Ecology, Life-History, and Behavior in the Australian Scincid Genus Egernia, with Comments on the Evolution of Complex Sociality in Lizards

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Ecology, Life-History, and Behavior in the Australian Scincid Genus Egernia, with Comments on the Evolution of Complex Sociality in Lizards Herpetological Monographs, 17, 2003, 145–180 Ó 2003 by The Herpetologists’ League, Inc. ECOLOGY, LIFE-HISTORY, AND BEHAVIOR IN THE AUSTRALIAN SCINCID GENUS EGERNIA, WITH COMMENTS ON THE EVOLUTION OF COMPLEX SOCIALITY IN LIZARDS 1 DAVID G. CHAPPLE School of Botany and Zoology, Australian National University, Canberra ACT 0200, Australia ABSTRACT: Squamate reptiles generally have been ignored in the search for a unified theory for the evolution of sociality due to the perception that they exhibit little social behavior beyond territoriality and dominance hierarchies and display polygynous mating systems. However a growing body of research has revealed unsuspected levels of social complexity and diversity in mating systems within the squamate lineage, particularly among the members of the Australian Scincid genus Egernia. Several species of Egernia are amongst the most highly social of all squamate reptiles, exhibiting stable social aggregations and high levels of long-term social and genetic monogamy. Social complexity is widespread within the Egernia genus, with reports of social aggregations in 23 of the 30 described species. The purpose of this review was to examine the potential for the Egernia genus as a model system for study of the evolution of sociality and monogamy within squamate reptiles. Current evidence indicates there is substantial variability in social complexity both within and between species, with social organization covering the spectrum from solitary to highly social. Four highly social Egernia species are known to live in stable social aggregations consisting of closely related individuals (adults, subadults, juveniles; i.e., ‘family’ groups) that appear to utilize chemical cues to recognize group members (kin recognition). Enhanced vigilance against predators is one presumed benefit of group membership. Additionally, juveniles within social groupings appear to receive low levels of indirect parental care. Several Egernia species create scat piles that mark group territories. Three Egernia species exhibit long-term social and genetic monogamy and several inbreeding avoidance strategies have been documented. However, it is currently unknown whether monogamy is widespread within Egernia. Egernia species occupy a broad range of habitats, although most are terrestrial, saxicolous or semi-arboreal. Several species display an attachment to a permanent home site, generally a rock crevice, burrow or tree hollow. Egernia species take 2–5 years to mature, live for 5–25 years, and are viviparous with litter size positively correlated with body size. Several Egernia species are herbivorous, with the degree of herbivory increasing with body size and during ontogeny in larger species. Most smaller species are either insectivorous or omnivorous. Species of Egernia have a wide range of reptilian, avian, and mammalian predators. Several larger species possess several behavioral and morphological features to prevent their extraction from rock crevices, including highly modified keeled scales and numerous defensive behaviors. Color pattern polymorphism is present in five Egernia species. Potential ecological correlates of sociality and monogamy are discussed. The life-history hypothesis predicts long-lived, late-maturing species should evolve complex sociality. The habitat availability hypothesis relies on the assumption that refugia may be limited in some ecological settings, and group formation is a consequence of co-habitation of available refugia. These hypotheses are not mutually exclusive, and testable predictions are formulated and discussed. Specific future research directions are outlined to take advantage of Egernia as a model system for comparative research on a lineage that represents an independent origin of social organization comparable to that found in birds and mammals. Key words: Color pattern polymorphism; Egernia; Habitat use; Herbivory; Life-history; Mating systems; Scincidae; Sociality. THE Australian Scincid genus Egernia com- understanding of the evolution of complex prises some of Australia’s largest, more ubiq- sociality and monogamous mating systems uitous and easily identifiable lizards (Cogger, in reptiles. Complex sociality appears to be 2000; Greer, 1989). Several species of Egernia widespread within the Egernia lineage, with are among the most highly social of all anecdotal reports of social aggregations docu- squamate reptiles, and recent research has mented for 23 of the 30 currently recognised suggested that studies focused on this genus species. The size, complexity, and stability of could provide a valuable contribution to our these aggregations appear to vary noticeably both among species, and among populations of the same species, indicating diversity of social 1 CORRESPONDENCE:e-mail,[email protected] organization within the genus. 