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Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation

  • Physiological ecology - Original research
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Abstract

Viviparous Phrynocephalus lizards (Agamidae) are mainly restricted to the Qinghai-Tibet Plateau of China. In this study, we used Phrynocephalus vlangalii females kept under seven thermal regimes for the whole gestation period to test the hypothesis that viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. All females at 24 °C and 93 % of the females at 28 °C failed to give birth or produced stillborns, and proportionally fewer females gave birth at 29 or 35 °C than at 32 °C. Though the daily temperatures encountered were unsuitable for embryonic development, 95 % of the females in nature and 89 % of the females thermoregulating in the laboratory gave birth. There was no shift in the thermal preferences of females when they were pregnant. Although thermal conditions inside natural burrows were unsuitable for embryonic development, mass and sprint speed were both greater in neonates produced in nature. Our data show that (1) long-term exposure of P. vlangalii embryos to temperatures outside the range of 29–35 °C may result in the failure of development, but daily or short-term exposure may not necessarily increase embryonic mortality; (2) low gestation temperatures slow but do not arrest embryonic development, and females produce high-quality offspring in the shortest possible time by maintaining gestation temperatures close to the upper thermal limit for embryonic development; and (3) viviparity is currently adaptive at high elevations because embryos in nature cannot fully develop without relying on maternal thermoregulation. Our data validate the hypothesis tested.

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Acknowledgments

Our experimental procedures complied with the current laws on animal welfare and research in China, and were approved by the Animal Research Ethics Committee of Nanjing Normal University (AREC2007-04-012). Funding for this work was supported by grants from the Natural Science Foundation of China (31071910 and 31200282) and Priority Academic Program Development of Jiangsu Higher Education Institutions. We thank Jian-Fang Gao, Ya-Qing Liu, Neng-Hui Sun and Xi-Dong Zhang for their help during the research.

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Authors and Affiliations

  1. Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing, 210046, Jiangsu, China

    Zheng Wang & Xiang Ji

  2. College of Forest Resources and Environment, Nanjing Forestry University, Nanjing, 210037, Jiangsu, China

    Zheng Wang

  3. Hangzhou Key Laboratory for Animal Adaptation and Evolution, School of Life Sciences, Hangzhou Normal University, Hangzhou, 310036, Zhejiang, China

    Hong-Liang Lu & Li Ma

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  1. Zheng Wang
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  2. Hong-Liang Lu
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  4. Xiang Ji
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Correspondence to Xiang Ji.

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Communicated by Raoul Van Damme.

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Wang, Z., Lu, HL., Ma, L. et al. Viviparity in high-altitude Phrynocephalus lizards is adaptive because embryos cannot fully develop without maternal thermoregulation. Oecologia 174, 639–649 (2014). https://doi.org/10.1007/s00442-013-2811-8

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