Social experience affects territorial and reproductive behaviours in male leopard geckos, eublepharis macularius

ANIMAL BEHAVIOUR, 2002, 63, 487–493
doi:10.1006/anbe.2001.1952, available online at http://www.idealibrary.com on
Social experience affects territorial and reproductive behaviours in male leopard geckos, Eublepharis macularius JON T. SAKATA*, AJAY GUPTA*, CHIEN-PEI CHUANG* & DAVID CREWS*†
*Institute for Neuroscience, University of Texas at Austin †Section for Integrative Biology, School of Biological Sciences, University of Texas at Austin (Received 18 December 2000; initial acceptance 20 February 2001; final acceptance 11 September 2001; MS. number: A8946R2) Social interactions have lasting effects on behaviour and physiology in a variety of organisms. In theleopard gecko, Eublepharis macularius, social experience alters neural metabolism and elevates circulatingconcentrations of androgens. In this study, we assessed the effects of social experience (housing withfemales versus housing in isolation) on the expression of social behaviours in male geckos (1) whengonadally intact, (2) following castration and (3) following testosterone administration. Given the neuraland endocrine changes following social experience, we hypothesized that social experience wouldincrease the capacity to display territorial and courtship behaviour in male leopard geckos. We found thatintact males previously housed with females (experienced males) displayed more territorial marking andmore activity when exposed to a neutral test arena relative to males housed in isolation (naïve males).
Experienced males continued to show more marking and activity in the testing arena relative to naïvemales following castration. However, the courtship behaviour of castrated naïve and experienced malesdid not differ significantly. Following testosterone administration, experienced males again showed moreactivity in the empty test arena and tended to show more courtship behaviour. In summary, we foundsupport for the hypothesis that social experience leads to changes in territorial and courtship behavioursand, moreover, found that male leopard geckos share some degree of commonality with other vertebratesin behavioural plasticity following social experience.
 2002 The Association for the Study of Animal Behaviour While much of the research in behavioural biology has dramatically affects subsequent behaviour. For example, focused on the persistent effects of early experiences on the presence of courting males facilitates ovarian growth Interactions with females affect the propensity to that experiences in adulthood, particularly social inter- display aggression in males of a variety of species (e.g.
actions, significantly affect phenotype. For example, aggressive experience and social environment alter the and courtship experience in adulthood significantly neuroendocrine system and the probability of displaying affects sexual preferences in male zebra finches, Taeniopy- sexual and aggressive behaviours in mammals (reviewed hood increases the capacity to display copulatory behav- iour in the absence of androgens in male rats, hamsters increases the sensitivity to the activational effects of and fish (e.g. Social status also affects androgens on the reinstatement of copulatory behaviour the neurochemical modulation of escape behaviour in and interaction with, individuals of the opposite sex Both species and strain within a species alter the effects of social and sexual experience on subsequent behaviour.
Correspondence: J. T. Sakata, Institute for Neuroscience, Patterson For example, in male rats but not in rhesus monkeys, Hall, University of Texas at Austin, Austin, TX 78712, U.S.A. (email: Macaca mulatta, mating experience can reverse the detri- [email protected]). A. Gupta, C-P. Chuang and D. Crews areat the Institute for Neuroscience, University of Texas at Austin, Austin, mental effects of social isolation on copulatory behaviour in adulthood (reviewed in Furthermore, in  2002 The Association for the Study of Animal Behaviour ANIMAL BEHAVIOUR, 63, 3
mice, early social experience facilitates the expression of housed all geckos individually in polypropylene con- both aggressive and copulatory behaviours in adulthood, but males selectively bred for aggressiveness show a 10 weeks, we maintained all individuals on a 14:10 h greater facilitation than males selectively bred for non- light:dark cycle, at 30 C, and provided water and crickets 5 days a week. From then on, we maintained individuals strains of mice and guinea pigs there is also significant on an LD 14:10 h cycle during which temperature ranged variation in experience-dependent changes in copulatory from 18 C at night to 30 C during the day. We provided water and mealworms three times a week. Crickets and mealworms were dusted with vitamin supplements. After behavioural plasticity in response to social experience are reaching sexual maturity, we placed males (1–1.5 years of likely to be correlated with differences in neural plasticity in brain regions modulating social behaviours.
