Do female leopard geckos (Eublepharis macularius) discriminate between previous mates and novel males? Lara D. LaDage1) & Michael H. Ferkin (Department of Biology, Ellington Hall, The University of Memphis, 3700 Walker Avenue, Memphis, TN 38152, USA) (Accepted: 8 March 2007)
Summary Females in numerous taxa engage in mating with more than one male within a breeding season, usually to gain direct or indirect benefits from their male partners. Although effort has been directed towards the benefits females derive from multiple mating, we have less information as to decisions females make when choosing to mate with more than one male and if her decision is contingent upon previous mating experience with a male. In some instances, females must decide whether or not to mate with a previous mate or a novel male, the outcome of which would have ramifications on the acquisition of direct and indirect benefits. In this study, we tested whether female leopard geckos, Eublepharis macularius, would forgo mating with a previous male partner in favor of a novel male. We found no difference in a female’s willingness to copulate with a previous mate versus a novel male. However, we found that smaller females initiated copulation termination with a previous mate whereas larger females allowed males to terminate copulations. This pattern was not exhibited when smaller females were paired with novel partners. Thus, smaller females appear to discriminate between previous mates and novel males, favoring novel males as mates. Keywords: multiple mating, novel male, previous mate, mate choice, leopard gecko.
Introduction Questions surrounding mating with multiple partners have provided a ripe area for research. The traditional view of multiple mating was that it provided 1)
Corresponding author’s e-mail address:
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© Koninklijke Brill NV, Leiden, 2007
Behaviour 144, 515-527 Also available online - www.brill.nl/beh
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advantages for males in that multiple mating allowed males to increase their fitness by mating with different females. The basis for this view is grounded in the idea that sperm is supposedly cheap to produce relative to eggs, thus males should be selected to fertilize the eggs of as many females as possible (Bateman, 1948; Trivers, 1972). More recently, researchers have focused on questions about multiple mating by females (Halliday & Arnold, 1987; Reynolds, 1996; Birkhead & Møller, 1998; Birkhead, 2000). The idea that sperm from one mating with one male is sufficient to fertilize a female’s eggs provides an apparent theoretical paradox. However, this paradox has had a degree of resolution by taking into account the benefits a female may receive by mating more than once. Females may gain direct benefits by mating with multiple males, reflected by increased fecundity, increased life span, and increased access to resources and/or decreased harassment by other males (Hunter et al., 1993; Andersson, 1994; Arnqvist & Nilsson, 2000; Møller & Jennions, 2001). Conversely, females may accrue indirect benefits by obtaining compatible and/or superior sperm, which results in an increase in the fitness of their offspring (Zeh & Zeh, 1996; Tregenza & Wedell, 1998; Yasui, 1998; Jennions & Petrie, 2000). Although, the literature on ‘why’ females mate with multiple partners is growing rapidly (Yasui, 1998; Jennions & Petrie, 2000; Barbosa & Magurran, 2006), we know less about the males females choose to mate with. With the exception of cases with forced or coerced copulation (Cordero, 1999), females can decide whether or not to mate with particular males and, in some situations, whether or not to mate with a previous mate or a novel male. This may be important in species where females are likely to encounter both a previous mate and novel males within the breeding season. To our knowledge, there are only six studies explicitly testing whether females prefer to mate with novel males versus previous mates. Studies of females in four species of invertebrates and a fish reported rejection of previous mates in favor of mating with novel males (Bateman, 1998; Zeh et al., 1998; Archer & Elgar, 1999; Eakley & Houde, 2004; Ivy et al., 2005). In contrast, a study on cannibalistic spiders found that females did not reject mating with a previous mate in favor of mating with a novel male (Fromhage & Schneider, 2005). As suggested by these mixed outcomes, a novel male preference is likely to be related to the ecology of the species and the importance of acquiring indirect benefits through mating with more than one male. However, because mating with more than one male appears to be a general pattern among most
