Maternal Effects Associated with Gestation Conditions in a Viviparous Lizard, Niveoscincus metallicus

Interpopulational variation in reproductive costs may affect variation in life history traits including reproductive investment (i.e. clutch mass relative to either maternal body mass or length). While the relationships between reproductive investment and costs of reproduction, especially costs to mobility, have been well studied in squamate reptiles, how these costs relate to investment and explain patterns within and between populations is not always straightforward. In the present study, we examined the relationship between reproductive investment and costs of reproduction (gravid and postpartum sprint speeds and maternal postpartum body condition) in two populations of a viviparous skink, Pseudemoia entrecasteauxii living in different habitat types. We found that costs of reproduction (i.e. impact on gravid and postpartum sprint speeds) depended on the interaction between relative reproductive burden (RRB) and population. There was no link between relative clutch mass (RCM) and maternal sprint speeds. Maternal postpartum body condition was not related to either RRB or RCM for either population. Gravid females living in the open habitat population showed significantly slower sprint speed compared with the same females immediately postparturition, and other gravid females living in a closed habitat population. Such females are likely to experience a higher cost of reproduction in terms of changes in sprint speed as well as exposure to predators and may show a behavioural shift to crypsis in order to compensate for locomotor impairment and to reduce the risk of predation. We suggest that factors which relate to costs of reproduction (i.e. sprint speeds) are complex and may involve multiple factors such as reproductive investment and habitat characteristics.

Relative clutch mass (RCM; the ratio of clutch to female body mass), a measure of the physical burden imposed on gravid females, is considered an important life history trait in reptiles. Several authors (Vitt and Congdon, 1978; Vitt, 1981; Vitt and Price, 1982; Seigel and Fitch, 1984) have hypothesized that RCM has evolved through differential mortality resulting from decreased locomotor ability and increased energetic costs of locomotion associated with transporting the added mass of the clutch. Three lines of evidence support this hypothesis or its assumptions. First, comparative studies (Vitt and Congdon, 1978; Vitt and Price, 1982; Seigel and Fitch, 1984) have shown that high RCM values are found in lizards that do not rely on fast movement for foraging and escaping (sit-and-wait foraging, cryptic escape behavior), and in oviparous snakes; low RCM is associated with active foraging and fleeing escape behavior in lizards, and with viviparity in snakes. Secondly, intraspecific studies have shown a reduction of sprint speed (Shine, 1980; Bauwens and Thoen, 1981; Garland, 1985; Seigel et al., 1987) or endurance (Seigel et al., 1987) in gravid lizards and snakes. Thirdly, differences among individuals in sprint speed and RCM have been identified in four scincid lizards (Shine, 1980) and one snake (Seigel et al., 1987). The latter studies strongly suggest that the added clutch mass exerts a direct negative effect on the locomotor performance of gravid females. In this note we document the relation between sprint velocity and RCM in gravid females of the lizard Lacerta vivipara. Lacerta vivipara is a small (adult body length: 45-65 mm) viviparous lizard that reproduces once a year. It is an agile lizard that forages actively on insects and other invertebrates (Avery, 1966; Itamies and Koskela, 1971; Koponen and Hietakangas, 1972; Pilorge, 1982), behaves like a typical heliotherm (Avery, 1976; Van Damme et al., 1987), and uses crypsis, flight and tail autotomy to escape from predators (Bauwens and Thoen, 1981). At parturition, this species has a remarkably high RCM (=clutch mass/female body mass after parturition). Mean values observed in different populations/years are: 0.81 (Bauwens and Thoen, 1981), 0.41-1.02 (Pilorge et al., 1983), 0.45-0.56 (Pilorge 1987) and 0.63 (this study). These values are among the highest reported for lizards in general (x = 0.29; range 0.05-0.68) as well as in live-bearing species (x = 0.31; range 0.13-0.48; recalculated from table 1 in Vitt and Price, 1982). During April 1984, we captured adult female lizards in the Belgian national nature reserve de Kalmthoutse heide (51?25'N, 4?25'E, Province of Antwerp, Belgium). They were mated in the laboratory and maintained individually in outdoor enclosures until parturition. About two weeks (x = 14.9 days, range: 8-25) before parturition, we determined sprint speeds of 17 gravid and 6 nongravid adult females by chasing them by hand down a 2 m racetrack (Huey et al., 1981). The t ack was constructed of plywood with walls 30 cm high positioned 15 cm apart; its floor was covered with carpet that provided excellent traction. Nine pairs of photocells measured the time the lizards needed to cover 8 consecutive intervals of 25 cm. Before test-

