Behavioral Ecology Advance Access originally published online on December 22, 2005
Behavioral Ecology 2006 17(2):206-211; doi:10.1093/beheco/arj019
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Kin discrimination in the social lizard Egernia saxatilis (Scincidae)
School of Biological Sciences A08, University of Sydney, New South Wales 2006, Australia
Address correspondence to R. Shine. E-mail: rics{at}bio.usyd.edu.au.
Received 24 August 2004; revised 29 April 2005; accepted 2 November 2005.
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ABSTRACT |
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The ability to discriminate kin from nonkin is critical for the evolution of kin-based sociality. Black rock skinks, Egernia saxatilis, are viviparous lizards that typically live in "nuclear families" consisting of an adult male, adult female, and one or more cohorts of juveniles. Laboratory trials showed that juvenile lizards can discriminate between the scent of adults from their own social group versus that of unfamiliar adults. Experiments in which we translocated individuals among family groups revealed that this discriminatory ability was based on familiarity with other individuals rather than genetic relatedness. For example, neither "fostered" juveniles nor their mothers displayed any scent-based kin discrimination when brought together after 2 months' separation. Thus, unlike the closely related (and also social) Egernia striolata, black rock skinks base kin discrimination on familiarity rather than genotypic similarity.
Key words: kin discrimination, Scincidae, sociality.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Kin recognition (the neural processes involved in the classification of kin) and subsequent kin discrimination (differences in behavioral responses toward kin vs. nonkin: Tang-Martinez, 2001
) are essential components of the evolution of "social" behavior (Komdeur and Hatchwell, 1999). If animals have long-term relationships with other specific individuals (e.g., as members of the same social group), we expect selection to favor the ability to quickly and reliably discriminate these familiar individuals from other conspecifics. Indeed, it is difficult to envisage the evolution of family groups, for example, in the absence of such discriminatory ability. The ability of an individual animal to identify genetically related conspecifics and alter its behavior based on this recognition has been documented among an extraordinarily diverse array of animals (e.g., both social, Panek and Gamboa, 2000, and nonsocial insects, Agarwala and Dixon, 1993; Faraji et al., 2000; fish, Arnold, 2000; Fitzgerald and Morrissette, 1992; lizards, Bull et al., 2001; Lena and De Fraipont, 1998; mammals, Heth et al., 1998; Mateo and Johnston, 2000; birds, Shorey et al., 1999; and amphibians, Masters and Forester, 1995; Pfennig et al., 1993).
Two main mechanisms have been proposed as to how individuals determine whether or not conspecifics are related to them. "Recognition by association" occurs when an animal learns the individually distinctive signals of familiar animals around it and treats these as kin, whereas "phenotype matching" is the use of a reference phenotype (either self or kin) against which other individuals are judged (Halpin, 1991). Recognition by association thereby requires individuals to have a period of association with one another before being recognized as kin. Phenotype matching, on the other hand, requires no such period of prior association, with the relatedness of newly encountered individuals being assessed based on how similar they are to the reference phenotype. Further research is required to determine the relative frequencies of phenotype matching versus recognition by association and the situations where each occurs (for further discussion of this issue, see Tang-Martinez, 2001; Todrank and Heth, 2001). The ability of individuals to recognize kin of varying relatedness is also expected to vary in different social systems (Pusey and Wolf, 1996), as is the recognition mechanism utilized.
The most robust tests of any theory are provided by comparing results across as wide a range of taxonomic groups as is possible. While there is increasing evidence of the presence of kin recognition mechanisms in reptiles, amphibians, and fish, studies on these taxa to date generally have interpreted this behavior as either a mechanism to avoid eating relatives in cannibalistic species (e.g., Gabor, 1996; Pfennig et al., 1993) or a mechanism to facilitate kin-based aggregation (e.g., Arnold, 2000). Due to the perceived lack of suitable study organisms, previous research on kin discrimination mechanisms in social vertebrates has concentrated on birds and mammals. There have been relatively few studies in other vertebrate taxa examining whether recognition by association or phenotype matching is used in the respective kin discrimination systems. However, recent research has documented a remarkable range of social systems within reptiles (see Clark, 2004; Greene et al., 2002; O'Connor and Shine, 2004) and amphibians (e.g., Gibbons et al., 2003). Reptiles, in particular, offer substantial benefits as study organisms in this field. They are generally easier to catch, house, and use in experiments than mammals and birds. Additionally, the juveniles of almost all mammal and bird species live with their parents when young. Such systems do not allow us to address the more fundamental issue of the evolution of family groups: why did juveniles "originally" start living with their parents? Australian lizards in the Mabuya skink lineage are of particular interest in this regard. At least half of the 29 species within the genus Egernia show some form of sociality, ranging from mother-offspring associations and short-term pairing by adults to large, long-term, extended family groups (Cogger, 2000; Gardner, 2000; Gardner et al., 2001).
