Embryonic responses to variation in oviductal oxygen in the lizard Sceloporus undulatus from New Jersey and South Carolina, USA

Viviparity in reptiles is hypothesized to evolve in cold climates at high latitudes and high elevations through selection for progressively longer periods of egg retention. Oxygen consumption of embryos increases during development and therefore longer periods of egg retention should be associated with maternal or embryonic features that enhance embryonic oxygen availability. We tested the hypotheses that embryos of the oviparous lizard Sceloporus undulatus from a high-latitude population in New Jersey are oviposited at more advanced developmental stages and have a higher growth rate at low oxygen partial pressures ( p O₂) than embryos from a low-latitude population in South Carolina. These hypotheses were rejected; embryos from the two populations did not differ in embryonic stage at oviposition, survival, rate of differentiation or growth in mass when incubated under simulated in utero conditions at low oxygen concentrations. We also estimated the effective p O₂ experienced by lizard embryos in utero . At an effective p O₂ of 8.6 kPa (9% O₂), development of S. undulatus embryos is arrested at Dufaure and Hubert stage 30 and at a dry mass of 0.8 mg. Physiological and morphological features of gravid females, embryos, or both, that facilitate oxygen uptake for developing embryos appear to be a critical early step during the evolution of reptilian viviparity. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 289–299.     

Evolution of viviparity in sceloporine lizards: in utero PO2 as a developmental constraint during egg retention

Reptilian viviparity evolves through selection for increasingly prolonged egg retention within the oviduct. In the majority of sceloporine lizard species, however, egg retention past the normal time of oviposition results in retarded or arrested embryonic development. In this study, we tested the hypothesis that the amount of embryonic development normally attained in utero is directly related to in utero oxygen partial pressure (PO(2)). The three species of sceloporine lizards we used are characterized by developmental arrest (Urosaurus ornatus), retarded development (Sceloporus virgatus), and normal development (Sceloporus scalaris) when eggs are retained. We incubated eggs of these species for 10 d under conditions that simulated retention in the oviduct at a range of experimental oxygen partial pressures (PO(2)). We estimated in utero PO(2) from a standard curve generated from the stage and dry mass of experimental embryos incubated for 10 d at known PO(2). The standard curve was then used to predict the PO(2) associated with the observed rate of development of embryos retained in utero. The results of this study showed that the degree of embryonic development attained in utero during egg retention was positively associated with in utero PO(2). The results indicate that oxygen availability in utero is associated with interspecific differences in the capacity to support intrauterine development in sceloporine lizards.     

Plasticity and limitations of extended egg retention in oviparous Zootoca vivipara (Reptilia: Lacertidae)

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. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 75–82.     

Does reduction of the eggshell occur concurrently with or subsequent to the evolution of viviparity in phrynosomatid lizards?

Viviparity and placentation have evolved many times within squamate reptiles, but the sequence in which the attendant morphological modifications occur remains unclear. In particular, it is unknown whether a reduction of the egg shell occurs concurrently with longer periods of egg retention (i.e. increasingly advanced stages of embryogenesis at oviposition) or whether such thinning occurs after viviparity has evolved. To investigate this question, we evaluated the prediction that shell morphology and permeability vary systematically with the capacity to support embryonic development in utero (as judged by the maximum embryonic stage attainable in utero) in five species of oviparous sccloporine lizards and one lizard species in the sister genus Urosuarus. Despite major differences among species in the capacity to support embryogenesis, shell morphology (structure, thickness) and physiology (permeability to water vapour) did not vary as predicted. These results raise the intriguing possibility that other features associated with simple placentation (e.g. increased oviductal and chorioallantoic vascular density) evolve concurrently with longer periods of egg retention and viviparity and that shell thinning may occur subsequent to the evolution of viviparity, at least in sceloporine lizards.     

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

The evolution of reptilian viviparity is favoured, according to the cold‐climate 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.     