Both excessive and restricted fetal growth are associated with changes in cardiac geometry and function at birth. There are significant issues when indexing cardiac parameters for body size in the neonatal period. The aims of this study were to determine to what extent cardiac geometry is dependent on body size in term and preterm neonates with restricted or excessive fetal growth and how this is affected by adiposity. This was a cross-sectional study of neonates born between 31 and 42 weeks of gestation, divided into three groups: (1) small-for-gestational age (SGA, birth weight > 2 SD below the mean); (2) large-for-gestational age (LGA, birth weight > 2 SD above the mean); and (3) appropriate-for-gestational-age controls (AGA, birth weight ≤ 2 SD from the mean). Cardiac geometry and function were compared between the study groups, adjusting for body size. The potential impact of infant adiposity and maternal disease was assessed. In total, 174 neonates were included, of which 39 were SGA, 45 were LGA and 90 were AGA. Body size was reflected in cardiac dimensions, with differences in cardiac dimensions disappearing between the SGA and AGA groups when indexed for body surface area (BSA) or thoracic circumference. The same was true for the differences in atrial and ventricular areas between the LGA and AGA groups. However, left ventricular inflow and outflow tract dimensions did not follow this trend as, when indexed for BSA, they were associated negatively with adiposity, resulting in diminished dimensions in LGA compared with AGA and SGA neonates. Adiposity was associated positively with left ventricular mass, right ventricular length and area and right atrial area. The SGA group showed increased right ventricular fractional area change, possibly reflecting differences in the systolic function of the right ventricle. We found evidence of altered diastolic function between the groups, with the mitral valve inflow E- to lateral E'-wave peak velocity ratio being increased in the LGA group and decreased in the SGA group. Cardiac geometry is explained by body size in both term and preterm AGA and SGA infants. However, the nature of the relationship between body size and cardiac dimensions may be influenced by adiposity in LGA infants, leading to underestimation of left ventricular inflow and outflow tract dimensions when adjusted for BSA. Adjustments for thoracic circumference provide similar results to those for BSA. Copyright © 2020 ISUOG. Published by John Wiley & Sons Ltd.

The effect of caudal autotomy on reproductive investment in females of a viviparous skink, Niveoscincus metallicus, was investigated to examine the relative importance of lipid depletion and energetic diversion to this activity. Although abdominal fat bodies are present, this species stores most of its energetic reserves in the tail. Since caudal fat is preferentially aggregated toward the base of the tail, autotomy and lipid depletion may be mutually exclusive events. Reproductive consequences following tail loss associated with significant loss of caudal fat were compared with those following autotomy involving no fat loss in two groups of females: females that had lost their tail during their most recent vitellogenic period; and females in which tail loss had occurred in a previous reproductive season. Caudal autotomy during vitellogenesis resulted in a significant reduction in litter size, irrespective of the position of tail loss, suggesting that smaller litters were a consequence of the diversion of energetic resources from reproduction to tail regeneration, rather than the loss of fat reserves per se. However, offspring from mothers that experienced tail loss during vitellogenesis without associated loss of fat reserves were significantly larger in size (snout–vent length and mass) and had longer tails than those from any other group. We suggest that this was probably achieved through facultative placental transfer during gestation, although the possibility that more yolk was allocated to each egg cannot be discounted. Sprint speed and the size of abdominal fat reserves at birth and postnatal growth were not correlated with either recency of autotomy or the location of the tail break.

