No abstract

The evolution of reptilian viviparity is favoured, according to the coldclimate hypothesis, at high latitudes or altitudes, where egg retention would entail thermal benefits for embryogenesis because of maternal thermoregulation. According to this hypothesis, and considering that viviparity would have evolved through a gradual increase in the extent of intrauterine egg retention, highland oviparous populations are expected to exhibit more advanced embryo development at oviposition than lowland populations. We tested for possible differences in the level of egg retention, embryo development time and thermal biology of oviparous Zootoca vivipara near the extreme altitudinal limits of the species distribution in the north of Spain (mean altitude for lowland populations, 235 m asl.; for highland populations, 1895 m asl.). Altitude influenced neither temperature of active lizards in the field nor temperature selected by lizards in a laboratory thermal gradient, and pregnant females selected lower temperatures in the thermal gradient than did males and nonpregnant females across altitudinal levels. Eggs from highland populations contained embryos more developed at the time of oviposition (Dufaure and Hubert's stages 33-35) than eggs of highland populations (stages 30-34) and partly because of this difference incubation time was shorter for highland embryos. When analysed for clutches from both altitudinal extremes at the same embryonic stage at oviposition (stage 33), again incubation time was shorter for highland populations, indicating genuine countergradient variation in developmental rate. Our results indicate that temperature is an environmental factor affecting the geographical distribution of different levels of egg retention in Z. vivipara, as predicted by the cold-climate hypothesis on the evolution of viviparity.

Pregnant female Zootoca vivipara select lower body temperatures than males or nonpregnant females, and this shift in the thermal preferendum is believed to be related to optimising the conditions for embryogenesis. Thus, subjecting embryos to the higher temperature selected by males and non-gravid females might have detrimental effects on embryonic development and on hatchling fitness, according to predictions of the ''maternal manipulation'' hypothesis on the evolution of viviparity. To test the role of gestation environment on embryonic development in oviparous Z. vivipara, we kept a number of gravid females at the temperature selected by non-gravid females in a laboratory thermal gradient, whereas control females were allowed to regulate their body temperature without restrictions. Developmental stage at oviposition was more advanced for embryos of the experimental clutches, which were heavier than those of the control group. Forced gestation temperature also affected hatching success (58.62% in the experimental treatment vs. 97.37% in the control group). In addition, hatchlings from females subjected to high temperatures during pregnancy were smaller, had shorter head length and performed worse in running trials. Our results fulfil the prediction of the ''maternal manipulation'' hypothesis, and suggest that the shift in female body temperature during pregnancy optimizes embryogenesis and hatchling phenotype by avoiding the negative effects of the high incubation temperatures preferred by non-gravid females.

The transition between oviparity and viviparity in reptiles is generally accepted to be a gradual process, the result of selection for increasingly prolonged egg retention within the oviduct. We examined egg retention plasticity in an oviparous strain of the lacertid lizard Zootoca vivipara, a species having both oviparous and viviparous populations. We forced a group of female Z. vivipara to retain their clutch in utero by keeping them in dry substrata, and assessed the effect on embryonic development and hatching success, along with offspring phenotype and locomotor performance. Forced egg retention for one additional week affected the developmental stage of embryos at oviposition, as well as hatchling robustness and locomotor performance. However, embryos from forced clutch retention treatment reached one stage unit more than control embryos at oviposition time. Embryos from control eggs were more developed than embryos from experimental eggs after approximately the same period of external incubation, showing that embryonic development is retarded during the period of extended egg retention, despite the high temperature inside the mother's body. Significant differences in external incubation time were only found in one of the two years of study. Hatching success was much lower in the experimental group with forced egg retention (21.1%) than in the control group (95.4%). Therefore, we conclude that there are limitations that hinder the advance of intrauterine embryonic development beyond the normal time of oviposition, and that extended egg retention does not represent clear advantages in this population of Z. vivipara. Nevertheless, the fact that some eggs are successful after forced egg retention could be advantageous for the females that are able to retain their clutch under unfavourable climatic conditions.