker 2002). These studies do not investigate explicitly the effect of female age on fertilization success; however, female cockroaches Nauphoeta cinerea that were older when first mated laid fewer offspring per clutch and fewer clutches than young mated females (Moore et al. 2001). Finally, last-male precedence declines with increasing female age in the fruit fly D. melanogaster (Mack et al. 2003). To date, no study has provided an adequate mechanism to explain these patterns, although a wealth of possibilities have been proposed (for comprehensive reviews, see Birkhead and Møller 1998; Simmons 2001).
Here, we assess the importance of female and male age on the quantity of sperm transferred to a female and explore whether sperm competitive ability varies with male age in the hide beetle Dermestes maculatus De Geer (Coleoptera: Dermestidae). The hide beetle is a small, carrion-feeding insect that forms aggregations on spatially and temporally patchy resources where individuals feed and mate (Archer and Elgar 1998). The influence of female age on male reproductive behavior is unknown, but male reproductive success varies with age. Seven-week-old males accrue more matings than 13-week- or 11-day-old males when in small competitive mating aggregations (Jones and Elgar 2004). Moreover, single-mated females accrue direct fertilization benefits—they lay larger clutches and fertilize a greater number and proportion of eggs—when mating with 7-week-old males (Jones and Elgar 2004). Recent data indicate that sperm viability, a qualitative measure of sperm, does not vary with male age (Hale J, unpublished data); however, although not tested explicitly, quantitative differences are thought to explain the observed low fertilization success of the youngest and oldest males (Jones and Elgar 2004). The effect of male age on sperm competitive ability has never been studied.
The aim of this study was twofold. First, we explored whether the quantity of sperm transferred by a male to a female during mating varied with male or female age. Second, we assessed the sperm competitive ability of males varying in age, by assessing the fertilization success of each of 2 males who were either the same or different age when mating with a single female of known age.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Culturing
Adult beetles were obtained from a large laboratory population that had been maintained for 15 generations at the University of Melbourne. Individuals were kept in a temperature-controlled room at 28 °C, on a 12:12 h light:dark cycle and fed ad libitum on a diet of dried bonemeal and water. Pupae were transferred to individual 5-ml vials prior to adult emergence to ensure virginity. On emergence, experimental adults were housed individually in plastic rearing containers (diameter = 68 mm, height = 28 mm) containing dried bonemeal and water and were maintained at 25 °C on a light and food regimen identical to the immature stages of the life cycle. Experimental animals were standardized for size (mean ± standard error [SE] female weight = 0.031 ± 0.002 g, female length = 5.29 ± 0.03 mm, male weight = 0.029 ± 0.001 g, male length = 5.21 ± 0.02 mm) but varied in age (see treatment groups below).
Age classes
On eclosion, males and females were assigned to 1 of 3 age categories (young, intermediate age, or old) and then maintained with ad libitum food and water in individual rearing containers (as above) for 9.78 ± 0.05 days (N = 63 young males), 9.50 ± 0.37 days (N = 23 young females), 41.96 ± 0.10 days (N = 70 intermediate-age males), 42.34 ± 0.11 days (N = 123 intermediate-age females), 91.78 ± 0.12 days (N = 65 old males), or 91.30 ± 0.19 days (N = 22 old females). These 3 age classes incorporate a large component of the life span of this species under laboratory conditions, as male hide beetles survive and will continue to mate for more than 4 months in the laboratory (Archer and Elgar 1998). All males were maintained as virgins until used in the experiment to ensure identical mating histories; however, a previous study found no evidence that fertilization success varied with male mating history, and thus, male age and mating experience are unlikely to be confounded (Jones and Elgar 2004).
