Behavioral Ecology Advance Access originally published online on June 11, 2004
Behavioral Ecology 2004 15(5):793-798; doi:10.1093/beheco/arh081
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No direct or indirect benefits to cryptic female choice in house crickets (Acheta domesticus)
Behavior, Ecology, Evolution and Systematics Section, Department of Biological Sciences, Illinois State University, Normal, IL 61790-4120, USA
Address correspondence to S. K. Sakaluk. E-mail: sksakal{at}ilstu.edu.
Received 21 April 2003; revised 22 September 2003; accepted 26 November 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Cryptic female choice in crickets occurs through the premature removal of a male's spermatophore after copulation, which terminates sperm transfer. Although it is known that this behavior can directly influence the paternity of offspring, its effects on female fitness have not been directly assessed. We tested the hypothesis that spermatophore removal by female house crickets (Acheta domesticus) confers fitness benefits on females, by randomly assigning mates to females but permitting some females to freely remove spermatophores after mating (cryptic-choice treatment) while forcing others to accept complete ejaculates (no-choice treatment). Although there was about a two-fold difference in the volume of ejaculate received by females of the two treatments, there were no significant differences in female longevity, reproductive output, or offspring quality, as measured by offspring mass and developmental time. Although differential spermatophore removal by females imposes strong sexual selection on males, the absence of a clear treatment effect suggests that females obtain no direct or indirect genetic benefits through their postcopulatory mating preferences.
Key words: Acheta domesticus, crickets, cryptic female choice, indirect genetic benefits, offspring fitness, spermatophore, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Female mate choice is a pervasive feature of most animal mating systems, but the benefits that females derive from their mating preferences often remain obscure (Andersson, 1994
). In species in which males provide material benefits to females or their offspring (e.g., food, shelter, parental care), females can obtain direct fitness benefits by preferentially mating with those males most likely to invest materially in females or their offspring. However, females often are extremely selective of their mates even in species in which males provide no material resources to females beyond sperm, leading some researchers to propose that females derive indirect genetic benefits by mating selectively (for reviews, see Andersson, 1994; Jennions and Petrie, 2000; Zeh and Zeh, 2003). Genetic benefits to mate choice can be broadly categorized into two main types: those that lead to an increase in hatching success, as may occur when female choice reduces the risk of mating with a genetically incompatible male (Zeh and Zeh, 1996, 1997), and those that lead to the increased viability of offspring, as may occur when females preferentially mate with genetically superior sires (for reviews, see Andersson, 1994; Jennions and Petrie, 2000).
Although the majority of empirical studies have focused on female precopulatory mating preferences and their fitness consequences, females of a number of insect species exhibit mechanisms that enable them to determine which males sire their offspring even after copulation has occurred (Eberhard, 1996). Such postcopulatory mechanisms are regarded as a form of "cryptic" female choice because they can lead to the differential fertilization success of males that, in the absence of any assessment of offspring paternity, remains covert. Females may favor particular males' gametes by remating quickly after copulating with less-preferred males, or by delaying oviposition until after copulating with desirable males (Thornhill, 1983). Females may also bias the paternity of their offspring by prematurely terminating copulations, failing to store transferred sperm, removing or ejecting stored sperm, or failing to provide nutrients to offspring sired by undesirable males (for reviews, see Eberhard, 1996; Thornhill and Alcock, 1983).
In crickets, females mate repeatedly throughout their lives with both the same and different males (Sakaluk and Cade, 1980; Sakaluk et al., 2002; Simmons, 1988; Wagner et al. 2001), and store sperm from their various mating partners over extended periods (Sakaluk, 1986). Copulations are completed with the transfer of an externally attached spermatophore, which remains attached outside the female's genital opening until she removes and eats it. During the time that the spermatophore is attached to the female's genitalia, there is a roughly linear increase in the number of sperm transferred to the female (Sakaluk, 1984, 2000; Simmons, 1986), and females often remove the spermatophore before complete sperm transfer has occurred (Sakaluk, 1984; Sakaluk and Eggert, 1996; Simmons, 1986). Females can greatly influence the paternity of their offspring through their spermatophore-removal behavior (Calos and Sakaluk, 1998; Sakaluk, 1986; Sakaluk and Eggert, 1996; Wedell, 1991), thereby affording them a powerful mechanism of cryptic mate choice. A number of studies have shown that the differential spermatophore removal behavior of females imposes strong sexual selection on males, affecting a variety of phenotypic attributes, including the size of food gifts synthesized by males (Fedorka and Mousseau, 2002; Sakaluk, 1984), body size (Bateman et al., 2001; Sakaluk, 1985; Simmons, 1986), and hind-wing morphology (Sakaluk, 1997).
