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.     

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.     

Comparisons of mitochondrial DNA (mtDNA) sequences (16S rRNA gene) between oviparous and viviparous strains of Lacerta vivipara: a preliminary study

The lizard Lacerta vivipara has allopatric oviparous and viviparous populations. The mitochondrial DNA (mtDNA) gene coding for the 16S rRNA was sequenced for several viviparous lizard populations from France, Switzerland, Bulgaria, Czech Republic, The Netherlands, Sweden, and for oviparous lizard populations from the Pyrenean and Cantabric Mountains. Seven distinct groups (three oviparous and four viviparous) were identified. The net nucleotide divergence between oviparous and viviparous haplotypes was 1.3% +/- 0.5 (mean +/- standard deviation). These results on mtDNA, together with other data obtained previously, led us to formulate a biogeographical scenario that could be tested by further research.     

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     

Cytokines in the oviparity/viviparity transition: evidence of the interleukin-1 system in a species with reproductive bimodality, the lizard Lacerta vivipara

Placental viviparity is a reproductive strategy usually attributed to mammals. However, it is also present in other vertebrate species, e.g. in Squamate reptiles. Although the immunological mechanisms that allow the survival of the semi-allogenic embryo in maternal tissues are still largely unknown, cytokines seem to play an important role in mammalian reproduction. Previous studies in our laboratory showed that interleukin-1 (IL-1), a cytokine associated with implantation in mice, is also expressed at the materno-fetal interface of placental viviparous Squamates. In this study, we used the model of Lacerta vivipara, which exhibits reproductive bimodality, that is, the coexistence of oviparous and viviparous populations. By means of immunohistochemistry and anti-human antibodies, we showed that uterine tissues of L. vivipara (seven oviparous and six viviparous animals) expressed the two IL-1 isoforms, IL-1alpha and IL-1beta, and the type I IL-1 receptor (IL-1R tI) both at the pre-ovulatory stage and during gestation, with no significant difference between oviparous and viviparous females. In L. vivipara, as in most oviparous Squamates, an important phase of embryonic development takes place in the mother's oviduct, before egg-laying. Moreover, although thinner than in oviparous females, an eggshell membrane persists throughout gestation in viviparous females also, which develop a very simple type of placenta. The data suggest that immunological mechanisms that allow the survival of the semi-allogenic embryo in maternal tissues are independent of the timing or intimacy of contact between maternal and fetal tissues.     

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.     

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.     

Refuge areas and suture zones in the Pyrenean and Cantabrian regions: geographic variation of the female MPI sex-linked alleles among oviparous populations of the lizard Lacerta (Zootoca) vivipara

The viviparous lizard Lacerta (Zootoca) vivipara exhibits several alleles of the mannose-6-phosphate isomerase (MPI) enzyme that are carried exclusively on the female W sex-chromosome. Previous studies showed that both the oviparous and viviparous forms of L. (Zootoca) vivipara have these female sex-linked alleles. We document the existence of geographic variation of these alleles among the oviparous populations of southwestern France and northwestern Spain. Two oviparous subgroups were identified: all females from the eastern and central Pyrenees and most females from Aquitaine and from the northern slope of the western Pyrenees exhibited the fast migrating alleles MPI¹¹⁰ or MPI¹²⁰, whereas all females from the Cantabric mountains, Spanish Basque country, and from the south slope of the western Pyrenees exhibited the slow migrating allele MPI⁹⁰. Populations with both fast and slow migrating alleles occurred at some stations in the upper Ossau valley (western Pyrenees) and also at a lowland station of south Aquitaine. The hypothesis that several oviparous forms could have retreated to different places of the Pyreneo-Iberian refugia during the Quaternary glaciations could explain the conservation or the evolution of the polymorphism of the MPI alleles, and that is consistent with the phylogeographic scenario previously proposed to account for the reproductive and cytogenetical variation observed in this species.     

