Lizards in 'nuclear families': a novel reptilian social system in Egernia saxatilis (Scincidae)

Recent research has revealed unsuspected complexity in social organization among squamate reptiles. In particular, large Australian scincid lizards of the genus Egernia have been reported to occur in large aggregations of closely related individuals. However, the 'nuclear family' structure found in many other 'social' organisms (especially birds) has not been reported from reptiles. Our field studies on black rock skinks (Egernia saxatilis) in southeastern Australia document exactly this pattern. We quantified group composition using behavioural observations at regular intervals over three field seasons, and took tissue samples for parentage analysis. On the focal rock outcrop 72% of lizards were typically found as part of a stable social grouping, with individuals physically associated with other group members in a third of observations. Eighty-five per cent of juveniles lived in social groups, 65% in family groups with at least one of their parents (including 39% with both parents as revealed by parentage analysis of five microsatellite loci). Broader sampling in surrounding areas revealed similar patterns of group size, composition and relatedness. Overall, of the groups that contained more than one adult, 83% contained a single adult pair. Long-term monogamy and group stability were evident from our genetic data, with up to three annual cohorts of full-sib offspring living with their biological parents. Our data expand the range of social systems known for reptiles, and reveal strong convergence towards 'nuclear family' systems in distantly related vertebrates.     

Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae)

The lizards of the Egernia group of Australia and Melanesia include some of the most distinctive members of the family Scincidae in morphology (including giant size, spinose scalation), ecology and behaviour. Social behaviour, including long‐term recognition of individuals and kin, mate fidelity and home site fidelity, is amongst the most complex known in squamate reptiles and is the subject of an expanding number of studies. Lack of a sound phylogeny for the Egernia group has limited our ability to understand the evolution and patterns of variation in social behaviour within this group, and evidence for the monophyly of the largest genus, Egernia (64% of the species), has been lacking. We present data derived from nucleotide sequences that establish a phylogenetic framework for the Egernia group. We used two mitochondrial sequences, the protein‐encoding ND4 gene and a ribosomal gene, 12s rRNA, and two nuclear sequences, the protein‐encoding c‐mos, and non‐encoding intron 7 of β‐fibrinogen. Our phylogenetic analyses show that Corucia of the Solomon Islands is the sister group of the rest of the Egernia group. The genus Egernia is paraphyletic, including four well‐supported monophyletic units, one of which is the sister lineage of the Tiliqua lineage (Tiliqua plus Cyclodomorphus). We suggest a revised taxonomic scheme that recognizes the major monophyletic lineages in Egernia (s.l.) as distinct genera. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 781–794.     

Interembryonic regions of the uterus of the viviparous lizard Mabuya brachypoda (Squamata: Scincidae)

Analysis of the structure and physiology of the uterine incubation chambers of viviparous squamates has provided insight concerning adaptations for gestation. However, the literature addressing the biology of the interembryonic regions of the uterus is very limited, presumably because it has been assumed that this area has little role in the development and support of embryos in viviparous squamates. This study was undertaken to examine the histology of the interembryonic regions of Mabuya brachypoda, a viviparous lizard with microlecithal ova and consequently substantial matrotrophic activity. The incubation chambers are oval, distended zones of the uterus, adjacent to the interembryonic regions. The wall of the interembryonic regions includes: mucosa, formed by a cuboidal or columnar epithelium with ciliated and nonciliated cells, and a lamina propria of vascularized connective tissue containing abundant acinar glands; myometrial smooth muscle consisting of inner circular and outer longitudinal layers; and serosa. The segment of the interembryonic region adjacent to the incubation chamber forms a transitional segment that displays folds of the mucosa that protrude into the uterine lumen. The limit of the incubation chamber is well defined by the long mucosal folds of the transitional segment. Long and thin extensions of extraembryonic membranes are present in the lumen of the transitional segment, outside of the incubation chamber region. The presence of abundant uterine glands and extraembryonic membranes in the interembryonic regions during gestation suggests uterine secretory activity and histotrophic transfer of nutrients to embryos in these regions.     