The effects of age on sperm transfer
To explore factors influencing sperm transfer, 69 females of known age class were assigned a male of known age class. Pairs were introduced to a petri dish (30-mm diameter, 10-mm height) and left to copulate. After a successful mating, the female was returned to her individual container and left for 40 min before being decapitated. The female reproductive tract was dissected out in 0.9% phosphate-buffered saline (PBS) solution (Sigma, Castle Hill, New South Wales, Australia). The spermatheca was transferred to a standard glass slide with 0.2 ml of 0.9% PBS and teased apart with fine dissecting needles to release the stored sperm. The slide was covered with a 22 x 22–mm glass coverslip, examined twice under a light microscope (x100 magnification), and scored for the presence and quantity of sperm. In the hide beetle, sperm are transferred in bundles, each containing 256 spermatozoa (Al-Taweel and Fox 1983). Separation of the sperm bundles using conventional techniques (Yusa 1996; Hayashi 1998; Hellriegel and Bernasconi 2000) was unsuccessful, and so we applied a rank measure of the amount of sperm transferred. Rank 0 = no sperm transferred, rank 1 = sperm was detected on the slide but no distinct sperm bundles were transferred, rank 2 = distinct sperm bundles were transferred but these covered less than 50% of the coverslip, and rank 3 = distinct sperm bundles were transferred that covered more than 50% of the coverslip. The distinction between ranks 2 and 3 was always unambiguous; the amount of sperm transferred was either substantially less than 50% coverage or close to 100%. Where sperm was not found, the male reproductive organs were dissected out within 24 h after mating; the male's mature sperm storage organ (the seminal vesicle) was removed and separated with dissecting needles on a glass slide and examined for the presence of sperm. Males that transferred sperm were discarded without dissection.
The effects of male age on fecundity and sperm competition
To investigate the relationships between sperm competitive ability, male age, and mating behavior, 2 males of similar or different ages were mated to a single virgin female and the outcome of sperm competition was assessed. A total of 98 intermediate-age virgin females were assigned to 1 of 9 female mating combinations consisting of 2 males of either similar or different ages. Each male was permitted a single copulation only, and males of all 3 age classes competed for fertilization success with males from every other age class (see Figure 3 for samples sizes). For each mating, an individual female was introduced to a petri dish (30-mm diameter, 10-mm height) with their first male. After a successful copulation, this male was removed and the process repeated with a second male.
|
Standard sterile male techniques were used to infer patterns of paternity (Boorman and Parker 1976
). This technique has been used successfully with no evidence of an irradiation effect on fertilization success (Archer and Elgar 1999). Twenty-four hours prior to the commencement of a trial, 1 of the 2 males within a pair was subjected to a sublethal dose of radiation (3.5 krad from a Cobalt-60 source) that renders sperm capable of fertilization but prevents embryo development. A balanced reciprocal design was used to control for the potential effects of irradiation, mating order, and age.
To assess fecundity and paternity success, mated females were provided with a water-soaked sponge (1 x 1 cm), a piece of ox liver (0.5 x 0.5 cm), and a piece of synthetic fur on which to lay eggs (3 x 3 cm). Food and water were replenished every 3 days; fur was replenished every second day for a total of 6 days. As female hide beetles can lay fertilized eggs for several weeks after a mating (Archer and Elgar 1999), this time period was short enough that sperm depletion would have no impact on the observed patterns of paternity. At 25 °C, egg viability can be determined by embryo pigmentation 48 h after oviposition (after Archer and Elgar 1999). For all females, eggs that developed characteristic eyespots were assigned to the nonirradiated male; eggs that remained opaque were assigned to the irradiated male. Females that failed to produce eggs within 6 days were dropped from analyses of fecundity and fertilization success as the majority (23 of 24 females) of female hide beetles commence oviposition within 30 h after their first mating (Featherston R, unpublished data).
Statistics
Variation in the probability of initiation of copulation, rank sperm transfer, and the number of eggs sired was analyzed using analyses of covariance (ANCOVAs) in JMP 4.0.2 (SAS Institute Inc, Cary, NC); data were transformed where necessary to achieve normality. Analyses exploring variation in the proportion of eggs sired were performed in MlwiN 1.2 (Rasbash et al. 2000) using a binomial response model with a logit-link function. This model included the total number of eggs laid as a denominator, thus accommodating the large observed variation in female fecundity. Significance levels were determined using Wald (
2) tests.
