[1].[J].Asian Herpetological Research,2013,4(4):225-232.[doi:10.3724/SP.J.1245.2013.000225]
 Zheng WANG,Li MA,Min SHAO,et al.Differences in Incubation Length and Hatchling Morphology among Five Species of Oviparous Phrynocephalus Lizards (Agamidae) from China[J].Asian Herpetological Research(AHR),2013,4(4):225-232.[doi:10.3724/SP.J.1245.2013.000225]


Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Original Article


Differences in Incubation Length and Hatchling Morphology among Five Species of Oviparous Phrynocephalus Lizards (Agamidae) from China
Zheng WANG12 Li MA3 Min SHAO3 Xiang JI2*
1 College of Forest Resources and Environment, Nanjing Forestry University, Nanjing 210037, Jiangsu, China
2 Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing 210046, Jiangsu, China
3 Hangzhou Key Laboratory for Animal Adaptation and Evolution, School of Life Sciences, Hangzhou Normal University, Hangzhou 310036, Zhejiang, China
Agamidae Phrynocephalus lizards oviparous species egg incubation incubation length hatchling morphology
We incubated eggs of five Phrynocephalus species (P. albolineatus, P. axillaries, P. grumgrzimailoi, P. helioscopus and P. przewalskii) at three constant temperatures (24 °C, 28 °C and 32 °C) to examine differences in incubation length and hatchling morphology among species and among temperature treatments. We combined data from this study with those reported previously for P. frontalis and P. versicolor to examine whether embryonic stage at laying is a causal factor for interspecific variation in incubation length, and whether the phylogenetic relationship inferred from hatchling morphology is consistent with the relationship based on mitochondrial DNA data. Mean values for incubation length differed among the five species studied herein and, in all these five species, incubation length decreased at a decreasing rate as temperature increased. In none of the five species did hatchling size (snout-vent length and body mass) and other morphological variables differ among the three temperature treatments. The seven oviparous Phrynocephalus lizards found in China differ from each other in hatchling morphology, and embryonic stage at laying is a causal factor of inter- and intra-specific variation in incubation length. The phylogenetic relationship inferred from hatchling morphology is not always consistent with the currently known relationship based on mitochondrial DNA data. Data from this study and those reported previously allow the conclusion that any Phrynocephalus species may have its unique position along the axis defined by hatchling morphology.