145 146 HERPETOLOGICAL MONOGRAPHS [No. 17 Understandably, initial investigations of cases of convergent evolution of similar social sociality in Egernia have focused on species systems within phylogenetically independent that display the most apparent and complex lineages to search for ecological correlates social organizations. Although several species related to the evolution or loss of social organi- were generally found in small groups (adult zation (Cahan et al., 2002), thus identifying pair and/or their offspring; E. saxatilis, O’Con- factors important in the evolution of sociality nor and Shine, 2003; E. striolata, Bonnett, (e.g., Crespi, 1994; Danforth, 2002; Duffy et al., 1999), Egernia cunninghami and E. stokesii 2000; Schwarz et al., 1998; Soucy and Danforth, were found to live in groups of up to 17 2002). Consequently, for each independent individuals (Duffield and Bull, 2002; Gardner origin of complex sociality two vital compo- et al., 2001; Stow et al., 2001; A. Stow, un- nents are required: 1) a well-resolved phylog- published data). These long-term behavioral eny to trace the evolution (and loss) of sociality and molecular studies also demonstrated that within the lineage; and 2) detailed ecological, social groupings in each of these species were behavioral and life-history information with stable between seasons and were comprised of which to correlate to evolutionary origins and closely related individuals (‘family’ groups). As loses of complex social organization (Cahan a result of such temporal stability in group et al., 2002; Hughes, 1998). structure, adult pairs in several species (E. Although phylogenetic relationships among cunninghami, E. saxatilis, E. stokesii) appear Egernia species are to date unresolved (see to be socially monogamous, also exhibiting Evolution, Systematics and Taxonomy sec- a high degree of genetic monogamy (Gardner tion), this review summarizes the ecological, et al., 2002; O’Connor and Shine, 2003; behavioral and life-history information avail- A. Stow, unpublished data). However, social able for Egernia to highlight potential corre- organization within Egernia is likely to cover lates of sociality and monogamy within the the spectrum from these examples of highly genus and present hypotheses relating to the social species to those that remain predomi- evolution of sociality within Egernia. However, nately solitary throughout their lives. any synthesis presented is inevitably prelimi- Squamate reptiles have been assumed to nary as the study of complex sociality and exhibit little social behavior beyond territori- monogamy in Egernia is still in its infancy. ality and dominance hierarchies (e.g., Bratt- Detailed study has been completed on only strom, 1974; Stamps, 1977) and consequently four species: E. cunninghami (Stow et al., reptilian examples are severely lacking in the 2001; A. Stow, unpublished data), E. saxatilis sociality literature. The widespread incidence (O’Connor and Shine, 2003), E. stokesii (Duf- of complex sociality (and the diversity of social field and Bull, 2002; Gardner et al., 2001, organization) within the Egernia genus 2002), and E. striolata (Bonnett, 1999). provides a unique opportunity to study the This review builds upon Greer’s (1989) brief independent evolution of sociality within a summary of Egernia ecology and behavior (as reptilian lineage. Likewise, monogamy such as part of an overview of Australian lizards) and that observed in E. cunninghami, E. saxatilis the work of Hutchinson (1993) and Gardner and E. stokesii (Gardner et al., 2002; O’Connor (1999). Although the review is focused pri- and Shine, 2003; A. Stow, unpublished data) marily on social behavior and mating systems, is relatively rare in lizards, because most spe- several other interesting traits (herbivory, cies exhibit polygynous mating systems (Bull, ontogenetic dietary shifts, burrowing, scat 2000). Therefore, Egernia also may provide piling, color pattern polymorphism) within insight into the independent evolution of the Egernia genus also are examined. monogamy in squamate reptiles. The factors responsible for promoting the EVOLUTION,SYSTEMATICS AND TAXONOMY evolution and loss of complex sociality are an The evolution of Egernia species from an essential component in the broader search for ancestral immigrant from New Guinea and its a unified theory for the evolution of sociality subsequent radiation across Australia has been within both vertebrate and invertebrate taxa examined in detail (Heatwole and Taylor, (e.g., Cahan et al., 2002). Recent attempts to 1987; Horton, 1972). Horton (1972) suggested obtain such a unified theory have relied on that the ancestor of Egernia (presumed to be 2003] HERPETOLOGICAL
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