Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles

Current studies on fetal membranes of reptiles are providing insight into three major historical transformations: evolution of the amniote egg, evolution of viviparity, and evolution of placentotrophy. Squamates (lizards and snakes) are ideal for such studies because their fetal membranes sustain embryos in oviparous species and contribute to placentas in viviparous species. Ultrastructure of the fetal membranes in oviparous corn snakes (Pituophis guttatus) shows that the chorioallantois is specialized for gas exchange and the omphalopleure, for water absorption. Transmission and scanning electron microscopic studies of viviparous thamnophine snakes (Thamnophis, Storeria) have revealed morphological specializations for gas exchange and absorption in the intra-uterine environment that represent modifications of features found in oviparous species. Thus, fetal membranes in oviparous species show morphological differentiation for distinct functions that have been recruited and enhanced under viviparous conditions. The ultimate in specialization of fetal membranes is found in viviparous skinks of South America (Mabuya) and Africa (Trachylepis, Eumecia), in which placentotrophy accounts for nearly all of the nutrients for development. Ongoing research on these lizards has revealed morphological specializations of the chorioallantoic placenta through which nutrient transfer is accomplished. In addition, African Trachylepis show an invasive form of implantation, in which uterine epithelium is replaced by invading chorionic cells. Ongoing analysis of these lizards shows how integration of multiple lines of evidence can provide insight into the evolution of developmental and reproductive specializations once thought to be confined to eutherian mammals.     

A neglected life-history trait: clutch-size variance in snakes

Most analyses of life-history traits have focused on mean values rather than their associated variance. We review published and original data on snakes, including records gathered over many years on single populations, to examine patterns in clutch-size variability in these animals. Within single populations, the coefficient of variation of clutch size did not vary significantly with maternal body size, or among years. The stability of clutch-size variance through time is consistent with experimental studies showing no significant influence of food intake rates on this characteristic. Clutch-size variances did not differ between viviparous and oviparous snakes, but were dependent upon allometric relationships involving maternal body size and the relationship between clutch size and body size. Clutch-size variability was highest in species with relatively variable female sizes, and with a high rate of increase in clutch size with increasing body size. These two factors acted to magnify the extent of clutch-size variability engendered by variability in maternal body sizes. The relationships among these variables were similar in the two squamate Suborders, but the larger body sizes and mean clutch sizes of snakes resulted in clutch-size variances being higher in snakes than in lizards.     

Sex differences in behavior associated with sex-biased mortality in an oviparous snake species

Sex differences in behavior associated with reproduction often result in sex-biased mortality. Male-biased mortality appears to be the prevalent pattern for birds and mammals, but recent work suggests that higher female mortality may be the norm for snakes, at least for viviparous species. Here we used radio-telemetry to examine sex-biased mortality in Texas ratsnakes Elaphe obsoleta , an oviparous species, and test the hypothesis that differences in behavior are associated with higher rates of mortality. Female ratsnakes had lower survival than male ratsnakes. For both sexes decreased survival was associated with higher activity and increased basking. Male ratsnakes were most active and basked most during the spring when mating occurred, which was when almost all male mortality occurred. Although female ratsnakes also moved and basked most during the mating season, they maintained relatively high levels of movement and basking through the summer and fall, and female mortality occurred throughout that period. Thus, contrary to the expectation that the cost of reproduction should be highest prior to egg laying for females of oviparous snakes, the mortality pattern documented here suggests the cost of reproduction is greatest following egg laying, similar to what has been found for females of viviparous species. As capital breeders (whether oviparous or viviparous), female snakes must rebuild energy reserves following a bout of reproduction, and the associated increase in foraging and basking required to do so increases female susceptibility to predation. Further studies are required to determine if female-biased mortality is the norm in snakes and if so, to determine the demographic and life-history consequences.     