If the type of social system affects mechanisms of kin discrimination, then we would expect to see variation in such mechanisms within Egernia. Although kin discrimination in this lineage has so far attracted little scientific attention, there is already evidence of variation in discrimination mechanisms. Vomeronasal cues are used by female sleepy lizards (Tiliqua rugosa) and gidgee skinks (Egernia stokesii) to recognize their own offspring, albeit possibly based on familiarity rather than genetic cues (Bull et al., 1994; Main and Bull, 1996). In contrast, juvenile tree skinks (Egernia striolata) discriminate between individuals using phenotypic similarity, not familiarity (Bull et al., 2001). By comparing the recognition mechanisms of closely related species with different social systems (as occurs within the Egernia lineage), we can begin to identify the selective forces involved in the evolution of these discrimination systems.
We examined kin recognition in the social lizard Egernia saxatilis to determine if kin discrimination was present in this species and, if so, whether discrimination was due to prior association or phenotype matching. To answer these questions we conducted the following trials. (1) Do mothers and juveniles recognize each other's scent? We tested whether juveniles and mothers could discriminate between the scent of their parent/offspring versus scent from an unrelated animal. (2) Is parent-offspring discrimination driven by familiarity or genetic similarity? On finding that juveniles raised with their mothers could discriminate between her scent and that of unrelated females, we tested whether this ability was based on recognition of genetically similar animals or a learned response to familiar individuals.
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METHODS |
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Study species
E. saxatilis is a medium-sized viviparous skink (up to 130-mm snout-vent length [SVL]) that inhabits rocky outcrops throughout southeastern Australia (Cogger, 2000
). It lives in groups, with the degree of sociality ranging from solitary animals to large aggregations (up to 13 individuals, including offspring from several cohorts), but it is most commonly found in small territorial "nuclear family" groups (one adult male, one adult female, and their current year's offspring: O'Connor and Shine, 2003). One to four offspring (mean 2.5) are born in late February/early March (unpublished data).
In January 2001, we hand captured 27 adult female E. saxatilis thought to be gravid (based on body mass) and an additional 14 males found with them. All animals were collected from Kanangra-Boyd National Park, Blue Mountains, New South Wales (150°0'11''E, 33°3'29''S for more details, see O'Connor and Shine, 2003), brought into the laboratory, and housed in the same groups in which they had been captured. At the completion of observations, all animals were released at their point of capture. Where a family group had been brought into captivity, all group members were released together. Animals were held in captivity for 3–4 months. Based on mass relative to SVL, at the time of their release all animals were in as good, or better, condition as animals in the wild. The sex of juveniles was not determined for this study as it is difficult to do so at such a young age and risks possible injury to the juvenile.
Experimental procedures
While in captivity, all lizards were housed in plastic nally bins (40 cm wide x 62 cm long x 40 cm high), each heated by a 60-W bulb suspended in the center of, and 10 cm above, the bin floor in a temperature-controlled room set at 25°C. Heat lamps came on daily at 0900 h and went off at 1700 h. A constant supply of water was available in the bins, and the lizards were fed three times a week (crickets, cat food, or cockroaches with Rep-Cal calcium and Herptivite dietary supplements added). Gravid females were housed in identical conditions to other lizards, and on giving birth all juveniles remained in their parents' enclosures (except for those used in the "adoption" experiment—see below).