We avoided incorporating pseudoreplication in our analyses of the variation in fecundity and fertilization success in sperm competition trials, by using the fertilization success (number and proportion of eggs sired) of the second male only from any mating pair. The results were qualitatively identical if the analyses were performed using only the first male to mate. Male irradiated status was included initially in all models but was dropped because it did not significantly explain any variation. We carried out planned comparisons, after our ANCOVA or binomial models, because we were interested only in how a particular male age class performed against other age classes (e.g., young males vs. young, intermediate-age, or old males: Quinn and Keough 2002). Unless otherwise stated, all presented averages are means ± SEs.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The effects of male and female age on sperm transfer
Presence of sperm
The probability of a male having sperm present in his mature sperm organ varied across the 3 age classes (
= 7.61, P = 0.02). All intermediate-age (n = 23) and old (n = 24) males had mature sperm present in their seminal vesicles; in contrast, mature sperm was found in the seminal vesicles of only 36% of young males (n = 22).
Copulation duration
All males performed behaviorally successful copulations (mean duration of copulation ± SE = 58.31 ± 4.05 s). There was no relationship between copulation duration and either male or female age (effect of male age: F2,58 = 0.77, P = 0.47; female age: F2,58 = 0.01, P = 0.99) and no significant interaction between male and female age classes (F4,58 = 2.28, P = 0.07). Copulation duration was also unrelated to either male or female weight (effect of male weight: F1,58 = 0.007, P = 0.79; female weight: F1,58 = 0.003, P = 0.96).
Probability of sperm transfer
Although copulations were behaviorally successful, not all males transferred sperm during copulation. The probability of a male transferring sperm to a female's spermatheca varied with his age (nominal logistic model: = 14.70, P = 0.0006; Figure 1): intermediate-age and old age males were more likely to transfer sperm than young males (post hoc tests, both P < 0.0001) and intermediate-age males were also more likely to transfer sperm than old males (P = 0.04). All females were equally likely to receive sperm irrespective of their age ( = 1.57, P = 0.46). There was no relationship between the probability of sperm transfer and copulation duration (
= 0.06, P = 0.81), male weight ( = 1.14, P = 0.28), or female weight ( = 1.00, P = 0.32).
|
Rank amount of sperm transferred
If all males are considered, the rank amount of sperm received by a female after a behaviorally successful mating depended on the age of her mate (F2,57 = 27.83, P < 0.0001; Figure 2a). Intermediate-age males transferred more sperm than either older or younger males (post hoc Student's t-tests, both P < 0.05); old males also transferred more sperm than young males (post hoc Student's t-test, P < 0.05). Females received comparable amounts of sperm irrespective of their age (F1,57 = 0.53, P = 0.59). There was no interaction between male and female age with respect to the amount of sperm transferred (F4,57 = 1.33, P = 0.27). There was also no significant effect of male weight (F1,57 = 1.90, P = 0.17), female weight (F1,57 = 0.28, P = 0.60), or copulation duration (
= 0.33, P = 0.57) on the rank amount of sperm transferred.
|
If only those males that transferred sperm successfully are considered, the amount of sperm transferred by a male varied with his age (F2,38 = 9.20, P = 0.0006; Figure 2b). Post hoc Student's t-tests revealed that intermediate-age and old males transferred more sperm than young males (both P < 0.05); but intermediate-age and old males transferred comparable rank amounts of sperm (P > 0.05). There was a trend suggesting that the amount of sperm transferred varied with female age (F2,38 = 2.70, P = 0.08), but there was no significant effect of male weight (F2,38 = 0.08, P = 0.78), female weight (F2,38 = 1.08, P = 0.31), or copulation duration (F2,38 = 0.59, P = 0.45). In this analysis, it was not possible to include the interaction between male age and female age because the 7 young males that transferred sperm did so to young and old females only.