The social elite: Habitat heterogeneity,complexity and quality in granite inselbergs influence patterns of aggregation in Egernia striolata (Lygosominae: Scincidae)

Habitat heterogeneity, structural complexity and habitat quality are key features of the environment that drive species' distribution and patterns of biological organization. Traditionally, pattern‐based studies have focused on faunal responses to biological systems. However, the influence of non‐biological environments such as insular rock outcrops on patterns of vertebrate distribution is conceivably as important, but has received less attention. Granite inselbergs are a naturally heterogeneous and spatially‐limited habitat. As such, they provide an opportunity for investigating whether environmental attributes influence social behaviour in animals that use these kinds of habitat, particularly lizards that are well adapted to saxicoline environments. We applied ecological theory to investigate the influence of habitat heterogeneity, structural complexity and habitat quality on patterns of home‐site occupancy in the crevice skink Egernia striolata (Lygosominea: Scincidae) from insular granite outcrops located within fragmented agricultural landscapes. We compared home‐site occupancy among solitary juveniles, solitary adults and lizard aggregations. We found significant differences in home‐site occupancy between aggregations and solitary lizard outcrop attributes measured at multiple spatial scales. The probability of a home‐site being occupied by an aggregation increased where large rock masses were present, on northern aspects near the core of the outcrop and in structurally variegated landscapes. Significantly more aggregations occupied home‐sites surrounded by high boulder cover and crevice microhabitat. We provide evidence that geophysical attributes of granite inselbergs and landscape context can influence patterns of lizard aggregation. Thus, we clearly document the environmental correlations of variability in sociality among subpopulations of Egernia striolata.     

Kin recognition and cannibalism in a subsocial spider

Evolution of cooperation and group living in spiders from subsocial family groups may be constrained by their cannibalistic nature. A tendency to avoid cannibalizing kin may facilitate tolerance among spiders and implies the ability to identify relatives. We investigated whether the subsocial spider Stegodyphus lineatus discriminates kin by recording cannibalism among juveniles in experiments during which amount of food and size difference among spiders in groups were varied. We hypothesized that family groups should be less cannibalistic than groups of mixed‐parental origin. Further, we tested whether food‐stress would influence cannibalism rates differently in kin and nonkin groups and the effect of relatedness on cannibalism within groups of spiders of variable size compared with those of homogenous size. In groups of six spiders, more spiders were cannibalized in nonsib groups than in sib groups under low food conditions. A tendency for nonkin biased cannibalism in starved spider pairs supported that kin recognition in S. lineatus is expressed when food is limited. Size variance of individuals within well‐fed groups of siblings and unrelated spiders had no influence on cannibalism rates. Apparently, both hunger and high density are important promoters of cannibalism. In addition to inclusive fitness benefits, we suggest that an ability to avoid cannibalizing kin will favour the evolution of cooperation and group living in phylogenetically pre‐adapted solitary species.     

Sexual dimorphism and female reproductive cycle in the scincid lizard Trachylepis vittata (Olivier, 1804) in Lebanon (Reptilia: Scincidae)

Sexual dimorphism and the female reproductive cycle were studied in a population of the viviparous lizard Trachylepis vittata at 2000 m a.s.l. on Mount Sannine, Lebanon. Females have larger body sizes than males and males have relatively larger heads than females. Females reach maturity at 56 mm snout-vent length. They spend at least six months in hibernation, from October to March. Adult females emerge from hibernation in April. Fertilization occurs mid-May and gestation lasts for 8-10 weeks. All females collected on the same date had embryos at the same embryonic developmental stage. Females produced 1-4 embryos. There is a significant positive relationship between female body size and number of embryos. Parturition lasts for two weeks and new-borns achieve adult size within about ten months.     

Field studies on a social lizard: Home range and social organization in an Australian skink,Egernia major

Abstract Although most reptiles have polygynous mating systems without long‐term pair bonds, one lineage of large scincid lizards in Australia is exceptional in this respect. Reports of complex sociality in the genus Egernia led us to conduct the first radiotelemetric field study of a species within this group. Land mullets (Egernia major) are large (60 cm total length), viviparous lizards from rainforest habitats in south‐eastern Australia. To document the spatial ecology and social organization of this species, we captured 12 adult lizards in the Barrington Tops area of eastern New South Wales and implanted them with miniature radiotransmitters. The lizards were released at their sites of capture and located daily for the next 6 weeks. All of the radiotracked lizards had discrete home ranges of approximately 10 000 m², based around well‐defined core areas (approximately 2000–3000 m²). Females tended to move further, and to range over wider areas, than did males. All of the radiotracked lizards lived in social groups consisting of one or more adult males and females plus juveniles of all age classes. Subgroups were apparent within one group of five radio‐tagged lizards: individual animals consistently shared their shelter sites and home ranges with one or more specific individuals. Male/female pairings were more frequent than expected under the null hypothesis of random association among individuals. The data in the present study support anecdotal reports of pair bonds in E. major and support suggestions that the social systems of species in this genus are more complex than those of previously studied reptiles.     

