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

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

Maternal basking behaviour determines offspring sex in a viviparous reptile

Two primary dichotomies within vertebrate life histories involve reproductive mode (oviparity versus viviparity) and sex determination (genotypic sex determination versus environmental sex determination). Although reptiles show multiple evolutionary transitions in both parameters, the co-occurrence of viviparity and environmental-dependent sex determination have heretofore been regarded as incompatible. Our studies on the viviparous lizard Niveoscincus ocellatus show that the extent of basking by a female influences the sex of her offspring. Critically, our data reveal this effect both in the field (via correlations between date of birth and litter sex ratio) and in a laboratory experiment (females with reduced basking opportunities produced more male offspring). Changes in thermoregulatory behaviour thus allow pregnant female lizards to modify the sex of their offspring.     

Are viviparous lizards from cool climates ever exclusively nocturnal? Evidence for extensive basking in a New Zealand gecko

Viviparity has evolved numerous times among squamate reptiles; however, the combination of viviparity and nocturnality is apparently rare among lizards. We used time‐lapse photography to examine evidence for diurnal activity in a viviparous lizard often described as nocturnal, the gecko Woodworthia ‘Otago/Southland’ from southern New Zealand (family Diplodactylidae). Evidence for diurnal emergence was extensive. Females have a higher incidence of basking compared to males, although no difference was detected between females in different reproductive conditions. Temperature loggers inserted into calibrated copper models were used to compare the body temperatures available to geckos in two basking positions and in two retreat types. Models in basking positions reached higher mean temperatures than models in retreats, although there was no significant effect of basking position or retreat type on model temperatures. Collectively, our results indicate that pregnant geckos that bask consistently could reduce gestation length by at least 14 days compared with females that remain in retreats. Extensive basking in this species adds to the growing evidence of diurno‐nocturnality in many New Zealand lepidosaurs, including other viviparous geckos. Our results lead us to question whether viviparity in lizards is ever compatible with ‘pure’ nocturnality in a cool climate. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

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     

Parturient behaviour of a viviparous skink: evidence for maternal cannibalism when basking opportunity is low

We documented the behaviour of pregnant McCann’s skinks (Oligosoma maccanni) before, during and after parturition. Females were maintained in captivity from early pregnancy under thermal environments differing in basking opportunity (low, mid and high regimes). Thermal regime during pregnancy had little influence on maternal behaviours, including basking behaviour prior to birth and the duration of, and site selection for, labour. The majority of births (78%) occurred in the open and warm areas. Most females (61%; n?=?102 births, n?=?36 females) aided offspring post-birth by biting them free of the enclosing extra-embryonic membrane. Some females from the low regime consumed non-viable offspring, but whether this is a consistent difference among females held under different basking regimes requires further study. Many females (c. 79%) also exhibited a brief transient decrease in control of hind-limbs post-birth. Further studies on other squamates are recommended to shed light on the evolutionary history and possible conservation consequences of maternal behaviour during parturition.     

Post‐birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance

The relatedness of individuals can have pronounced effects on behavioural interactions, as engaging in mutually beneficial behaviours with kin can increase inclusive fitness. Parental care can be particularly important for kin discrimination in birds and mammals, but similar studies have not been conducted on species exhibiting more rudimentary forms of care. Maternal attendance of young is ubiquitous among viviparous temperate pitvipers, but the adaptive value of this behaviour has received little attention. We sought to determine if being deprived of a maternal attendance period as neonates altered how cottonmouths (Agkistrodon piscivorus Lacépède), a common North American pitviper, responded to kin vs. non‐kin. We measured the affiliative behaviour of related and unrelated juvenile–juvenile and mother–juvenile pairs that had been allowed a maternal attendance period or had been separated since birth. We found that maternal attendance was not required for sibling or mother–offspring recognition, but did enhance female affiliative behaviour overall, and particularly that of sisters. In contrast, related juveniles that were separated at birth showed a reversal of the sex‐specific affiliative behaviour observed in maternally attended juveniles. Post‐birth separation had only a modest effect on mother–juvenile affiliative behaviour, and no effect on the strong affiliation between mothers and daughters. The patterns of affiliative behaviour observed in maternally attended snakes corresponded to patterns that have emerged from previous captive and field studies of pitvipers; however, the behaviour of juveniles separated at birth was atypical. Thus, it is possible that maternal attendance plays some role in the development of adaptive sex‐specific and kin‐directed affiliative behaviour in pitvipers.     

Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier‐born offspring are more likely to survive through their first winter and are larger following that winter, than are later‐born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent–offspring conflict in the evolution of maternal effects on parturition date.     

Nesting in a thermally challenging environment: nest‐site selection in a rock‐dwelling gecko,Oedura lesueurii (Reptilia: Gekkonidae)

In egg‐laying species, maternal oviposition choice can influence egg survival and offspring phenotypes. According to the maternal‐preference offspring‐performance hypothesis, females should choose oviposition sites that are optimal for offspring fitness. However, in thermally challenging environments, maternal oviposition behaviour may be constrained by the limited availability of suitable oviposition sites. We investigated nest‐site selection in a nocturnal lizard [velvet gecko Oedura lesueurii (Duméril and Bibron)] that inhabits a thermally challenging environment in south‐eastern Australia. The viability of these gecko populations is critical for the persistence of an endangered snake species (Hoplocephalus bungaroides Wagler) that feeds heavily on velvet geckos. Female geckos chose nest sites nonrandomly, with 87% of nests (N = 30) being laid in deep crevices. By contrast, only 13% of clutches were laid under rocks, which were the most readily available potential nest sites. Nest success in crevices was high (100%), but no eggs hatched from nests under rocks. Temperatures in nest crevices remained relatively low and constant throughout the incubation period (mean = 22.7 °C, range 21.0–24.5 °C), whereas thermal regimes under rocks showed large diurnal fluctuations. Geckos selected crevices that were deeper, had less canopy cover, and were warmer than most available crevices; in 85% of cases, such crevices were used simultaneously by more than one female. The thermally distinctive attributes of nest sites, and their frequent communal use, suggest that nest sites are a scarce resource for female velvet geckos, and that the shading of rock outcrops through vegetation encroachment may influence nest success in this species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 250–259.     

Modelling exposure to selected temperature during pregnancy: the limitations of squamate viviparity in a cool-climate environment

Behavioural thermoregulation is important for the success of cool‐climate lizards, and a basis of the cold‐climate hypothesis for the evolution of viviparity in squamate reptiles. The temperature (T_sel) selected by pregnant females in a thermal gradient is considered to be optimal for embryonic development; however, exposure to T_sel throughout pregnancy has been difficult to estimate in small‐bodied lizards as temperature‐sensitive telemetry is impractical. In addition, the value of maternal thermophily during pregnancy is controversial: some studies have shown elevated T_sel, whereas others have found lowered T_sel or no change during pregnancy. We estimated indirectly the overall exposure to T_sel during the 4–5 months of pregnancy of the cool‐climate, sub‐alpine species Oligosoma maccanni (McCann's skink, 3–6 g) from southern New Zealand. The thermal environment available to skinks was modelled using temperature loggers inside validated copper models in basking and retreat sites. Pregnant skinks were able to achieve mean T_sel (28.9 °C) in the field very infrequently (4–15% of each month during the final 4 months of pregnancy). In field thermoregulatory studies, pregnant females did not bask more frequently and did not show altered field body temperature compared with non‐pregnant adults, suggesting that all skinks (whether pregnant or not) thermoregulate maximally whenever conditions allow. Further research on cool‐climate lizards should address the significance for offspring phenotypes of low and variable exposure to T_sel during pregnancy, as well as the significance of temperatures for embryos in maternal bodies (viviparity) versus nest sites (oviparity) arising from differences in maternal body size. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96 , 541–552.     