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vertebrates (Halliday & Arnold, 1987; Birkhead, 2000), further testing is needed to determine if females avoid breeding with a previous mate in lieu of breeding with a novel male. Thus, the objective of the present study is to study the occurrence of mate preference in female leopard geckos, Eublepharis macularius. Specifically, we will assess whether or not female leopard geckos modify mating behaviors when paired with a previous mate versus a novel male. Female geckos make an excellent model for addressing this issue, in that female leopard geckos readily mate more than once before ovipositing (L. Kradochvil, personal communication). Second, leopard geckos can discriminate between familiar and unfamiliar opposite-sex conspecifics (Steele & Cooper, 1997) and distinguish between two familiar opposite-sex conspecifics (LaDage & Ferkin, 2006). Finally, egg production and fertility is greater in polyandrous compared with monandrous female leopard geckos, suggesting females may benefit from mating with multiple males (L. LaDage, unpublished data). Specifically, we test the hypothesis that female leopard geckos discriminate between previous mates and novel males and modify mating behaviors during paired encounters with them. There are two mutually exclusive predictions associated with this hypothesis. First, female geckos will prefer to mate again with a previous mate. Second, female geckos will prefer to mate with a novel male. The alternative hypothesis is that female leopard geckos do not discriminate between previous mates and novel males and either show no mating preference or the inability to discriminate among males. To test between these two hypotheses we measured the mating preferences of female leopard geckos by pairing them sequentially with either a previous mate or a novel male. We compared female rejection of males, duration of copulation, and the behaviors surrounding coitus between females paired with a novel male and females paired with a previous mate. We also recorded if copulation was terminated by the female or if it was jointly terminated by both the male and the female. We used differences within each of these behaviors as measures of a female’s preference for a particular male.
Material and methods Animals All leopard geckos used in this study were hatched and individually reared in the laboratory, 2-3 years old and proven breeders from the previous season.
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Before, during and after the study, male and female geckos were housed individually in opaque Plexiglas enclosures (60.9 × 30.5 × 20.3 cm, length × width × height) with paper toweling substrate. Geckos were provided with a halved plastic cup as shelter. Crickets and mealworms dusted with calcium powder and multivitamins were provided three times a week while access to water was unrestricted. All geckos were maintained on a photoperiod of 14L:10D to simulate a day length prevalent during the breeding season. Subjects and treatment groups We began the experiment with 50 size-matched, sexually receptive females. We ascertained receptivity by visual inspection of follicular growth, apparent through the translucent abdomen wall (Rhen et al., 2000). These females were randomly assigned to two treatment groups. One group consisted of females who were mated to males and, 24 h later, re-mated to the same males (previous mate treatment). The other group was comprised of females who were mated to males and, 24 h later, re-mated to different males (novel male treatment). In this group, the previous mate and the novel male were matched for body size. Within group two, a male used as the ‘previous mate’ for one female was used as the ‘novel male’ for a different female. In this way, we controlled for a male’s recent sexual history; during the second round of matings in both the previous mate treatment and the novel male treatment, all males had mated exactly once, 24 h earlier. Testing procedure All tests were conducted between 1400 and 1600 h in the male’s home enclosure. Female geckos underwent two encounters with males. During the first encounter, each female was removed from her home enclosure and placed into a male’s enclosure for 10 min. After the 10-min encounter, the females were returned to their home enclosures. Females who failed to mate during the first encounter with the male were excluded from the study. Ten females failed to mate from the novel male treatment whereas 9 females failed to mate in the previous mate treatment. One female from the previous mate treatment was removed from the experiment due to injuries inflicted by the male during the first encounter. The remaining 40 females who mated during the first encounter were allowed to continue in the experiment and undergo a second encounter with a male gecko, 24 h after the first encounter with a male
