The relationship between generation gland morphology and armour in Dragon Lizards (Smaug): a reassessment of ancestral states for the Cordylidae

in Amphibia-Reptilia
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To substantiate the claim of a relationship between generation gland morphology and degree of body armour in cordylid lizards, we studied the nine species in the genus Smaug. We predicted that well armoured species in this clade will have multi-layer generation glands, and lightly armoured species two-layer glands. Gland type was determined using standard histological techniques after sectioning a glandular patch of one adult male per species. A total of 133 specimens were examined for data on tail and occipital spine lengths (which were used as indicators of armour). We found that species with multi-layer generation glands (S. giganteus, S. breyeri, and S. vandami) have relatively long tail and occipital spines, while species with two-layer glands (S. mossambicus, S. regius, S. barbertonensis, S. warreni, and an undescribed species) have relatively short spines. Smaug depressus possesses both multi-layer and two-layer glands, and this variation was linked to regional variation in spine length. An ancestral state reconstruction for the Cordylidae showed that the two-layer state always results from the reduction of layers from a multi-layer precursor, and that reduction always culminates in two-layer glands and not in one-layer glands. This finding suggests that the one-layer state in the Ninurta-Chamaesaura-Pseudocordylus clade is most probably plesiomorphic, and therefore the ancestral state at the Cordylidae and Cordylinae nodes. Given the observed relationship between type of generation gland and body armour, this finding would suggest that the most recent common ancestor of the Cordylidae was lightly armoured.

The relationship between generation gland morphology and armour in Dragon Lizards (Smaug): a reassessment of ancestral states for the Cordylidae

in Amphibia-Reptilia



  • BatesM.F. (2005): Taxonomic history and geographical distribution of the Pseudocordylus melanotus (A. Smith, 1838) and P. microlepidotus (Cuvier, 1829) complexes (Sauria: Cordylidae). Navors. nas. Mus. Bloemfontein 21: 37-112.

  • BranchW.R. (1998): Field Guide to Snakes and Other Reptiles of Southern Africa. Struik PublishersCape Town.

  • BroadleyD.G. (1966): The herpetology of south-east Africa. Unpubl. PhD thesis University of Natal Pietermaritzburg.

  • CooperW.E. Jr.Van WykJ.H.MoutonP.le F.N. (1996): Pheromonal detection and sex discrimination of conspecific substrate deposits by the rock-dwelling cordylid lizard Cordylus cordylus. Copeia 1996: 839-845.

  • CooperW.E. Jr.Van WykJ.H.MoutonP.le F.N. (1999): Discrimination between self-produced pheromones and those produced by individuals of the same sex in the lizard Cordylus cordylus. J. Chem. Ecol. 25: 197-208.

  • De VilliersF.A.MoutonP.le F.N.FlemmingA.F. (2015): Generation glands of cordylid lizards: mechanism of secretion transfer to the environment. Amphiba-Reptilia 36: 351-360.

  • De WaalS.W.P. (1978): The Squamata (Reptilia) of the Orange Free State South Africa. Mem. nas. Mus. Bloemfontein 11: +i-iii 1-160.

  • GreenbaumE.StanleyE.L.KusambaC.MoningaW.M.GoldbergS.R.BurseyC.R. (2012): A new species of Cordylus (Squamata: Cordylidae) from the Marungu Plateau of south-eastern Democratic Republic of the Congo. Afr. J. Herpetol. 61: 14-39.

  • HaywardJ.MoutonP.le F.N. (2007): Group location in the group-living lizard, Cordylus cataphractus: the significance of occupancy and a group signal. Amphibia-Reptilia 28: 329-335.

  • HerselmanY.M. (1991): A revision of the taxonomic status of Pseudocordylus capensis (Reptilia: Cordylidae). Unpubl. MSc thesis University of Stellenbosch Stellenbosch.

  • HewsD.K.BenardM.F. (2001): Negative association between conspicuous visual display and chemosensory behaviour in two phrynosomatid lizards. Ethology 107: 839-850.

  • JacobsenN.H.G. (1989): A herpetological survey of the Transvaal. Unpubl. PhD thesis University of Natal Pietermaritzburg.

  • JaredC.AntoniazziM.M.SilvaJ.R.M.C.FreymüllerE. (1999): Epidermal glands in Squamata: microscopical examination of precloacal glands in Amphisbaena alba (Amphisbaenia, Amphisbaenidae). J. Morphol. 241: 197-206.

  • LososJ.B.MoutonP.le F.N.BickelR.CorneliusI.RuddockL. (2002): The effect of body armature on escape behaviour in cordylid lizards. Anim. Behav. 64: 313-321.

  • LouwS.BurgerB.V.Le RouxM.Van WykJ.H. (2011): Lizard epidermal secretions. II. Chemical characterization of the generation gland secretion of the Sungazer, Cordylus giganteus. J. Nat. Prod. 74: 1364-1369.