Barabanov A. V., Ananjeva N. B. 2007. Catalogue of the available scientific species group names for lizards of the genus Phrynocephalus Kaup, 1825 (Reptilia, Sauria, Agamidae). Zootaxa, 1399: 1–57
Du W. G., Ji X., Zhang Y. P., Lin Z. H., Xu X. F. 2010a. Geographic variation in offspring size of a widespread lizard (Takydromus septentrionalis): Importance of maternal investment. Biol J Linn Soc, 101: 59–67.
Du W. G., Warner D. A., Langkilde T., Robbins T., Shine R. 2010b. The physiological basis of geographic variation in rates of embryonic development within a widespread lizard species. Am Nat, 176: 522–528
Dufaure J. P., Hubert J. 1961. Table de développement du lézard vivipare: Lacerta (Zootoca) vivipara Jacquin. Arch Anat Micr Morph Exp, 50?: 309–328
Gozdzik A., Fu J. Z. 2009. Are toad-headed lizards Phrynocephalus przewalskii and P. frontalis (Family Agamidae) the same species? Defining species boundaries with morphological and molecular data. Russ J Herpetol, 16: 107–118
Guo X. G., Wang Y. Z. 2007. Partitioned Bayesian analyses, dispersal–vicariance analysis, and the biogeography of Chinese toad-headed lizards (Agamidae: Phrynocephalus): A re-evaluation. Mol Phylogenet Evol, 45: 643–662
Hao Q. L., Liu H. X., Ji X. 2006. Phenotypic variation in hatchling Mongolian racerunners (Eremias argus) from eggs incubated at constant versus fluctuating temperatures. Acta Zool Sin, 52: 1049–1057
Ji X., Bra?a F. 1999. The influence of thermal and hydric environments on incubating eggs and embryonic use of energy and nutrients in the wall lizard Podarcis muralis. Comp Biochem Physiol A, 124: 205–213
Ji X., Huang H. Y., Hu X. Z., Du W. G. 2002. Geographic variation in female reproductive characteristics and egg incubation in the Chinese skink, Eumeces chinensis. Chin J Appl Ecol, 13: 680–684
Ji X., Wang Y. Z., Wang Z. 2009. New species of Phrynocephalus (Squamata, Agamidae) from Qinghai, Northwest China. Zootaxa, 1988: 61–68
Jin Y. T., Li L. Q., Liu N. F. 2013. Elevation-related variation in life history traits among Phrynocephalus lineages on the Tibetan Plateau: Do they follow typical squamate ecogeographic patterns??J Zool, 290: 293–301
Li C., Lian X., Bi J. H., Fang H., Maul T. L., Jiang Z. G. 2011. Effects of sand grain size and morphological traits on running speed of toad-headed lizard Phrynocephalus frontalis. J Arid Environ, 75: 1038–1042
Li H., Ding G. H., Zhou Z. S., Ji X. 2013. Fluctuations in incubation temperature affect incubation duration but not morphology, locomotion and growth of hatchlings in the sand lizard Lacerta agilis (Lacertidae). Acta Zool (Stockholm), 94: 11–18
Li H., Wang Z., Chen C., Ji X. 2012. Does the variance of incubation temperatures always constitute a selective force for the origin of reptilian viviparity? Curr Zool, 58: 812–819
Lin L. H., Ma X. M., Li H., Ji X. 2010. Phenotypic variation in hatchling Chinese ratsnakes (Zaocys dhumnades) from eggs incubated at constant temperatures. J Therm Biol, 35: 28–33
Noble D., Qi Y., Fu J. Z. 2010. Species delineation using Bayesian model-based assignment tests: A case study using Chinese toad-headed agamas (genus Phrynocephalus). BMC Evol Biol, 10: 197
Qi Y., Wan H. F., Gu H. J., Wang Y. Z. 2011. Do displays and badges function in establishing the social structure of male toad-headed lizards, Phrynocephalus vlangalii??J Ethol, 29: 381–387
Qu Y. F., Gao J. F., Mao L. X., Ji X. 2011a. Sexual dimorphism and female reproduction in two sympatric toad-headed lizards, Phrynocephalus frontalis and P. versicolor (Agamidae). Anim Biol, 61: 139–151
Qu Y. F., Li H., Gao J. F., Ji X. 2011b. Embryonic thermosensitivity and hatchling morphology differ between two coexisting lizards. Acta Oecol, 37: 375–380
Qu Y. F., Li H., Gao J. F., Xu X. F., Ji X. 2011c. Thermal preference, thermal tolerance and the thermal dependence of digestive performance in two coexisting Phrynocephalus lizards (Agamidae), with a review of species studied. Curr Zool, 57: 684–700
Shu L., Zhang Q. L., Qu Y. F., Ji X. 2011. Thermal tolerance, selected body temperature thermal dependence of food assimilation and locomotor performance in the Qinghai toad-headed lizard, Phrynocephalus vlangalii. Acta Ecol Sin, 30: 2036–2042
Sun B. J., Li S. L., Xu X. F., Zhao W. G., Luo L. G., Ji X., Du W. G. 2013. Different mechanisms lead to convergence of reproductive strategies in two lacertid lizards (Takydromus wolteri and Eremias argus). Oecologia, 172: 645–652
Sun Y. Y., Du Y., Yang J., Fu T. B., Lin C. X., Ji X. 2012. Is the evolution of viviparity accompanied by a relative increase in maternal abdomen size in lizards? Evol Biol, 39: 388–399
Tang X. L., Yue F., Ma M., Wang N. B., He J. Z., Chen Q. 2012. Effects of thermal and hydric conditions on egg incubation and hatchling phenotypes in two Phrynocephalus lizards. Asian Herpetol Res, 3: 184–191
Wang Y. J., Li W. H., Zhao W., Yu N. N., Liu, N. F. 2011. Geographic variation in clutch size and egg size for the lizard Phrynocephalus prezewalskii (Squamata: Agamidae). Asian Herpetol Res, 2: 97–102
Wang Y. Z., Fu J. Z. 2004. Cladogenesis and vicariance patterns in the toad-headed lizard Phrynocephalus versicolor species complex. Copeia, 2004: 199–206
Wang Y. Z., Zeng X. M., Fang Z. L., Liu Z. J., Wu G. F., Papenfuss T. J., Macey R. J. 1996. A new species of Phrynocephalus: Phrynocephalus zetanensis sp. nov. Zool Res, 17(1): 27–29
Wang Y. Z., Zeng X. M., Fang Z. L., Wu G. F. 1999. Study on the relationships of classification, phylogenetics, and distribution of the genus Phrynocephalus spp. (Sauria: Agamidae), with the paleogeographic changes during Cenozoic era in Tibet plateau. Zool Res, 20 (3): 178–185
Wang Y. Z., Zeng X. M., Fang Z. L., Wu G. F., Liu Z. J., Papenfuss T. J., Macey R. J. 2002. A valid species of the genus Phrynocephalus: P. putjatia and a discussion on taxonomy of Phrynocephalus hongyuanensis (Sauria: Agamidae). Acta Zootaxon Sin, 27: 372–383
Wang Z., Lu H. L., Ma L., Ji X. 2013a. Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. Oecologia, doi:10.1007/s00442-013-2811-8
Wang Z., Lu H. L., Ma L., Ji X. 2013b. Differences in thermal preference and tolerance among three Phrynocephalus lizards (Agamidae) with different body sizes and habitat use. Asian Herpetol Res, 4: 214–220
Zeng Z. G., Zhao J. M., Sun B. J. 2013. Life history variation among geographically close populations of the toad-headed lizard (Phrynocephalus przewalskii): Exploring environmental and physiological associations. Acta Oecol, 51: 28–33
Zhang X. D., Ji X., Luo L. G., Gao J. F., Zhang L. 2005. Sexual dimorphism and female reproduction in the Qinghai toad-headed lizard Phrynocephalus vlangalii. Acta Zool Sin, 51: 1006–1012
Zhao K. T. 1999. Phrynocephalus Kaup, 1825. In Zhao E. M., Zhao K. T., Zhou K. Y. (Eds.), Fauna Sinica, Reptilia (Squamata: Lacertilia), Vol. 2. Beijing: Science Press, 151?193

更新日期/Last Update: 2016-01-25