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gecko. During the second encounter, female geckos were allowed to interact for 10-min with either their previous mate (the male from the first encounter) or a novel male. Thus, we had two treatment groups in encounter 2, females that were paired with a previous mate and females that were paired with a novel male. The second encounter, like the first encounter, took place in the male’s home cage. As with the first encounter, the females were returned to their home enclosures after encounter 2. During the first and second encounters, we recorded whether a female mated with the male and, if she did mate, the duration of the copulation. We also recorded if copulation was terminated by the female or if it was jointly terminated by both the male and the female (hereafter, referred to as mutual termination). Our pilot data indicated that males did not terminate copulations without cooperation of the females. Therefore, the termination of copulation may reflect a differential behavioral response by the female in regard to mate choice. Female-terminated copulations were obvious, in that the female actively terminated the copulation by thrashing and biting the male while the male attempted to continue intromission. In all cases where the female attempted to terminate copulations, the male always acquiesced. In mutual termination, the female remained motionless while the male dismounted. Lastly, we recorded the time from introduction of the female into the male’s home enclosure, until the time the male first attempted to bite the female’s tail (hereafter, referred to as latency to tail grab). Tail grabbing and biting is a typical component of courtship in this species (Brillet, 1991). We utilized latency to tail grab as an indicator of a male’s motivation to mate; higher latencies reflected a lower motivation to copulate. All behavioral observations were conducted from behind a blind by a single observer, and recorded with a video camera recorder for further review (Sony Handycam Vision CCD-TRV65). A second observer scored the behavioral measures from the videotape and was blind to the treatment groups. The testing procedure was approved by the Institutional Animal Care and Use Committee at The University of Memphis. Statistics To assure female body weight did not differ between treatments and to verify that all individuals were properly size-matched when randomly assigning individuals to treatment groups, we used ANCOVA with male body weight as
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the covariate. As expected from our weight matching assignments, we found no differences between treatments in female body weight when controlling for male body weight (F1,37 = 0.544, p = 0.456). Next, we used a Fisher’s exact test to determine if rejection of a male differed between females introduced to a previous partner or a novel male. For several species, female body weight has been a relevant variable in determining the number of partners and/or number of copulations, in addition to copulation duration. Studies have shown that larger females in several species copulate more often and with more males, as well as copulate longer, than smaller females (e.g., Rowe & Arnqvist, 1996; Bergstrom et al., 2002; Schäfer & Uhl, 2004; Fitze et al., 2005). Thus, we first performed linear regression, with both latency to tail grab and duration of copulation regressed on female body weight, to determine if female body weight was correlated to either variable. The results of the linear regression indicated no significant relationship between female body weight and the two variables (latency to tail grab: r 2 = 0.073, p = 0.653; copulation duration: r 2 = 0.022, p = 0.892). Thus, we used a two factor ANOVA with repeated measures on encounter to determine if latency to tail grab and copulation duration differed between the first and second encounters, as well as between matings with a previous mate and a novel male in the second encounter. Finally, we used a chi-squared test to ascertain if encounter and treatment group (previous mate or novel male) could predict differences in femaleinitiate copulation termination and mutual copulation termination. We also used logistic regression to ascertain if termination of copulation was related to treatment groups, as well as female body weight and the interaction between treatment and female body weight. We centered female body weight data so as to ensure the y-intercept was the predicted value for an average individual (Wainer, 2000). We entered predictors en bloc and performed forward selection and backward elimination to substantiate our results. We used the χ 2 test of the model coefficients to ascertain the goodness of contribution from the predictor set, while assuring model fit using the −2 log likelihood statistic. Additionally, we used Wald’s χ 2 to ascertain the significant contributions of the predictor variables to the model. All statistics were performed using either the SPSS statistical package (version 11.0; SPSS, Chicago, IL, USA) or the SAS statistical package (version 9.1; SAS Institute, Cary, NC, USA).