The effects of male age on fecundity and sperm competition
Copulation duration
There was no difference in the duration of copulation between the first and second male to mate with a female (mean duration of first copulation = 51.41 ± 2.84 s, second copulation = 47.39 ± 2.69 s, matched pairs t-test: t = 1.03, N = 99 females, P = 0.31). This pattern was consistent across the 9 male mating groups (F8,90 = 1.23, P = 0.29).
Fecundity
Three twice-mated females (1 IY female and 2 IO females) that failed to commence oviposition after 6 days were dropped from subsequent analyses.
There was no overall difference between the groups in the percentage of clutches with 2 sires (nominal logistic regression: 
= 9.18, P = 0.33; Figure 3a). However, notably, only 40% of the females that mated to 2 young males (YY females) produced clutches with 2 sires.
The mean number of eggs laid was comparable across the 9 female mating treatments (F8,76 = 0.34, P = 0.95; Figure 3b), but clutches sired by 2 males were considerably larger than clutches sired by a single male (mean clutch size of females with a single sire = 23.29 ± 5.62, N = 31 females; 2 sires = 216.8 ± 12.6, N = 67 females; F1,76 = 73.48, P < 0.0001). Neither the interaction between female mating treatment and the number of sires per clutch (F8,76 = 0.29, P = 0.97) nor female weight (F1,76 = 1.37, P = 0.25) explained a significant amount of variation in the number of eggs laid.
As single-mated females lay significantly smaller clutches when compared with twice-mated females (McNamara KB, unpublished data), and there is a significant effect of number of sires on clutch size, number of sires was considered as an additional variable in subsequent analyses of the number of eggs sired.
Within a female treatment, the probability of sperm being transferred by both males (probability of a female receiving sperm after a mating with a Y male = 0.36, I male = 0.96, O male = 0.75) was positively correlated with the proportion of clutches with 2 sires (rs = 0.74, P = 0.02; Figure 4).
|
Sperm competition
The number of eggs sired by the second male varied significantly across the 9 female mating treatments (F2,85 = 2.21, P = 0.03; Figure 5a). Planned comparisons within male age classes revealed that intermediate-age males competing against their own age class sired fewer eggs than when competing against either young (II males vs. YI males: P = 0.01) or old (II males vs. OI males: P = 0.05) males. In addition, old males tended to sire more eggs when competing against a young compared with an intermediate-age male (YO vs. IO: P = 0.07). All other comparisons were nonsignificant (P > 0.17). There was a significant effect of the number of sires in a clutch on the number of eggs sired by the focal male (mean number of eggs sired by the second male in single-male clutches = 15.68 ± 5.51, N = 31 clutches; 2-male clutches = 141.45 ± 13.50, N = 67 clutches; F1,85 = 41.02, P < 0.001).
|
The proportion of eggs sired by the second male varied substantially across the female mating treatments (
= 18.88, P = 0.02; Figure 5b). Planned comparisons within age classes revealed that intermediate-age males sired proportionally more eggs when competing against young males than when competing against their own age class (II vs. YI: P = 0.01) and that old males sired proportionally more eggs when their competitor was younger than when he was an intermediate-age male (YO vs. IO: P = 0.02). No other comparison was significant (all P > 0.12). |
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
This study has 3 key findings. First, many hide beetle males were sexually mature and capable of fertilization 10 days after adult eclosion: 36% of 10-day-old males had sperm present in their mature sperm organs. However, even sexually immature males performed behaviorally successful copulations. Second, the probability of sperm transfer and the amount of sperm transferred varied with male, but not female, age. Intermediate-age and old males were more likely to transfer sperm successfully and also transferred a greater quantity of sperm than young males. Old males were less likely to transfer sperm than intermediate-age males; however, if they were successful, they transferred comparable amounts of sperm. Finally, sperm competitive ability varied with male age. On average, intermediate-age males achieved greater fertilization success when competing against young or old males than when competing against other intermediate-age males. Old males were poor competitors against intermediate-age males, but they tended to achieve higher rates of fertilization when competing against young males. Combined, our sperm transfer and fertilization data suggest that the quantity of sperm transferred by a male is an important factor determining sperm competitive success. It is also likely that when the amount of sperm transferred by competing males is similar (such as for intermediate-age and old males), age-dependent variation in the quality of spermatozoa or seminal products transferred during mating may influence fertilization success.