United in adversity: Aridity and cold influence aggregation behaviour in a social lizard,Egernia stokesii

Sociality has evolved independently many times in a diverse array of animal taxa. While sociality in some invertebrates, birds and mammals is relatively well understood, complex social behaviour in Squamate reptiles is a comparatively recent discovery. The extent to which social behaviour is phylogenetically constrained, or free to respond to environmental conditions is a key question in understanding sociality. We sampled 74 aggregations involving 137 individuals of a social lizard (Egernia stokesii) from 13 sites across a 96 250 km² area showing a wide range of environmental conditions. Over all locations, 70% of the lizards were found in aggregations, supporting the previous suggestion that aggregation in this species is phylogenetically constrained. However, the size of aggregations was negatively related to spatial variation in aridity and daily variation in maximum temperature, suggesting that social behaviour also varied in response to harsh environmental conditions. Lizards aggregated more in arid areas and on cold days. Our results show that it is overly simplistic to regard social behaviour in E. stokesii as either phylogenetically constrained or environmentally determined. A more nuanced appreciation of the extent to which social behaviour is free to vary in response to environmental conditions improves our understanding of social behaviour in Squamate reptiles.     

Genetic evidence for kin-based female social structure in common eiders (Somateria mollissima)

Kin-based social groups are commonly studied among cooperativelybreeding species but have been less studied in "nontraditional"group breeding systems. We investigated the presence of kin-basedsociality among females in the common eider (Somateria mollisima),a colonial nesting sea duck that exhibits high levels of natalphilopatry in females. Previous studies of female socialityin common eiders have been restricted to observations duringbrood rearing. However, aggregations of female common eidersare also observed during other periods of the life cycle suchas colony arrival and nesting. Here we apply a novel, empiricalframework using molecular markers and field sampling to geneticallycharacterize female social groups at several stages of the commoneider life cycle. When compared with mean estimates of interindividualrelatedness for the entire colony, significantly higher levelsof relatedness were found between females within groups arrivingto the colony in flight, between females and nearest neighborsat the time of nest site selection, and between groups of femalesdeparting the colony with ducklings. Both full-sibling and half-siblingequivalent relationships were also found within these groups.Therefore, throughout each of several stages including in-flightcolony arrival, nesting, and brood rearing, we provide the firstgenetically confirmed evidence of female kin-based social groupsin common eiders and anseriformes in general.     

A phylogenetic analysis of variation in reproductive mode within an Australian lizard (Saiphos equalis, Scincidae)

Saiphos equalis , a semi-fossorial scincid lizard from south-eastern Australia, is one of only three reptile species world-wide that are known to display geographic variation in reproductive mode. Uniquely, Saiphos equalis includes populations with three reproductive modes: oviparous with long (15-day) incubation periods; oviparous with short (5-day) incubation periods; and viviparous (0-day incubation periods). No Saiphos populations show 'normal' scincid oviparity (> 30-day incubation period). We used mitochondrial nucleotide sequences ( ND2 and cytochrome b ) to reconstruct relationships among populations from throughout the species' distribution in New South Wales, Australia. Under the phylogenetic species concept, phylogenetic analyses are consistent with the oviparous and viviparous populations of S. equalis being conspecific. Phylogenetic analyses suggest that the long incubation period oviparous lineage is the sister group to all other populations; and that the viviparous populations belong to a cluster of weakly supported clades basal to the short-incubation-period oviparous clade. These clades correspond to variation in reproductive mode and geographic location.     