Freeze tolerance in Aporrectodea caliginosa and other earthworms from Finland

Earthworms that live in subarctic and cold temperate areas must deal with frost even though winter temperatures in the soil are often more moderate than air temperatures. Most lumbricid earthworms can survive temperatures down to the melting point of their body fluids but only few species are freeze tolerant, i.e. tolerate internal ice formation. In the present study, earthworms from Finland were tested for freeze tolerance, and the glycogen reserves and glucose mobilization (as a cryoprotectant) was investigated. Freeze tolerance was observed in Aporrectodea caliginosa, Dendrobaena octaedra, and Dendrodrilus rubidus, but not in Lumbricus rubellus. A. caliginosa tolerated freezing at -5 degrees C with about 40% survival. Some individuals of D. octaedra tolerated freezing even at -20 degrees C. Glycogen storage was largest in D. octaedra where up to 13% of dry weight consisted of this carbohydrate, whereas the other species had only 3-4% glycogen of tissue dry weight. Also glucose accumulation was largest in D. octaedra which was the most freeze-tolerant species, but occurred in all four species upon freezing. It is discussed that freeze tolerance may be a more common phenomenon in earthworms than previously thought.     

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.     

Freezing survival, body ice content and blood composition of the freeze-tolerant European common lizard, Lacerta vivipara

To investigate the freeze tolerance of the European common lizard, Lacerta vivipara, we froze 17 individuals to body temperatures as low as -4 degrees C under controlled laboratory conditions. The data show that this species tolerates the freezing of 50% of total body water and can survive freezing exposures of at least 24-h duration. Currently, this represents the best known development of freeze tolerance among squamate reptiles. Freezing stimulated a significant increase in blood glucose levels (16.15+/- 1.73 micromol x ml(-1) for controls versus 25.06 +/- 2.92 micromol x ml(-1) after thawing) but this increase had no significant effect on serum osmolality which was unchanged between control and freeze-exposed lizards (506.0 +/- 23.8 mosmol x l(-1) versus 501.0 +/- 25.3 mosmol x l(-1), respectively). Tests that assessed the possible presence of antifreeze proteins in lizard blood were negative. Recovery at 5 degrees C after freezing was assessed by measurements of the mean time for the return of breathing (5.9 +/- 0.5 h) and of the righting reflex (44.8 +/- 4.5 h). Because this species hibernates in wet substrates inoculative freezing may frequently occur in nature and the substantial freeze tolerance of this lizard should play a key role in its winter survival.     

Avoidance of intracellular freezing by the freezing-tolerant New Zealand Alpine weta Hemideina maori (Orthoptera: Stenopelmatidae)

Calorimetric analysis indicates that 82% of the body water of Hemideina maori is converted into ice at 10 degrees C. This is a high proportion and led us to investigate whether intracellular freezing occurs in H. maori tissue. Malpighian tubules and fat bodies were frozen in haemolymph on a microscope cold stage. No fat body cells, and 2% of Malpighian tubule cells froze during cooling to -8 degrees C. Unfrozen cells appeared shrunken after ice formed in the extracellular medium. There was no difference between the survival of control tissues and those frozen to -8 degrees C. At temperatures below -15 degrees C (lethal temperatures for weta), there was a decline in survival, which was strongly correlated with temperature, but no change in the appearance of tissue. It is concluded that intracellular freezing is avoided by Hemideina maori through osmotic dehydration and freeze concentration effects, but the reasons for low temperature mortality remain unclear. The freezing process in H. maori appears to rely on extracellular ice nucleation, possibly with the aid of an ice nucleating protein, to osmotically dehydrate the cells and avoid intracellular freezing. The lower lethal temperature of H. maori (-10 degrees C) is high compared to organisms that survive intracellular freezing. This suggests that the category of 'freezing tolerance' is an oversimplification, and that it may encompass at least two strategies: intracellular freezing tolerance and avoidance.     

Overwintering adaptations in the lettuce root aphid Pemphigus bursarius (L.)