Male age at first reproduction varies substantially across species (Sterns 1992). In insects, sexual maturity is correlated with physiological traits such as testis size, sperm length, and accessory gland size (Pitnick et al. 1995; Baker et al. 2003). Delayed male maturation may also reflect investment in behavioral traits required to attract females. In the lekking Hawaiian picture-wing fly Drosophila grimshawi, adult males age for approximately 12 days before they commence the stereotypical courtship behaviors required for female acceptance of a mating attempt (Johansson et al. 2005). Whether this period is also required to ensure sperm maturation is unknown. Our data suggest that all male hide beetles are behaviorally mature and capable of mating, but as only 36% of young males had sperm present in their sperm storage organs, physiological maturation of sperm may take longer for some males (see also, Al-Taweel and Fox 1983). The sexual maturation period of male hide beetles clearly reflects the amount of time required for sperm production (Al-Taweel and Fox 1983), but it may also permit the development of the pheromone glands utilized in mate attraction (Shaaya 1981; Jaskulska et al. 1987; Rakowski et al. 1989). Further, it is possible that a male hide beetle's reproductive accessory glands also develop during this period. In insects, substances produced in the accessory glands are known to influence factors such as fertilization, oviposition, and sperm retention (Gillott 2003), and it has been suggested that accessory gland development is a better indicator of sexual maturity than the presence of mature sperm in sperm storage organs (Baker et al. 2003).
Why do young male hide beetles engage in matings when the majority have insufficient or no sperm to transfer? The most parsimonious explanation for this is that the cost of mating for males is relatively low in contrast to other species (for a recent review, see Wedell et al. 2002). This is supported by the fact that a male's previous mating history has little impact on fertilization success (Jones and Elgar 2004) and that males are able to fertilize eggs successfully even after mating with 4 females (Jones et al. 2006). A further factor that is likely to have some influence is that under natural conditions, resources such as females are patchily distributed (Archer and Elgar 1998). Thus, unless a male is able to determine exactly when he is physiologically mature, engaging in matings whenever the opportunity arises is probably the most beneficial. Clearly, from a female perspective, this introduces the possibility of receiving insufficient sperm to fertilize a complete egg compliment. However, as female hide beetles mate readily and multiply, these costs will be substantially lower than for species with a monandrous mating strategy (Jones 2001).
Our study confirms that, in the hide beetle, age-related variation in fertilization success is correlated with sexual maturation and is determined, at least in part, by numerical representation of sperm in a female's reproductive tract (sensu, the raffle model, Parker 1990) and failure of the males to transfer sperm (sensu, Garcia-Gonzalez 2004). Intermediate-age males transferred consistently the greatest amount of sperm in a single mating and were highly successful in sperm competitive interactions against young and old males. Conversely, young males transferred small amounts or no sperm and fared poorly in sperm competition trials. Moreover, old males were less likely to transfer sperm during mating and have lower fertilization success than intermediate-age males, even in the absence of competition (Jones and Elgar 2004), although it is worth noting our rank measure of quantity was conservative, particularly at the upper limit of our rank. We did not test explicitly whether the quality of sperm produced by the oldest males was also reduced; however, preliminary evidence suggests that sperm viability, a recently employed measure of sperm quality (Garcia-Gonzalez and Simmons 2005; Harris and Moore 2005), does not vary with male age (Hale J, unpublished data). Whether other measures such as sperm motility or survival (Kidd et al. 2001) are more relevant indicators of sperm quality in the hide beetle remains to be investigated. We similarly cannot confirm that single-sired clutches reflect a failure to transfer sperm per se rather than the failure of transferred sperm to fertilize a female's eggs. However, this appears conceivable given that the percentage of double-male clutches within each female mating treatment correlated closely with the overall probability that the 2 males in that group would transfer sperm (Figure 4).
