Altitudinal variation in egg retention and rates of embryonic development in oviparous Zootoca vivipara fits predictions from the cold‐climate model on the evolution of viviparity

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.

Adaptive responses to cool climate promotes persistence of a non-native lizard

“…from 15 May to 15 September). While embryo retention and faster developmental rate have evolved repeatedly in lizards in cool climates [21][22][23][24], our results demonstrate that such adaptations can arise very rapidly. Extant wall lizard populations in England were introduced less than 100 years ago, with the target populations tracing their origins back to between two and eight decades [15].…”

Variation of Reproductive Traits and Female Body Size in the Most Widely-Ranging Terrestrial Reptile: Testing the Effects of Reproductive Mode, Lineage, and Climate

“…We note, however, that in several cases where two samples from contrasting environments were obtained within the same primary study (samples 4 vs. 5 in French Pyrenees; 24 vs. 25 in the east of European Russia—“Appendix”; southern Sweden vs. northern Sweden—Uller and Olsson 2003), hatchling mass was higher in colder climates. At the same time, hatchlings from females coming from higher vs. lower latitudes in West Siberian plain (samples 30–32 vs. 33–36—“Appendix”), and higher versus lower altitudes in northern Spain (Rodríguez-Díaz and Braña 2012), did not differ in their mass. Thus, the available data on geographic variation of hatchling mass in Z. vivipara provide no unequivocal support for Prediction 6.…”

“…Data for stages are from Heulin et al (2002), Lindtke et al (2010) (EO clade), Braña et al (1991), Rodríguez-Díaz and Braña (2012) (WO clade), stage 40 corresponds to fully developed newborns (Dufaure and Hubert 1961). Data for hatchling mass are from “Appendix”…”

“…Eggs laid by the oviparous Z. vivipara females possess true eggshell but contain embryos at later developmental stages than the freshly laid eggs of most other lacertid lizard species and have a relatively short incubation period of 26–37 days (Braña et al 1991; Heulin et al 2002; Lindtke et al 2010; Rodríguez-Díaz and Braña 2012). …”

“…The emerging body size cline corresponds to Bergmann’s rule (larger body size in colder climates: Blackburn et al 1999), but the underlying mechanism is a direct response to environmental constraint rather than genetic divergence (Adolph and Porter 1996). In Z. vivipara , a marginally significant Bergmann’s cline was reported for altitudinal variation within an oviparous clade in northern Spain (Rodríguez-Díaz and Braña 2012). We tested whether this trend is consistent across the whole range (Prediction 4).…”