Lerista bougainvillii,a case study for the evolution of viviparity in reptiles

Many factors, both environmental and biotic, have been suggested to facilitate or hinder the evolution of viviparity (live-bearing) in reptiles. Viviparity has evolved recently within the Australian scincid lizard Lerista bougainvillii and the species includes oviparous, viviparous, and reproductively intermediate (with prolonged egg retention) populations; thus, it offers an exceptional opportunity to evaluate the validity of these hypotheses. We carried out such tests by (i) comparing environmental conditions over the geographic ranges occupied by oviparous, viviparous, and intermediate populations (to identify possible selective forces for the evolution of viviparity), and (ii) comparing morphological, reproductive and ecological traits of L. bougainvillii with those of other sympatric scincid species (to identify traits that may have predisposed this taxon to the evolution of viviparity). The areas occupied by viviparous L. bougainvillii are significantly colder than those occupied by both their intermediate and oviparous conspecifics, in accord with the “cold-climate” hypothesis for reptilian viviparity. Rainfall is similar over the ranges of the three forms. Climatic unpredictability (as assessed by the magnitude of year-to-year thermal variation) is lower for viviparous animals, in contradiction to published speculations. Comparison with 31 sympatric scincid species showed that L. bougainvillii is not atypical for most of the traits we measured (e.g., body size, clutch size, thermal preferenda and tolerances). However, oviparous L. bougainvillii do display several traits that have been suggested to facilitate the evolution of viviparity. For example, pregnancy does not reduce locomotor ability of females; the lizards are semi-fossorial; even the oviparous females produce only a single clutch of eggs per year; and they ovulate relatively late in summer, so that the time available for incubation is limited.     

Length of activity season drives geographic variation in body size of a widely distributed lizard

Understanding the factors that drive geographic variation in life history is an important challenge in evolutionary ecology. Here, we analyze what predicts geographic variation in life‐history traits of the common lizard, Zootoca vivipara, which has the globally largest distribution range of all terrestrial reptile species. Variation in body size was predicted by differences in the length of activity season, while we found no effects of environmental temperature per se. Females experiencing relatively short activity season mature at a larger size and remain larger on average than females in populations with relatively long activity seasons. Interpopulation variation in fecundity was largely explained by mean body size of females and reproductive mode, with viviparous populations having larger clutch size than oviparous populations. Finally, body size‐fecundity relationship differs between viviparous and oviparous populations, with relatively lower reproductive investment for a given body size in oviparous populations. While the phylogenetic signal was weak overall, the patterns of variation showed spatial effects, perhaps reflecting genetic divergence or geographic variation in additional biotic and abiotic factors. Our findings emphasize that time constraints imposed by the environment rather than ambient temperature play a major role in shaping life histories in the common lizard. This might be attributed to the fact that lizards can attain their preferred body temperature via behavioral thermoregulation across different thermal environments. Length of activity season, defining the maximum time available for lizards to maintain optimal performance, is thus the main environmental factor constraining growth rate and annual rates of mortality. Our results suggest that this factor may partly explain variation in the extent to which different taxa follow ecogeographic rules.     

The evolution of viviparity within the Australian scincid lizardLerista bougainvillii

The semi-fossorial scincid lizard, Lerista bougainvillii , is oviparous throughout its extensive range in south-eastern mainland Australia. However, two widely separated (by approximately 1000 km) island populations are viviparous; in these populations the eggshell is lost and females retain their offspring in utero until embryogenesis complete. One mainland population in south-eastern Victoria shows an intermediate condition, in which the eggshells are incomplete and uterine embryogenesis is prolonged.
Morphological and electrophoretic analyses confirm a high degree of morphological and genetic similarity between populations (i.e. there is no evidence for the presence of more than one species), and phenetic analyses of these data show that each of the two disjunct viviparous populations more closely resembles adjacent oviparous populations than the other viviparous group. Hence, we infer that viviparity may have arisen twice within L. bougainvillii , in both cases on offshore islands with a cold climate.     