Although numerous studies have addressed the fitness benefits of precopulatory mate choice in a wide array of animal taxa, the benefits of cryptic mating preferences, whether direct or indirect, remain almost virtually unexplored (but see Ward, 1998). Female crickets could, in theory, derive both direct and indirect genetic benefits via their spermatophore-removal behavior. It is known, for example, that male crickets transfer substances in their ejaculates that stimulate egg production and oviposition in females (Destephano and Brady, 1977; Loher, 1979; Murtaugh and Denlinger, 1987). If females are not physically ready to allocate nutrients to egg maturation and oviposition at a time that is optimal from the male's standpoint, spermatophore removal may function to regulate the receipt of oviposition stimulants and egg-production stimulants in a manner that is coincident with the fitness interests of females. In addition, Simmons (1991) showed that female field crickets (Gryllus bimaculatus) retain their spermatophores longer after matings with more distantly related males, suggesting that there may also be indirect genetic benefits to differential spermatophore removal by females. To investigate the potential benefits of cryptic female choice in crickets, pre- and postcopulatory mechanisms need to be decoupled. We tested the hypothesis that spermatophore removal by female house crickets (Acheta domesticus) confers direct or indirect benefits on females, by randomly assigning mates to females but permitting some females to freely remove spermatophores after mating while forcing others to accept complete ejaculates. We predicted that females permitted to exercise cryptic mating preferences after mating would exhibit higher survival or reproduction than would females experimentally prevented from doing so.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experimental protocol
Crickets were obtained from Fluker Farms (Baton Rouge, LA), a commercial supplier that maintains a standing population of about 35 million A. domesticus (Fluker D, personal communication). The stock population has been regularly infused over a 10-year period with crickets from a strain known as American Mix, originating from crickets obtained from six widely separated regions of the USA and subjected to the 36 possible population x population crosses (Woodring J, personal communication); these practices were designed to maintain genetic variation and vigor of the stock colony.
Crickets were housed in ventilated 55-l plastic containers (59 x 43 x 30.5 cm). Late-instar females were held in a separate terrarium to ensure their virginity upon the adult molt. All crickets were provisioned with egg cartons for shelter and had access to food (Fluker's cricket chow) and water (in small plastic vials plugged with cotton wicks) provided ad libitum. Upon adult eclosion, crickets were housed in an incubator at 28 ± 2°C on a 12-h light/12-h dark cycle opposite to the ambient photoperiod.
Virgin adult females were randomly assigned to one of two treatments in which (1) females were permitted to freely remove a male's spermatophore any time after mating (cryptic-choice treatment; n = 18), or (2) females were prevented from removing the spermatophore until 60 min had elapsed (no-choice treatment; n = 16), a period corresponding to the time required for the spermatophore to be completely emptied of sperm (Sakaluk, 2000). Females were weighed to the nearest 0.1 mg at 6 days of adult age, and first paired the following day with a sexually experienced male of similar age. Matings were staged in specially constructed Plexiglas viewing chambers (7.7 x 10.6 x 3.4 cm) and observed under red-light illumination during the dark phase of the photoperiod. Each pair was observed for 2 h or until copulation occurred, after which the crickets were returned to their individual holding cages (ventilated 0.5-l plastic containers provisioned with ample food, water, and a weigh boat filled with moistened peat moss to serve as an oviposition substrate), housed within an environmental chamber maintained on the same light and temperature regimes. Females were paired the next day and each subsequent day with a different randomly selected male, until they had mated a total of five times. Females that failed to complete their five matings within a 10-day period were excluded from the experiment; there were only four such females, three that died before completing the mating sequence (two cryptic-choice and one no-choice), and one that mated only four times in 10 days (no-choice). The net result of this protocol is that females of both treatments were each mated five times with different males, but females in the cryptic-choice treatment received varying amounts of ejaculate from their respective partners, whereas no-choice females always received an invariant amount (i.e., a complete ejaculate) from their assigned mates.