Age-specific variation in male fertilization success has several implications for females. Given that young and old males provide females with inadequate sperm for fertilization (see Jones and Elgar 2004), selection should favor females that are able to discriminate against these age classes. This may be the case in the hide beetle: in competitive mating aggregations, young and old males lose mating opportunities to intermediate-age rivals (Jones and Elgar 2004), although this pattern may be difficult to interpret in species in which it is difficult to distinguish between male performance and female preference (Jones et al. 2006). However, female hide beetles are highly polyandrous (Archer and Elgar 1999) and gain direct fertilization benefits from a remating or multiple-mating strategy (McNamara KB, unpublished data). This polyandrous mating strategy may allow females to avoid fertilization by older males with potentially lower quality sperm as intermediate-age males are more likely to outcompete their older and young rivals in sperm competition (see also, Radwan 2003; Radwan et al. 2005). Whether female hide beetles have any influence on patterns of sperm utilization after mating (Eberhard 1996) or whether the observed weak effect of female age on the amount of sperm transferred has any subsequent effect on the outcomes of sperm competition (Eberhard 1996; Mack et al. 2003) require further investigation.
Finally, we cannot exclude the possibility that the quality and/or quantity of seminal products, transferred during mating, also covaries with male age. Reports from 59 insect species, covering 6 orders, suggest that seminal products may influence female reproduction and oviposition behavior (Eberhard 1996). Moreover, deterioration of accessory products responsible for agglutinating individual sperm into bundles could conceivably impair successful sperm transfer or affect sperm storage (Simmons 2001). This may impede sperm movement through a female's viscous reproductive tract (Trivers 1985; Hayashi 1998) and have particularly severe consequences for males if the likelihood of sperm competition is high (Scott and Richmod 1990; Simmons 2001).
|
ACKNOWLEDGEMENTS |
|---|
We thank the Royal Society (a Travelling Fellowship to T.M.J.) and the Australian Research Council (grant DP0209680) for financial support.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Al-Taweel AA and Fox DP. (1983) Germ cell differentiation and kinetics in the testis of Dermestes Coleoptera. Cytologia 48:605–620.[Web of Science]
Archer MS and Elgar MA. (1998) Cannibalism and delayed pupation in hide beetles, Dermestes maculatus DeGeer (Coleoptera: Dermestidae). Aust J Entomol 37:158–161.[CrossRef]
Archer MS and Elgar MA. (1999) Female preference for multiple partners: sperm competition in the hide beetle, Dermestes maculatus (DeGeer). Anim Behav 58:669–675.[CrossRef][Web of Science][Medline]
Baker RH, Denniff M, Futerman P, Fowler K, Pomiankowski A, Chapman T. (2003) Accessory gland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni. Behav Ecol 14:607–611.
Beck CW and Powell LA. (2000) Evolution of female mate choice based on male age: are older males better mates? Evol Ecol Res 2:107–118.
Birkhead TR and Møller AP. (1998) Sperm competition and sexual selection(Academic Press, London).
Boorman E and Parker GA. (1976) Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecol Entomol 1:145–155.[CrossRef]
Delisle J. (1995) Effect of male and female age on the mating success of the oblique-banded leafroller Choristoneura rosaceana (Lepidoptera, Tortricidae) under different ecological conditions. J Insect Behav 8:781–799.[CrossRef]
Eberhard WG. (1996) Female control: sexual selection by cryptic female choice(Princeton University Press, Princeton (NJ)).