breeding cage with three to four intact, cycling female In this study, we investigated the effects of extensive social experience on the behavioural phenotype of the housed in the same environmental chamber (LD 14:10 h leopard gecko, Eublepharis macularius. In a previous study, cycle; temperatures ranged from 18 C at night to the effects of extensive social experience on neural 30 C during the day). Males were left in their respective metabolism and sex steroid hormone concentrations housing conditions for 1–2 years and then tested for present study was to assess the behavioural correlates ofthese neural and hormonal changes. The leopard geckois a medium-sized lizard indigenous to western India, Behavioural Testing
Pakistan and Turkey, and is an interesting model systemin which to study the biological basis of individual The experimental design is summarized in differences in behaviour. Early experience, namely First, we investigated behavioural differences between embryonic incubation temperature, not only determines gonadally intact males housed in isolation (i.e. naïve gonadal sex in this species, but also has profound effects males, N=11) versus males housed with intact females on adult neuroendocrine and behavioural phenotypes (i.e. experienced males, N=10). We placed males in a hatched from eggs incubated at a temperature that pro- paper towel, and observed activity and scent-marking duces primarily males (32.5 C) have elevated concen- behaviours for 5 min. We recorded the duration of active trations of androgens and depressed concentrations of movement and scent marking. We defined activity as oestrogens relative to males from eggs incubated at a movement of the body and limbs in any direction (i.e.
temperature that produces primarily females (30 C) ambulation). Scent marking is a characteristic territorial behaviour in which the preanal pores are pressed down thermore, males and females hatched from eggs incu- onto the substrate and swiped laterally. Because we con- bated at warmer incubation temperatures are more sidered scent marking and activity as separate behaviours, aggressive in adulthood than individuals from cooler our measures of activity duration do not include scent- marking duration. If we did not observe the behaviour of iment we investigated the effects of social experiences in interest, we assigned a duration of zero. We tested each adulthood on behavioural phenotype by comparing the male twice (day 1 and 4), separated by 3 days.
behaviours of socially experienced and naïve male geckos Thereafter, we obtained a rough estimate of the sexual when gonadally intact, following castration and follow- vigour of the experienced males by testing them in the ing androgen replacement. We hypothesized that, rela- neutral arena with a receptive female. We did not test tive to socially naïve males, experienced males would be naïve males to preclude any social experience with (1) more territorial, (2) more likely to display courtship females prior to castration. In these tests, we placed the behaviour following castration and (3) more sensitive males in a test arena freshly lined with paper towels and to the activational effects of androgens on courtship allowed them to habituate for 5 min. Thereafter, we placed a receptive female in the arena and observedcourtship behaviour. Courtship behaviour in this specieshas previously been described We first screened females with sexually vigorous males and classi- Animals and Procedures
fied only females that remained motionless and did notbite back in response to courtship as receptive. We We reared male leopard geckos in isolation until sexual recorded whether the male body-gripped the stimulus maturity. All males were hatched from eggs incubated at female within 5 min after her introduction. We tested 32.5 C. We only used males hatched from eggs incubated each male three times, each occasion separated by 5 days.
at 32.5 C because the effects of social experience on brain All experienced males in this experiment courted females metabolism have been previously investigated in males on at least one of the three tests. We also placed naïve males in the test arenas three times for the same duration because an aim of this study was to assess the behavioural (i.e. 10 min) to equalize the amount of exposure to the correlates of these neural and hormonal changes. We test chamber and to ensure that differences in behaviour SAKATA ET AL.: SOCIAL EXPERIENCE ALTERS BEHAVIOUR
Table 1. Experimental design and statistical analysis
Average duration of activity as well as the percentage of tests in which scent-marking, body-gripping and mounting behaviours were displayed were calculated for each male within each phase (i.e.