THE PHYSIOLOGICAL ECOLOGY OF REPTILIAN EGGS AND EMBRYOS. AND THE EVOLUTION OF VIVIPARITY WITHIN THE CLASS REPTILIA

1. Eggs of Crocodilia and Chelonia, like those of birds, have a pair of egg membranes separating a thick layer of albumen from the calcareous shell. In contrast, eggs of oviparous Lepidosauria have only a single shell membrane, upon which relatively small amounts of calcium carbonate are deposited; and the volume of albumen in eggs is extraordinarily small at the time of oviposition. 2. With the possible exception of certain geckos and some chelonians, eggs of oviparous reptiles seem always to absorb water from the substrate during the course of normal incubation. In so far as the rate of water absorption exceeds the rate of water loss by transpiration from exposed surfaces, the eggs swell during incubation. The term ‘cleidoic’ cannot be used to describe eggs of this type. 3. Embryos of lizards and snakes influence the water potential of extra-embryonic fluids contained within their eggs, thereby maintaining or increasing the gradient in water potential that drives water absorption. 4. Embryos of Crocodilia and Chelonia obtain a substantial portion of the calcium used in ossification of skeletal elements from the inner surfaces of the eggshell. In contrast, embryonic lizards and snakes draw upon extensive reserves of calcium present in the yolk, and obtain little (if any) calcium from the eggshell. 5. All reptilian embryos seem to produce substantial quantities of urea as a detoxification product of protein catabolism. Contrary to expectation, uricotelism may not be common among reptilian embryos, even in those few instances where development takes place within a hard, calcareous egg. 6. In eggs of Crocodilia and Chelonia, respiratory gases seem to pass by diffusion through pores in the calcareous eggshell and through spaces between the fibres of the pair of egg membranes. No pores have been observed in the shell of lepidosaurian eggs, and so gases presumably diffuse between the fibres of the single (multilayered) shell membrane. 7. Metabolism of reptilian embryos is temperature-dependent, as is true for most ectothermic organisms. For each species, there appears to be a particular temperature at which embryonic development proceeds optimally, and departures from this optimum elicit increases in developmental anomalies and/or embryonic mortality. 8. Viviparity has evolved on numerous occasions among species of the Squamata, but seemingly never among Crocodilia or Chelonia. Since the evolution of viviparity entails a progressive reduction in the eggshell, only those organisms whose embryos do not depend upon the eggshell as a source of calcium may have the evolutionary potential to become viviparous. 9. Evolutionary transitions from oviparity to viviparity could have been driven by selection related to (i) thermal benefits to embryos consequent upon retention of eggs within the body of a parent capable of behavioural thermoregulation; (ii) protection of the eggs from nest predators and/or soil microbes; and (iii) more effective exploitation of a seasonal food resource by early emerging young.     

Placental calcium provision in a lizard with prolonged oviductal egg retention

A prominent scenario for the evolution of viviparity and placentation in reptiles predicts a step-wise pattern with an initial phase of prolonged oviductal egg retention accompanied by progressive reduction in eggshell thickness culminating in viviparity; calcium placentotrophy evolves secondarily to viviparity. Saiphos equalis is an Australian scincid lizard with a reproductive mode that is uncommon for squamates because eggs are retained in the oviduct until late developmental stages, and the embryonic stage at oviposition varies geographically. We studied calcium mobilization by embryos in two populations with different oviductal egg retention patterns to test the hypothesis that the pattern of nutritional provision of calcium is independent of the embryonic stage at oviposition. Females from one population are viviparous and oviposit eggs containing fully formed embryos, whereas embryos in oviposited eggs of the second population are morphologically less mature, and these eggs hatch several days later. The reproductive mode of this population is denoted as prolonged oviductal egg retention. Yolk provided the highest proportion of calcium to hatchlings in both populations. Eggs of both populations were enclosed in calcified eggshells, but shells of the population with prolonged egg retention had twice the calcium content of the viviparous population and embryos recovered calcium from these eggshells. Placental transfer accounted for a substantial amount of calcium in hatchlings in both populations. Hatchling calcium concentration was higher in the population with prolonged egg retention because these embryos mobilized calcium from yolk, the eggshell and the placenta. This pattern of embryonic calcium provision in which both a calcified eggshell and placentotrophy contribute to embryonic nutrition is novel. The reproductive pattern of S. equalis illustrates that calcified eggshells are compatible with prolonged oviductal egg retention and that viviparity is not requisite to calcium placentotrophy.     

Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention

The evolutionary transition between oviparity and viviparity in squamate reptiles presumably occurs via a gradual increase in the duration of egg retention, the production of thinner eggshells, and increases in the vascularity of maternal and embryonic tissues. The 'ease' of this transition may differ among taxa. For example, in the genus Sceloporus , the scalaris species group contains both oviparous and viviparous species, and female Sceloporus scalaris can extend egg retention facultatively in response to the absence of a suitable site for oviposition without impairing embryonic development. In contrast, the undulatus species group contains only oviparous species, and, while female Sceloporus virgatus can extend egg retention, doing so retards embryonic development. I tested several hypotheses that would explain the greater ability of 5. scalaris than S. virgatus to extend egg retention. In this study, female S. scalaris retained eggs for 19 d without affecting the mortality of embryos, total developmental time, or dry mass of hatchlings. In contrast, when female S. virgatus retained eggs for 18 d, embryos had very high mortality and eggs took significantly longer to hatch than control (non-retained) eggs, although the dry mass of hatchlings was not affected. The ability of S. scalaris females to retain eggs with little negative effect on embryonic development was associated with relatively large chorioallantois, relatively thin eggshells, and relatively small clutch masses. These observations suggest that phylogenetic differences in the ability to extend egg retention may facilitate or constrain the evolution of viviparity in some lineages.     

Fetal nutrition in lecithotrophic squamate reptiles: Toward a comprehensive model for evolution of viviparity and placentation

The primary pattern of embryonic nutrition for squamate reptiles is lecithotrophy; with few exceptions, all squamate embryos mobilize nutrients from yolk. The evolution of viviparity presents an opportunity for an additional source of embryonic nutrition through delivery of uterine secretions, or placentotrophy. This pattern of embryonic nutrition is thought to evolve through placental supplementation of lecithotrophy, followed by increasing dependence on placentotrophy. This review analyzes the relationship between reproductive mode and pattern of embryonic nutrition in three lecithotrophic viviparous species, and oviparous counterparts, for concordance with a current model for the evolution of viviparity and placentation. The assumptions of the model, that nutrients for oviparous embryos are mobilized from yolk, and that this source is not disrupted in the transition to viviparity, are supported for most nutrients. In contrast, calcium, an essential nutrient for embryonic development, is mobilized from both yolk and eggshell by oviparous embryos and reduction of eggshell calcium is correlated with viviparity. If embryonic fitness is compromised by disruption of a primary source of calcium, selection may not favor evolution of viviparity, yet viviparity has arisen independently in numerous squamate lineages. Studies of fetal nutrition in reproductively bimodal species suggest a resolution to this paradox. If uterine calcium secretion occurs during prolonged intrauterine egg retention, calcium placentotrophy evolves prior to viviparity as a replacement for eggshell calcium and embryonic nutrition will not be compromised. This hypothesis is integrated into the current model for evolution of viviparity and placentation to address the unique attributes of calcium nutrition. The sequence of events requires a shift in timing of uterine calcium secretion and the embryonic mechanism of calcium retrieval to be responsive to calcium availability. Regulation of uterine calcium secretion and the mechanism of embryonic uptake of calcium are important elements to understanding evolution of viviparity and placentation. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Potential targets for selection during the evolution of viviparity in cold-climate reptiles

