Maternal care in a social lizard: links between female aggression and offspring fitness

ANIMAL BEHAVIOUR, 2008, 76, 1249e1257 doi:10.1016/j.anbehav.2008.06.009

Available online at www.sciencedirect.com

Maternal care in a social lizard: links between female aggression and offspring fitness D. L. SI NN , G. M . W HI LE & E. WA PST RA

School of Zoology, University of Tasmania (Received 23 March 2008; initial acceptance 7 May 2008; final acceptance 3 June 2008; published online 18 July 2008; MS. number: D-08-00198)

Infanticide is an important mortality factor for juveniles in a wide variety of taxa, and is thought to be an important influence on the evolution of pair bonding and parental care of offspring. Many parents, in response to conspecific infanticide, may alter their behavioural aggressiveness towards conspecifics in an adaptive manner to favour their offsprings’ fitness. Research on conspecific aggression as an infanticidal counter-strategy by parents, however, has largely focused on mammals and birds. Owing to the almost ubiquitous occurrence of altricial young/parental provisioning of offspring in these taxa, our ability to test comparative hypotheses regarding the initial evolution of parental care is limited. Recent evidence of highly variable social systems within a monophyletic social lizard clade (Egernia spp.) provides an opportunity to further our knowledge in this regard. We examined patterns of aggressiveness towards a conspecific model by females from a wild population of social lizards (White’s skink, Egernia whitii), while also documenting the first-year growth and survival of their offspring in the field. Female aggression increased during pregnancy and was maintained at a high level during postpartum periods, relative to aggressiveness during mating periods. We also observed consistent interindividual expression of aggressiveness in females, and offspring from more aggressive female behavioural phenotypes had higher rates of survival, but not growth, over their first year of life. These results suggest that relatively ‘simple’ forms of parental care (i.e. territoriality combined with kin tolerance) may favour offspring fitness and therefore parental care, without necessarily entailing the costs of full parental provisioning of offspring. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: behavioural phenotype; Egernia whitii; infanticide; maternal aggression; parental care; White’s skink

Infanticide is a significant source of juvenile mortality in more than 1300 animal taxa (Hrdy 1979). Several hypotheses suggest that infanticide could be an adaptive strategy for its perpetrators (see Ro¨del et al. 2008). For example, immigrating male lions, Panthera leo, often kill infants they have not fathered to speed up the return of females to sexual receptivity (Packer & Pusey 1983), and female rodents often kill other females’ offspring to gain food and nest resources, and to reduce future competition between their own and others’ young (Agrell et al. 1988). Although infanticide can be advantageous for perpetrators, it is obviously disadvantageous to the parents of killed offspring. Because of this, infanticide is

Correspondence: D. L. Sinn, School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania 7001, Australia (email: david.sinn@ utas.edu.au). 0003e 3472/08/$34.00/0

thought to have been a major selective force in the evolution of parental care, pair bonding (Agrell et al. 1988; Van Schaik & Kappeler 1997; Ebensperger 1998a) and female territoriality (Wolff & Peterson 1998). One mechanism by which parents can protect their offspring from the risk of infanticide is through active defence against intruders, such as increased aggressiveness towards conspecifics. The increase in aggressive behaviour in pregnant females, or females in the presence of their offspring, is referred to as maternal aggression (Archer 1988; Maestripieri 1992). In most mammalian species, maternal aggression increases during the middle to later stages of pregnancy or after parturition, reaching its peak at some point during lactation, and then declines as the progeny approach independence (Svare & Mann 1981; Svare 1990). While there is debate on the effectiveness of female aggression to protect against infanticide (Ebensperger 1998a, b), a marked increase in female