To allow animals to attain their preferred body temperatures before trials commenced, recognition experiments were run in the afternoon between 1200 and 1600 h. Trials were run in containers identical to those used to house the lizards, in rooms also set at 25°C. In the center of each bin, a basking area was formed by placing a terracotta tile (20 x 20 x 1 cm) on the floor with a heat lamp suspended 10 cm above it. A single test animal was placed in each bin and allowed 10 min to settle down. During this period, scents were obtained from the two scent source animals by running a 2-cm-long cotton wool bud six times along their dorsal surface and six times across their ventral surface (avoiding the cloacal area). These buds, one from a familiar/related animal and one from an unrelated unfamiliar animal, were then placed on the tile, in the middle of the opposite edges of the tile. The buds were held in place using small balls of adhesive (Blutak).
All trials were videotaped for 15 min using an overhead camera. Scoring commenced when a lizard first encountered one of the buds and continued for 10 min. If a lizard did not encounter one of the buds within 5 min, we scored the last 10 min of the trial. Pilot studies indicated that 10 min provided enough time for multiple investigations of each scent source. Scent stimuli were randomly allocated with respect to side on the tile, and the scorer was unaware of which stimulus was in which position. If an animal did not "visit" both scent stimuli during the scoring period, the trial was excluded from analysis (because no comparison of response intensity was possible). Likewise, trials were excluded if the animal moved a cotton bud out of the field of view of the camera (by knocking the bud over or carrying it away).
Individuals were used a maximum of twice in trials as the focal animal. For example, a juvenile that had been "fostered out" was used in a trial to determine if it could determine the scent of its genetic mother and again in a trial to see if it could recognize the scent of its foster mother. Similarly, the scent of that juvenile was used in trials with the two adults as focal animals. In such cases, at least 48 h lapsed between successive trials using the same individual (either as a scent source or as a focal animal). All treatments were run in random order. Equipment was washed with 70% alcohol between experiments.
A visit to a scent occurred when the test animal's head was within 2 cm of the cotton bud. For each visit, we scored:
- Time—time spent with neck or head within 2 cm of the bud;
- Tongue flicks—number of times the tongue was flicked in and out within 2 cm of the scent; and
- Bites—cotton bud taken into the mouth.
Do mothers and juveniles recognize each other's scent?
We tested to see if juveniles responded more to the scent of their mothers than to the scent of an unrelated female and tested maternal recognition of offspring scent in a similar fashion. Because unfamiliar animals are also likely to be genetically dissimilar, it is possible that any discrimination in these trials confounds genetic similarity with familiarity. This confounding effect is dealt with in the cross-fostering experiment below.
Is parent-offspring discrimination driven by familiarity or genetic similarity?
As juvenile-mother dyads (above) had had up to 2 months to form bonds and learn to recognize each other, we also conducted a second set of trials where juveniles and mothers were separated within 24 h of birth—the "fostering" manipulation. In this experiment, when two females gave birth to two or more juveniles within a day of each other, then one of the juveniles from each female was reciprocally cross-fostered. This manipulation left these females with one (or more) offspring of their own plus one from another female. If a third offspring was present or no other females gave birth within a day, then one juvenile was placed in a "kindergarten" with other juveniles but no adults. This procedure provided four categories of scents:
- Related familiar—own offspring "living with mother";
- Related unfamiliar—own offspring fostered out (to either another female or the kindergarten);
- Unrelated familiar—unrelated offspring "fostered in"; and
- Unrelated unfamiliar—unrelated offspring housed elsewhere (control).
As the aim of this experiment was to test whether discrimination was via phenotype matching or recognition by association, we cross-fostered offspring to females that had been collected from different outcrops. It is unlikely that any of the foster families were genetically similar to the juveniles that we fostered to them. Thus, if juveniles (and mothers) show similar levels of response to familiar relatives (living with mother treatment) as they do to familiar foster animals (fostered in) and no difference in response to an unfamiliar but related individual (fostered out treatment) as compared to the control lizards (unfamiliar, unrelated), then phenotype matching cannot be invoked as a basis for any observed kin discrimination.
At the same time as the fostering experiment, we had 11 juveniles living in captivity with both parents. These were included in the above trials as living with mother. We also used these juveniles to test kin discrimination by, and of, adult males in the group.
Both diet and local environment can influence an individual's scent (Schellinck et al., 1997). To remove these possible confounding influences, all animals were housed in the same environment and fed the same food for 2–3 months prior to the experiments.