Incubation regimes of cold-climate reptiles: the thermal consequences of nest-site choice, viviparity and maternal basking

Cold-climate reptiles show three kinds of adaptation to provide warmer incubation regimes for their developing embryos: maternal selection of hot nest sites; prolonged uterine retention of eggs; and increased maternal basking during pregnancy. These traits may evolve sequentially as an oviparous lineage invades colder climates. To compare the thermal consequences of these adaptations, I measured microhabitat temperatures of potential nest sites and actual nests of oviparous scincid lizards ( Bassiana duperreyi ), and body temperatures of pregnant and non-pregnant viviparous scincid lizards ( Eulamprus heatwolei ). These comparisons were made at a site where both species occur, but close to the upper elevational limit for oviparous reptiles in south-eastern Australia. Viviparity and maternal basking effort had less effect on mean incubation temperature than did maternal nest-site selection. Eggs retained in utero experienced bimodal rather than unimodal diel thermal distributions, but similar mean incubation temperatures. Often the published literature emphasizes the ability of heliothermic (basking) reptiles to maintain high body temperatures despite unfavourable ambient weather conditions; this putative ability is central to many hypotheses on selective forces for the evolution of viviparity. In cold climates, however, opportunities for maternal thermoregulation to elevate mean body temperatures (and thus, incubation temperatures) above ambient levels may be severely limited. Hence, at least over the broad elevational range in which oviparous and viviparous species live in sympatry, maternal selection of 'hot' nests may be as effective as is viviparity in providing favourable incubation regimes.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 145–155.     

Intraspecific phylogeography of Lacerta vivipara and the evolution of viviparity

The lacertid lizard Lacerta vivipara is one of the few squamate species with two reproductive modes. We present the intraspecific phylogeny obtained from neighbor-joining and maximum-parsimony analyses of the mtDNA cytochrome b sequences for 15 individuals from Slovenian oviparous populations, 34 individuals from western oviparous populations of southern France and northern Spain, 92 specimens from European and Russian viviparous populations, and 3 specimens of the viviparous subspecies L. v. pannonica. The phylogeny indicates that the evolutionary transition from oviparity to viviparity probably occurred once in L. vivipara. The western oviparous group from Spain and southern France is phylogenetically most closely related to the viviparous clade. However, the biarmed W chromosome characterizing the western viviparous populations is an apomorphic character, whereas the uniarmed W chromosome, existing both in the western oviparous populations and in the geographically distant eastern viviparous populations, is a plesiomorphic character. This suggests an eastern origin of viviparity. Various estimates suggest that the oviparous and viviparous clades of L. vivipara split during the Pleistocene. Our results are discussed in the framework of general evolutionary models: the concept of an oviparity-viviparity continuum in squamates, the cold climate model of selection for viviparity in squamates, and the contraction-expansion of ranges in the Pleistocene resulting in allopatric differentiation.     

A phylogeny of Chinese species in the genus Phrynocephalus (Agamidae) inferred from mitochondrial DNA sequences

We investigated the phylogenetic relationships among most Chinese species of lizards in the genus Phrynocephalus (118 individuals collected from 56 populations of 14 well-defined species and several unidentified specimens) using four mitochondrial gene fragments (12S rRNA, 16S rRNA, cytochrome b, and ND4-tRNA(LEU)). The partition-homogeneity tests indicated that the combined dataset was homogeneous, and maximum-parsimony (MP), neighbor-joining (NJ), maximum-likelihood (ML) and Bayesian (BI) analyses were performed on this combined dataset (49 haplotypes including outgroups for 2058bp in total). The maximum-parsimony analysis resulted in 24 equally parsimonious trees, and their strict consensus tree shows that there are two major clades representing the Chinese Phrynocephalus species: the viviparous group (Clade A) and the oviparous group (Clade B). The trees derived from Bayesian, ML, and NJ analyses were topologically identical to the MP analysis except for the position of P. mystaceus. All analyses left the nodes for the oviparous group, the most basal clade within the oviparous group, and P. mystaceus unresolved. The phylogenies further suggest that the monophyly of the viviparous species may have resulted from vicariance, while recent dispersal may have been important in generating the pattern of variation among the oviparous species.     