1249 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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aggressiveness during lactation in mammals is likely to have evolved in species whose offspring are especially at risk from conspecifics (Archer 1988; Clutton-Brock 1991). Indeed, direct protection of offspring through aggressive behaviour is likely to be more effective protection against conspecifics than against heterospecific predators, where large differences in body size and weaponry usually exist (Maestripieri 1992). Maternal care of offspring is common in most mammal and many bird species but rarer in reptiles (except for crocodiles, where maternal care is nearly ubiquitous: Shine 1988; Webb & Manolis 2002). For example, in the majority of lizards maternal care has been reported only to the extent of protection of eggs (Huang 2006) or assistance to emerge from vitellogenic membranes (Lanham & Bull 2000). In general, most lizards are highly precocial, and juveniles disperse soon after hatching/birth. However, recent research has begun to identify a number of reptile species in which longer-term associations between offspring and their parents occur (Jenssen et al. 1989; Halloy & Halloy 1997; Bull & Baghurst 1998). In particular, lizards within the Egernia genus display relatively complex sociality with considerable variation in social organization both between and within species, with at least 15 of the 29 currently recognized species living in extended ‘family’ groups (e.g. Stow et al. 2001; Chapple 2003; O’Connor & Shine 2003). The size of these family aggregations varies considerably both between and within species. Some taxa are solitary, some are found in small groups (pairs of adults or mothers with their offspring), and others occur in groups of up to 17 individuals (e.g. E. cunninghamii: Stow et al. 2001). Although the level of these parente offspring interactions varies substantially within the genus itself, and is substantially lower than in other vertebrate species (i.e. full parental provisioning), it nevertheless shows a greater level of parental care than previously reported in most lizard species. Parenteoffspring recognition in Egernia is common (Main & Bull 1996; Bull et al. 2001), and parents show relatively high levels of kin tolerance, with offspring maintaining long-term associations with parents within the natal home range. Although it has been suggested that offspring benefit from this association with parents through increased access to basking locations, foraging opportunities and retreat sites (Bull & Baghurst 1998; O’Connor & Shine 2004; Langkilde et al. 2007), the exact benefits of this association to juveniles have yet to be determined in wild populations. One likely benefit to offspring is increased protection from infanticidal conspecifics, since by both males and females infanticide has been observed in a number of Egernia species (Bartlett 1981; Lanham & Bull 2000; O’Connor & Shine 2004). However, little is known of potentially adaptive patterns of the behaviour of females (i.e. conspecific aggression) which may favour increased fitness of their offspring. We addressed this issue by examining conspecific aggression by females in a wild population of Egernia lizards. White’s skinks, Egernia whitii, live in small but stable social groups (Chapple & Keogh 2006; G. While, unpublished data). Males and females are both highly territorial, and are aggressive towards conspecifics outside

of pair bonds (biting, chasing) with fights potentially resulting in serious injury or death (Chapple 2003). Both sexes maintain territories year round, and form pair bonds within a males’ territory, which usually includes related offspring and subadults. Reproduction is annual, with mating occurring during the austral spring (Septembere October) and gestation spanning 3e4 months (Chapple 2003). Females in this population give birth to one to four offspring; most offspring disperse but one juvenile normally remains in the parental home range for up to 3 years (G. While, unpublished data). Specifically, we tested the hypothesis that female Egernia become more aggressive towards conspecifics after the birth of their offspring, and that increased aggression by females covaries positively with their offsprings’ fitness. We did so by examining individual consistency and mean-level patterns of aggression in female Egernia from a wild population throughout their reproductive cycle, including early mating periods, pregnancy and postpartum periods. We then combined our data on female aggressiveness with field-based data on offspring growth and survival over their first year of life. This allowed us to document the relationship between female aggression and several fitness-related traits in a natural population to identify putative adaptive behavioural patterns of parental care.

METHODS

Study Population White’s skink is a medium-sized (up to 100 mm snoute vent length, SVL) viviparous lizard found throughout a broad altitudinal (0e1600 m) and habitat (coastal heaths, grasslands and forests) range in southeastern Australia (Wilson & Swan 2003). We used E. whitii from a population on the east coast of Tasmania, Australia (42 570 S, 147 880 E). Individuals at the study site are found in a discrete patch of open grassland (200  200 m) in close association with excavated burrows or rock crevices, which they use as permanent retreat sites. Males and females are sexually monomorphic, become reproductively mature at approximately 3 years and have an overall life span of 9e10 years (Chapple 2003; While et al. 2007). Average birth dates for females in this population are variable across years, but occur during the latter half of the austral summer (Januaryemid February). To assess conspecific aggression, we captured adult female Egernia twice during their reproductive cycle in 2006e2007. Lizards were captured by attaching mealworms to the end of a fishing line and placing the mealworm in front of the lizard. After grabbing the mealworm, lizards were lifted into a collection bucket. The first capture occurred during the mating season (21 Septembere11 October). At this first collection all individuals were assayed for conspecific aggression, and then released within 3 days at their point of capture. The second capture was at the end of gestation (9 DecembereJanuary 24); females were again assayed for aggression. After this second collection period and behavioural assay, females remained in the laboratory until parturition (18