  • MaddisonW.P.MaddisonD.R. (2011): Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at

  • MadersonP.F.A. (1986): The tetrapod epidermis: a system protoadapted as a semiochemical source. In: Chemical Signals in Vertebrates vol. 4 p. 13-25. DuvallD.Müller-SchwarzeD.SilversteinR.M. Eds Plenum PressNew York.

  • MoutonP.le F.N.FlemmingA.F. (2001): Osteoderm function in the lizard family Cordylidae. Proceedings of the Sixth International Congress of Vertebrate Morphology, Jena, Germany, July 21-26, 2001. J. Morphol. 248: 264.

  • MoutonP.le F.N.Van WykJ.H. (1997): Apaptive radiation in cordyliform lizards: an overview. Afr. J. Herpetol. 46: 78-88.

  • MoutonP.le F.N.FlemmingA.F.BroeckhovenC. (2014): Generation gland morphology in cordylid lizards: an evolutionary perspective. J. Morphol. 275: 456-464.

  • MoutonP.le F.N.FlemmingA.F.SearbyC.A. (1998): Active generation glands present in neonates of some cordylid lizards: a case study of Cordylus macropholis (Sauria: Cordylidae). J. Morphol. 235: 177-182.

  • MoutonP.le F.N.FlemmingA.F.StanleyE.D. (2012): Synchronised versus asynchronised breeding in cordylid lizards: an evolutionary perspective. J. Zool. 288: 191-198.

  • MoutonP.le F.N.Janse van RensburgD.A.Van WykJ.H. (2010): Epidermal glands in cordylid lizards with special reference to generation glands. Zool. J. Linn. Soc. 158: 312-324.

  • OrdT.J.PetersR.A.ClucasB.StampsJ.A. (2007): Lizards speed up visual displays in noisy motion habitats. Proc. R. Soc. B 274: 1057-1062.

  • PiankaE.R.VittL.J. (2003): Lizards: Windows to the Evolution of Diversity. University of California PressBerkeley.

  • R Core Team (2017): A language and environment for statistical computing. Vienna Austria. Retrieved from

  • ReissigJ. (2014): Girdled Lizards and Their Relatives. Natural History Captive Care and Breeding. Edition ChimairaFrankfurt am Main.

  • SearbyC.A. (2002): Histological description of generation glands and their functional relationship to the shedding cycle in cordylid lizards. Unpubl. MSc thesis University of Stellenbosch Stellenbosch.

  • StanleyE.L.BatesM.F. (2014): Here be dragons: a phylogenetic and biogeographical study of the Smaug warreni species complex (Squamata: Cordylidae) in southern Africa. Zool. J. Linn. Soc. 172: 892-909.

  • StanleyE.L.BauerA.M.JackmanT.R.BranchW.R.MoutonP.le F.N. (2011): Between a rock and a hard polytomy: rapid radiation in the rupicolous girdled lizards (Squamata: Cordylidae). Mol. Phylogenet. Evol. 58: 53-70.

  • Van WykJ.H.MoutonP.le F.N. (1992): Glandular epidermal structures of cordylid lizards. Amphibia-Reptilia 12: 1-12.


  • View in gallery

    Photomicrographs of a) the ventral aspect of the thigh of a cordylid lizard, showing the patch of generation glands and the row of femoral gland pores; and cross-sections through b) a protruding two-layer type generation gland of Smaug depressus, (NMB R10876) showing the two mature generation layers; c) a protruding multiple-layer type generation gland of S. vandami (NMB R8545) showing the multiple mature generation layers; (GG = generation gland; MG = mature generation layer; PG = presumptive generation layer; FG = femoral gland; SG = stratum germinativum).

  • View in gallery

    Photographs of eight Smaug species depicting differences in body colour and spinosity.

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    Photographs depicting a) the four lateral tail spines on whorls three and four that were measured for each individual of Smaug investigated (the insert shows how the spine measurement was performed), and b) the two outer occipital spines on each side of the head that were measured for each individual of Smaug investigated. Spine measurements were taken along the long axis of the outer or both of the two occipital scales.

  • View in gallery

    Ancestral state reconstruction of generation gland type for the Cordylidae. The phylogenetic tree is based on the maximum-likelihood analyses of Stanley et al. (2011) and Stanley and Bates (2014). Pie charts show the relative likelihood of each generation gland type at the respective nodes.

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    Morphological data for samples of the nine species of Smaug examined for this study. Determination of tail and occipital spine ratios is explained under ‘Materials and methods’.

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    Scatterplots of tail spine ratio (= ln tail spine length)/ln(SVL)) versus occipital spine ratio (= ln occipital spine length)/ln(SVL)) for a) 66 individuals, representing eight of the nine Smaug species, and b) 37 individuals of S. depressus from various localities in the Soutpansberg region. Solid symbols represent species/populations displaying multi-layer generation glands, and open symbols represent species/populations with two-layer generation glands.


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