The balance of energy allocated to development and growth of different body compartments may incur allocation conflicts and can thereby entail physiological and evolutionary consequences. ...Regeneration after autotomy restores the functionality lost after shedding a body part but requires a strong energy investment that may trade-off with other processes, like reproduction or growth. Caudal autotomy is a widespread antipredator strategy in lizards, but regeneration may provoke decreased growth rates in juveniles that could have subsequent consequences. Here, we assessed the growth of intact and regenerating hatchling wall lizards (
Podarcis muralis
) exposed to different food regimens. Regenerating juveniles presented slightly but significantly lower body growth rates than individuals with intact tails when facing low food availability, but there were no differences when food was supplied ad libitum. Regenerating individuals fed ad libitum increased their ingestion rates compared to intact ones during the period of greatest tail growth, which also reveals a cost of tail regeneration. When resources were scarce, hatchlings invested more in tail regeneration in relation to body growth, rather than delay regeneration to give priority to body growth. We propose that, in juvenile lizards, regeneration could be prioritized even at the expense of body growth to restore the functionality of the lost tail, likely increasing survivorship and the probability to reach reproductive maturity. Our study indicates that food availability is a key factor for the occurrence of trade-offs between regeneration and other growth processes, so that environmental conditions would be determinant for the severity of the costs of regeneration.
In many litter-bearing mammals and in a few viviparous reptiles the sex ratio of the entire brood or the sex of the adjacent fetuses induces sex-specific differences in the hatchling's phenotype. ...This study examines whether the sex of incubation neighbours affects hatchling characteristics in oviparous common lizards (Lacerta vivipara). Oviparous common lizards lay eggs with thin eggshells and, therefore, are an optimal model organism for studying the effects of hormone leakage among developing embryos since the strongest evidence for prenatal sex ratio effects on offspring development comes from viviparous populations of the same species. Groups of three eggs were incubated together and were categorised according to the sex of the resulting hatchlings as either homosex (three hatchlings of the same sex) or heterosex (one male or one female hatchling plus two siblings of the opposite sex). Hatchlings incubated adjacent to siblings of the same sex had larger body mass and body condition. Males tended to have lower ventral scale counts when incubated with other males. Conversely, females tended to have more ventral scales when incubated with other females, indicative of a more feminised phenotype. There was also a significant interaction between hatchling sex and incubation environment with respect to the length of the fourth digit of the hindlimb, likely indicative of masculinisation in heterosex females. This study suggests steroid diffusion between adjacent eggs in a minimally manipulative experiment and provides the first evidence for developmental effects of the exogenous hormonal environment in near natural conditions in an oviparous amniote. Implications of these results for the evolution of within-clutch sex ratio are discussed.
Autotomy has evolved independently several times in different animal lineages. It frequently involves immediate functional costs, so regeneration evolved in many instances to restore the ...functionality of that body part. Caudal autotomy is a widespread antipredator strategy in lizards, although it may affect energy storage, locomotion dynamics, or survival in future encounters with predators. Here, we assessed the effect of tail loss on the locomotor performance of wall lizards (Podarcis muralis), as well as the recovery of locomotor functionality of lizards with regenerated tails, and the movement dynamics of shed tails that were either intact or having regenerated portions. Tail loss had no effect on locomotion over unhindered spaces, possibly due to compensation between a negative effect on the stride of front limbs, and a positive effect of losing mass and friction force. We found a clear negative impact of tail loss on locomotion in spaces with interspersed obstacles, in which tailed lizards jumped larger distances when leaving the obstacles. Besides, lizards that used the tail to push off the ground were able to approach the obstacles from further, so that the tail seemed to be useful when used during jumping. Regeneration fully restores lizard's locomotor capacities, but tail antipredator value, as indicated by the intensity of post‐autotomic movements, is only partially retrieved. From these results, we propose that, together with the recovery of post‐autotomy antipredator capacities, the restoration of the organismal locomotor performance may have been an important, yet frequently neglected factor in the evolution of lizard's regeneration ability.
Autotomy is a drastic antipredator defense consisting of the voluntary shedding of a body part to escape from the predators. The loss of a body part may impair locomotion, feeding or mating, so ...animals may face a higher predation risk shortly after autotomy. Thus, until regeneration is completed, prey may adjust their behavior to reduce predation risk, and this could involve secondary costs. We assessed the effect of tail loss on the antipredator behavior of wall lizards (Podarcis muralis), comparing the behavior of tailed and tailless individuals exposed to a predatory snake (Coronella austriaca) scent, under controlled experimental conditions. Tailless lizards spent significantly more time performing behaviors with antipredatory significance (e.g., moving slowly), whereas tailed individuals performed exploratory walking for significantly more time. Moreover, tailless lizards spent more time basking, which probably increases the effectiveness of their cryptic design and decreases detection by predators. Lizards intensified the tongue flick rates when exposed to a pungent control or snake scents, as compared to their response to a neutral control. Besides, both tailed and tailless lizards intensified some aspects of their antipredator behavior (walking slowly and avoiding refuge use) when exposed to snake scent, which indicates discrimination of the smell of predatory snakes. Lizards decreased refuge use when exposed to predator scents, probably because the refuges are evaluated as unsafe due to a high concentration of snake scents. To conclude, our experiments showed that, after losing their tails, wall lizards modify their behavior in a way that likely minimizes predation risk.
Behavioural responses of tailed (grey) and tailless (white) wall lizards (Podarcis muralis) exposed to predator snake (Coronella austriaca) scents. Values are mean (± SE) total time spent by the lizards in each activity during the trial.