SINN ET AL.: MATERNAL CARE IN A SOCIAL LIZARD

Januarye16 February; mean birth date  SD ¼ 29 January  7.43 days). After parturition, all females that gave birth were once again assayed for conspecific aggression within 3 days of the birth of the final offspring (determined by oviduct palpation). Morphological measurements of females (total length, SVL 1 mm and mass 0.1 g) were taken at each collection period and immediately after parturition, and offspring mass and SVL were also taken prior to release of family groups at their mother’s point of capture after the second collection period (offspring sex was not determined as neonate female Egernia retain hemipenes, Chapple 2003). All subjects were toe-clipped, which allowed for unique identification of all individuals (see Ethical Note). Most females collected in DecembereJanuary were pregnant (73%), and completed parturition asynchronously over several days (While et al. 2007; While & Wapstra 2008). Seven females had one offspring, 16 produced two young and five had three young. We calculated relative clutch mass (RCM) for each female by dividing the total clutch mass by the postpartum maternal mass (Shine 1980). To assess the role of a female’s aggressiveness in the growth and survival of her offspring, we recaptured all surviving offspring over a 28-day period in 2007e2008 after their first overwinter period and repeated weight and length measurements. Male and female Egernia territories are based on protection of crevice sites, which are a key limiting resource (Chapple 2003). Therefore, we also determined whether offspring recruited to their mother’s territory by making multiple observations of juvenile crevice use in 2007e2008. This included 2e10 sightings for each offspring (average sighting per offspring  SD ¼ 3.50  2.29), and we considered a juvenile to have recruited to its mother’s territory if it was seen using a crevice site within its mother’s territory more than once in 2007e2008. Previous analyses of offspring space use have shown that offspring are extremely sitespecific in their first year after birth, with low levels of variation in space use (G. While, unpublished data). We considered offspring survival to be equivalent to recruitment into the population (either into their mother’s territory or elsewhere) after the year of release. Immigration of unmarked individuals into the site is low (since 2003, <10% of the population each season is represented by unmarked individuals, none of which are first-year juveniles: G. While, unpublished data), and the site is flanked on all sides by physical barriers (e.g. roads and unsuitable habitat), so estimates of offspring survival are unlikely to be compromised by high levels of dispersal out of the study site.

Conspecific Aggression Tests At each collection period female lizards were moved into temperature- and light-controlled rooms at the University of Tasmania, Hobart, Australia where they received behavioural assays (at 16  C; 14:10 h light:dark regime). Lizards were housed individually in rectangular plastic terraria (30  60 cm and 40 cm high), except for postpartum females, which were held with their offspring.

Terraria contained a basking rock and light at one end of the container, and a shelter at the opposite end of the container which was maintained at 15 cm from the closest edge of the basking rock. Food (mealworms) and water were available ad libitum. Home terraria were used for aggression tests; terraria had opaque sides that allowed for testing only one lizard at a time. All lizards received two conspecific aggression tests at each collection period given by a single experimenter (D.L.S.) on 2 test days, 24 and 48 h after collection. Behavioural tests were run in the afternoon between 1400 and 1700 hours so that lizards could obtain their preferred body temperature before each test (Stapley 2006), and test order was randomized among individual lizards on each test day. Conspecific aggression tests consisted of the experimenter approaching the front of the test container (i.e. the side nearest the basking rock), and touching the lizard with a realistic soft plasticine model of an E. whitii attached at the end of a fishing rod (model dimensions: head width: 15.7 mm; head depth: 12.3 mm; head length: 17.6 mm; SVL: 87 mm). Lizards were presented with the conspecific model after a 60 s acclimation to the presence of the observer, but only if they were found on and remained on the basking rock at the start of tests. Subjects were touched on the centre of the snout by the model up to 10 times, or until they fled into or on top of the shelter. Models were scented with Egernia urine and faeces collected from unrelated laboratory animals. During the first behavioural assays, we maintained distinct ‘male’ and ‘female’ models by using only one type of scent on two separate but otherwise physically similar models (both ‘male’ and ‘female’ scented models were within 0.3 mm for head width, body depth and SVL). Mean levels of conspecific aggression scores (see below) for females did not differ between the two ‘sex’ models (paired t test: t43 ¼ 1.27, P ¼ 0.21); therefore, subsequent behavioural tests used a single model scented with a mixture of both male and female scent. We assume that our tests measured a generalized response to a conspecific independent of the sex of the intruder. We used an act-frequency approach to measuring behaviours in aggression tests (Buss & Craik 1983; Sinn & Moltschaniwskyj 2005). Four behaviours were measured in tests: the number of touches required before the lizard fled; the number of back arches (a display whereby the spine of the lizard was bent to form a concave arch); the number of times the lizard displayed with an open mouth; and the number of times the subject actively bit the model. Behaviours in tests were recorded for the entire duration of stimulus presentation (i.e. the number of touches) with an audio cassette recorder and hand-held timer. Behaviour was scored as a multiple frequency if the lizard performed the behaviour anew after each touch with the model. Conspecific aggression tests given to postpartum females were identical to those described above, except that they were given only once and offspring were also present in small clear plastic containers (10 cm diameter) underneath their mother’s shelter. We gave conspecific tests only once to postpartum females because the four observed variables were highly correlated in the two tests