Fox CW, Hickman DL, Raleigh EL, Mousseau TA. (1995) Paternal investment in a seed beetle (Coleoptera, Bruchidae): influence of male size, age and mating history. Ann Entomol Soc Am 88:100–103.[Web of Science]
Garcia-Gonzalez F. (2004) Infertile matings and sperm competition: the effect of "nonsperm representation" on intraspecific variation in sperm precedence patterns. Am Nat 164:457–472.[CrossRef][Web of Science][Medline]
Garcia-Gonzalez F and Simmons LW. (2005) The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J Evol Biol 18:1097–1103.[CrossRef][Web of Science][Medline]
Gillott C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Ann Rev Entomol 48:163–184.[CrossRef][Web of Science][Medline]
Gonzalez-Solis J and Becker PH. (2002) Mounting frequency and number of cloacal contacts increase with age in common terns Sterna hirundo. J Avian Biol 33:306–310.[CrossRef]
Green DJ, Peters A, Cockburn A. (2002) Extra-pair paternity and mate-guarding behaviour in the brown thornbill. Aust J Zool 50:565–580.[CrossRef]
Green K. (2003) Age-related variation in mean sperm length, in the rove beetle Aleochara bilineata. J Insect Physiol 49:993–998.[CrossRef][Web of Science][Medline]
Hansen TF and Price DK. (1995) Good genes and old age do old mates provide superior genes. J Evol Biol 8:759–778.
Harris WE and Moore PJ. (2005) Sperm competition and male ejaculate investment in Nauphoeta cinerea: effects of social environment during development. J Evol Biol 18:474–480.[CrossRef][Web of Science][Medline]
Hayashi F. (1998) Sperm co-operation in the fly-fish, Parachauliodes japonicus. Funct Ecol 12:347–350.[CrossRef]
Hayashi F. (1999) Ejaculate production schedule and the degree of protandry in fishflies (Megaloptera: Corydalidae). Funct Ecol 13:178–189.[CrossRef]
Hellriegel B and Bernasconi G. (2000) Female-mediated differential sperm storage in a fly with complex spermathecae, Scatophaga stercoraria. Anim Behav 59:311–317.[CrossRef][Web of Science][Medline]
Hoysak DJ and Liley NR. (2001) Fertilization dynamics in sockeye salmon and a comparison of sperm from alternative male phenotypes. J Fish Biol 58:1286–1300.[CrossRef]
Hoysak DJ, Liley NR, Taylor EB. (2004) Raffles, roles, and the outcome of sperm competition in sockeye salmon. Can J Zool 82:1017–1026.[CrossRef]
Jaskulska B, Rakowski G, Cymborowski B. (1987) The effect of juvenile hormone on aggregative behaviour of Dermestes maculatus. Biochem Physiol 87A:771–773.[CrossRef]
Johansson BG, Jones TM, Widemo F. (2005) Costs of pheromone production in a lekking Drosophila. Anim Behav 69:851–858.[CrossRef]
Jones TM. (2001) A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J Insect Behav 14:385–399.[CrossRef]
Jones TM, Balmford A, Quinnell RJ. (2000) Adaptive female choice for middle-aged mates in a lekking sandfly. Proc R Soc Lond B Biol Sci 267:681–686.[Medline]
Jones TM and Elgar MA. (2004) The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle. Proc R Soc Lond B Biol Sci 271:1311–1318.[Medline]
Jones TM, McNamara KB, Colvin PGR, Featherston R, Elgar MA. (2006) Mating frequency, fecundity and fertilization success in the hide beetle, Dermestes maculatus. J Insect Behav 19:357–371.[CrossRef]
Kidd SA, Eskenazi B, Wyrobek AJ. (2001) Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 75:237–248.[CrossRef][Web of Science][Medline]
Kokko H. (1998) Good genes, old age and life-history trade-offs. Evol Ecol 12:739–750.[CrossRef]
LaMunyon CW. (2001) Determinants of sperm precedence in a noctuid moth Heliothis virescens: a role for male age. Ecol Entomol 26:388–394.[CrossRef]
Mack PD, Priest NK, Promislow DEL. (2003) Female age and sperm competition: last-male precedence declines as female age increases. Proc R Soc Lond B Biol Sci 270:159–165.[Medline]
Manning JT. (1985) Choosy females and correlates of male age. J Theor Biol 116:349–354.[CrossRef]
McNamara KB, Jones TM, Elgar MA. (2004) Female reproductive status and mate choice in the hide beetle, Dermestes maculatus. J Insect Behav 17:337–352.[CrossRef]
Moore AJ, Gowaty PA, Wallin WG, Moore PJ. (2001) Sexual conflict and the evolution of female mate choice and male social dominance. Proc R Soc Lond B Biol Sci 268:517–523.[Medline]
Parker GA. (1990) Sperm competition games—raffles and roles. Proc R Soc Lond B Biol Sci 242:120–126.
