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Am Nat. 2013 Aug;182(2):223-33. doi: 10.1086/670809. Epub 2013 Jun 18.

Stage dependence of phenotypical and phenological maternal effects: insight into squamate reptile reproductive strategies.

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Centre d'Etudes Biologiques de Chizé, Centre National de la Recherche Scientifique (CNRS) Unité Propre de Recherche 1934, 79360 Villiers en Bois, France.


Enhanced thermal conditions have been credited as a driving force for the evolution of viviparity, particularly in squamate reptiles, among which it has independently evolved more than 100 times. However, maternal thermoregulation is also a critical component of reproduction in oviparous squamates, for which considerable embryonic development occurs prior to oviposition. When carrying eggs, oviparous mothers modify thermoregulation in a manner similar to that of pregnant females. To further understand the role of temperature in influencing reproductive strategies, it is critical that we elucidate the degree to which thermal sensitivity varies across developmental stages. We studied stage-dependent embryonic sensitivity in a viviparous snake, the aspic viper (Vipera aspis). We manipulated female body temperature at different stages of pregnancy-early development, early embryonic growth, and late embryonic growth-by imposing two contrasting daily thermal cycles that mimicked reproductive (warm) and nonreproductive (cool) female temperature profiles. Thermal sensitivity of offspring phenotype was stage dependent, with offspring quality more negatively affected when exposure to cool temperatures occurred early in development. In contrast, developmental rate was slowed by the cooler cycle, independent of the timing of the exposure. Given the more persistent effect on phenology, phenological effects likely provide a greater driving force for complete embryonic retention (i.e., viviparity).

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