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given within each week during the first and second collection periods (all within-week Spearman rank correlations for each of the four variables were >0.4 and significant at P < 0.01; 8 comparisons, 4 at each collection period). The behaviours assessed within conspecific tests were highly intercorrelated and loaded strongly on a single common component in principal components analyses at each collection period (Table 1). Therefore, to reduce the number of variables used in subsequent analyses and to facilitate use of a reliable single score (e.g. Buss & Craik 1983), we computed aggregate scale scores (Tabachnick & Fidell 1996). Scale scores were computed by summing the normalized observed variables ‘number of touches’, ‘number of back arches’, ‘number of mouth opens’ and ‘number of bites’. Since observed behaviours were taken twice for October and December collection periods, but only once for postpartum testing, we first halved October and December collection scores and then normalized observed variables according to the grand mean of all three sample periods. This method allowed each observable behaviour to contribute equally to each period’s aggression scale score, and also allowed for scores to vary mathematically in mean and variance. At all times, higher scores represent more aggressive overall responses. For example, high scores indicate animals that acted aggressively towards conspecific models, by actively displaying towards models (mouth open and back arch), biting models and requiring more touches before fleeing. Conversely, lower scores represent individuals that were relatively less aggressive, and fled after fewer ‘strikes’ with the model while not displaying aggressively towards it. Aggression scores were rightskewed, therefore log-transformed scores or nonparametric tests were used for any statistical tests with assumptions of univariate normality. Average sprint speed as a measure of physical performance was assessed after each behavioural assay by using a race track 2 m long and 5 cm wide with five infrared sensors at 50 cm intervals. Average sprint speeds were highly repeatable for individual females between the first and second collection period (two-way mixed-model intraclass correlation coefficient: r ¼ 0.81, F23,23 ¼ 5.29, P < 0.001) and also between October collections and after giving birth (r ¼ 0.62, F23,23 ¼ 2.66, P < 0.01).

Data Analysis To examine mean-level patterns of female aggression we used repeated-measures ANOVA on log-transformed

aggression scores, with collection period as a withinindividual factor (three levels: mating season, pregnancy and postpartum scores). We characterized the level of phenotypic consistency in female aggression scores across these same three periods with a two-way mixed-model intraclass correlation coefficient (McGraw & Wong 1996; hereafter referred to as ‘repeatability’: Boake 1989). Of the 37 female lizards caught in DecembereJanuary, 28 were repeat individuals from SeptembereOctober, and thus an N of 28 was used to calculate repeatability from early mating periods to gestation. Twenty-seven females collected in DecembereJanuary were given postpartum tests and therefore contributed to repeatability analysis from gestation to postpartum periods. Nineteen females were repeat females across all three tests, and were the only individuals to contribute to the mean-level repeated-measures model. We calculated Spearman rank correlations between average sprint speed scores and aggression scores at October and December 2006 collections, to test whether lizard response to the conspecific model was altered by a female’s performance ability. Spearman rank correlations between female SVL and aggression scores during October 2006 collections were used to determine whether aggressiveness was influenced by differences in size between individual lizards. Since we also used the same sizestandardized model, this analysis also provided information on whether aggressiveness was relative to size differences between the subject female and our standardized lizard model. We tested whether aggressiveness was due to habituation to laboratory conditions by correlating postpartum female aggression scores with the number of days a female spent in captivity in 2006e2007, with day 1 for each female starting from when she was brought into the laboratory during the DecembereJanuary collection period. We used four analyses to characterize the potential for selection on female conspecific aggression. First, we tested whether female lizards adjusted their level of aggression according to their clutch size (one, two or three offspring) in 2006e2007 with a one-way KruskaleWallis test. Second, we calculated the Spearman rank correlation between female aggression and overall reproductive effort (RCM) in 2006e2007. Third, we assessed the influence of female aggressiveness on offsprings’ first-year growth in the wild by using a general linear model (GLM) with the PROC GLM procedure in SAS STAT version. 9.2 (SAS Institute Inc., Cary, NC, U.S.A.). Offspring SVL at time of capture in 2007e2008 was entered as the dependent variable, with SVL at birth, capture date in 2007e2008,

Table 1. Loadings on a single principal component of discrete behaviours observed in White’s skink, Egernia whitii during conspecific aggression tests early in the mating season, in the third trimester of female pregnancy and 72 h postpartum Behaviour Number of touches Number of back arches Number of mouth opens Number of bites Variance explained (%) No. of females