Viviparity (live-bearing) has evolved from oviparity (egg-laying) in more than 100 lineages of squamate reptiles (lizards and snakes). This transition generally has occurred in cool climates, where thermal differentials between eggs in the (cool) nest versus the (warm) maternal oviduct influence embryonic development, in ways that may enhance offspring fitness. To identify specific traits potentially under selection, we incubated eggs of a montane scincid lizard at conditions simulating natural nests, maternal body temperatures, and an intermediate stage (2-week uterine retention of eggs prior to laying). Incubation at maternal temperatures throughout incubation affected the hatchling lizard’s activity level and boldness, as well as its developmental rate, morphology, and locomotor ability. A treatment that mimicked the initial stages of the transition toward viviparity had a major effect on some hatchling traits (locomotor speeds), a minor effect on others (tail length, total incubation period) and no effect on yet others (offspring behaviors). More generally, different aspects of the phenotype are sensitive to incubation conditions at different stages of development; thus, the evolution of reptilian viviparity may have been driven by a succession of advantages that accrued at different stages of embryogenesis.     

Arrested embryonic development: a review of strategies to delay hatching in egg-laying reptiles

Arrested embryonic development involves the downregulation or cessation of active cell division and metabolic activity, and the capability of an animal to arrest embryonic development results in temporal plasticity of the duration of embryonic period. Arrested embryonic development is an important reproductive strategy for egg-laying animals that provide no parental care after oviposition. In this review, we discuss each type of embryonic developmental arrest used by oviparous reptiles. Environmental pressures that might have directed the evolution of arrest are addressed and we present previously undiscussed environmentally dependent physiological processes that may occur in the egg to bring about arrest. Areas for future research are proposed to clarify how ecology affects the phenotype of developing embryos. We hypothesize that oviparous reptilian mothers are capable of providing their embryos with a level of phenotypic adaptation to local environmental conditions by incorporating maternal factors into the internal environment of the egg that result in different levels of developmental sensitivity to environmental conditions after they are laid.     

Influence of the evolution of viviparity on eggshell morphology in the lizard Lerista bougainvillii

In reptiles, the evolutionary transition from egg-laying to live-bearing is thought to involve a gradual increase in the duration of egg retention, with progressively more development occurring prior to oviposition, and culminating in the birth of fully developed offspring. However, prolonging the retention of fully-shelled eggs within the oviducts may pose serious gas-exchange problems for the embryos. Thus, evolutionary increases in the period of intrauterine retention may require correlated decreases in the thickness of eggshells and/or their degree of calcification to allow for adequate embryonic gas exchange. To test this evolutionary model, eggs of three distinct reproductive forms of the scincid lizard Lerista bougainvillii were examined to determine the evolutionary relationships between the thickness of the shell membrane, degree of eggshell calcification, and the duration of uterine egg retention. These comparisons revealed the predicted pattern of correlated shifts in eggshell morphology and embryonic stage at oviposition. Evolutionary increases in the duration of egg retention were accompanied by decreases in the thickness of the eggshell membrane and degree of eggshell calcification. This evolutionary model suggests that there may be a tradeoff between the advantages of extended egg retention and the disadvantages of a thinner eggshell. On the basis of this tradeoff, I propose that oviparous taxa with relatively thin eggshells may be preadapted to evolve viviparity. Comparative examination of the limited data available on eggshell thickness in lizards supports this possibility. © 1996 Wiley-Liss, Inc.     

Seasonal shifts along the oviparity–viviparity continuum in a cold‐climate lizard population

Squamate embryos require weeks of high temperature to complete development, with the result that cool climatic areas are dominated by viviparous taxa (in which gravid females can sun‐bask to keep embryos warm) rather than oviparous taxa (which rely on warm soil to incubate their eggs). How, then, can some oviparous taxa reproduce successfully in cool climates – especially late in summer, when soil temperatures are falling? Near the northern limit of their distribution (in Sweden), sand lizards (Lacerta agilis) shift tactics seasonally, such that the eggs in late clutches complete development more quickly (when incubated at a standard temperature) than do those of early clutches. That acceleration is achieved by a reduction in egg size and by an increase in the duration of uterine retention of eggs (especially, after cool weather). Our results clarify the ability of oviparous reptiles to reproduce successfully in cool climates and suggest a novel advantage to reptilian viviparity in such conditions: by maintaining high body temperatures, viviparous females may escape the need to reduce offspring size in late‐season litters.     