All animals were released at their original point of capture on completion of the trials. Where juveniles had been fostered out, these were released adjacent to their mother's original point of capture (at the same time as their mother was released nearby), thus maintaining the genetic substructuring of the population while reducing the possibility of parental aggression toward unfamiliar offspring.
Statistical analysis
Data were nonnormally distributed and thus were analyzed nonparametrically. Analyses were corrected for ties and run in Systat 9.0 (SPSS, 1998) or Statview 5.0 (SAS Institute, 1998).
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RESULTS |
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Do juveniles discriminate between scent of their mothers versus scent from unrelated females?
Combining the "related familiar" and "related unfamiliar" treatments, we found no indication that offspring discriminated between their own mother's scent and that of an unrelated female (Wilcoxon signed-rank: n = 34, all nonsignificant; Figure 1). This result was not affected by whether or not the juvenile was living with its mother.
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Do juveniles discriminate between scent from familiar females versus that from unfamiliar females?
Testing offspring that were familiar with an adult female's scent regardless of relatedness (i.e., combining the related familiar and "unrelated familiar" treatments), offspring visited the scents of familiar and unfamiliar females equally (Wilcoxon signed-rank: Z = 1.60, p = .11, n = 32; Figure 1) but spent more time at the scent of the familiar female (Z = 2.48, p = .013, n = 32; time per visit: Z = 1.90, p = .057, n = 32; Figure 1) and tongue flicked this scent more often (Z = 2.349, p = .019, n = 32; flicks per visit: Z = 1.67, p = .095, n = 32; Figure 1). There was no difference in this respect between familiar females based on actual maternity (i.e., genetic mothers vs. foster mothers; all comparisons nonsignificant).
Do mothers discriminate between the scent of their own offspring versus scent from unrelated offspring?
Females visited the scent from their own offspring more often than the scent from an unrelated unfamiliar juvenile (Wilcoxon signed-rank: Z = –2.56, p = .011, n = 41; Figure 2). The results were similar regardless of whether the juvenile was familiar or not (living with mother: Z = –1.78, p = .076, n = 24; fostered out: Z = –1.94, p = .052, n = 17; Figure 2). All other comparisons were nonsignificant.
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Do mothers discriminate between the scent of a familiar juvenile versus scent from an unfamiliar juvenile?
There was no significant difference in any behavior in any treatment between that shown toward scent from a familiar juvenile and toward scent from a control juvenile (Figure 2).
Do juveniles discriminate between the scent of their fathers versus that from unrelated males?
Juveniles visited the scent of their father more often (Wilcoxon signed-rank: Z = –2.06, p = .04, n = 11; Figure 3), and tongue flicks per visit approached significance (Z = –1.90, p = .058, n = 11; Figure 3). All other comparisons were nonsignificant.
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Do fathers discriminate between the scent of their offspring and scent from unrelated juveniles?
Adult males showed no differences in their responses to the scent of their offspring versus that of control juveniles (Figure 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Using scent alone, juvenile E. saxatilis were able to discriminate between the scent of adults from their own family group and scent from unfamiliar unrelated adults. Juveniles did not discriminate between the scent of their unfamiliar biological mother and that of a control female. They did, however, distinguish the scent of familiar females (whether their biological mother or unrelated) from that of other females. Juveniles also discriminated between the scent of their familiar biological father and that of an unfamiliar, unrelated adult male. Thus, juvenile black rock skinks use recognition by association to distinguish kin from nonkin.
Our field and laboratory studies on E. saxatilis suggest that such an ability to distinguish between kin and nonkin (especially, for juveniles to recognize their own parents) would confer substantial fitness advantages in this species. Juvenile black rock skinks are the focus of adult aggression throughout the year. This aggression is so intense that it may have been a major selective force for sociality within the species (O'Connor and Shine, 2004). In laboratory trials, the presence of a related adult significantly reduced the amount of aggression directed against the juvenile by an unfamiliar adult (O'Connor and Shine, 2004). Under this scenario, there would be strong selection on the ability of juveniles to avoid contact with unfamiliar (and thus unfriendly) adults and stay within their parents' territorial boundaries.