Intraspecific Phylogeography of Lacerta vivipara and the Evolution of Viviparity

The lacertid lizard Lacerta vivipara is one of the few squamate species with two reproductive modes. We present the intraspecific phylogeny obtained from neighbor-joining and maximum-parsimony analyses of the mtDNA cytochrome b sequences for 15 individuals from Slovenian oviparous populations, 34 individuals from western oviparous populations of southern France and northern Spain, 92 specimens from European and Russian viviparous populations, and 3 specimens of the viviparous subspecies L. v. pannonica. The phylogeny indicates that the evolutionary transition from oviparity to viviparity probably occurred once in L. vivipara. The western oviparous group from Spain and southern France is phylogenetically most closely related to the viviparous clade. However, the biarmed W chromosome characterizing the western viviparous populations is an apomorphic character, whereas the uniarmed W chromosome, existing both in the western oviparous populations and in the geographically distant eastern viviparous populations, is a plesiomorphic character. This suggests an eastern origin of viviparity. Various estimates suggest that the oviparous and viviparous clades of L. vivipara split during the Pleistocene. Our results are discussed in the framework of general evolutionary models: the concept of an oviparity–viviparity continuum in squamates, the cold climate model of selection for viviparity in squamates, and the contraction–expansion of ranges in the Pleistocene resulting in allopatric differentiation.     

DOES VIVIPARITY EVOLVE IN COLD CLIMATE REPTILES BECAUSE PREGNANT FEMALES MAINTAIN STABLE (NOT HIGH) BODY TEMPERATURES?

Viviparity (live bearing) has evolved from egg laying (oviparity) in many lineages of lizards and snakes, apparently in response to occupancy of cold climates. Explanations for this pattern have focused on the idea that behaviorally thermoregulating (sun-basking) pregnant female reptiles can maintain higher incubation temperatures for their embryos than would be available in nests under the soil surface. This is certainly true at very high elevations, where only viviparous species occur. However, comparisons of nest and lizard temperatures at sites close to the upper elevational limit for oviparous reptiles (presumably, the selective environment where the transition from oviparity to viviparity actually occurs) suggest that reproductive mode has less effect on mean incubation temperatures than on the diel distribution of those temperatures. Nests of the oviparous scincid lizard Bassiana duperreyi showed smooth diel cycles of heating and cooling. In contrast, body temperatures of the viviparous scincid Eulamprus heatwolei rose abruptly in the morning, were high and stable during daylight hours, and fell abruptly at night. Laboratory incubation experiments mimicking these patterns showed that developmental rates of eggs and phenotypic traits of hatchling B. duperreyi were sensitive to this type of thermal variance as well as to mean temperature. Hence, diel distributions as well as mean incubation temperatures may have played an important role in the selective forces for viviparity. More generally, variances as well as mean values of abiotic factors may constitute significant selective forces on life-history evolution.     

Further evidence of the existence of oviparous populations of Lacerta (Zootoca) vivipara in the NW of the Balkan Peninsula

The lizard Lacerta (Zootoca) vivipara, which is viviparous in the greatest part of its distribution range, has however some oviparous populations on the southern margin of its range. The present study aimed at determining the reproductive mode and the ATA (aspartate transaminase) enzyme characteristics of four populations in Slovenia and one population in Croatia. The Slovenian females studied here presented an oviparous reproductive mode which strongly resembled those observed in the oviparous populations of south-western France and north-western Spain. Our electrophoresis analyses revealed the existence of two distinct alleles, ATA-150 and ATA-200, in the oviparous populations of Slovenia. These alleles were identical to those observed in the French and Spanish oviparous group and were distinct from the allele ATA-100 characterizing the viviparous populations that we had previously studied. Although we did not study the reproductive mode of Croatian females, the allele ATA-200 observed in one population of Croatia strongly suggested that this population might also be oviparous.     

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

The European common lizard, Zootoca vivipara, is the most widespread terrestrial reptile in the world. It occupies almost the entire Northern Eurasia and includes four viviparous and two oviparous lineages. We analysed how female snout-vent length (SVL), clutch size (CS), hatchling mass (HM), and relative clutch mass (RCM) is associated with the reproductive mode and climate throughout the species range and across the evolutionary lineages within Z. vivipara. The studied variables were scored for 1,280 females and over 3,000 hatchlings from 44 geographically distinct study samples. Across the species range, SVL of reproductive females tends to decrease in less continental climates, whereas CS corrected for female SVL and RCM tend to decrease in climates with cool summer. Both relationships are likely to indicate direct phenotypic responses to climate. For viviparous lineages, the pattern of co-variation between female SVL, CS and HM among populations is similar to that between individual females within populations. Consistent with the hypothesis that female reproductive output is constrained by her body volume, the oviparous clade with shortest retention of eggs in utero showed highest HM, the oviparous clade with longer egg retention showed lower HM, and clades with the longest egg retention (viviparous forms) had lowest HM. Viviparous populations exhibited distinctly lower HM than the other European lacertids of similar female SVL, many of them also displaying unusually high RCM. This pattern is consistent with Winkler and Wallin’s model predicting a negative evolutionary link between the total reproductive investment and allocation to individual offspring.     