Mating season OctobereSeptember

Pregnancy DecembereJanuary

Postpartum care

0.89 0.84 0.81 0.63 64.1 37

0.92 0.90 0.81 0.70 70.4 37

0.86 0.87 0.81 0.76 68.7 27

SINN ET AL.: MATERNAL CARE IN A SOCIAL LIZARD

Ethical Note Collection of lizards and experimental methods were approved by the University of Tasmania Animal Ethics Committee and the Tasmanian Department of Primary Industries and Water. Toes were removed with surgicalgrade iris scissors that were disinfected before and after each foot/lizard. Full toes were removed, since partial natural digit loss is common in this species, similar to other skinks (Hudson 1996). Toe clipping of lizards involved clipping only one toe per foot and no visual signs of distress were observed during the procedure. Blood loss during toe clipping was either nonexistent or minimal and ceased within 2e3 s. Physiological stress responses (i.e. corticosterone) to toe clipping are several degrees of magnitude lower than stress responses to microchip implants in lizards, and are no different from those induced by handling during size measurements (Langkilde & Shine 2006). We did not observe any adverse effects on the lizards from biting the model lizard, which was soft and ‘gave way’ when bitten. RESULTS There were significant mean-level changes in female aggression during the reproductive cycle (repeated-measures

ANOVA: F2,36 ¼ 6.91, P < 0.01; Fig. 1). Specifically, female aggression scores increased almost two-fold from early mating periods to pregnancy (F1,18 ¼ 10.14, P < 0.01), and were maintained, but did not increase, during postpartum care (F1,18 ¼ 0.08, P ¼ 0.78). Within this overall mean-level increase, however, there was significant repeatability in individual female aggression scores from early mating periods to gestation (r ¼ 0.58, F27,27 ¼ 2.37, P < 0.05) and from gestation to postpartum care (r ¼ 0.93, F26,26 ¼ 14.96, P < 0.001). Thus, while females in general increased their aggression over time, relative rank order aggressiveness among females was maintained (e.g. some females were consistently more aggressive than others). There was no relationship between a female’s aggression and her sprinting ability (early mating: rS ¼ 0.15, N ¼ 37, P ¼ 0.36; pregnancy: rS ¼ 0.27, N ¼ 35, P ¼ 0.12), nor between aggression and overall size (early mating: rS ¼ 0.31, N ¼ 26, P ¼ 0.13; pregnancy: rS ¼ 0.04, N ¼ 32, P ¼ 0.81; postpartum: rS ¼ 0.03, N ¼ 28, P ¼ 0.87). Importantly, female aggression was not influenced by habituation to laboratory conditions, as postpartum aggression scores were not correlated with the period of time a female spent in captivity (range 7e30 days: rS ¼ 0.11, N ¼ 28, P ¼ 0.58). Consequently, we concluded that our conspecific aggression scores measured an individual females’ inherent aggressiveness, independent of her performance ability, size or habituation to laboratory conditions. There was no relationship between a female’s aggressiveness and her relative reproductive output (RCM: all Spearman rank correlations for RCM and the three aggression scores were small and nonsignificant at P > 0.05). There were also no differences in postpartum conspecific aggression scores between females that gave birth to one, two or three offspring (KruskaleWallis test, two-tailed: c22 ¼ 0.961, P ¼ 0.62). A GLM including SVL at birth, capture date, date of birth, female aggression and presence/absence of offspring within a mother’s home range explained over half the variation (R2 ¼ 0.53) in offspring growth in our data; however, this model failed

0.8 0.7 0.6 Log aggression

date of birth, female log-transformed aggression score, presence/absence of offspring within their mother’s home range, and the interaction between log female aggression scores and presence/absence of offspring within their mother’s home range as independent variables (N ¼ 19). Owing to the large number of explanatory factors relative to our sample size in this model, we used a backward elimination technique on the two-way interaction in this model at P < 0.25 (Quinn & Keough 2002). Reptile growth is strongly influenced by date of birth (e.g. Warner & Shine 2005, 2007) and we predicted that if females were providing indirect benefits to their young then offspring growth may also be strongly influenced by offspring presence in their mother’s home range (and the two-way interaction with female aggressiveness). Fourth, we assessed the effect of a female’s aggressiveness in Decembere January 2006e2007 on the proportion of her clutch that survived into their second year in the field by using a generalized linear model using the PROC GENMOD procedure in SAS STAT version 9.2, with a binomial distribution and a logit link function (Littell et al. 2002). The number of offspring in a female’s clutch that recruited to the following postwinter activity season divided by her clutch size was entered as the dependent variable, with average offspring mass at birth, female aggression score and date of birth as explanatory variables (N ¼ 27). For the growth and survival models, we used a female’s aggression score from October collections only, to maximize statistical power. Female aggression scores were highly correlated across all reproductive periods (see Results). Growth and survival models were checked for both statistical outliers and normality of residuals, and no violations were found.

