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.     

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.     

The effect of ambient temperature on turkey embryonic development at oviposition

Stage of embryonic development at oviposition was measured in turkey breeder hens maintained in relatively warm and cool environments. The premise was that variations in embryonic development at oviposition might account for the decreased hatchability associated with warm summer temperatures. No treatment effect was found, as judged by somite counts after 52 h of incubation. Variation in embryonic development was as great within a hen as between hens, indicating that causative factor(s) other than stage of development at oviposition is the reason for reduced hatch of fertile eggs during periods of relatively high environmental temperature.     

Reptilian endothermy: a field study of thermoregulation by brooding diamond pythons

Miniature temperature-sensitive radiotransmitters were surgically implanted into free-ranging adult diamond pythons ( Morelia s. spilota ), which are medium-sized boid snakes of south-eastern Australia. Four female pythons oviposited during the study, and constructed incubation mounds. These apparently provided excellent insulation, and the snakes maintained high (approx. 31 C) and relatively constant body temperatures throughout the two-month incubation period. They apparently maintained these temperatures primarily by endogenous heat production (shivering thermogenesis), but also basked briefly on most mornings.
Brooding females maintained a body temperature differential above ambient of about 9C, occasionally up to 13C; their temperatures were significantly higher amd less variable than those of non-brooding females or males. The energetic cost of brooding must be high, but these costs may be outweighed by the benefits of rapid embryonic development and high embryonic survivorship.     

Potential targets for selection during the evolution of viviparity in cold-climate reptiles

Viviparity (live-bearing) has evolved from oviparity (egg-laying) in more than 100 lineages of squamate reptiles (lizards and snakes). This transition generally has occurred in cool climates, where thermal differentials between eggs in the (cool) nest versus the (warm) maternal oviduct influence embryonic development, in ways that may enhance offspring fitness. To identify specific traits potentially under selection, we incubated eggs of a montane scincid lizard at conditions simulating natural nests, maternal body temperatures, and an intermediate stage (2-week uterine retention of eggs prior to laying). Incubation at maternal temperatures throughout incubation affected the hatchling lizard’s activity level and boldness, as well as its developmental rate, morphology, and locomotor ability. A treatment that mimicked the initial stages of the transition toward viviparity had a major effect on some hatchling traits (locomotor speeds), a minor effect on others (tail length, total incubation period) and no effect on yet others (offspring behaviors). More generally, different aspects of the phenotype are sensitive to incubation conditions at different stages of development; thus, the evolution of reptilian viviparity may have been driven by a succession of advantages that accrued at different stages of embryogenesis.     

Gold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus

Evolutionary origins of viviparity among the squamate reptiles are strongly associated with cold climates, and cold environmental temperatures are thought to be an important selective force behind the transition from egg-laying to live-bearing. In particular, the low nest temperatures associated with cold climate habitats are thought to be detrimental to the developing embryos or hatchlings of oviparous squamates, providing a selective advantage for the retention of developing eggs in utero, where the mother can provide warmer incubation temperatures for her eggs (by actively thermoregulating) than they would experience in a nest. However, it is not entirely clear what detrimental effects cold incubation temperatures may have on eggs and hatchlings, and what role these effects may play in favouring the evolution of viviparity. Previous workers have suggested that viviparity may be favoured in cold climates because cold incubation temperatures slow cmbryogenesis and delay hatching of the eggs, or because cold nest temperatures are lethal to developing eggs and reduce hatching success. However, incubation temperature has also been shown to have other, potentially long-term, effects on hatchling phcnotypcs, suggesting that cold climates may favour viviparity because cold incubation temperatures produce offspring of poor quality or low fitness. We experimentally incubated eggs of the oviparous phrynosomatid lizard, Sceloporus virgatus, at temperatures simulating nests in a warm (low elevation) habitat, as is typical for this species, and nests in a colder (high elevation) habitat, to determine the effects of cold incubation temperatures on embryonic development and hatchling phenotypes. Incubation at cold nest temperatures slowed embryonic development and reduced hatching success, but also affected many aspects of the hatchlings' phenotypes. Overall, the directions of these plastic responses indicated that cold-incubated hatchlings did indeed exhibit poorer quality phenotypes; they were smaller at hatching (in body length) and at 20 days of age (in length and mass), grew more slowly (in length and mass), had lower survival rates, and showed greater fluctuating asymmetry than their conspecifics that were incubated at warmer temperatures. Our findings suggest that cold nest temperatures are detrimental to S. virgatus, by delaying hatching of their eggs, reducing their hatching success, and by producing poorer quality offspring. These negative effects would likely provide a selective advantage for any mechanism through which these lizards could maintain warmer incubation temperatures in cold climates, including the evolution of prolonged egg retention and viviparity.     

Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard

Interspecific comparisons suggest a strong association between cool climates and viviparity in reptiles. However, intraspecific comparisons, which provide an opportunity to identify causal pathways and to distinguish facultative (phenotypically plastic) effects from canalized (genetically fixed) responses, are lacking. We documented the reproductive traits in an alpine oviparous lizard, and manipulated thermal regimes of gravid females and their eggs to identify proximate causes of life‐history variation. Embryonic development at oviposition was more advanced in eggs laid by females from high‐elevation populations than in eggs produced by females from lower elevations. In the laboratory, experimentally imposed low maternal body temperatures delayed oviposition and resulted in more advanced embryonic development at oviposition. Warm conditions both in utero and in the nest increased hatching success and offspring body size. Our intraspecific comparisons support the hypothesis that viviparity has evolved in cold‐climate squamates because of the direct fitness advantages that warm temperatures provide developing offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 642–655.     

恒定和波动温度下丽斑麻蜥孵出幼体的表型变异

作者以丽斑麻蜥(Eremias argus)为模型动物研究恒定和波动孵化温度对孵化成功率和孵出幼体表型的影响。卵在四个恒定[24 ,27 ,30 and 33 (±0·3)℃]、一个波动温度下孵化。不同温度处理下的孵化成功率相同,但孵出幼体表型不同。孵化期随孵化温度升高呈指数式缩短;在相同平均温度下,波动温度孵化卵的孵化期比恒温孵化卵长。在所有被检表型特征中,幼体的干重、剩余卵黄干重和运动表现更易受孵化温度影响。总体而言,低温(24℃、27℃)孵出幼体运动表现最佳,高温(33℃)孵出幼体最差、温和温度(30℃和波动温度)孵出幼体居中。本文研究数据显示: (1)丽斑麻蜥卵每日短期暴露于潜在致死的极端温度下对孵化成功率和孵出幼体形态特征无明显的不利效应; (2)温度波动对孵出幼体运动表现无促进作用,对孵化期的影响则不同于平均值相同的恒定温度。     

Geographic variation in hatchling size in an oviparous skink: effects of maternal investment and incubation thermal environment

Geographic variation in offspring size can be viewed as an adaptive response to local environmental conditions, but the causes of such variation remain unclear. Here, we compared the size and composition of eggs laid by female Chinese skinks (Plestiodon chinensis) from six geographically distinct populations in southeastern China to evaluate geographic variation in hatchling size. We also incubated eggs from these six populations at three constant temperatures (24, 28 and 32 °C) to evaluate the combined effects of incubation temperature and population source on hatchling size. Egg mass and composition varied among populations, and interpopulation differences in yolk dry mass and energy content were still evident after accounting for egg mass. Population mean egg mass and thus hatchling mass were greater in the colder localities. Females from three northern populations increased offspring size by laying larger eggs relative to their own size. Females from an inland population in Rongjiang could increase offspring size by investing relatively more dry materials and thus more energy into individual eggs without enlarging the size of their eggs. The degree of embryonic development at oviposition was almost the same across the six populations, so was the rate of embryonic development and thus incubation length at any given temperature. Both incubation temperature and population source affected hatchling traits examined, but the relative importance of these two factors varied between traits. Our data show that in P. chinensis hatchling traits reflecting overall body size (body mass, snout‐vent length and tail length) are more profoundly affected by population source. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 283–296.     