Uterine and eggshell structure and histochemistry in a lizard with prolonged uterine egg retention (Lacertilia,Scincidae, Saiphos)

The eggshell of lizards is a complex structure composed of organic and inorganic molecules secreted by the oviduct, which protects the embryo by providing a barrier to the external environment and also allows the exchange of respiratory gases and water for life support. Calcium deposited on the surface of the eggshell provides an important nutrient source for the embryo. Variation in physical conditions encountered by eggs results in a tradeoff among these functions and influences eggshell structure. Evolution of prolonged uterine egg retention results in a significant change in the incubation environment, notably reduction in efficiency of gas exchange, and selection should favor a concomitant reduction in eggshell thickness. This model is supported by studies that demonstrate an inverse correlation between eggshell thickness and length of uterine egg retention. One mechanism leading to thinning of the eggshell is reduction in size of uterine shell glands. Saiphos equalis is an Australian scincid lizard with an unusual pattern of geographic variation in reproductive mode. All populations retain eggs in the uterus beyond the embryonic stage at oviposition typical for lizards, and some are viviparous. We compared structure and histochemistry of the uterus and eggshell of two populations of S. equalis, prolonged egg retention, and viviparous to test the hypotheses: 1) eggshell thickness is inversely correlated with length of egg retention and 2) eggshell thickness is positively correlated with size of shell glands. We found support for the first hypothesis but also found that eggshells of both populations are surprisingly thick compared with other lizards. Our histochemical data support prior conclusions that uterine shell glands are the source of protein fiber matrix of the eggshell, but we did not find a correlation between size of shell glands and eggshell thickness. Eggshell thickness is likely determined by density of uterine shell glands in this species. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Fundamentals of viviparity: comparison of seasonal changes in the uterine epithelium of oviparous and viviparous Lerista bougainvillii (Squamata: Scincidae)

Distinct differences in epithelial response between oviparous and viviparous species of skinks led us to investigate morphological differences in the uterus of a species that exhibits bi-modal reproduction and that may indicate specialities for the different requirements of viviparity and oviparity. The uteri of females from oviparous and viviparous populations of the Australian scincid lizard, Lerista bougainvillii, are described in detail to determine whether the occurrence of uterodomes and the plasma membrane transformation, found in other viviparous species but not oviparous species, are indeed features characteristic of viviparity. Oviductal tissue was dissected at three different stages of reproduction from lizards from both populations: 1) vitellogenic, 2) gravid or pregnant, and 3) non-reproductive or quiescent. Tissue was observed using both scanning and transmission electron microscopy. Lerista bougainvillii has a simple placental morphology with simple squamous epithelium. In contrast to mammals and other viviparous skinks, L. bougainvillii does not undergo a plasma membrane transformation, but early signs of placentation in viviparous individuals are indicated by changes in the uterine surface that occur largely after embryonic stage 30. There are no obvious cellular differences between the uteri of oviparous and viviparous L. bougainvillii at the non-reproductive and vitellogenic phase of the reproductive cycle but throughout gestation/gravidity, the cellular differences that could be related to the changing functional requirements with the retention of the viviparous embryo, became apparent. A plasma membrane transformation with ensuing uterodome formation does not occur, which suggests that these more sophisticated changes are a feature of advanced placental development in reptiles.     