Effects of Maternal Basking and Food Quantity during Gestation Provide Evidence for the Selective Advantage of Matrotrophy in a Viviparous Lizard

The evolution of matrotrophy (i.e., direct supply of nutrients by the mother during gestation) may be associated with high maternal energy availability during gestation. However, we lack knowledge about the selective advantages of matrotrophic viviparity (live-bearing) in reptiles. In reptiles, the interaction between body temperature and food intake affect maternal net energy gain. In the present study, we examined the effects of basking and food availability (2 by 2 factorial design) during gestation on offspring phenotype in a matrotrophic viviparous lizard (Pseudemoia entrecasteauxii). Subsequently, we investigated if the maternal effects were context-dependent using offspring growth rate as an indicator of the adaptive significance of matrotrophy. Offspring were exposed either to the same thermal conditions as their mothers experienced or to thermal conditions different from those experienced by their mothers. We provide the first evidence that an interaction between maternal thermal and maternal food conditions during gestation strongly affects offspring phenotype, including date of birth, body size and performance ability, which affect offspring fitness. Offspring growth rate was dependent on offspring thermal conditions, but was not influenced by maternal effects or offspring sex. Matrotrophic viviparity provided gravid females with the means to enhance offspring fitness through greater energetic input to offspring when conditions allowed it (i.e., extended basking opportunity with high food availability). Therefore, we suggest that selective advantages of matrotrophic viviparity in P. entrecasteauxii may be associated with high maternal energy availability during gestation.     

Reproducing lizards modify sex allocation in response to operational sex ratios

Sex-allocation theory suggests that selection may favour maternal skewing of offspring sex ratios if the fitness return from producing a son differs from that for producing a daughter. The operational sex ratio (OSR) may provide information about this potential fitness differential. Previous studies have reached conflicting conclusions about whether or not OSR influences sex allocation in viviparous lizards. Our experimental trials with oviparous lizards (Amphibolurus muricatus) showed that OSR influenced offspring sex ratios, but in a direction opposite to that predicted by theory: females kept in male-biased enclosures overproduced sons rather than daughters (i.e. overproduced the more abundant sex). This response may enhance fitness if local OSRs predict survival probabilities of offspring of each sex, rather than the intensity of sexual competition.     

Do operational sex ratios influence sex allocation in viviparous lizards with temperature‐dependent sex determination?

Under certain environmental situations, selection may favour the ability of females to adjust the sex ratio of their offspring. Two recent studies have suggested that viviparous scincid lizards can modify the sex ratio of the offspring they produce in response to the operational sex ratio (OSR). Both of the species in question belong to genera that have also recently been shown to exhibit temperature-dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field-based experiments, and conduct the first field-based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring.     

The sooner the better: reproductive phenology drives ontogenetic trajectories in a temperate squamate (Podarcis muralis)

Understanding variations in individual trajectories is a crucial evolutionary issue. Terrestrial ectotherms from temperate regions typically face thermal constraints and limited activity periods. Developmental conditions (i.e. embryonic life) and reproductive timing (laying date) should induce phenotypic variations and influence subsequent ontogenetic trajectories (growth and survival). We studied these combined influences in an oviparous squamate, the wall lizard (Podarcis muralis), comprising a multiple clutch species with natural variations in laying date for the first clutch. We experimentally manipulated maternal basking opportunities during gravidity (3, 6 or 9 h per day) and incubation temperature (23 or 29 °C). Early laying date positively influenced winter survival in both incubation treatments. Survival was significantly lower in cool than warm‐incubated individuals (14.8% and 73.6%, respectively) because of delayed hatching date and reduced activity period before winter. Individuals from cool incubation temperature were slightly smaller but had a higher body condition and grew faster during the first month of life. Offspring behaviour was driven by complex interactions between gravidity and incubation treatments. Under cool incubation temperature, defensive behaviour was high, independently of gravidity treatment. Warm incubated individuals showed low defensive response except when maternal basking opportunities were restricted to 3 h. Defensive behaviour at birth had a positive influence on survival in cool‐incubated individuals. The results of the present study highlight the long‐term influence of hatching date that integrates female reproductive timing and incubation conditions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 00, 000–000.     

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.     

Guppies control offspring size at birth in response to differences in population sex ratio

Females that invest adaptively in their offspring are predicted to channel more resources to the sex that will be at an advantage in the prevailing environmental conditions. Here, we report, for the first time, that female Trinidadian guppy, Poecilia reticulata, respond in reproductively distinct ways when faced with differences in operational sex ratio. We show that females assigned to a female‐biased sex ratio produce larger male offspring than females in an environment in which males predominate. Given the link between size at birth and fitness, and the marked reproductive skew in this species, larger male offspring are expected to have reproductive advantages in guppy populations with an excess of females. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 414–419.     