0.5 0.4 0.3 0.2 0.1 0

Prefertilization

Pregnancy

Postpartum

Female reproductive stage Figure 1. Mean-level female aggression in Egernia whitii throughout the reproductive cycle (N ¼ 19). Mean-level patterns are presented for only those females that completed all three behavioural assays (prefertilization, during pregnancy and during postpartum care). Error bars represent SEs.

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to reach statistical significance (F5,13 ¼ 2.88, P ¼ 0.06). Although offspring SVL at birth (F1,18 ¼ 4.32, P ¼ 0.06) and birth date (F1,18 ¼ 4.47, P ¼ 0.05) were related to offspring growth (larger offspring and those born earlier tended to grow faster), we did not detect any direct relationship between a female’s aggressive phenotype and her offspring’s growth (F1,18 ¼ 0.46, P ¼ 0.51). Furthermore, there was no interaction between a female’s aggressive phenotype and offspring presence within her home range on subsequent offspring growth (F1,18 ¼ 0.19, P ¼ 0.67). Instead, we detected a significant positive influence of a female’s aggression on the survival characteristics of her clutch independent of offspring size or birth date (Table 2). Specifically, the odds of a female’s proportional clutch survival increased 1.39 times with a 1 unit increase in female aggressiveness (lower 95% confidence interval, CI ¼ 1.05 times, upper 95% CI ¼ 1.84 times). Neither birth date nor average offspring mass explained significant variation in clutch survival (Table 2).

DISCUSSION To demonstrate maternal care for offspring clearly, we need to show that females significantly alter their behaviour in the presence of their offspring in such a way that benefits their young (O’Connor & Shine 2004). Our study is one of the first to demonstrate a potentially adaptive behavioural pattern of maternal care in a natural population of lizards. Previous hypotheses on the evolution of maternal care predict that an overall behavioural response by females (i.e. increased aggressiveness) could favour offspring fitness in one of two ways: either indirectly through territory protection, which decreases conspecific harassment overall and therefore increases offspring survival or opportunities to bask and feed (i.e. territory defence hypothesis: Paul et al. 1980; Maestripieri 1992), or by direct protection of young from infanticidal conspecifics (i.e. pup protection hypothesis: Paul 1986; Maestripieri 1992). Overall, our data suggest that females increased their aggressiveness during their reproductive cycle, and this increased aggressiveness resulted in increased rates of survival but not growth in offspring. We also detected significant and consistent phenotypic variation between individual females in their inherent aggressiveness, suggesting that even with apparent directional selection on female aggressiveness, withinpopulation variation in aggressiveness is currently being maintained, instead of eroded. Thus, it appears that while a single overall reproductive strategy at the level of female type (i.e. all females increase aggressiveness through pregnancy) is currently being favoured by selection (i.e. Table 2. Generalized linear model of a female’s aggressive phenotype on her offspring’s subsequent first-year survival (N ¼ 27) Source Birth date Average offspring mass Female aggression

Estimate

c21

P

0.06 3.50 0.33

1.57 1.35 5.82

0.21 0.24 0.02

strategy optimization: Shine 1988; Huang 2006), a single aggression strategy at the level of individual females has not (i.e. not all females are highly aggressive). Below, we discuss these results in the light of current knowledge of adaptive patterns of parental care and consistent individual differences in aggression in animals. Female lizards in our study were more aggressive towards conspecifics during postpartum periods relative to their levels of aggressiveness during the mating season; however, the timing of this increase in aggression occurred during gestation and was then maintained through postpartum periods. While this behavioural adjustment could be interpreted as ‘parental care’ (e.g. Graves 1989; Greene et al. 2002), increased aggressiveness did not appear to be directly related to the presence of young. This fits well with what we know from other Egernia systems and closely related lizard taxa, where the mechanism of parental protection is indirect. For example, in black rock skinks, E. saxatilis, females are less aggressive to their kin than they are to unrelated offspring, but do not behave differently towards adult conspecifics depending on their kins’ presence (O’Connor & Shine 2004). Similarly, female sleepy lizards, Tiliqua rugosa, show little close contact with their offspring after birth, despite a strong overlap between juvenile and mothers’ home ranges over extended periods of time (Bull & Baghurst 1998). Further evidence that female aggressiveness was not directly related to the presence of offspring was the fact that females did not adjust their aggressiveness levels according to their clutch size or relative clutch mass (an essential feature of the pup protection hypothesis: Ebensperger 1998a, b). However, given that E. whitii lives in long-term stable family groups (Chapple & Keogh 2006), we should expect selection to occur on parental behaviours that would benefit their offspring in such a way as to increase offspring fitness. One key benefit of parental care for offspring could be increased growth, if juveniles received less conspecific harassment or increased basking opportunities (and therefore more opportunity to feed) because of increased aggression by their mothers (e.g. Clutton-Brock 1991). Indeed, in controlled laboratory conditions, Egernia offspring from more aggressive parents tended to bask more often than those from less aggressive ones (O’Connor & Shine 2004). However, despite this clear reasoning and appropriate behavioural response by females witnessed in our study, we were unable to detect strong relationships between a female’s level of aggression and her subsequent offsprings’ growth, even for those offspring that lived within their mother’s territory. Instead, offspring growth was primarily a result of birth date and size at birth; this is a common pattern found in many squamate lizard growth studies (Niewiarowski 2001; Warner & Shine 2005, 2007). Therefore, while indirect benefits such as increased growth for offspring are a plausible result of increased female aggression (e.g. O’Connor & Shine 2004), our data suggest that, in the wild, other factors such as size at birth, birth date, temperature and food availability are likely to be more important determinants of offspring growth than their mother’s aggressive phenotype, even within habitats saturated by