Adaptive significance of food income in European snakes: body size is related to prey energetics

Feeding strategies and diet patterns have been extensively investigated in vertebrates and, more specifically, in snakes. Although it has been hypothesized that prey species may differ in terms of energy content, almost no theoretical or practical study has been carried out to determine actual nutritional values of the common prey types of wild snakes. Our model taxa were a selection of widely distributed and well known European snake species, which have all been studied in depth: approximately 76% of their diet is composed of mammals, reptiles, and insects. We therefore selected a single model species for each of these categories and proceeded with the analyses. Nutritional values were determined using a standard procedure: lizards and mice were richer in proteins than insects (crickets); insects and mice were richer in lipids than lizards, and mice and crickets have a higher energy content than lizards; lizards were rich in ashes. We then applied our experimental results to a selected sample of European terrestrial snakes (11 populations, ten species, seven genera, two families) characterized by different body size (50–160 cm total length) and reproductive strategies (oviparous versus viviparous), aiming to correlate these parameters with patterns of energy income. A direct relationship was found between body mass/body length ratio (BCI, body condition index) and meal energetics: the higher the BCI, the higher was the metabolic requirement, whereas BCI was independent of species or of reproductive system effect. Large‐sized snakes thus need a highly diversified and more energy‐rich diet than smaller snakes, supporting previous hypotheses. The simple applicability of this method could be of valuable support in further comparative research work, reducing experimental costs and stimulating further ecological, behavioural, and, possibly, phylogenetic comparisons. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 307–317.     

Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard

We used modern comparative methods to examine the evolution of scent-mediated antisnake behavior in the rock-dwelling velvet gecko (Oedura lesueurii). The selective agent is a snake species (broad-headed snake, Hoplocephalius bungaroides) that feeds primarily on velvet geckos by remaining sedentary in rock crevices for days or weeks, waiting to ambush lizards. The past and present distribution of this predator is well documented because of its threatened conservation status. We used this information to sample lizards from three populations distributed with snakes (sympatric) and three populations that appear never to have been distributed with snakes (allopatric) in each of two widespread but geographically distinct genetic groups of velvet gecko (as determined using allozyme electrophoresis). Wild-caught immature geckos from sympatric populations showed higher tongue-flick rates and stronger shifts in locomotion (increased duration of crawling and remaining stationary while pressed against the rock) toward snake-scented rocks than did lizards from allopatric populations. However, predation environment did not significantly affect a lizard's tendency to display other typical antisnake tactics such as tail waving or fleeing. These results were highly repeatable across the two sampled genetic groups of velvet gecko, despite demonstrable genetic divergence between groups. Experiments with hatchling lizards that had no experience with predators indicate that qualitative components of antisnake behaviors are probably inherited. The method of phylogenetically independent contrasts strongly suggests that the presence or absence of snakes has driven the evolution of behavior in velvet geckos. Collectively, these results provide support for an often suggested but speculative expectation that prey can adapt to predation pressure on a local scale.     

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     

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.     

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.     

Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development

Energy consumption during development has been measured in many oviparous lizards, but not in viviparous lizards in utero. It has always been assumed that energy consumption by embryos of viviparous lizards during development is similar to that of oviparous species. Estimation of energy consumption of viviparous lizards in vivo are confounded by the possible influence of pregnancy on maternal metabolism. Here we separated maternal and embryonic metabolism in measurements of pregnant Eulamprus tympanum throughout pregnancy. Our data support the hypothesis that the energetic cost of development in viviparous lizards (19.8 kJ g(-1)) is similar to that in oviparous lizards (mean 16.2 kJ g(-1)), at least for a species with a simple placenta. An increase in maternal metabolism of 29% above that for non-pregnant E. tympanum goes to maintain pregnancy, and represents an important component of the reproductive effort in E. tympanum.     

