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

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.

Climate change, thermal niches, extinction risk and maternal‐effect rescue of toad‐headed lizards, Phrynocephalus, in thermal extremes of the Arabian Peninsula to the Qinghai—Tibetan Plateau

“…Mode of reproduction was highly correlated with elevation (Table 2c), with viviparous species occurring at higher elevations than oviparous species. This result supports the hypothesis that once viviparity evolved in Phrynocephalus it was adaptive (Wang et al 2014) on the Qinghai-Tibetan Plateau. Our result is also consistent with the cold-climate hypothesis (Shine 1985) for spread of viviparity.…”

Thermal constraints and the influence of reproduction on thermoregulation in a high‐altitude gecko (Quedenfeldtia trachyblepharus)

“…More efficient thermoregulation by gravid females may allow their offspring to hatch early. More generally, modified thermoregulation, particularly during reproduction, may be a key aspect allowing terrestrial ectotherms to exploit cold climates (Lourdais et al ., ; Wang et al ., ). Empirical evidence supports the notion that active thermoregulation is prevalent in habitats with low thermal quality (Blouin‐Demers & Nadeau, ).…”

“…Among Iguanidae, Liolaemus reaches the southernmost latitudes in Patagonia and up to 3000 m in the Andes of Northern Chile (Marquet et al, 1989). Finally, the agamid Phrynocephalus vlangalii can reach 4500 m in the Qinghai Tibet Plateau (Wang et al, 2014). Reproductive mode (i.e.…”

“…Reproductive mode (i.e. the evolution of viviparity) and maternal basking strategies play a key role in the adaptation to cold climates (Shine, 1995;Lourdais et al, 2013;Wang et al, 2014). Extended embryonic retention and improved maternal control of developmental temperature likely provide significant advantages over oviparity in cold climates (Arribas & Galan, 2005;Rodriguez-Diaz & Brana, 2012).…”

Impacts of maternal characteristics and temperature on juvenile survival in the crocodile lizard: Implications for conservation

“…In addition, both field observations and experimental manipulations demonstrate that warm climate may advance the timing of reproduction in many other animals, from invertebrates to mammals (Parmesan, 2006(Parmesan, , 2007. This is because increasing temperatures shorten the gestation period through accelerating embryonic developmental processes in both viviparous and oviparous species (Lu, Wang, Tang, & Du, 2013;Ma et al, 2014;Tang et al, 2012;Wang et al, 2016;Wang, Lu, Ma, & Ji, 2013). Nonetheless, early parturition could also be the result of influence from other biotic and abiotic factors (e.g., food availability and genetic variability) that differed in captivity (Du, 2006;Quinn, Unwin, & Kinnison, 2000).…”