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Results All continuous data conformed to assumptions of normality and homogeneity of variances. All data are reported as the mean ± SEM. The rejection of males by females and the latency to tail grab were not affected by whether a female gecko mated with a previous mate or a novel male. Females rejected a similar proportion of males during the encounter 2, regardless of whether the male was a previous mate or a novel male (11.1% vs. 17.6%, respectively; Fisher’s exact test, p = 0.537). The latency to tail grab did not differ between encounters (F1,38 = 1.096, p = 0.302), treatments (F1,38 = 0.084, p = 0.774) or the interaction between encounter and treatment (F1,38 = 0.689, p = 0.412). Specifically, the mean ± SEM for the latency to tail grab was similar for males during encounter 1 in treatment 1 (82.65 ± 11.54 s) and treatment 2 (65.05 ± 11.16 s), and during encounter 2 with either a previous mate (86.0 ± 20.88 s) or a novel male (94.10 ± 18.03 s). The duration of copulation was not affected by whether a female gecko mated either with a previous mate or a novel male (F1,38 = 0.962, p = 0.333), encounter (F1,38 = 3.060, p = 0.088), or the interaction between encounter and treatment (F1,38 = 0.695, p = 0.410). That is, the mean ± SEM for the duration of copulations was similar for males during encounter 1 in treatment 1 (43.30 ± 4.33 s) and treatment 2 (42.55 ± 4.19 s), as well as encounter 2 with a previous mate (57.55 ± 7.44 s) and encounter 2 with a novel male (47.60 ± 5.36 s). We found no differences in copulation termination based on either encounter or treatment (χ 2 = 0.473, p = 0.4914). Interestingly, however, we found that body weight of the female affected whether she terminated copulation with a previous mate. From our logistic regression analysis, we found that our set of predictors (treatment, female body weight and treatment by female body weight) significantly contributed to termination (χ 2 = 4.716, p = 0.030). We also found our predictors were adequate to account for termination; our model did not differ from the hypothetical model (χ 2 = 48.586, p = 0.097). Both the forward selection and backward elimination technique yielded female body weight and the interaction of treatment and female body weight as the contributing predictors in the final analysis. Finally, an analysis of the individual predictor variables indicated that the interaction between female body weight and treatment significantly predicted whether copulations were female-terminated or mutuallyterminated (χ 2 = 3.919, p = 0.048), whereas female body weight alone
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Figure 1. Probability of mutual copulation termination related to female body weight for females remated to a previous mate. Open circles (◦) represent predicted probabilities derived from the logistic regression equation. Darkened circles (•) represent observed values.
did not (χ 2 = 0.795, p = 0.373). We plotted observed values against the predicted probabilities from the regression equation, showing that smaller females paired with a previous mate were more likely to terminate copulation than were larger females paired with a previous mate (Figure 1).
Discussion We determined whether female leopard geckos displayed a mating preference for either a previous mate or a novel male. Specifically, we tested the hypothesis that female leopard geckos discriminate between previous mates and novel males and modified mating behaviors during paired encounters with them. The alternative hypothesis was that female leopard geckos do not exhibit a mating preference between previous mates and novel males. Overall, the results of our study provided partial support for both hypotheses. To our knowledge, this is the first report of female mate choice between previous mates and novel males in reptiles and the second such report in vertebrates (Eakley & Houde, 2004). Most of our results were consistent with the alternative hypothesis that female leopard geckos do not exhibit behavioral preferences for previous mates or novel males. First, we found that female geckos were equally likely
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to reject copulation attempts by previous mates as they were to reject copulation attempts by novel males. These results were similar to those found in cannibalistic spiders (Fromhage & Schneider, 2005) and hide beetles (Archer & Elgar, 1999), where all females remated, regardless of whether the males were previous or novel partners. Also, Zeh et al. (1998) found that female pseudoscorpions accepted sperm packets less often from previous partners than with novel males when the interval between copulations was 1.5 h. However, the female pseudoscorpions accepted sperm packets at similar rates with both previous and novel partners after 48 h had passed. Conversely, studies on guppies and two species of crickets showed that females preferred to mate with novel males (Bateman, 1998; Eakley & Houde, 2004; Ivy et al., 2005). Direct comparison of our results and the studies on guppies and crickets are tenuous, in that in the present study, we allowed female geckos to mate sequentially with either a previous or a novel male, whereas female guppies and crickets were given equal access to both a previous mate and a novel male. Next, we found no difference in copulation