Ionic and osmotic environment of developing elasmobranch embryos

Synopsis The elasmobranchs display a variety of ionic and osmotic environments for developing embryos. Oviparous species protect their eggs with a tough, fibrous capsule which is highly permeable to ions and urea even at oviposition. Thus the embryonic tissues are bathed by a solution ionically similar to sea water. In the more advanced reproductive style ofSqualus acanthias (a lecithotrophic live bearer) early embryos in egg capsules are retained in utero and bathed in a solution osmotically similar to maternal plasma. Several months into the 22 month gestation period the embryos can iono- and osmoregulate in a uterine solution resembling sea water. Embryos of more advanced viviparous species develop in a solution that is ionically and osmotically similar to maternal plasma. Iono- and osmoregulation by these embryos would appear to be unnecessary. Clearly, in the oviparous elasmobranchs, the ability of the embryo to regulate salts and urea is present at the earliest stage of development. The need for elasmobranch embryos to regulate osmolytes was reduced or delayed as viviparity evolved.     

Gold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus

Evolutionary origins of viviparity among the squamate reptiles are strongly associated with cold climates, and cold environmental temperatures are thought to be an important selective force behind the transition from egg-laying to live-bearing. In particular, the low nest temperatures associated with cold climate habitats are thought to be detrimental to the developing embryos or hatchlings of oviparous squamates, providing a selective advantage for the retention of developing eggs in utero, where the mother can provide warmer incubation temperatures for her eggs (by actively thermoregulating) than they would experience in a nest. However, it is not entirely clear what detrimental effects cold incubation temperatures may have on eggs and hatchlings, and what role these effects may play in favouring the evolution of viviparity. Previous workers have suggested that viviparity may be favoured in cold climates because cold incubation temperatures slow cmbryogenesis and delay hatching of the eggs, or because cold nest temperatures are lethal to developing eggs and reduce hatching success. However, incubation temperature has also been shown to have other, potentially long-term, effects on hatchling phcnotypcs, suggesting that cold climates may favour viviparity because cold incubation temperatures produce offspring of poor quality or low fitness. We experimentally incubated eggs of the oviparous phrynosomatid lizard, Sceloporus virgatus, at temperatures simulating nests in a warm (low elevation) habitat, as is typical for this species, and nests in a colder (high elevation) habitat, to determine the effects of cold incubation temperatures on embryonic development and hatchling phenotypes. Incubation at cold nest temperatures slowed embryonic development and reduced hatching success, but also affected many aspects of the hatchlings' phenotypes. Overall, the directions of these plastic responses indicated that cold-incubated hatchlings did indeed exhibit poorer quality phenotypes; they were smaller at hatching (in body length) and at 20 days of age (in length and mass), grew more slowly (in length and mass), had lower survival rates, and showed greater fluctuating asymmetry than their conspecifics that were incubated at warmer temperatures. Our findings suggest that cold nest temperatures are detrimental to S. virgatus, by delaying hatching of their eggs, reducing their hatching success, and by producing poorer quality offspring. These negative effects would likely provide a selective advantage for any mechanism through which these lizards could maintain warmer incubation temperatures in cold climates, including the evolution of prolonged egg retention and viviparity.     