following castration and following testosterone implantation). Both experimental phases and all four behaviours were analysed in one two-way MANOVA (independent variables: group and experimentalphase; dependent variable: behaviour).
following castration would not be due to differences in test (one test was missing for four males, and two tests, for one male). Behavioural scores for males who needed Thereafter, we gonadectomized all males under cold reimplantation did not differ significantly from those anaesthesia, returned them to an isolate cage, and who did not need reimplantation, and, therefore, this was allowed them 1 week to recover from surgery. We ignored in the analysis. Four days after their final test, we returned naïve males to their original home cage, and killed the males by rapid decapitation and checked them housed experienced males in the isolate cages in which for intact implants and for evidence of testicular growth.
they had been housed for 2 days prior to castration.
We excluded one experienced male from the experiment Therefore, following castration, both groups of males following castration because he had residual testes (i.e.
were housed in cages in which they were familiar. Testing began 1 week after castration, and tests were separated by4 days. We conducted 20 postcastration tests. We placed Statistical Analyses
with a fresh paper towel for 5 min (habituation period) First, we analysed group differences in the proportion and recorded durations of activity and scent marking.
of males that showed activity or scent marking in the Thereafter, we placed a receptive female in the arena and empty test arena when gonadally intact. We categorized observed males for courtship behaviour. If the male failed males as ‘active’ if they were active on at least one of the to body-grip the female within 5 min, we terminated the two tests, and as ‘inactive’ if they were inactive on both test. However, if the male did body-grip the female within tests. We used the same categorization for scent-marking 5 min, we continued the test for up to 10 min to allow for behaviour. We analysed group differences using a likeli- mounting. We stopped testing immediately if and when a hood ratio test. Furthermore, we analysed group differ- male mounted. All males stopped courting by the 20th ences in the average duration of activity (across days 1 and 4) using a univariate analysis of variance (ANOVA).
After the postcastration tests, we implanted males sub- The distribution of average activity durations did cutaneously under cold anaesthesia with a Silastic testos- not deviate significantly from normality (Shapiro–Wilk W test: W=0.95, N=21, P=0.144).
For the analysis of behavioural differences between approximate physiological levels of T in adult males and naïve and experienced males when castrated and follow- effectively elicits courtship behaviour in castrated males ing T replacement, we analysed four behavioural par- ameters (average duration of activity in the empty test all males every 4 days with a receptive female in the chamber, the percentage of tests in which the male testing arena using the paradigm described above (range scent-marked in the empty test chamber, the percentage 8–10 tests/male). We initially placed implants on the back of tests in which the male body-gripped the female and (tests 1–5) but, because of frequent wound breaks, we the percentage of tests in which the male mounted the moved the implants to an area just behind the shoulders female) across both experimental phases using a two-way after the fifth test. If implants were missing from the repeated measures multivariate ANOVA. The between- male, the male was not tested and was reimplanted subject variables were group (naïve versus experienced) immediately with the same implant. Testing resumed and experimental phase (castrated versus T-implanted) 4 days after reimplantation (i.e. at the time of the next and the within-subject variable was behaviour (i.e. the scheduled test). Five males were not tested for at least one four behavioural parameters). We also included the ANIMAL BEHAVIOUR, 63, 3
Figure 1. Relative to gonadally intact naïve males (N=11; ), intact
experienced males (N=10; ) showed more activity (longer average duration) in the empty test arena, and a significantly greater percentage of experienced males scent-marked in the arena.