duration among females that were paired with a previous mate or those paired with a novel male. Fromhage & Schneider (2005) also found that female cannibalistic spiders did not differ in copulation duration depending on previous mating experience with a male. In contrast, female hide beetles copulated longer with novel males than they did with previous mates (Archer & Elgar, 1999). Lastly, we found no differences in behavior of females or males during the two encounters. The latency for males to tail grab was not affected by previous mating experiences (either none or one mating 24 h previous). For females, copulation duration and copulation termination did not differ between their two encounters with males. Therefore, female and male leopard geckos did not appear to alter their copulatory behaviors between the first and second encounter, independent of whether they were mating with a previous mate or a novel male. Given that female geckos exhibited no other behavioral discrimination between males, it appears that they do not modify mating behaviors when mated to either novel males or previous mates at the pre-copulatory stage. Therefore, novel male discrimination may not be important at the pre-copulatory stage in this species, but may be involved in the termination of copulation. We found some support for the hypothesis that female leopard geckos discriminate between previous mates and novel males in terms of copulation termination. Copulation termination differed when females were mated
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with a previous mate compared with a novel male; however, this was contingent upon female body weight. Specifically, smaller females were more likely than larger females to terminate copulations with a previous mate, but not with a novel male. Although our experimental design precluded testing if larger females mated more often than smaller females, female body weight has been shown to influence female copulatory behavior in other taxa; larger female mate more often, copulate longer and have a greater number of partners than do smaller females (Rowe & Arnqvist, 1996; Schäfer & Uhl, 2004; Fitze et al., 2005). Interestingly, our results do not support the view that larger females should mate more often than do smaller females. Previous studies have shown that larger females suffer lower relative costs associated with physical damage sustained during copulations and/or costs associated with finding a mate as compared to the costs suffered by smaller females (Milinski & Bakker, 1992; Birkhead & Møller, 1998; Shine et al., 2000; Schäfer & Uhl, 2004). Also, for many squamates, female fecundity increases with body size, thus larger females are more likely to be courted by males (Avery, 1975; Olsson, 1993). Our data were not in agreement with the results reported in these studies. Instead, our findings suggest that for female leopard geckos, body weight is correlated with the termination of copulation with a previous mate. Future studies may want to specifically address whether there is a possible effect on copulation termination due to body size, sperm storage capacity and experience with a particular male (i.e., a novel male versus a previous mate). Why did body weight correlate with the termination of copulation with a previous mate? We speculate that differences in copulation terminations by smaller and larger female geckos may be associated with hypotheses that focus on the storage of sperm from previous matings (Schäfer & Uhl, 2004). Although not tested explicitly in the present study, female geckos may gain indirect benefits if they copulate with multiple males (Madsen et al., 1992; Birkhead & Møller, 1993; Parker et al., 1996; Olsson & Madsen, 1998; Pearse & Avise, 2001). However, the benefits may be difficult to acquire for smaller females, as they have less sperm storage capacity relative to that of a larger female (Schäfer & Uhl, 2004). Thus, by terminating copulation with a previous mate, a small female gecko may limit the amount of his sperm that she needs to store, which would allow her room to store sperm from a novel male. By comparison, larger female geckos may not need to terminate copulations with a previous mate because she may have sufficient
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space available to store his sperm as well as sperm from novel males. Female leopard geckos can store sperm from one or two matings for several months, producing upwards of 6 fertile clutches over the course of the laying season (L. LaDage, unpublished data). By terminating copulations with previous mates, smaller female geckos may allow for the sperm from future matings, and potentially facilitate sperm competition, sperm mixing, and the opportunity for post-copulatory sperm manipulation, leading to the acquisition of indirect benefits (Zeh & Zeh, 1996; Birkhead & Møller, 1998; Birkhead, 2000; Olsson & Madsen, 2001; Calsbeek & Sinervo, 2004).
Acknowledgements We thank Chee Lam and Rich Simmons for their technical assistance and Dr. David Crews for providing the original breeding stock of leopard geckos. Two anonymous reviewers offered helpful comments on an earlier draft of this manuscript. This work was supported by NSF grant IOB 04444553 and NIH grant HDO 49525 to M.H.F. We dedicate this paper to the memory of Dr. Bill Gutzke.
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