After copulations by females assigned to the no-choice treatment, females were confined in narrow test tubes for 60 min to prevent premature spermatophore removal, after which the spermatophore was removed with fine forceps. For females assigned to the cryptic-choice treatment, males were removed from the mating chamber immediately after mating to eliminate any effect of mate guarding on female spermatophore-removal behavior (Bateman and MacFadyen, 1999; Loher and Rence, 1978; but see Khalifa, 1950; Sakaluk and Cade, 1980). Once these females had voluntarily removed their spermatophores, they were held for 60 min in narrow test tubes to control for any detrimental effects of test-tube confinement on the no-choice females. If a cryptic-choice female failed to remove the spermatophore after 60 min had elapsed (n = 4), it was removed with forceps and the female was placed in a test tube as described above. Females of both groups were prevented from consuming the spermatophore after its removal to eliminate any nutritional effects of spermatophore consumption on female fitness (Simmons, 1988).
Oviposition dishes were replaced every 5 days up until the female's death or up to a maximum of 100 days, for females surviving more than 100 days. For each female, oviposition dishes were housed communally in a small plastic shoebox (34.3 x 20.3 x 10.2 cm) maintained under the same environmental conditions as before. Dishes were moistened every other day until nymphs ceased to emerge. Newly hatched nymphs were counted daily, and the first 25 offspring emerging for a given female were reared communally in a separate shoebox until they reached adulthood. Nymphs were provided with ample water and pieces of egg carton for cover, but they were reared on a moderately stressful diet in which nymphs were deprived of food every other day (see Sakaluk et al., 2002). After hatching had ceased for at least 1 week, the peat moss within oviposition dishes was air-dried, and any unhatched eggs were counted using a stereo-microscope by an observer blind to the treatment group from which the eggs originated; to aid in this process, a Fisher Vortex Genie was used to break up any dried clumps of peat moss within which some eggs might have remained concealed.
For each female, we recorded a number of parameters presumed to be related to female (or offspring) fitness: female longevity (time from adult eclosion until death), time to first hatch (interval between a female's initial mating and the day on which nymphs first emerged), number of nymphs produced, total fecundity (number of nymphs plus the number of any unhatched eggs), number of days over which hatching occurred, percentage of nymphs surviving to adulthood, offspring developmental time (time from hatching until adult eclosion), and offspring mass at adult eclosion (a reliable predictor of adult body size at this stage of development; Gray, 1997a). We assumed that all of these parameters would be positively correlated with female fitness, except for time to first hatch (we assumed that, all else being equal, early reproduction would be favored over later reproduction) and offspring developmental time (we assumed that more rapid development would be favored over a longer time to maturity).
Statistical analyses
We used failure-time analysis (Fox, 1993) to compare differences in female survivorship between the two treatments, using PROC LIFETEST in SAS (SAS Institute, 2000). To assess differences in female reproductive success across treatments, we first reduced the number of variables to obtain uncorrelated predictors of reproductive output and offspring performance using principle components analysis (PCA). We derived the principal components (PCs) using PROC FACTOR in SAS (SAS Institute, 2000), retaining only those factors with an eigenvalue exceeding 1.0. We subsequently compared PC scores across treatments by using MANOVA (PROC GLM; SAS Institute, 2000). In the analysis of female reproductive success, one female had no offspring survive to adulthood, so we were unable to obtain direct measurements of offspring developmental time and offspring mass for this replicate. This posed a potential difficulty because PCA does not accommodate missing values for any of the original variables. However, because both developmental time and offspring mass were significantly correlated with time to hatch (r = –.42, p =.02 and r =.39, p =.03, respectively), we derived estimates of the two missing values for this replicate by extrapolating from a regression of each variable on time to hatch.