Figure 2. (a) Following castration, experienced males (N=9; )
showed more activity (longer average duration) and displayed
scent-marking behaviour in the empty test chamber on a greater
identity of the male as a random variable nested within percentage of tests than naïve males (N=11; ). However, there group; adding this factor eliminates the variability among were no differences in the percentage of tests in which males subjects due to individual differences from the error term body-gripped or mounted stimulus females. (b) Following testoster- one implantation, experienced males showed increased duration of were arcsine square-root transformed to improve normal- activity in the empty test chamber, and there was a trend for ity. We used Pillai’s trace as our multivariate statistic experienced males to show more body-gripping and mounting because it is the most robust to deviations from multivari- behaviour. *Significant group differences.
ate normality and homogeneity of variance–covariancematrices There was a significant main effect of behaviour in all analyses because we used different scales of measurement for the behavioural scores; these *experimental phase*behaviour (F3,15 P=0.043). Because we were particularly interested in For all analyses, we set =0.05. All statistics were done group differences within each experimental phase, we ran imental design and statistical approach are outlined in In the analysis of group differences following cas- tration, there was a significant effect of group (MANOVA:F =10.0, P=0.005), and overall, experienced males had elevated scores. More importantly, there was a significantgroup*behaviour interaction (F Behavioural Differences between Experienced and
quently, we ran four separate univariate ANOVAs with Naïve Males
group as the sole independent variable. Average activityduration (F =11.7, P=0.003) and the percentage of Whereas all naïve and experienced males were active nificantly greater in experienced males, whereas there when placed in the test chamber, a significantly greater were no significant differences between the groups in the percentage of experienced males displayed scent-marking percentage of tests with body grips (F Furthermore, although the percentage of active males was In the analysis of group differences following T implan- equal across the groups, the average activity duration tation, there was a significant main effect of group was significantly higher in experienced males (ANOVA: =5.2, P=0.035), and overall, experienced males had elevated scores. Although the group*behaviour P=0.132), we analysed each behaviour separately using Following castration and following testosterone a univariate ANOVA to assess which behavioural par- ameters contributed most to this overall difference We found that only the average duration of activity =62.0, P<0.001) and experimental phase was significantly elevated in experienced males relative to =21.7, P<0.001). Overall, experienced males had =4.5, P=0.050). However, the difference elevated scores, and scores following T implantation were in the percentage of tests with courtship behaviour significantly higher than those following castration.
approached significance (body grips: F More importantly, there were a number of significant SAKATA ET AL.: SOCIAL EXPERIENCE ALTERS BEHAVIOUR
DISCUSSION
Similarly, copulatory behaviour is less severely affected bynovel environments in sexually experienced male rats In this study, we analysed the behavioural differences than in naïve males, and a difference in anxiety in between adult males given extensive social experience response to handling and novelty is thought to underlie (i.e. males housed with females for 1–2 years: experienced males) and males housed in isolation for the same Taken together, these data indicate that more active duration (naïve males). We analysed differences while male geckos show more territorial behaviour. A similar gonadally intact, following castration and following tes- phenomenon is found in mice. Male mice selected for tosterone (T) replacement and we investigated aggressiveness show higher rates of ambulation than mice group differences in activity, scent-marking and court- selected for nonaggressiveness (reviewed in ship behaviours. We found that, relative to naïve males, Seasonal changes in activity are correlated with experienced males displayed more territorial marking changes in territoriality in green anoles, Anolis carolinensis behaviour in the empty test arena when gonadally intact and following castration. Experienced males were also parallel between agonistic behaviour and ambulation in more active in the empty arena, and this difference was the test chamber is that both are inversely related to the found under all hormonal conditions. There were no amount of fear or anxiety experienced by the individual.