Thermal acclimation of heart rates in reptilian embryos

In many reptiles, the thermal regimes experienced by eggs in natural nests vary as a function of ambient weather and location, and this variation has important impacts on patterns of embryonic development. Recent advances in non-invasive measurement of embryonic heart rates allow us to answer a long-standing puzzle in reptilian developmental biology: Do the metabolic and developmental rates of embryos acclimate to local incubation regimes, as occurs for metabolic acclimation by post-hatching reptiles? Based on a strong correlation between embryonic heart rate and oxygen consumption, we used heart rates as a measure of metabolic rate. We demonstrate acclimation of heart rates relative to temperature in embryos of one turtle, one snake and one lizard species that oviposit in relatively deep nests, but found no acclimation in another lizard species that uses shallow (and hence, highly thermally variable) nests. Embryonic thermal acclimation thus is widespread, but not ubiquitous, within reptiles.     

Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity

Viviparity in squamate reptiles is presumed to evolve in cold climates by selection for increasingly longer periods of egg retention. Longer periods of egg retention may require modifications to other reproductive features associated with the evolution of viviparity, including a reduction in eggshell thickness and clutch size. Field studies on the thermal and reproductive biology of high (HE) and low (LE) elevation populations of the oviparous lizard, Sceloporus scalaris, support these expectations. Both day and night-time temperatures at the HE site were considerably cooler than at the LE site, and the activity period was 2 h shorter at the HE than at the LE site. The median body temperature of active HE females was 2°C lower than that of LE females. HE females initiated reproduction earlier in the spring than LE females, apparently in order to compensate for relatively low temperatures during gestation. HE females retained eggs for about 20 days longer than LE females, which was reflected by differences in the degree of embryonic development at the time of oviposition (stages 35.5–37.0 versus stages 31.0–33.5, respectively). These results support the hypotheses that evolution of viviparity is a gradual process, and is favored in cold climates. Females in the HE population exhibited other traits consistent with presumed intermediate stages in the evolution of viviparity; mean eggshell thickness of HE eggs (19.3 m) was significantly thinner than that of LE eggs (26.6 m) and the size-adjusted clutch sizes of HE females (9.4) were smaller than those of LE females (11.2).     

Incubation time in reptilian eggs

An allometric analysis of reptilian incubation time was performed. Incubation time increased with increasing egg mass (allometric exponent = 0.14, r²= 0.31). However, significant heterogeneity was found within the Reptilia for this character. If periods of developmental arrest are excluded the orders Crocodylia, Testudinata, and the suborder Serpentes have the shortest incubation times and the lizards the longest. Significant differences within lizard families were also observed (Iguanidae, Agamidae, Gekkonidae, and Lacertidae have shorter incubation times than the Varanidae and Teiidae). Preliminary analyses indicate the heterogeneity in incubation time observed within the Squamata is correlated with differences in brain mass; this is similar to findings for mammals. The variation in incubation time indicates the existence of differences in growth rates in reptilian groups and suggests a partial explanation for the observed distribution of viviparity within the Squamata.     

Reptilian viviparity in cold climates: testing the assumptions of an evolutionary hypothesis

Viviparity (live-bearing) in reptiles often is interpreted as an adaptation to cold climates. This hypothesis relies on (i) body temperatures of gravid females being higher than soil (nest) temperatures; (ii) embryonic development being accelerated by this temperature difference; and (iii) survivorship of hatchlings being increased if eggs hatch before the advent of cold weather in autumn. I gathered data to test these assumptions, using eight species of scincid lizards in a high-elevation area of southeastern Australia. Due to behavioural thermoregulation, body temperatures of gravid lizards average ca. 7°C higher than soil (nest) temperatures. Oviparous female lizards retain eggs in utero for ca. 50% of development. Laboratory studies show that a temperature increase from 17°C (mean nest temperature) to 24°C (mean lizard temperature) reduces incubation periods of eggs by >40 days in heliothermic species, and <20 days in a thigmothermic species. In the field, soil temperatures drop to lethally low levels shortly after the usual time of hatching. Simple calculations show that without the acceleration of development caused by uterine retention, eggs could not hatch prior to the onset of these low temperatures in the field. These results support the major assumptions of the “cold climate hypothesis” for the evolution of reptilian viviparity.