To assess variation within females in their spermatophore removal behavior across multiple matings, we calculated the repeatability of the spermatophore-removal time of those females permitted to freely remove the spermatophore after mating. Repeatability measures the extent to which differences between individuals contributes to the overall variation in a trait (Boake, 1989). Repeatability was determined as the intraclass correlation in spermatophore-removal time, derived from a one-way ANOVA by using PROC GLM of SAS (SAS Institute, 2000). The intraclass correlation coefficient (ri) was calculated as [groups MS – error MS] / [groups MS + (n – 1) error MS], where n = the number of repeated measures per individual (MS = mean square)(Zar, 1996).
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RESULTS |
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The mean spermatophore attachment duration of females in the cryptic-choice treatment (25.7 ± 12.0 min [mean ± SD]) was less than half of that of females in the no-choice treatment (59.3 ± 0.9 min). Although there was both considerable within- and between variation in the time at which females removed the spermatophore in the cryptic-choice treatment, spermatophore attachment duration was significantly repeatable (ri =.19, F13,56 = 2.20, p =.02). This remained true even when the four females who failed to remove the spermatophore after one of their five matings were included in the analysis (ri =.27, F17,72 = 2.83, p =.001).
There was no difference between treatments in the mean mass (±SE) of females measured at 6 days of adult age (cryptic-choice: 510.1 ± 17.5 mg; no-choice: 464.5 ± 22.5; t test [equal variances], t = 1.62, p =.12). There were no significant correlations between female mass and the total number of eggs produced, offspring survival, or female survival in either of the two treatments (all p >.05), so female body mass was not included as a covariate in any comparisons of reproductive output. Within the cryptic-choice treatment, there was no significant correlation between female body mass and the time at which the female removed the spermatophore (r =.22, p =.38).
The mean survival and reproductive success of females in the two treatments is shown in Table 1. Failure-time analysis revealed no significant difference in female survival across treatments (Wilcoxon 
2 = 0.71, p =.40) (Figure 1). There were a number of correlations among reproductive parameters in both treatments (Table 2). Specifically, the number of nymphs produced was positively correlated with both total egg production and hatching period for females in both treatment groups. Similarly, total egg production was positively correlated with the hatching period. Because such correlations complicate the interpretation of any treatment effects on female fitness, our analysis focused on the PCs.
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Three PCs with eigenvalues greater than one summarized more than 80% of the variation in female reproductive success (Table 3). Rotated factor scores show that PC1 represents predominantly female reproductive output, with high positive loadings on the total number of eggs laid, number of nymphs emerging, and the period over which offspring hatched (Table 4). PC2 appears to represent nymph quality, with high scores resulting from offspring of larger mass and showing more rapid development; longer times to hatch also contributed to higher PC2 scores, but variation in hatch time was markedly reduced (Table 1). PC3 appears to represent a tradeoff between offspring survival and offspring mass at sexual maturity. High scores on PC3 result from high survivorship, and low scores result from higher offspring mass and longer periods over which offspring hatch (Table 4). A MANOVA of the three PCs showed no significant effect of treatment on the factor scores (Wilks's
= 0.90, F3,30 = 1.11, p =.36).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Females that were permitted to exert cryptic mating preferences retained their spermatophores less than half as long, on the average, as females offered no such choice. Based on the trajectory of sperm transfer from the spermatophore (Sakaluk, 2000
), we estimate that cryptic-choice females received less than half the total volume of ejaculate than did no-choice females. Although we did not control for differences in the mating history of the males to whom females were mated, we are confident that such variation did not appreciably influence the relative numbers of sperm received by females of the two treatments because the number of sperm contained in successive spermatophores is known to be highly repeatable in crickets (Schaus and Sakaluk, 2003). Because sperm are recruited for fertilizations in direct proportion to their relative abundance in the female's spermatheca (Sakaluk, 1986; Sakaluk and Eggert, 1996; Simmons, 1987), it is virtually certain that the spermatophore-removal behavior of females markedly reduced the fertilization success of some males in the cryptic-choice treatment. Although we do not know which, if any, phenotypic traits were correlated with female retention of the spermatophore, these results demonstrate that female spermatophore-removal behavior constitutes a potentially powerful mechanism of cryptic choice, as has been demonstrated in other cricket species (Sakaluk, 1984, 1985, 1997; Simmons, 1986).