Pitnick S, Markow TA, Spicer GS. (1995) Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci USA 92:10614–10618.
Proulx SR, Day T, Rowe L. (2002) Older males signal more reliably. Proc R Soc Lond B Biol Sci 269:2291–2299.[Medline]
Quinn GP and Keough MJ. (2002) Experimental design and data analysis for biologists(Cambridge University Press, Cambridge (UK)).
Radwan J. (2003) Male age, germline mutations and the benefits of polyandry. Ecol Lett 6:581–586.[CrossRef][Web of Science]
Radwan J, Michalczyk L, Prokop Z. (2005) Age dependence of male mating ability and sperm competition success in the bulb mite. Anim Behav 69:1101–1105.[CrossRef]
Rakowski G, Sorensen KA, Bell WJ. (1989) Responses of dermestid beetles, Dermestes maculatus, to puffs of aggregation pheromone extract (Coleoptera: Dermestidae). Entomol Gen 14:211–215.
Rasbash J, Browne W, Goldstein H, Yang M, Plewis I, Healy M, Woodhouse G, Draper D, Langford I, Lewis T. (2000) A user's guide to MLwiN(Institute of Education, London).
Rogers CE and Marti OG. (1997) Once-mated beet armyworm (Lepidoptera: Noctuidae): effects of age at mating on fecundity, fertility, and longevity. Environ Entomol 26:585–590.[Web of Science]
Schafer MA and Uhl G. (2002) Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour. Behav Ecol Sociobiol 51:368–377.[CrossRef][Web of Science]
Scott D and Richmod RC. (1990) Sperm loss by re-mating Drosophila melanogaster females. J Insect Physiol 36:451–456.[CrossRef]
Service PM, Fales AJ. (1993) Evolution of delayed reproductive senescence in male fruit-flies: sperm competition. Genetica 91:111–125.[CrossRef][Web of Science][Medline]
Shaaya E. (1981) Sex pheromone of Dermestes maculatus De Geer (Coleoptera, Dermestidae). J Stored Prod Res 17:13–16.[Medline]
Simmons LW. (2001) Sperm competition and its evolutionary consequences in the insects(Princeton University Press, Princeton (NJ)).
Sterns SC. (1992) The evolution of life histories(Oxford University Press, New York).
Taylor PW, Kaspi R, Mossinson S, Yuval B. (2001) Age-dependent insemination success of sterile Mediterranean fruit flies. Entomol Exp Appl 98:27–33.[CrossRef]
Tregenza T and Wedell N. (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73.[CrossRef][Medline]
Trivers R. (1985) Social evolution(Benjamin Cummings, Menlo Park (CA)).
Wedell N, Gage MJG, Parker GA. (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320.[CrossRef]
Wedell N and Ritchie MG. (2004) Male age, mating status and nuptial gift quality in a bushcricket. Anim Behav 67:1059–1065.[CrossRef]
Yusa Y. (1996) Utilization and degree of depletion of exogenous sperm in three hermaphroditic sea hares of the genus Aplysia (Gastropoda: Opisthobranchia). J Molluscan Stud 62:113–120.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||