Comparison of nutrient transport across the placenta of lizards differing in placental complexity

We have reviewed published and new quantitative data on the net uptake of nutrients by embryos of oviparous and viviparous lizards that vary in chorioallantoic placental complexity to better understand the evolution of complex placentae. We assessed net nutrient uptake during embryonic development by measuring the total dry mass, or the mass of separate nutrients, in the egg at about the time of ovulation and in the neonate. There is no significant difference in the fresh egg to neonate dry mass ratio of oviparous and viviparous species that have simple placentae, indicating that there is little, if any, net uptake of nutrients by viviparous species with simple chorioallantoic placentae. In contrast, there is significant uptake of dry matter and individual nutrients across the placenta of species with complex chorioallantoic placentae. Species of the genus Niveoscincus have a range of placentae and nutrient uptakes, even among populations of one species, suggesting that further studies among populations of single species are required. Data are available for relatively few clades, and all the data for the three most complex chorioallantoic placental types are derived from a single genus. Thus, further research on new genera of lizards is required to overcome the potentially confounding effects of phylogeny in our analyses.     

The influence of thermal biology on road mortality risk in snakes

Road mortality is a significant threat to terrestrial vertebrates in many areas, and the novel thermal environment of black-topped roads may represent ecological traps for some species and demographic groups. We investigated the relationship between ambient temperature and on-road detection in a snake assemblage in southeastern Louisiana by comparing observations of live snakes on a black-topped road, across measurements of air temperature and road temperature on survey days. Analyses indicated on-road detection of snakes was significantly influenced by ambient temperature conditions for five snake species. Additionally, road temperatures, and the difference between air and road temperatures, were strong drivers of on-road snake detections. Permutation analysis methods revealed that significant temperature related group (species or sex) structure exists in occurrences of snakes on the roadway, and that road temperature was the strongest driver of species differences. We also compared how air and road temperatures affected occurrence on the road between sexes in the colubrid snakes Nerodia fasciata, Nerodia cyclopion, Thamnophis proximus, and Pantherophis obsoletus. Males and females of the viviparous species N. fasciata, N. cyclopion, and T. proximus diverged significantly in temperature preferences, with females found under warmer conditions, while males and females of the oviparous species P. obsoletus did not. Road temperature was also the strongest driver of differences between sexes. Our results indicate that black-topped roads are an ecological trap that is heavily influenced by sex, reproductive condition, and species specific thermoregulatory requirements, particularly for viviparous species.     

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.     

Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development

Energy consumption during development has been measured in many oviparous lizards, but not in viviparous lizards in utero. It has always been assumed that energy consumption by embryos of viviparous lizards during development is similar to that of oviparous species. Estimation of energy consumption of viviparous lizards in vivo are confounded by the possible influence of pregnancy on maternal metabolism. Here we separated maternal and embryonic metabolism in measurements of pregnant Eulamprus tympanum throughout pregnancy. Our data support the hypothesis that the energetic cost of development in viviparous lizards (19.8 kJ g⁻¹) is similar to that in oviparous lizards (mean 16.2 kJ g⁻¹), at least for a species with a simple placenta. An increase in maternal metabolism of 29% above that for non-pregnant E. tympanum goes to maintain pregnancy, and represents an important component of the reproductive effort in E. tympanum.     

EVOLUTION OF VIVIPARITY: A PHYLOGENETIC TEST OF THE COLD‐CLIMATE HYPOTHESIS IN PHRYNOSOMATID LIZARDS

The evolution of viviparity is a key life‐history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the “cold‐climate” hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold‐climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS‐based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg‐laying) season, strongly supporting the cold‐climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold‐climate hypothesis: the presence of viviparous species restricted to low‐elevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change.     