Dentition and tooth replacement pattern in Chalcides (Squamata; Scincidae)

This study was undertaken as a prerequisite to investigations on tooth differentiation in a squamate, the Canarian scincid Chalcides. Our main goal was to determine whether the pattern of tooth replacement, known to be regular in lizards, could be helpful to predict accurately any stage of tooth development. A growth series of 20 laboratory-reared specimens, aged from 0.5 month after birth to about 6 years, was used. The dentition (functional and replacement teeth) was studied from radiographs of jaw quadrants. The number of tooth positions, the tooth number in relation to age and to seasons, and the size of the replacement teeth were recorded. In Chalcides, a single row of pleurodont functional teeth lies at the labial margin of the dentary, premaxillary, and maxillary. Whatever the age of the specimens, 16 tooth positions were recorded, on average, in each quadrant, suggesting that positions are maintained throughout life. Replacement teeth were numerous whatever the age and season, while the number of functional teeth was subject to variation. Symmetry of tooth development was evaluated by comparing teeth two by two from the opposite side in the four jaw quadrants of several specimens. Although the relative size of some replacement teeth fitted perfectly, the symmetry criterion was not reliable to predict the developmental stage of the opposite tooth, whether the pair of teeth compared was left-right or upper-lower. The best fit was found when comparing the size of successive replacement teeth from the front to the back of the jaw. Every replacement tooth that is 40-80% of its definitive size is followed, in the next position on the arcade, by a tooth that is, on average, 20% less developed. Considering teeth in alternate positions (even and odd series), each replacement tooth was a little more developed than the previous, more anterior, one (0.5-20% when the teeth are from 10-40% of their final size). The latter pattern showed that tooth replacement occurred in alternate positions from back to front, forming more or less regular rows (i.e., "Zahnreihen"). In Chalcides, the developmental stage of a replacement tooth in a position p can be accurately predicted provided the developmental stage of the replacement tooth in position p-1 or, to a lesser degree, in position p-2 is known. This finding will be particularly helpful when starting our structural and ultrastructural studies of tooth differentiation in this lizard.     

Fine‐scale genetic structuring in a group‐living lizard,the gidgee skink (Egernia stokesii)

By constraining gene flow, group living and natal philopatry can result in fine‐scale genetic structure. Although the genetic structure of some group‐living lizards has been characterised, studies are few compared with those for group‐living bird and mammal species. The Egerniinae group of lizards exhibits a high diversity of social structures, making it a useful group for comparative studies of genetic structure across a broader range of social taxa. A well‐studied member of Egerniinae is Egernia stokesii, a lizard that forms long‐term pair bonds and stable social groups and exhibits natal philopatry and limited dispersal. Evidence exists for consistent E. stokesii social structure across seven close but disconnected rocky outcrops within a 40 × 10 km area. We used summary statistics, analysis of molecular variance, Bayesian clustering, and discriminant analysis of principal components to assess if E. stokesii exhibit a consistent pattern of fine‐scale genetic structure across the same seven outcrops. Due to E. stokesii social structure and constrained dispersal, we predicted significant genetic structuring – based on microsatellite markers – among outcrops. We found significant fine‐scale genetic structuring and evidence for two genetic clusters. We discuss features of E. stokesii biology and ecology that may explain our findings. Some rocky outcrops, and some social groups, contained lizards from both genetic clusters. An examination of the composition of mixed cluster social groups did not detect any notable patterns. Therefore, further work is necessary to identify how the observed patterns may have arisen. Future investigations in E. stokesii and other group‐living lizard species are likely to contribute greatly to our understanding of the genetic consequences of group living.     

Kin recognition by the predatory mite Iphiseius degenerans: discrimination among own, conspecific, and heterospecific eggs

1. Kin recognition is important in many social insects, but has also been found in several nonsocial insects such as parasitoids, where it plays an important role in oviposition behaviour. In nonparasitic arthropods, however, the fitness of ovipositing females also depends on the oviposition behaviour of related and unrelated females, especially when eggs are oviposited in clusters by several females. 2. In this paper, kin recognition in a predatory mite, Iphiseius degenerans, is studied. Mothers are capable of determining offspring sex ratio, and cannibalism on juvenile stages is a common phenomenon. Therefore, kin recognition is expected to occur in this predator. 3. Oviposition behaviour of this species is particularly interesting because it alternates foraging bouts in flowers with deposition of a single egg at a time on a leaf, where predation risk is lower. The eggs are not scattered but are deposited in clusters. After feeding in a flower, females therefore have to locate clusters of eggs. 4. Experiments on two‐choice arenas showed that females prefer to oviposit close to conspecific eggs rather than close to heterospecific eggs. Females also showed a preference for ovipositing near closely related conspecific eggs rather than more distantly related eggs. 5. Females tended to displace eggs of heterospecifics more frequently than eggs of conspecifics. 6. These behavioural observations show that females can discriminate not only between conspecific and heterospecific eggs but also between eggs that vary in degree of relatedness. This enables females to oviposit in clusters containing related eggs and thus avoid cannibalism by non‐kin and/or produce adaptive sex ratios despite the fact that the adults commute between flowers and leaves.     