The effect of caudal autotomy on reproductive investment in females of a viviparous skink, Niveoscincus metallicus, was investigated to examine the relative importance of lipid depletion and energetic diversion to this activity. Although abdominal fat bodies are present, this species stores most of its energetic reserves in the tail. Since caudal fat is preferentially aggregated toward the base of the tail, autotomy and lipid depletion may be mutually exclusive events. Reproductive consequences following tail loss associated with significant loss of caudal fat were compared with those following autotomy involving no fat loss in two groups of females: females that had lost their tail during their most recent vitellogenic period; and females in which tail loss had occurred in a previous reproductive season. Caudal autotomy during vitellogenesis resulted in a significant reduction in litter size, irrespective of the position of tail loss, suggesting that smaller litters were a consequence of the diversion of energetic resources from reproduction to tail regeneration, rather than the loss of fat reserves per se. However, offspring from mothers that experienced tail loss during vitellogenesis without associated loss of fat reserves were significantly larger in size (snout–vent length and mass) and had longer tails than those from any other group. We suggest that this was probably achieved through facultative placental transfer during gestation, although the possibility that more yolk was allocated to each egg cannot be discounted. Sprint speed and the size of abdominal fat reserves at birth and postnatal growth were not correlated with either recency of autotomy or the location of the tail break.

Captive breeding is an important conservation measure that may restore and enhance wild populations of rare and endangered species. Multiple anthropogenic hazards have brought the crocodile lizard, Shinisaurus crocodilurus, to the brink of extinction. We initiated a captive breeding program and quantified female reproductive traits, including reproductive timing, litter size, litter mass, and neonate size. To identify the internal and external factors affecting female reproductive function, we then analyzed how maternal age is related to body size, temperature, and female reproductive traits. We found that larger female crocodile lizards produced more offspring than smaller ones, as both litter size and litter mass were positively related to maternal body size. In contrast, neonate size was independent of maternal body size. Maternal reproductive output varied among different age groups. Young and old females had significantly smaller living litter size and mass than middle-aged females. Among captive females, one-third exhibited early parturition in autumn and winter instead of the following spring, a pattern probably associated with higher ambient temperatures in captivity. Although female reproductive output and neonatal body size did not differ between early- and normal-parturition females, offspring from the former group died earlier than those from the latter. Our study highlights the danger of climate change in hastening parturition, a phenomenon that could significantly hamper neonate survival and impede population recruitment.

Summary Tail loss has repeatedly been associated with the impairment of locomotor performance in lizards. However, although the immediate impact of tail loss may be severe, most previous studies have failed to establish how long such locomotory costs persist. We investigated both the short‐term (24–36 h) and long‐term (4 and 12 weeks) consequences of tail loss on locomotor performance in a viviparous ground‐dwelling skink, Niveoscincus metallicus (O’Shaughnessy 1874). Sprint speed, climbing ability and stamina were measured as performance variables. The locomotor performance of both adult males and pregnant females were tested during the study. Male and female lizards responded differently to tail loss, although the immediate impact of autotomy on performance was generally minor. In males caudal autotomy imposed a significant immediate impact on sprint speed, while in females stamina was reduced immediately after autotomy. Females regenerated their tails significantly faster than males. Recovery of locomotor performance over the 3‐month duration of the study was observed in females (for endurance capacity) but not males (for sprint speed). Overall, the impact of tail loss on locomotor performance was generally limited or short‐lived in N. metallicus.

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.