Geographic variation in avian incubation periods and parental influences on embryonic temperature

Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incubation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incubation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized.     

Thermal performance of squamate embryos with respect to climate,adult life history,and phylogeny

Reptiles are important model systems for examining the effect of temperature during development on the phenotype of individuals after hatching or birth. To assess whether squamate embryos exhibit adaptive variation in thermal biology, we derived three parameters: an index of developmental rate (DRI), the upper thermal limit for successful incubation, and the lower thermal limit for development for 28 species of lizard and 12 species of snake. The associations between developmental parameters and climatic and life‐history variables were examined using both conventional statistics and phylogenetically controlled analyses. Residual DRI (i.e. DRI corrected for stage at oviposition and hatchling mass) was strongly associated with phylogenetic relationship. By contrast, the upper limit for development was negatively related to the amount of precipitation during the warmest quarter of the year, and the lower thermal limit for development was positively related to temperature during the warmest quarter of the year and the activity body temperatures of adults. These latter observations indicate that embryonic thermal physiology is adapted to large‐scale environmental patterns, and that global climate change will impact embryonic development directly through impacts on nest temperature per se, as well as indirectly through impacts on the ability of gravid females to select suitable nest sites. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Effects of constant and fluctuating temperatures on egg survival and hatchling traits in the northern grass lizard (Takydromus septentrionalis, Lacertidae)

To understand how nest temperatures influence phenotypic traits of reptilian hatchlings, the effects of fluctuating temperature on hatchling traits must be known. Most investigations, however, have only considered the effects of constant temperatures. We incubated eggs of Takydromus septentrionalis (Lacertidae) at constant (24 degrees C, 27 degrees C, 30 degrees C and 33 degrees C) and fluctuating temperatures to determine the effects of these thermal regimes on incubation duration, hatching success and hatchling traits (morphology and locomotor performance). Hatching success at 24 degrees C and 27 degrees C was higher, and hatchlings derived from these two temperatures were larger and performed better than their counterparts from 30 degrees C and 33 degrees C. Eggs incubated at fluctuating temperatures exhibited surprisingly high hatching success and also produced large and well-performed hatchlings in spite of the extremely wide range of temperatures (11.6-36.2 degrees C) they experienced. This means that exposure of eggs to adversely low or high temperatures for short periods does not increase embryonic mortality. The variance of fluctuating temperatures affected hatchling morphology and locomotor performance more evidently than did the mean of the temperatures in this case. The head size and sprint speed of the hatchlings increased with increasing variances of fluctuating temperatures. These results suggest that thermal variances significantly affect embryonic development and phenotypic traits of hatchling reptiles and are therefore ecologically meaningful.     

Effects of nest temperature and moisture on phenotypic traits of hatchling snakes (Tropidonophis mairii, Colubridae) from tropical Australia

Previous research on developmentally plastic responses by reptile embryos has paid relatively little attention to tropical species, or to possible interactions between the effects of thermal and hydric regimes. In the present study, eggs of keelback snakes ( Tropidonophis mairii ), from a tropical area with strong temporal and spatial variation in soil temperatures and moisture levels, were incubated. The phenotypic traits of hatchling snakes (body size, shape, muscular strength) were affected by moisture content of the incubation medium (vermiculite plus 100% vs. 50% water by mass), by mean incubation temperatures (25.7 vs. 27.9 °C) and by diel thermal variation (diel range 6.0 vs. 8.4 °C). Interactions between these factors were negligible. Cooler, more thermostable, moister conditions resulted in larger offspring, a trait under strong selection in this population. Thermal and hydric conditions covary in potential nest-sites (e.g. deeper nests are more thermostable as well as moister). This covariation may influence the evolution of reaction norms for embryogenesis. For example, if moister nests enhance offspring fitness and are cooler, then selection will favour the ability to develop in cool as well as moist conditions. Thus, the evolution of optimal incubation conditions with respect to one variable (e.g. temperature) may be driven by patterns of association with another variable (e.g. soil moisture) among natural nest-sites. Perhaps for this reason, the thermal optimum for incubation is surprisingly low in this tropical species.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 159–168.     