Thermoregulation in four Australian lizards of the genus Egernia (Sauria: Scincidae)

Mean thermal preferenda for the head and body were found to be similar in Egernia whitei, E. cunninghami, and E. bungana (range in T_H= 33.6^o -33.8^o C; range in T_B= 34.0^o-35.3^oC). However, those for E. majors were significantly lower (T_H= 31.1^o C, T_B=32.9^oC). Significant differences were found between mean head and body preferred temperatures in E. cunninghami and E. major. Higher temperatures were tolerated by the body than the head in all four species. Gaping was not observed to occur prior to cessation of respiration in any of the four species during radiant or solar heating. Based upon thermal preferenda and critical thermal maxima data, thermal safety margins for body temperature were calculated for E. whitei and E. cunninghami Postural orientation to the sun's rays increased and decreased heat gain. The seeking of shade was the most effective method employed by all four species for reducing head and body temperature.     

Kin discrimination and sex ratios in a parasitoid wasp

Sex ratio theory provides a clear and simple way to test if nonsocial haplodiploid wasps can discriminate between kin and nonkin. Specifically, if females can discriminate siblings from nonrelatives, then they are expected to produce a higher proportion of daughters if they mate with a sibling. This prediction arises because in haplodiploids, inbreeding (sib-mating) causes a mother to be relatively more related to her daughters than her sons. Here we formally model this prediction for when multiple females lay eggs in a patch, and test it with the parasitoid wasp Nasonia vitripennis. Our results show that females do not adjust their sex ratio behaviour dependent upon whether they mate with a sibling or nonrelative, in response to either direct genetic or a range of indirect environmental cues. This suggests that females of N. vitripennis cannot discriminate between kin and nonkin. The implications of our results for the understanding of sex ratio and social evolution are discussed.     

Perspectives: Hamilton's Legacy: Mechanisms of Kin Recognition in Humans

The behavior literature is replete with examples of individuals exhibiting costly acts that benefit someone else. These examples troubled Darwin so much so that he thought they would be fatal to his theory of natural selection. A century later, W. D. Hamilton refined that theory by showing, quantitatively, that such acts could be favored if the individuals involved were relatives. His theory of inclusive fitness is generally considered one of the greatest theoretical advances in evolution since Darwin's time. Less appreciated from Hamilton's 1964 paper is the hypothesis that mechanisms favoring accurate kin recognition will also be selected. Here, I review those recognition mechanisms and survey the literature on human kin recognition. Although not often considered, humans both produce cues to kinship that vary with genetic relatedness and have perceptual abilities to detect these cues in others and assess that relatedness. The potential functions of these abilities are discussed. Importantly, gaps in our understanding of the development and use of recognition mechanisms are noted.     

Isospora viridanae N. Sp., an Intranuclear Coccidian Parasite from the Canarian Skink, Chalcides viridanus (Lacertilia: Scincidae)

A caryotropic species of coccidium, Isospora viridanae n. sp. (Apicomplexa: Eimeriidae). has been found as a parasite in the Canarian skink, Chalcides viridanus Gravenhorst, 1851, from Tenerife, Spain, and is described here as a new species. Fully sporulaled oocysts of Isospora viridanae are spherical and measure 21.6 (1 7.6–23.4) nm in diameter. Mtcropyle, oocyst residuum and polar granule are ali absent. Oocysts of this coccidian, with a smooth bilayered wall, contain 2 ovoid sporocysts 13.2 (11.7–14.0) by 9.5 8.2–10 5) μm. A sporocyst residuum is present as well as a Stieda body and a substieda body. Most oocysts are found to be at the beginning of sporulanon when excreted and show 2 spherical sporoblasts. Sporulation is completed within 24 to 48 h at 23 × 2°C Sporozoites are 13–14 μm long and are about 2.5–3 μ m wide. Endogenous stages of schizogony and gamogony develop in the nuclei of epithelial cells from the small intestine of the skink. Comparisons with other species of the genus found in lacertilian hosts indicate that it is a new species.