Late stage deferral of parturition in the viviparous lizard Niveoscincus ocellatus (Gray 1845): implications for offspring quality and survival

The ability of viviparous lizards to defer parturition after completion of embryonic development is a potentially key strategy for enhancing offspring fitness. Using the spotted snow skink, Niveoscincus ocellatus , we investigated the ability of females to defer birth if placed into cold conditions at the same time, for 1, 2 or 3 weeks at the end of gestation. The ability to defer birth was compared between two populations at each end of the species' altitudinal range. We hypothesized that females from the high elevation population would be less likely to defer parturition under extended periods of poor conditions, thus ensuring that young were not born too late in the season. In all but the 3-week treatment group from the high elevation population, females were able to defer birth when placed under cold conditions: for all groups, there was no treatment effect on offspring phenotype at birth, dispersal distance or survivorship after release. However, there was a significant negative effect of treatment on offspring growth measured after release, with the results differing between the populations. Females from the high elevation population were less able to defer birth under long periods (3 weeks) of cold conditions, and this was accompanied by a decrease in viability of the offspring.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 735–746.     

Extended gestation with late‐autumn births in a cool‐climate viviparous gecko from southern New Zealand (Reptilia: Naultinus gemmeus)

Abstract Female viviparous lizards from temperate locations in the Southern Hemisphere (New Zealand, Tasmania (Australia), South Africa and South America) often have reproductive activity spanning many months of the year. In contrast, vitellogenesis and pregnancy are often confined to the spring/summer months in viviparous species from temperate zones of the Northern Hemisphere. An extreme Southern Hemisphere example is the nocturnal common gecko from New Zealand, Hoplodactylus maculatus (Gray 1845), in which females exhibit biennial reproduction with pregnancy lasting up to 14 months in a cool‐climate population. Here, we examined whether such an extended reproductive cycle also occurs in a diurnal species, the jewelled gecko Naultinus gemmeus (McCann 1955), at a similar latitude. Palpation was used to assess reproductive condition non‐invasively. In contrast to the nearby higher‐altitude population of H. maculatus, N. gemmeus reproduces annually. Vitellogenesis occurs from autumn to spring in both species, but pregnancy ends after about 7 months in N. gemmeus. Birth occurs in the seemingly unpropitious season of mid‐ to late autumn, a pattern that may be unique for lizards from cool‐temperate zones. We hypothesize that there are major differences between populations of N. gemmeus and H. maculatus with respect to survival of autumn‐born neonates and/or costs to females from remaining pregnant over winter. Museum specimens of N. gemmeus support anatomical inferences from palpation; they also suggest that vitellogenesis may begin before the end of pregnancy (which may be essential to completing each reproductive cycle within a year) and that some populations may show gestation in utero over winter, as in H. maculatus. Extended gestation appears to be a common response to cool climates for Southern Hemisphere lizards that have independently evolved viviparity.     

Age‐related change in melanin‐based coloration of Barn owls (Tyto alba): females that become more female‐like and males that become more male‐like perform better

Ornament expression fluctuates with age in many organisms. Whether these changes are adaptively plastic is poorly known. In order to understand the ultimate function of melanin‐based ornaments, we studied their within‐individual fluctuations and their covariation with fitness‐related traits. In barn owls (Tyto alba), individuals vary from reddish‐brown pheomelanic to white, and from immaculate to marked with black eumelanic spots, with males being less reddish and less spotted than females. During the first molt, both sexes became less pheomelanic, females displayed larger spots and males fewer spots, but the extent of these changes was not associated with reproduction. At subsequent molts, intra‐individual changes in melanin‐based traits covaried with simultaneous reproduction changes. Adult females bred earlier in the season and laid larger eggs when they became scattered with larger spots, whereas adults of both sexes produced larger broods when they became whiter. These results suggest that the production of melanin pigments and fitness‐related life‐history traits are concomitantly regulated in a sex‐specific way. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 689–704.     

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.