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aggressive conspecifics as seen in many Egernia species (O’Connor & Shine 2003). An alternative key benefit of parental care could be increased survival of offspring, if female aggression increases protection from infanticidal conspecifics (O’Connor & Shine 2004; Langkilde et al. 2007). Our data provide support for this protection hypothesis, as small increases in female aggressiveness almost doubled the odds of clutch survival into its first year. Many Egernia species, including E. whitii, are infanticidal (G. While, personal observation; Lanham & Bull 2000; O’Connor & Shine 2004), and mortality rates for juveniles over their first year are high (Chapple 2003, 2005). Thus, a plausible explanation for the positive influence of female aggressiveness on offspring survival would be that more aggressive females are more successful at fending off attacks from male or female conspecifics, therefore increasing the survival of their kin. Physical parental protection from infanticidal conspecifics fits well with what we know from this and other Egernia species. In this same population of Egernia, females maintain territories year round, and female aggression is not related to home range size during the mating season (G. While, D.L. Sinn & E. Wapstra, unpublished data); increased female aggression therefore is probably not related to expanding or maintaining territory boundaries. In a different species of Egernia (E. saxatilis), Langkilde et al. (2007) found that within a single season, philopatric juveniles did not necessarily obtain better habitat, in terms of crevice size, sun exposure and vegetation cover, than juveniles that dispersed. In both cases, a lack of apparent functionality for aggressiveness outside of parental care and a lack of advantage for offspring recruited to mothers’ territories via habitat characteristics support the idea that philopatric offspring may gain survival benefits from close proximity with their tolerant mothers that show aggression towards conspecifics, outside of any indirect territory protection by females in Egernia lizards. Of course, there are alternative explanations for the positive directional influence of female aggression on offspring survival. For example, an offspring’s aggressive phenotype should also influence its survival. If we assume that aggression is to some extent heritable (Bakker 1986; Sinn et al. 2006), then more aggressive females could have given birth to more aggressive offspring, and more aggressive juveniles could have enjoyed higher survival rates in 2007e2008 at our study site for reasons unidentified here, but possibilities include increased competitive abilities or ability to repel threatening conspecifics. The key point here is that selection on aggression in parents and offspring may be uncoupled, so the positive relationship between female aggressiveness and offspring survival could have arisen if behaviours were heritable and more aggressive juveniles were favoured during our field season of measurement. Clearly, given the documented behavioural patterns in females seen here, we believe the more parsimonious explanation is that offspring from more aggressive mothers were less likely to die from infanticidal conspecifics. However, further understanding of parental care in Egernia should be significantly enhanced by understanding interactions between offsprings’ and mothers’