Thermal constraints on embryonic development as a proximate cause for elevational range limits in two Mediterranean lacertid lizards

Local adaptation and range restrictions in alpine environments are central topics in biogeographic research with important implications for predicting impacts of global climate change on organisms. Temperature is strongly coupled to elevation and greatly affects life history traits of oviparous reptiles in mountain environments. Thus, species may encounter barriers for expanding their ranges if they are unable to adapt to the changing thermal conditions encountered along elevational gradients. We sought to determine whether thermal requirements for embryonic development provide a plausible explanation for elevational range limits of two species of lacertid lizards that have complementary elevational ranges in a Mediterranean mountain range (Psammodromus algirus is found at elevations below 1600 m and Iberolacerta cyreni is found at elevations above 1600 m). We combined experimental incubation of eggs in the laboratory with modelled estimates of nest temperature in the field. In both species, increasing temperature accelerated development and produced earlier hatching dates. The species associated with warmer environments (P. algirus) experienced an excessive hatching delay under the lowest incubation temperature. Moreover, newborns from eggs incubated at low temperatures showed poor body condition and very slow rates of postnatal growth. In contrast, eggs of the strictly alpine species I. cyreni exhibited shorter incubation periods than P. algirus that allowed hatching before the end of the active season even under low incubation temperatures. This was countered by lower reproductive success at higher temperatures, due to lower hatching rates and higher incidence of abnormal phenotypes. Elevational range limits of both species coincided well with threshold temperatures for deleterious effects on embryonic development. We suggest that incubation temperature is a major ecophysiological factor determining the elevational range limits of these oviparous lizards with predictable consequences for mountain distributions under future warmer climates.     

Evolutionary innovations of squamate reproductive and developmental biology in the family Chamaeleonidae

The availability of molecular phylogenies has greatly accelerated our understanding of evolutionary innovations in the context of their origin and rate of evolution. Here, we assess the evolution of reproductive mode, developmental rate and body size in a group of squamate reptiles: the chameleons. Oviparity is ancestral and viviparity has evolved at least twice: Bradypodion and members of the Trioceros bitaeniatus clade are viviparous. Viviparous species are medium‐sized as a result of convergence from either small‐sized ancestors or large‐sized ancestors, respectively, but do not differ from oviparous species in clutch size, hatchling size or the trade‐off between clutch and hatchling size. Basal chameleons (Brookesia, Rhampholeon and Rieppeleon) are small‐sized and have developmental rates comparable with those of other lizards. Derived chameleons (Calumma, Chamaeleo, Trioceros and Furcifer) are mostly large‐sized and all have relatively slow developmental rates. Several clades of derived chameleons also exhibit developmental arrest (embryonic diapause or embryonic diapause plus cold torpor) and incubation periods extend to 6–10 months or more. Developmental arrest is associated with dry, highly seasonal climates in which the period favourable for oviposition and hatching is short. Long incubation periods thus ensure that hatching occurs during the favourable season following egg laying. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 656–668.     

Modelling development of reptile embryos under fluctuating temperature regimes

An increase in temperature, within bounds, will accelerate development of reptile embryos, and morphogenesis can be normal over a range of temperatures despite those varying rates of development. Less well understood is the form of the relationship that best describes variation in developmental rate with temperature. In this article, we apply a linear degree.hour model, an empirical curvilinear model, a biophysical model, and a polynomial model to data on rates of embryonic development and temperature in the pig-nosed turtle Carettochelys insculpta from northern Australia. The curvilinear models, which have been applied with success to development of insects, describe the embryonic development of turtles well. When fluctuating temperatures extend beyond the constant temperatures that support successful incubation, the curvilinear models continue to perform well, whereas the linear model predictions fail. Sensitivity analysis indicates that under some circumstances, incubation duration may be increased by diel temperature fluctuations, independent of an influence of mean temperature. In other circumstances, incubation duration may be decreased, and in still other circumstances, diel temperature fluctuations will have no impact on incubation duration. This adds an additional dimension to our understanding of how thermal regimes can be selected or manipulated by reptiles to optimise incubation duration and the timing of offspring emergence.     