Evolutionary stability of sex chromosomes in snakes

Amniote vertebrates possess various mechanisms of sex determination, but their variability is not equally distributed. The large evolutionary stability of sex chromosomes in viviparous mammals and birds was believed to be connected with their endothermy. However, some ectotherm lineages seem to be comparably conserved in sex determination, but previously there was a lack of molecular evidence to confirm this. Here, we document a stability of sex chromosomes in advanced snakes based on the testing of Z-specificity of genes using quantitative PCR (qPCR) across 37 snake species (our qPCR technique is suitable for molecular sexing in potentially all advanced snakes). We discovered that at least part of sex chromosomes is homologous across all families of caenophidian snakes (Acrochordidae, Xenodermatidae, Pareatidae, Viperidae, Homalopsidae, Colubridae, Elapidae and Lamprophiidae). The emergence of differentiated sex chromosomes can be dated back to about 60 Ma and preceded the extensive diversification of advanced snakes, the group with more than 3000 species. The Z-specific genes of caenophidian snakes are (pseudo)autosomal in the members of the snake families Pythonidae, Xenopeltidae, Boidae, Erycidae and Sanziniidae, as well as in outgroups with differentiated sex chromosomes such as monitor lizards, iguanas and chameleons. Along with iguanas, advanced snakes are therefore another example of ectothermic amniotes with a long-term stability of sex chromosomes comparable with endotherms.     

Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca

We exposed females of a highly placentotrophic viviparous scincid lizard (Pseudemoia pagenstecheri) to various environmental factors during pregnancy, and quantified the effects of these treatments on their offspring. The clear result was that the phenotypes of neonatal lizards can be substantially modified by the environment that their mother experiences during gestation. Restricting prey availability to the females reduced the size of their offspring. Limiting the females' basking opportunities delayed their seasonal timing of parturition, and modified body proportions (tail length relative to snout-vent length) of the neonates. More surprisingly, female lizards that were regularly exposed to the scent of sympatric lizard-eating snakes gave birth to offspring that were heavier, had unusually long tails relative to body length, and were highly sensitive to the odour of those snakes (as measured by tongue-flick responses). The neonates' antipredator responses were also modified by the experimental treatment to which their mother was exposed. The modifications in body mass, tail length and response to snake scent plausibly reduce the offspring's vulnerability to predatory snakes, and hence may constitute adaptive maternal manipulations of the neonatal phenotype. Received: 6 July 1998 / Accepted: 5 December 1998     

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.     

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.     

Molecular evidence for a terrestrial origin of snakes

Biologists have debated the origin of snakes since the nineteenth century. One hypothesis suggests that snakes are most closely related to terrestrial lizards, and reduced their limbs on land. An alternative hypothesis proposes that snakes are most closely related to Cretaceous marine lizards, such as mosasaurs, and reduced their limbs in water. A presumed close relationship between living monitor lizards, believed to be close relatives of the extinct mosasaurs, and snakes has bolstered the marine origin hypothesis. Here, we show that DNA sequence evidence does not support a close relationship between snakes and monitor lizards, and thus supports a terrestrial origin of snakes.     

Energy and nutrient utilisation by embryonic reptiles

Most reptiles are oviparous, with the developing embryos relying on the contents of the yolk to sustain development until hatching (lecithotrophy). The yolk is composed primarily of lipid and protein, which act as an energy source and the essential components to build embryonic tissue. Nevertheless, yolk and the resulting embryos contain many other nutrients, including inorganic ions, vitamins, carotenoids, water and hormones. Apart from water and oxygen, which may be taken up by eggs, and some inorganic ions that can come from the eggshell or even from outside the egg, everything required by the embryo must be in the egg when it is laid. Approximately 20% of squamate reptiles are viviparous, exhibiting a variety of placental complexities. Species with complex placentae have reduced yolk volumes, with the mother augmenting embryonic nutrition by provision across the placenta (placentotrophy). Despite assumed advantages of placentotrophy, only 5 out of approximately 100 lineages of viviparous squamates exhibit substantial placentotrophy. This paper reviews available and recent information on the yolk contents of a variety of squamate reptiles to ask the question, how are nutrients transported from the yolk to the embryo or across the placenta? Although, current available data suggest that, in broad terms, yolk is taken up by embryos without discrimination of the nutrients, there are some apparent exceptions, including the very long chain polyunsaturated fatty acids. In addition, fundamental differences in the patterns of energy utilisation in lizards and snakes suggest fundamental differences in lipid profiles in these taxa, which appear to reflect the differences between placentotrophic and lecithotrophic viviparous lizards.