Although there was about a two-fold difference in the volume of ejaculate received by females of the two treatments, there were no significant differences in female longevity, fecundity or offspring production. Thus, postcopulatory spermatophore removal does not appear to confer direct benefits on females, as might be expected if spermatophore removal functioned to regulate the receipt of oviposition stimulants and egg-production stimulants in a manner that was commensurate with the long-term reproductive interests of females. However, the absence of any treatment effect does not negate the possibility of compensatory effects between different constituents of the ejaculate. For example, a positive effect accruing to a reduction in the level of harmful seminal substances transferred when the spermatophore is prematurely removed (see Chapman et al., 1995; Johnstone and Keller, 2000; Wolfner, 2002), could be outweighed by a negative effect arising from fewer sperm available for fertilizations. In any event, the absence of an effect of varying ejaculate volume on female longevity and fecundity is consistent with previous work on female field crickets, Gryllus bimaculatus (Tregenza and Wedell, 1998; but see Wagner et al., 2001).
Although there were no apparent direct benefits to female spermatophore removal behavior, females might still accrue indirect genetic benefits by prematurely removing the spermatophores of undesirable males, while retaining those of preferred mates. If this were the case, we might expect higher hatching success and greater nymph production of females permitted to remove their spermatophore if premature spermatophore removal functioned to prevent the transfer of genetically incompatible sperm, or higher offspring quality (as evidenced by more rapid development or greater adult mass) if premature spermatophore removal functioned to bias sperm transfer in favor of males possessing "good genes." However, a MANOVA of the PC scores that appear to best represent female reproductive output (PC1) and offspring quality (PC2) revealed no significant difference between treatments. The absence of a clear treatment effect suggests that within the bounds of the choice of mates that females were offered, females obtained no indirect genetic benefits through their spermatophore-removal behavior.
One final observation appears to weigh against the use of premature spermatophore removal as a means of obtaining indirect genetic benefits: spermatophore removal by individual females was significantly repeatable across multiple matings. If females were using spermatophore removal as a means of increasing the representation of sperm of preferred males, we might expect spermatophore attachment times to vary according to variation in the quality of mates that females encounter. The repeatability of spermatophore attachment duration suggests, however, that some females are intrinsically early-spermatophore removers, whereas others are late-spermatophore removers. Even if that were the case, the observed repeatability (0.19) still leaves ample scope for selective spermatophore removal arising as a consequence of variation both between and within females in the perceived quality of their mates.
Finally, it remains possible that a lack of genetic variation in male quality could account for both a failure to find evidence of indirect genetic benefits and the repeatability of female spermatophore removal, a possibility that cannot be ignored in a study involving commercially reared crickets. However, the size of the source population and rearing practices of the supplier makes it highly unlikely that our crickets were inbred (see Methods). Moreover, recent studies of A. domesticus obtained from commercial suppliers has revealed significant heritable variation in traits deemed critical to male reproductive success, including male body size (Gray, 1997b; Ryder and Siva-Jothy, 2001) and immune function (Ryder and Siva-Jothy, 2001).
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ACKNOWLEDGEMENTS |
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We thank T.M. Ivy and two anonymous reviewers for constructive comments on the manuscript, C.F. Thompson and W.L. Perry for helpful suggestions on the design of the study, and D. Fluker and J. Woodring for graciously sharing information on cricket rearing practices used at Fluker Farms. This research was funded by grants from the Graduate School at Illinois State University, the Beta Lambda Chapter of the Phi Sigma Biological Honors Society, and the Orthopterist's Society to R.R.F. and a grant from the National Science Foundation (IBN-0126820) to S.K.S.
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