Hummingbird incubation: Female attentiveness and egg temperature

Summary Incubating hummingbirds adjust nest attentiveness patterns in different habitats to permit both regulation of egg temperatures for embryonic development and foraging of the adult for positive energy balance. Anna's (Calype anna) and Black-chinned (Archilochus alexandri) Hummingbirds nesting in California chaparral left the nest six to nine times during each daylight hour. Eggs usually cooled only 3–6°C during absences but sometimes cooled up to 20°C during long absences. One Anna's Hummingbird became torpid for 4.5 h at night following a rainy day; the eggs survived cooling to 11°C and hatched two days later. A Costa's Hummingbird (Calypte costae) nesting in the California desert also left the nest several times per hour in early morning and late afternoon, but shaded the eggs almost continuously during the middle of the day. A Purple-crowned Fairy (Heliothryx barroti) in the warm lowland tropics of Panama left her eggs unattended for a few relatively long periods each day rather than many short periods as do temperate zone species. This pattern is typical of other tropical hummingbirds as well probably because equable ambient temperatures mean thermoregulation of eggs is not as critical a problem as it is in other habitats. In the temperate zone, hummingbirds exhibit behavioral adaptations (timing of reproduction, segmented foraging pattern) and physiological adaptations (torpor and hypothermia) for successful incubation. Embryonic development is successful even when egg temperatures fluctuate widely.     

Influence of incubation temperature on hatchling phenotype in reptiles

Incubation temperature influences hatchling phenotypes such as sex, size, shape, color, behavior, and locomotor performance in many reptiles, and there is growing concern that global warming might adversely affect reptile populations by altering frequencies of hatchling phenotypes. Here I overview a recent theoretical model used to predict hatchling sex of reptiles with temperature-dependent sex determination. This model predicts that sex ratios will be fairly robust to moderate global warming as long as eggs experience substantial daily cyclic fluctuations in incubation temperatures so that embryos are exposed to temperatures that inhibit embryonic development for part of the day. I also review studies that examine the influence of incubation temperature on posthatch locomotion performance and growth because these are the traits that are likely to have the greatest effect on hatchling fitness. The majority of these studies used artificial constant-temperature incubation, but some have addressed fluctuating incubation temperature regimes. Although the number of studies is small, it appears that fluctuating temperatures may enhance hatchling locomotor performance. This finding should not be surprising, given that the majority of natural reptile nests are relatively shallow and therefore experience daily fluctuations in incubation temperature.     

产卵于温暖且热稳定巢内的蜥蜴具有相对较高但较窄范围的孵化温度

作者用蜡皮蜥(Leiolepis reevesii)为模型动物,检验产卵于温暖且热稳定巢内的蜥蜴应有相对较高但较窄的孵化温度的假设。卵在三个恒定温度(27、30和33℃)、一个波动温度处理下孵化。温度的平均值而非方差影响孵化期,27、30和33℃的平均孵化期分别为101.1、69.6和55.3d。幼体性别不受孵化温度影响。不同处理孵出的幼体仅有稍许形态差异,但运动表现差异显著。27℃孵出幼体在跑道上的表现比其它处理孵出幼体差。卵能在27℃和33℃下孵化,但这两个孵化温度并不适宜。蜡皮蜥适宜的孵化温度范围可能处于最频繁的巢温变化范围(28℃-32℃)内。与其它在低温生境或温暖生境但产卵于浅巢的有鳞类爬行动物相比较,蜡皮蜥有相对较高但较窄适宜的卵孵化温度。因此,作者的数据支持上述假设。