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     

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.     

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.     

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.     

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.     

From oviparity to viviparity: a preliminary note on the morphometric differentiation between oviparous and viviparous species assigned to the genus Liolaemus (Reptilia, Squamata, Liolaemidae)

Embryonic growth requires a considerable internal space in viviparous female lizards and this need for space should be reflected in their external morphometry. External morphological differences associated with the reproductive mode in 12 viviparous and 18 oviparous species of Liolaemus lizards were identified. Size differences between viviparous and oviparous species were elucidated by axilla-groin/snout-vent relationship. Axilla-groin distance, considered a size estimator of visceral cavity, surpassed 50% of snout-vent length in viviparous females, while it is always less than 50% in oviparous females. This difference between the two reproductive modes is statistically significant.     

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.     

Variation in body size and sexual size dimorphism in the most widely ranging lizard: testing the effects of reproductive mode and climate

Reproductive mode, ancestry, and climate are hypothesized to determine body size variation in reptiles but their effects have rarely been estimated simultaneously, especially at the intraspecific level. The common lizard (Zootoca vivipara) occupies almost the entire Northern Eurasia and includes viviparous and oviparous lineages, thus representing an excellent model for such studies. Using body length data for >10,000 individuals from 72 geographically distinct populations over the species' range, we analyzed how sex‐specific adult body size and sexual size dimorphism (SSD) is associated with reproductive mode, lineage identity, and several climatic variables. Variation in male size was low and poorly explained by our predictors. In contrast, female size and SSD varied considerably, demonstrating significant effects of reproductive mode and particularly seasonality. Populations of the western oviparous lineage (northern Spain, south‐western France) exhibited a smaller female size and less female‐biased SSD than those of the western viviparous (France to Eastern Europe) and the eastern viviparous (Eastern Europe to Far East) lineages; this pattern persisted even after controlling for climatic effects. The phenotypic response to seasonality was complex: across the lineages, as well as within the eastern viviparous lineage, female size and SSD increase with increasing seasonality, whereas the western viviparous lineage followed the opposing trends. Altogether, viviparous populations seem to follow a saw‐tooth geographic cline, which might reflect the nonmonotonic relationship of body size at maturity in females with the length of activity season. This relationship is predicted to arise in perennial ectotherms as a response to environmental constraints caused by seasonality of growth and reproduction. The SSD allometry followed the converse of Rensch's rule, a rare pattern for amniotes. Our results provide the first evidence of opposing body size—climate relationships in intraspecific units.     

A phylogenetic analysis of variation in reproductive mode within an Australian lizard (Saiphos equalis, Scincidae)

Saiphos equalis , a semi-fossorial scincid lizard from south-eastern Australia, is one of only three reptile species world-wide that are known to display geographic variation in reproductive mode. Uniquely, Saiphos equalis includes populations with three reproductive modes: oviparous with long (15-day) incubation periods; oviparous with short (5-day) incubation periods; and viviparous (0-day incubation periods). No Saiphos populations show 'normal' scincid oviparity (> 30-day incubation period). We used mitochondrial nucleotide sequences ( ND2 and cytochrome b ) to reconstruct relationships among populations from throughout the species' distribution in New South Wales, Australia. Under the phylogenetic species concept, phylogenetic analyses are consistent with the oviparous and viviparous populations of S. equalis being conspecific. Phylogenetic analyses suggest that the long incubation period oviparous lineage is the sister group to all other populations; and that the viviparous populations belong to a cluster of weakly supported clades basal to the short-incubation-period oviparous clade. These clades correspond to variation in reproductive mode and geographic location.     