significant differences in courtship behaviour following Males that are less stressed by handling and by placement castration between experienced and naïve males, but into the test arena are more likely to explore and mark experienced males tended to show more courtship their territory. Interestingly, male rats are less aggressive in strange cages, and it is proposed that this is due to Experienced males were more likely to display agonistic marking behaviour in the empty chamber than naïve There is considerable species variation in the effects of males both when gonadally intact and following cas- heterosexual social experience on the propensity to show sexual behaviour after castration and after hormone elevated concentrations of androgens relative to naïve replacement. We found that socially experienced male geckos were not significantly more robust to castration is androgen dependent, it is possible that the difference in than naïve males. Sexual experience also has negligible marking behaviour between experienced and naïve males effects on postcastration sexual behaviour in dogs when intact was due to this hormonal difference. How- whereas in hamsters and mice, differences ever, that this behavioural difference persisted following between experienced and naïve males persist up to 3–4 castration suggests that the difference could be androgen independent. Aggression outside of the breeding season Although the effect of sexual experience on rat has been found independent of androgens in some copulatory behaviour following castration is less robust, significant differences between sexually experienced and underlie the differences found here. Interestingly, the display of territorial behaviour during the nonbreeding season is independent of androgens in older male ever, socially experienced male geckos tend to show more European starlings, Sturnus vulgaris, but not in young, less courtship behaviour following T replacement relative to naïve males, and similar results have been found in rats experience increases aggressiveness in male rats in an Furthermore, gonadally intact male geckos that has been postulated that social experiences may be more scent-mark in the empty test chamber are more likely to critical in modulating the expression of agonistic behav- court stimulus females (J. T. Sakata, A. Gupta, C-P Chuang & D. Crews, unpublished data), and the fact that intact experienced males marked more than intact naïve males The amount of activity shown during the habituation suggests that experienced males are more likely to court period was the parameter most reliably affected by social females than naïve males when gonadally intact. Similar experience. Experienced males were significantly more differences in sexual behaviour between intact experi- active when intact, following castration and following T enced and naïve male rodents have also been reported administration, and this difference was not due to a difference in the proportion of tests in which males were between geckos and rats, there appear to be differences in active and data not shown). Naïve males tended the effects of social experience on robustness to castration to show little activity in the neutral test arena; this but conservation in its effects on sexual behaviour in the inactivity could be analogous to freezing behaviour in rodents during open-field tests, a behaviour that reflects We hypothesize that the behavioural differences the individuals’ level of anxiety or fear between experienced and naïve male geckos could be The relationship between open-field behaviour causally linked to experience-dependent alterations in and anxiety, however, has not been investigated in rep- metabolic activity in the key limbic brain areas. Gonad- tiles. When gonadally intact, naïve males also showed ally intact experienced male geckos have elevated more fleeing behaviour in the empty test arena (data not metabolic capacity in caudal hypothalamic areas such as shown), and this is consistent with this interpretation.
the ventromedial hypothalamus (VMH) and anterior ANIMAL BEHAVIOUR, 63, 3
hypothalamus (AH) relative to naïve males motor and neural circuits that sustain mounting undergo Both areas have been implicated in the control of attrition sooner following androgen withdrawal. Finally, territorial and sexual behaviour in a number of species that this hierarchy was seen in both experienced and naïve males suggests that the hierarchy is not socially Because differences in metabolic capacity may reflectdifferences in baseline neural activity Acknowledgments
Research was funded by NSF DGE-9616181 (J.T.S.), ations in the AH and VMH represent an increased prim- Howard Hughes Medical Institute Fellowship (A.G.), ing to display agonistic and sexual behaviours. These Barry M. Goldwater Foundation Scholarship (A.G.) and increases in metabolic capacity, however, do not seem to NIMH 41770 (D.C.). Special thanks to Sam Field for be sufficient to produce an increased robustness to cas- his statistical advice and to Sarah Woolley, Eun-jin Yang, tration, and it is possible that increases in other nuclei Dr Judy Stamps and three anonymous referees for their such as the preoptic area and/or amygdala are necessary comments on the manuscript. The research presented here was evaluated and approved by the Institutional ences between gonadally intact experienced and naïve Animal Care and Use Committee of the University of males are due to experience effects on brain metabolism, Texas at Austin (Protocol No. 00083102).
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