heritable behavioural phenotypes (e.g. Le Galliard et al. 2003; Cote et al. 2007). Long-term data collection on mothers’ and their offsprings’ aggressive phenotypes is currently underway in this system. The variation in and repeatability of female aggressiveness coupled with the clear positive relationship between female aggressiveness and offspring survival begs the question why distinct female aggressive phenotypes are maintained throughout reproduction. Several evolutionary mechanisms could account for this variation. For example, trade-offs are a key component of evolutionary thought (Roff & Fairbairn 2007). In the present example, increased aggressiveness during parental care may also mean that these females are also more aggressive in other functional contexts, such as mating or general activity levels, thus increasing their risk of injury, exposure to predators and energy expenditure (Huntingford & Turner 1987; Marler & Moore 1988; Shine 1988; but see Huang 2007). Indeed, in some fish, individuals that are most aggressive towards conspecifics are also the boldest in predator inspection trials (Huntingford 1976; Bell 2005). Thus, although increased aggressiveness may increase the probability of offspring survival, there are potential costs to increases in this behavioural trait (Agrell et al. 1988). It may also be that the relationship between female aggression and offspring survival is not stable through time; instead, depending on changing environmental conditions (such as conspecific densities or fluctuating sex ratios, Le Galliard et al. 2005), greater levels of maternal aggression may or may not favour offspring survival. Fluctuating selection based on food availability has been shown to maintain variation in behavioural phenotypes in other systems (e.g. Dingemanse et al. 2004; Boon et al. 2007). Empirical evidence supporting these explanations for the maintenance of consistent behavioural phenotypes remains largely unexplored in Egernia and other animal systems (Maynard Smith & Harper 1988; Wolf et al. 2007). Understanding the processes by which selection maintains variation in female aggressiveness should contribute to our knowledge of evolutionary mechanisms resulting in direct provisioning and care of offspring. It is becoming increasingly clear that many lizards in the genus Egernia show complex patterns of sociality, including patterns of maternal care (this study; O’Connor & Shine 2004). Given this within-clade variation in sociality and their monophyletic status, the Egernia lineage should be especially useful for understanding key evolutionary transitions in the evolution (and loss) of parental care (O’Connor & Shine 2004). The evolution of parental care in reptilian taxa could have arisen through a series of intermediate evolutionary steps, ranging from no parental care to tolerance of kin and to full offspring recognition and protection, all as an evolutionary by-product of group living in saturated habitats (Chapple 2003). One such intermediate step may have involved an increase in maternal care of offspring, providing indirect or direct protection from threatening conspecifics or potential predators (Shine 1988). Our results are most parsimonious with the idea that maternal care in Egernia lizards functions to protect their offspring, and not necessarily to provide other indirect benefits such as better growth

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environments. Increases in maternal aggression during reproduction may enable kin to gain survival benefits from close physical proximity with tolerant mothers, outside of any direct parental provisioning or even protection of kin per se. Understanding behavioural processes that result in successful maternal care of offspring is likely to yield further insights into the proximate mechanisms responsible for ultimate patterns of parental care across many phylogenetically distinct taxa.

Acknowledgments The School of Zoology at UTAS provided financial assistance to enable laboratory work and preparation of the manuscript. Tobias Uller provided helpful suggestions regarding data analysis and interpretation, and two anonymous referees provided additional advice on the manuscript. This work was also partially funded by the Holsworth Wildlife Research Fund, the Environmental Futures Network and the Association for the Study of Animal Behaviour (to G.W.). References ¨ nen, H. 1988. Counter-strategies to Agrell, J., Wolff, J. O. & Ylo infanticide in mammals: costs and consequences. Oikos, 83, 507e517. Archer, J. 1988. The Behavioural Biology of Aggression. Cambridge: Cambridge University Press. Bakker, T. C. M. 1986. Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study. Behaviour, 98, 1e144. Bartlett, R. D. 1981. Notes on Egernia cunninghami kreffti, an Australian skink. British Herpetological Society Bulletin, 4, 36e37. Bell, A. M. 2005. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). Journal of Evolutionary Biology, 18, 464e473. Boake, C. R. B. 1989. Repeatability: its role in evolutionary studies of mating behavior. Evolutionary Ecology, 3, 173e182. Boon, A. K., Re´ale, D. & Boutin, S. 2007. The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecology Letters, 10, 1094e1104. Bull, C. M. & Baghurst, B. C. 1998. Home range overlap of mothers and their offspring in the sleepy lizard, Tiliqua rugosa. Behavioral Ecology and Sociobiology, 42, 357e362. Bull, C. M., Griffin, C. L., Bonnet, M., Gardner, M. G. & Cooper, S. J. B. 2001. Discrimination between related and unrelated individuals in the Australian lizard Egernia striolata. Behavioral Ecology and Sociobiology, 50, 173e179. Buss, D. M. & Craik, K. H. 1983. The act frequency approach to personality. Psychological Review, 90, 105e126. Chapple, D. G. 2003. Ecology, life-history, and behavior in the Australian scincid genus Egernia, with comments on the evolution of complex sociality in lizards. Herpetological Monographs, 17, 145e180. Chapple, D. G. 2005. Life history and reproductive ecology of White’s skink, Egernia whitii. Australian Journal of Zoology, 53, 353e360. Chapple, D. G. & Keogh, J. S. 2006. Group structure and stability in social aggregations of White’s skink, Egernia whitii. Ethology, 112, 247e257. Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton, New Jersey: Princeton University Press.

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