Pemphigus bursarius (L.) is a host alternating root-feeding aphid with a proportion of the population overwintering as asexual hiemalis in the soil. These hiemalis must be sufficiently cold tolerant to survive at the temperatures they would experience in winter, and also be able to overcome a period of prolonged starvation brought about by the absence of secondary host plants. Cold tolerance experiments showed field collected hiemalis to be considerably more cold hardy than laboratory summer apterae, with an LTemp(50) of -13.1 degrees C compared with 2.3 degrees C. In a constant exposure at 0 degrees C some field collected hiemalis survived for 18 days, while no summer apterae survived more than 8 h. Hiemalis, collected from the field in winter and induced in the laboratory, had significantly higher levels of triglycerides, 12.8% fresh weight (39.9% dry wt.) and 11.4% fresh weight (43.7% dry wt.), respectively, compared with summer apterae with a value of 7.1% fresh weight (32.5% dry wt.). These two adaptations of increased cold tolerance and accumulation of energy reserves confirm that the hiemalis morph is adapted for overwintering and hence physiologically distinct from summer morphs, and in turn, contribute to the success of the asexual life cycle strategy in this species.     

Desiccation stress at sub-zero temperatures in polar terrestrial arthropods

Cold tolerant polar terrestrial arthropods have evolved a range of survival strategies which enable them to survive the most extreme environmental conditions (cold and drought) they are likely to encounter. Some species are classified as being freeze tolerant but the majority of those found in the Antarctic survive sub-zero temperatures by avoiding freezing by supercooling. For many arthropods, not just polar species, survival of desiccating conditions is equally important to survival of low temperatures. At sub-zero temperatures freeze avoiding arthropods are susceptible to desiccation and may lose water due to a vapour diffusion gradient between their supercooled body fluids and ice in their surroundings. This process ceases once the body fluids are frozen and so is not a problem for freeze tolerant species. This paper compares five polar arthropods, which have evolved different low temperature survival strategies, and the effects of exposure to sub-zero temperatures on their supercooling points (SCP) and water contents. The Antarctic oribatid mite (Alaskozetes antarcticus) reduced its supercooling point temperature from -6 to -30 degrees C, when exposed to decreasing sub-zero temperatures (cooled from 5 to -10 degrees C over 42 days) with little loss of body water during that period. However, Cryptopygus antarcticus, a springtail which occupies similar habitats in the Antarctic, showed a decrease in both water content and supercooling ability when exposed to the same experimental protocol. Both these Antarctic arthropods have evolved a freeze avoiding survival strategy. The Arctic springtail (Onychiurus arcticus), which is also freeze avoiding, dehydrated (from 2.4 to 0.7 g water g(-1) dry weight) at sub-zero temperatures and its SCP was lowered from c. -3 to below -15 degrees C in direct response to temperature (5 to -5.5 degrees C). In contrast, the freeze tolerant larvae of an Arctic fly (Heleomyza borealis) froze at c. -7 degrees C with little change in water content or SCP during further cold exposure and survived frozen to -60 degrees C. The partially freeze tolerant sub-Antarctic beetle Hydromedion sparsutum froze at c. -2 degrees C and is known to survive frozen to -8 degrees C. During the sub-zero temperature treatment, its water content reduced until it froze and then remained constant. The survival strategies of such freeze tolerant and freeze avoiding arthropods are discussed in relation to desiccation at sub-zero temperatures and the evolution of strategies of cold tolerance.     

Development of the uterine shell glands during the preovulatory and early gestation periods in oviparous and viviparous Lacerta vivipara

The evolutionary process leading to the emergence of viviparity in Squamata consists of lengthening the period of egg retention in utero coupled with marked reduction in the thickness of the eggshell. We used light microscopy and scanning electron microscopy to study uterine structure during the reproductive cycle of oviparous and viviparous females of the reproductively bimodal Lacerta vivipara. We compared the structure of the uterine shell glands, which secrete components of the eggshell, during preovulatory and early gestation phases of the reproductive cycle and also compared histochemistry of the eggshells. The uterine glands of both reproductive forms undergo considerable growth within a period of a few weeks during folliculogenesis and vitellogenesis preceding ovulation. The majority of the proteinaceous fibers of the shell membrane are secreted early in embryonic development and the uterine glands regress shortly thereafter. This supports previous observations indicating that, in Squamata, secretion of the shell membrane occurs very rapidly after ovulation. The most striking differences between reproductive modes were larger uterine glands at late vitellogenesis in oviparous females, 101 microm compared to 60 microm in viviparous females, and greater thickness of the shell membrane during early gestation in oviparous females (52-73 microm) compared to viviparous females (4-8 microm). Our intraspecific comparison supports the conclusions of previous studies that, prior to ovulation, the uterine glandular layer is less developed in viviparous than in oviparous species, and that this is the main factor accounting for differences in the thickness of the shell membrane of the two reproductive forms of squamates.     