Reproductive mode may determine geographic distributions in Australian venomous snakes (Pseudechis,Elapidae)

Summary Why are viviparous squamate reptiles more common in cold climates, and oviparous ones in warmer areas? The usual explanation is that (1) oviparous squamates cannot reproduce successfully in cold areas because soil temperatures are too low for embryonic development; and (2) viviparous squamates experience lower survivorship or reproductive success than oviparous taxa in warmer areas. These hypotheses suggest that the boundaries of geographic distributions of congeneric oviparous and viviparous squamates should be predictable from data on thermal tolerances of embryos, and estimated temperatures of soils and gravid female reptiles throughout the potential geographic range of the taxon. In large venomous Australian snakes of the genus Pseudechis, distributional boundaries of oviparous and viviparous taxa can be accurately predicted from such data. This predictive ability, if substantiated by studies of other reproductively biomodal squamate taxa, would support the putative role of reproductive mode as a direct determinant of reptilian geographic distributions.     

Biogeography of Lacerta (Zootoca) vivipara: reproductive mode and enzyme phenotypes in Bulgaria

Lacerta (Zootoca) vivipara , has allopatric oviparous and viviparous populations viviparity is observed from central France and the British Isles to Scandinavia and Russia, while oviparity is restricted to northern Spain and southwestern France, i e the extreme southwestern part of the range Recent observations in the Rila, Balkan, Vitocha, Pirin and Rhodopes mountains indicate that Bulgarian populations of Lacerta (Zootoca) vivipara are indeed viviparous The electrophoretic study of allozymes and the estimation of genetic distances indicate that viviparous lizards from northwest and central France are more closely related to those of Bulgaria, than to the oviparous lizards of southwest France and northwest Spain Variations in reproductive mode and allozymes are not directly related to geographic distances between populations, nor to their latitude populations located at the southwest limit of distribution are oviparous and exhibit alleles ATA^-150 or ATA^-200, whereas, at a comparable latitude, the Bulgarian populations are viviparous and exhibit allele ATA^-100 characteristic of other distant viviparous populations These findings underline the orginality of the oviparous southwestern populations They do not contradict our previous biogeographic scenario     

Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards?

Pregnant females modify their thermoregulatory behaviour in many species of viviparous (live-bearing) reptiles, typically maintaining higher and more stable body temperatures at this time. Such modifications often have been interpreted as adaptations to viviparity, functioning to accelerate embryonic development and/or modify phenotypic traits of hatchlings. An alternative possibility is that similar maternal thermophily may be widespread also in oviparous species and if so, would be a pre-adaptation (rather than an adaptation) to viviparity. Because eggs are retained in utero for a significant proportion of development even in oviparous reptiles, maternal thermophily might confer similar advantages in oviparous as in viviparous taxa. Experimental trials on montane oviparous scincid lizards (Bassiana duperreyi) support the pre-adaptation hypothesis. First, captive females (both reproductive and non-reproductive) selected higher temperatures than males. Second, experimentally imposing thermal regimes on pregnant females significantly affected their oviposition dates and the phenotypic traits (body shape, running speed) of their hatchlings. Thus, as for many other behavioural correlates of pregnancy in viviparous reptiles, maternal thermophily likely may have already been present in the ancestral oviparous taxa that gave rise to present-day viviparous forms.     

Comparison of the cold hardiness capacities of the oviparous and viviparous forms of Lacerta vivipara

The lizard Lacerta vivipara has allopatric oviparous and viviparous populations. The cold hardiness strategy of L. vivipara has previously been studied in viviparous populations, but never in oviparous ones. The present study reveals that both the oviparous and viviparous individuals of this species are able to survive in a supercooled state at -3 degrees C for at least one week when kept on dry substrates. The mean crystallisation temperatures of the body, around -4 degrees C on dry substrata and -2 degrees C on wet substrata, do not differ between oviparous and viviparous individuals. All the individuals are able to tolerate up to 48-50% of their body fluid converted into ice, but only viviparous individuals were able to stabilize their body ice content at 48%, and hence were able to survive even when frozen at -3 degrees C for times of up 24 hours. Ice contents higher than 51% have been constantly found lethal for oviparous individuals. This suggests that, in L. vivipara, the evolution towards a higher degree of freezing tolerance could parallel the evolution of the viviparous reproductive mode, a feature believed to be strongly selected under cold climatic conditions. This is the first report, among reptiles, of an intraspecific variation regarding the freeze tolerance capacities.     

Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards

Reproduction entails costs, and disentangling the relative importance of each stage of the reproductive cycle may be important to assess the costs and benefits of different reproductive strategies. We studied the early costs of reproduction in oviparous and viviparous lizard females of the bimodal reproductive species Zootoca vivipara. Egg retention time in oviparous females is approximately one-third of the time in viviparous females. We compared the vitellogenesis and egg retention stages that are common to both reproductive modes. Precisely, we monitored the thermoregulatory behaviour, the weight gain and the immunocompetence of the females. Moreover, we injected an antigen in half of the females (immune challenge) to study the trade-offs between reproductive mode and immune performance and between different components of the immune system. Finally, we experimentally induced parturition in viviparous females at the time of egg laying in oviparous females. Oviparous and viviparous females did not show strong differences in response to the immune challenge. However, viviparous females spent more time thermoregulating while partially hidden and gained more weight than oviparous females. The greater weight gain indicates that the initial period of egg retention is less costly for viviparous than for oviparous females or that viviparous females are able to save and accumulate energy at this period. This energy may be used by viviparous females to cope with the subsequent costs of the last two-third of the gestation. Such an ability to compensate the higher costs of a longer egg retention period may account for the frequent evolution of viviparity in squamate reptiles.     

Evolutionary and biogeographical implications of the karyological variations in the oviparous and viviparous forms of the lizard Lacerta (Zootoca) vivipara

The lizard Lacerta ( Zootoca ) vivipara has two modes of reproduction and is variable karyologically. We describe its karyological variation from literature data and from new data on two viviparous populations from France, on two oviparous populations from the Pyrenees in south-western France and on three oviparous populations recently discovered in Slovenia. Males have 36 chromosomes, whereas females have only 35 chromosomes in all viviparous populations and in the Pyrenean oviparous populations. This karyotype has been interpreted to result from a fusion of an ancestral sexual W chromosome with an autosome from the Zl or from the Z2 pair. The karyotype formula is 32 autosomes + ZIZ2W for the female and 32 autosomes + Z1Z1Z2Z2 for the male. The karyotype of the Slovenian oviparous populations, 34 autosomes + ZW in the male and 34 autosomes +ZW in the female, represents an evolutionary stage that preceded the chromosomal fusion. There is minor karyological variation, mainly concerning the W and Z2 chromosomes, within the Pyrenean oviparous populations. This parallels the geographic variation of the W-linked alleles of the MPI enzyme and suggests that allopatric differentiation of these oviparous populations might have occurred in the vicinity of the Pyrenees during the Pleistocene.
The viviparous populations from western Europe carry a metacentric W chromosome, whereas oviparous populations from south-western Europe and eastern viviparous populations both show an acrocentrie, or a subtelocentrie. W chromosome. This suggests that the acrocentric-subtelocentric W is a primitive character and that viviparity probably arose in an eastern lineage of the species.     

Sunny side up: lethally high, not low, nest temperatures may prevent oviparous reptiles from reproducing at high elevations

Oviparous (egg-laying) lizards and snakes generally inhabit warmer climates than do related viviparous (live-bearing) taxa. This pattern is widely attributed to the failure of oviparous reproduction in cold climates, but the thermal regimes of potential nest-sites above and below the elevational cut-off for oviparous reproduction have never been quantified. We studied oviparous ( Bassiana duperreyi ) and viviparous ( Eulamprus heatwolei ) scincid lizards at such a site in the Brindabella Range of south-eastern Australia. Miniature data-loggers monitored temperatures of nest-sites and lizards in midsummer, partway through the incubation period of eggs in natural nests. Our results contradict the simplistic notion that mean nest temperatures determine this elevational limit for oviparity. Instead, potential nest-sites with average temperatures suitable for embryogenesis in Bassiana are available well above the threshold elevation. However, thermal minima decrease consistently with elevation and thus the maximum temperature needed for any given mean incubation temperature increases rapidly with elevation. Potential nest-sites above the elevational threshold can only attain mean temperatures high enough to sustain embryogenesis by having lethally high thermal maxima. Such nest-sites are available close to the soil surface, but cannot support development. In contrast, behavioural thermoregulation allows viviparous lizards to maintain high mean body temperatures concurrently with relatively low maximum temperatures, regardless of elevation. Paradoxically, oviparous reptiles may be restricted to low elevations not because nests that provide appropriate mean incubation temperatures are unavailable further up the mountain, but because eggs laid in such shallow nests would overheat.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 325–334.