Extraembryonic membrane development in a reproductively bimodal lizard, Lacerta (Zootoca) vivipara

Reproductive mode has been remarkably labile among squamate reptiles and the evolutionary transition from oviparity to viviparity commonly has been accompanied by a shift in the pattern of embryonic nutrition. Structural specializations for placental transfer of nutrients during intrauterine gestation are highly diverse and many features of the extraembryonic membranes of viviparous species differ markedly from those of oviparous species. However, because of a high degree of evolutionary divergence between the species used for comparisons it is likely that the observed differences arose secondarily to the evolution of viviparity. We studied development of the extraembryonic membranes and placentation in the reproductively bimodal lizard Lacerta vivipara because the influence of reproductive mode on the structural/functional relationship between mothers and embryos can best be understood by studying the most recent evolutionary events. Lecithotrophic viviparity has evolved recently within this species and, although populations with different reproductive modes are allopatric, oviparous and viviparous forms interbreed in the laboratory and share many life history characteristics. In contrast to prior comparisons between oviparous and viviparous species, we found no differences in ontogeny or structure of the extraembryonic membranes between populations with different reproductive modes within L. vivipara. However, we did confirm conclusions from previous studies that the tertiary envelope of the egg, the eggshell, is much reduced in the viviparous population. These conclusions support a widely accepted model for the evolution of squamate placentation. We also found support for work published nearly 80 years ago that the pattern of development of the yolk sac of L. vivipara is unusual and that a function of a unique structure of squamate development, the yolk cleft, is hematopoiesis. The structure of the yolk sac splanchnopleure of L. vivipara is inconsistent with a commonly accepted model for amniote yolk sac function and we suggest that a long standing hypothesis that cells from the yolk cleft participate in yolk digestion requires further study.     

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.     

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.     

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.     

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.     

Is the Evolution of Viviparity Accompanied by a Relative Increase in Maternal Abdomen Size in Lizards?

Female reptiles with viviparous reproduction should leave space for their eggs that reach the maximum mass and volume in the oviducts. Is the evolution of viviparity accompanied by a relative increase in maternal abdomen size, thus allowing viviparous females to increase the amount of space for eggs? To answer this question, we compared morphology and reproductive output between oviparous and viviparous species using three pairs of lizards, which included two Eremias, two Eutropis and two Phrynocephalus species with different reproductive modes. The two lizards in each pair differed morphologically, but were similar in the patterns of sexual dimorphism in abdomen and head sizes and the rates at which reproductive output increased with maternal body and abdomen sizes. Postpartum females were heavier in viviparous species, suggesting that the strategy adopted by females to allocate energy towards competing demands differs between oviparous and viviparous species. Reproductive output was increased in one viviparous species, but decreased in the other two, as compared with congeneric oviparous species. The space requirement for eggs did not differ between oviparous and viviparous females in one species pair, but was greater in viviparous females in the other two pairs greater in relative clutch mass and relative litter mass. In the two Phrynocephalus species, viviparous females produced heavier clutches than did oviparous females not by increasing the relative size of the abdomen, but by being more full of eggs. In none of the three species pairs was the maternal abdomen size greater in the viviparous species after accounting for body size. Our data show that the evolution of viviparity is not accompanied by a relative increase in maternal abdomen size in lizards. Future work could usefully investigate other lineages of lizards to determine whether our results are generalisable to all lizards.     

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.     

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.     

Maternal body-volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity

A few species of squamate reptiles contain both oviparous (egg-laying) and viviparous (live-bearing) populations, and thus offer exceptional opportunities to test adaptationist hypotheses on the determinants of reproductive output. We focus on the hypothesis that maternal body-volume constrains reproductive output in squamate reptiles. If females are “full” of eggs, what happens when viviparity evolves within a lineage? Eggs increase in volume and mass during development, primarily due to the uptake of water, so how can they be accommodated within the mother's abdomen? We predict that the resultant increase in relative clutch mass (RCM) will be lessened by (1) a decrease in reproductive output (by reducing the number or size of offspring), and/or (2) an increase in maternal body-volume (via modifications of size or shape of adult females). Our comparisons of conspecific oviparous and viviparous lizards (Lerista bougainvillii) confirm that live-bearers carry heavier clutches (in both absolute and relative terms) and show the predicted shifts in body size and shape of reproductive females. However, offspring size and number were unaffected by the evolution of viviparity, and the shifts in maternal morphology were too small to fully offset the increase in clutch mass. Thus, RCMs increased by 50%, indicating that viviparous females produced clutches which more completely filled the space available in the abdominal cavity. We conclude that maternal body-volume does play a role in determining reproductive output, but that the observed clutch masses may be optimized, rather than maximized, with respect to the abdominal space available.     

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.     

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.