Karyological investigations of populations of the lizard Zootoca vivipara (Juaquin, 1787) from the Baltic Sea basin (western region of Russia)

Populations of the lizard Zootoca vivipara (Juaquin, 1787) (Lacertidae, Sauria) from Western and Central Europe are poorly differentiated in morphology. However, they differ from each other by several karyotype markers and their reproductive mode (oviparous and viviparous types). Here we report for the first time the results of combined investigations of Z. vivipara from Eastern Europe (the Baltic Sea basin of Western Russia). The karyotype and reproductive mode of the specimens from four previously not examined populations in Kaliningrad region have been studied. It has been shown that these lizards have viviparous mode of reproduction and their karyotypes vary on morphology of W-sex chromosomes. Females possess 2n = 35 : 32 A + Z1Z2W, with W--SV and 2n = 35 : 32 A + Z1Z2W, with W--A/ST. We have identified these populations karyologically and have first revealed that they belong to two different viviparous forms of nominative subspecies Z. v. vivipara, namely to its "western" and "Russian (eastern)" forms. These data have confirmed that the Baltic Sea basin in Eastern Europe is a zone of secondary contact of these chromosomal forms of Z. v. vivipara. The results obtained do not now allow us to speak about their sympatry, parapatry and (or) hybridization events. The results suggest that during postglasial time "western" form might colonize this region from western Europe whereas "Russian (eastern)" form might do it from Southern-Eastern Europe. It has been recommended to save the biodiversity of Z. vivipara in Kaliningrad region, namely the peripheral and very rare on vast territory of Russia "western" form and unique for western region of Russia "Russian (eastern)" form.     

Multiple origins of viviparity,or reversal from viviparity to oviparity? The European common lizard (Zootoca vivipara,Lacertidae) and the evolution of parity

The evolution of viviparity in squamates has been the focus of much scientific attention in previous years. In particular, the possibility of the transition from viviparity back to oviparity has been the subject of a vigorous debate. Some studies have suggested this reversal is more frequent than previously thought. However, none of them provide conclusive evidence. We investigated this problem by studying the phylogenetic relationships between oviparous and viviparous lineages of the reproductively bimodal lizard species Zootoca vivipara . Our results show that viviparous populations are not monophyletic, and that several evolutionary transitions in parity mode have occurred. The most parsimonious scenario involves a single origin of viviparity followed by a reversal back to oviparity. This is the first study with a strongly supported phylogenetic framework supporting a transition from viviparity to oviparity.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 1–11.     

Tyrosine phosphorylated proteins in the reproductive tract of the viviparous lizard Eulamprus tympanum and the oviparous lizard Lampropholis guichenoti

Plastic changes occur in the morphology of the uterus at various stages of the reproductive cycle in both oviparous and viviparous lizards and these may be influenced by estrogen. Estrogen driven phosphorylation of effector proteins on tyrosine residues plays a major role in the plastic modulation of uterine anatomy and physiology in vertebrates. We used electrophoresis and Western blotting to characterize the phosphotyrosine protein profiles at various stages of the reproductive pathway in an oviparous lizard Lampropholis guichenoti and a viviparous lizard Eulamprus tympanum. L. guichenoti displayed major bands in the 200-35 kDa range and a triplet of bands of molecular masses 61 kDa, 52 kDa and 48 kDa in 50% of specimens and a 38 kDa band in all specimens. In contrast, E. tympanum samples all displayed a single major band at 40 kDa, which was significantly elevated at the early pregnancy stage. Somewhat paradoxically, the viviparous species, which has the more complex uterine epithelial changes during pregnancy, has the fewest phosphotyrosine bands, so how tyrosine phosphorylation is affected during the evolution of viviparity is not clear.     

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.     

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.