Summary Locomotor impairment and shift in thermal preferences during gestation have been documented in some lizards, but few studies have investigated their timing. Here, endurance capacity, sprint speed and selected body temperature of gravid females of the viviparous lizard Lacerta vivipara (Jacquin) were measured weekly before and after parturition. Significant temporal variation of endurance and sprint speed was detected. A marked decrease in locomotor abilities occurred 2 weeks before parturition (c. 35% for endurance and 25% for sprint speed). A rapid recovery was observed a few days after parturition for endurance, while sprint speed recovered more slowly. A physical impairment due to body mass was detected for endurance capacity, but not for sprint speed. The recovery of locomotor abilities after parturition was independent of the intensity of reproductive investment. Mass‐independent variation in locomotor performances might be explained by physiological consequences of reproduction independent of the physical burden. Females basking under laboratory conditions selected low body temperatures during the final month of gestation (29·8 °C ± 0·12 SE) and a drastic increase occurred in the few days following parturition (33·4 °C ± 0·13 SE). These results call for a more detailed investigation of the mechanisms underlying trade‐offs between reproduction, locomotion and thermoregulation in lizards.

Chemoreception is a common mechanism used by many species to detect the presence of a potential predator and subsequently respond to it. The perceived risk of predation may force retreat to suboptimal conditions, forcing a trade-off between the risk of predation and the ability to acquire resources. Responses to chemical cues of predators vary as a result of past experience, ontogeny, or reproductive state. The basking regime maintained by gravid females of the viviparous skink, Eulamprus tympanum, may directly alter sex ratios of offspring produced through temperature-dependent sex determination. The avoidance of predator scents may restrict basking ability and, in turn, alter the sex of offspring produced. We measured responsiveness to chemical cues using tongue flicks as an indicator of chemical discrimination in adult females and neonates and in females of different reproductive condition. We then measured activity rates and basking behavior of females in experimental enclosures in the presence of various chemical stimuli to determine whether basking opportunity is compromised by the presence of a predator scent. Neonates respond significantly more than nonreproductive adult females to all chemical stimuli suggesting an age-specific shift in response, whereas adult females respond differently depending upon reproductive state. Under laboratory conditions, gravid females modify their behavior and forego the opportunity to bask when there is a perceived predation risk. However, further experimentation conducted under field conditions would be necessary to test fully the hypothesis that basking opportunity is compromised by the presence of a predator stimulus and, in turn, could alter offspring sex ratios.

Environmental (i.e. non-genetic) maternal effects have the potential to associate the environmental conditions faced by mothers during gestation or before egg laying with the phenotype of their offspring. For this reason, maternal effects may play a major role in determining offspring phenotype independently of the genotype of the individuals, and can thus be considered a mechanistic basis of phenotypic plasticity. Despite the ecological and evolutionary implications of environmental maternal effects, few studies have experimentally investigated this phenomenon in reptiles. Here we report the results of an experimental laboratory study on the effects of maternal feeding rate and density on offspring locomotor performance in the common lizard (Lacerta vivipara). Lacerta vivipara is a viviparous lizard, and viviparity enhances the probability of a maternal influence on offspring phenotype. We focused on a particular phenotypic trait, maximal sprint running speed, because this trait is thought to be selectively important in squamates. Sprint speed was a repeatable trait, and it varied significantly among families. Maternal feeding rate significantly affected sprint speed, whereas density had no effect on this trait. The effect of maternal feeding rate differed according to the sex of the offspring and their body size, resulting in significant two-way and three-way interactions among these factors. In other words, the maternal feeding rate changed the shape of the allometric relationship between-speed and size, but differently for males and females. The complexity of such effects makes it extremely difficult to offer an adaptive interpretation, but emphasizes the role played by the environment in shaping phenotypes among generations.