In species where adults commit infanticide, as occurs in E. saxatilis, we expect strong selection for kin discrimination by adults (e.g., Joseph et al., 1999; Pfennig et al., 1999). In contrast, we documented only one significant difference (number of visits) in the responses of adults to the scent of their offspring (whether familiar or not) versus that of unrelated juveniles. This apparent lack of discrimination by adults toward offspring is surprising, given the presence of parental care in E. saxatilis. For parents to care only for their own offspring, they must have some method of identifying these offspring. E. saxatilis provides indirect care for its offspring by allowing them to remain within the parental territory (O'Connor and Shine, 2004). The scarcity of unrelated offspring in the parental territory and high aggression, including infanticide, shown by adults toward juveniles other than their own (O'Connor and Shine, 2004) indicate some mechanism of group recognition, though not one detected in this study. It is important to emphasize that a lack of discrimination, such as that found in our study, does not necessarily mean a lack of recognition: simply that recognition was not detected using our methodology.
Where the costs of making errors in recognizing kin are high, kin recognition by phenotype matching is unlikely to evolve (Keller, 1997; Reeve, 1989). As a result of access to higher quality resources and protection from conspecific aggression, juvenile E. saxatilis living within parental territories are likely to have higher fitness than those living outside parental territories (O'Connor DE and Shine R, unpublished data). Therefore, in E. saxatilis, if the inclusive fitness cost of excluding kin from the territory is high and the confidence in paternity is also high, then recognition by association is likely to offer a more reliable method for kin recognition than would phenotype matching. Although our study found no evidence for phenotype matching within E. saxatilis, it should also be noted that we did not explicitly test for this among familiar animals. That is, we did not test whether individuals could determine familiar kin from familiar nonkin. Although recognition using indirect indicators such as spatial and temporal cues has been proposed in other systems, these are unlikely to apply to black rock skinks. Field observations have confirmed that nongroup members travel through the territories of social groups, and the physical boundaries of the territories fluctuate. Use of indirect cues in such a system would result in a continual shifting of group membership.
Because E. saxatilis appears to recognize kin based on prior association rather than phenotype matching, the results of our study contrast with those from research on the closely related species E. striolata. A study by Bull et al. (2001) concluded that E. striolata recognize their kin based on phenotype recognition. The precise social system of E. striolata is currently unclear: this species is mainly solitary in some parts of its range (Bustard, 1970) but found in social groups in others (Bonnett, 1999). In saxicoline habitats, E. striolata appears to have a similar social system to that of E. saxatilis (personal observation). The two taxa are morphologically very similar and probably sister species (reviewed in Chapple, 2003). Why then do they apparently use different systems to recognize related conspecifics? The answer may lie in different experimental designs rather than species divergence per se. We presented E. saxatilis with a mixture of either familiar or unfamiliar animals, whereas Bull et al. (2001) presented E. striolata with a range of individuals that were all unfamiliar but differed in their degree of genetic similarity to the focal animal. If kin recognition in these species is context dependent, these differing designs might have revealed different results. That is, both species may be able to use both mechanisms, with the two studies differing in which type of kin discrimination system is most powerfully detectable. Regardless, our study tested lizards against cues that mimic those in the natural environment; and in the E. saxatilis system at least (where the fragmented habitat results in high within-outcrop relatedness; O'Connor, 2003), familiarity may provide a more reliable signal of relatedness than would phenotype matching alone.
Clearly, it would be useful to resolve the apparent difference in kin recognition mechanisms utilized by E. striolata and E. saxatilis, by applying the same methods to studies of both taxa. More generally, species within the Egernia lineage provide ideal opportunities for further research into the relationship between social systems and kin recognition mechanisms. Contrasting the kin recognition mechanisms of social reptiles with those of other social animals (both vertebrate and invertebrate) will also provide further insight into the evolution of this widespread behavior.
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ACKNOWLEDGEMENTS |
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Permits were provided by the New South Wales National Parks and Wildlife Service and the Animal Ethics Committee of the University of Sydney. The study was funded by grants to R.S. from the Australian Research Council and to D.E.O'C. by the Peter Rankin Trust Fund for Herpetology, Ethel Mary Read Research Grants and the Joyce W. Vickery Scientific Research Fund.
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