Parent-offspring conflicts are widespread given that resources are often limited. Recent evidence has shown that availability of water can trigger such conflict during pregnancy in viviparous squamate species (lizards and snakes) and thus questions the role of water in the evolution of reproductive modes. Here, we examined the impact of water restriction during gravidity in the oviparous form of the bimodal common lizard (Zootoca vivipara), using a protocol previously used on the viviparous form. Females were captured in early gravidity from six populations along a 600 m altitudinal gradient to investigate whether environmental conditions (altitude, water access and temperature) exacerbate responses to water restriction. Females were significantly dehydrated after water restriction, irrespective of their reproductive status (gravid vs. non-reproductive), relative reproductive effort (relative clutch mass), and treatment timing (embryonic development stage). Female dehydration, together with reproductive performance, varied with altitude, probably due to long term acclimation or local adaptation. This moderate water-based intergenerational conflict in gravid females contrasts sharply with previous findings for the viviparous form, with implications to the evolutionary reversion from viviparity to oviparity. It is likely that oviparity constitutes a water-saving reproductive mode which might help mitigate intensive temperature-driven population extinctions at low altitudes.

The aim of this study was to determine the predictive value of maternal serum lipid levels during late pregnancy for neonatal body size. This study was conducted from January 1, 2011 to July 31, 2012 at a Maternal and Child Health Hospital. Fasting blood glucose, serum triglyceride, total cholesterol, HDL and LDL were estimated in maternal collected before delivery. Detailed anthropometry of the neonates was performed. Women who delivered a large for gestational age baby were older, taller, had a higher pre-pregnancy weight, higher pre-pregnancy BMI, and higher weight gain during pregnancy than women who delivered an appropriate for gestational age infant. After adjusting for maternal age, pre-pregnancy BMI, weight gain during pregnancy, parity, neonatal sex and gestational age at delivery, we found that only maternal HDL level was inverse associated with birth weight, length and head circumference (p<0.05). On logistic regression analysis, the significant metabolic predictors of large for gestational age was HDL (OR 0.57, 95%CI: 0.38-0.84, per 1 mmol/L increase) after adjusting for the confounders. Maternal serum HDL level determined in maternal blood taken close to delivery was independently associated with neonatal size and was the independent predictor for large for gestational age.

ObjectiveTo estimate associations between changes in maternal arterial pressure during normotensive pregnancies and offspring birthweight and body composition at birth.Study DesignProspective study of 762 pregnant normotensive Colorado women, recruited from outpatient obstetrics clinics. Repeated arterial pressure measurements during pregnancy were averaged within the second and third trimesters, respectively. Multivariable regression models estimated associations between second to third trimester changes in arterial pressure and small-for-gestational-age birthweight, fat mass, fat-free mass, and percent body fat.ResultsA greater second to third trimester increase in maternal arterial pressure was associated with greater odds of small-for-gestational-age birthweight. Greater increases in maternal diastolic blood pressure were associated with reductions in offspring percent body fat (−1.1% in highest versus lowest quartile of increase, 95% confidence interval: −1.9%, −0.3%).ConclusionsMid-to-late pregnancy increases in maternal arterial pressure which do not meet clinical thresholds for hypertension are associated with neonatal body size and composition.

The ubiquitous presence of endocrine-disrupting chemicals (EDCs) in the environment is of major concern. Studies on oviparous reptiles have significantly advanced knowledge in this field; however, 30% of reptilian species are viviparous (live-bearing), a parity mode in which both yolk and a placenta support embryonic development, thus exposure to EDCs may occur via multiple routes. In this first study of endocrine disruption in a viviparous lizard (Niveoscincus metallicus), we aimed to identify effects of the oestrogen mimic diethylstilbestrol (DES) on gonadal development. At the initiation of sexual differentiation, pregnant N. metallicus were treated with a single dose of DES at 100 or 10µgkg(--1), a vehicle solvent or received no treatment. There was no dose-response effect, but the testes of male neonates born to DES-exposed mothers showed reduced organisation of seminiferous tubules and a lack of germ cells compared with those from control groups. The ovaries of female neonates born to DES-exposed mothers exhibited phenotypic abnormalities of ovarian structure, oocytes and follicles compared with controls. The results indicate that, in viviparous lizards, maternal exposure to oestrogenic EDCs during gestation may have profound consequences for offspring reproductive fitness.