Highlights
Both tailed and tailless lizards intensified some aspects of their antipredator behavior when exposed to snake scents, which indicates discrimination of the smell of predatory snakes.
Regardless of the presence of predator signals, tailless lizards, which have reduced defensive capabilities, spent more time performing behaviors with probable antipredatory significance, while tailed lizards performed exploratory movements for longer.
Abstract
Residual yolk is assumed to be an important source of energy and nutrients during early life in nonmammalian amniotes. Available data show that the mean size of residual yolk is far smaller ...in lizards than in turtles, snakes, crocodiles, and birds, raising a question of whether residual yolk is of functional significance in lizards. Here, we compared data from 26 lizard species with those from other nonmammalian amniotes to test the hypothesis that residual yolk is functionally less significant in species producing more fully developed offspring. In our sample, species mean offspring water contents ranged from 73% to 84% of body wet mass; species mean proportions of carcass dry mass, fat-body dry mass, and residual yolk dry mass to offspring dry mass ranged from 84% to 99%, 0% to 5.0%, and 0% to 14.4%, respectively. Lizards are, on average, more fully developed at hatching or birth than snakes, as revealed by the fact that the mean proportion of carcass dry mass to body dry mass and offspring water contents were both higher in lizards than in snakes. We conclude that the functional significance of residual yolk during early life is generally less evident in lizards. Even in the lizards where residual yolk is of potential functional significance, this portion of yolk contributes little, if any, to postembryonic growth. Future work could usefully collect data across a wider spectrum of reptile taxa to establish a precocial–altricial continuum and test the hypothesis that species with a smaller amount of residual yolk are closer to the precocial end of the continuum.
Lacertid lizards exhibit sexual dimorphism in size corrected values for abdomen (always larger in females) and head (larger in males) lengths. Relative abdomen length increased with SVL in females ...but did not in males. The mean abdomen/head ratio for juvenile lizards (sexes pooled) was lower than that of females but did not differ from that of males in any of the studied species. Therefore, the ontogenetic development of the main body segments (abdomen and head) was isometric in male lizards, whereas female abdomen exhibited positive allometric growth. Standardized independent contrasts (Felsenstein's method) of female abdomen to head ratio and of the slope of the regression of clutch size on SVL explained a significant amount of variation in sexual size dimorphism in a stepwise multiple regression model. The fact that sexual size dimorphism was best explained by variables related to female reproductive investment, together with the ontogenetic trajectories of body segments suggest that sexual size dimorphism results mainly from variation in female size. Despite the suggested prominent role of selection on female body size in determining the outcome of size dimorphism, there was also evidence of selection for increased body size in males, which were the largest sex in species with low selective pressure towards increased female size (constant clutch size or low fecundity slope over size). Evidence for intersexual food (prey size) partitioning was weaker than expected from the widespread dimorphism in body size or relative head size found among lacertid lizards. Furthermore, the development of "body segments" was in some instances inconsistent with the competitive hypothesis, the largest sex having relatively smaller trophic structures.
Pregnant female
Zootoca vivipara
select lower body temperatures than males or nonpregnant females, and this shift in the thermal preferendum is believed to be related to optimising the conditions for ...embryogenesis. Thus, subjecting embryos to the higher temperature selected by males and non-gravid females might have detrimental effects on embryonic development and on hatchling fitness, according to predictions of the “maternal manipulation” hypothesis on the evolution of viviparity. To test the role of gestation environment on embryonic development in oviparous
Z. vivipara
, we kept a number of gravid females at the temperature selected by non-gravid females in a laboratory thermal gradient, whereas control females were allowed to regulate their body temperature without restrictions. Developmental stage at oviposition was more advanced for embryos of the experimental clutches, which were heavier than those of the control group. Forced gestation temperature also affected hatching success (58.62% in the experimental treatment vs. 97.37% in the control group). In addition, hatchlings from females subjected to high temperatures during pregnancy were smaller, had shorter head length and performed worse in running trials. Our results fulfil the prediction of the “maternal manipulation” hypothesis, and suggest that the shift in female body temperature during pregnancy optimizes embryogenesis and hatchling phenotype by avoiding the negative effects of the high incubation temperatures preferred by non-gravid females.
Females of several lizard species modify their body temperature during pregnancy, probably in connection with the optimisation of hatchling phenotypes. We studied variations in the temperature ...selected by gravid females compared with those selected by males and non-gravid females in an oviparous population of
Zootoca vivipara (Jacquin, 1797) (Squamata: Lacertidae) of Northern Spain and examined the effects of incubation temperature on the phenotypic variation of hatchlings. Cloacal temperatures of gravid females active in the field were lower than those of males and non-gravid females, as well as the temperatures selected in a thermal gradient created in the laboratory (mean±s.d.: 32.33±1.27
°C for gravid females; 34.05±1.07
°C for males and non-gravid females). Effects of temperature were assessed by incubating eggs at five constant temperatures (21, 25, 29, 32 and 34
°C). Incubation time decreased as temperature increased, following a negative exponential function. Incubation temperatures also affected the hatchlings’ morphology: hatchlings incubated at 34
°C had shorter heads than those from other temperatures. Survival at 34
°C (58%) was significantly lower than at the other temperatures (mean 93%). Pregnant females select lower body temperature, approaching the temperatures that optimise hatchling phenotypes, according to predictions of the maternal manipulation hypothesis on the evolution of viviparity. The shift in preferred temperature by pregnant females would result in only a very short delay, if any, of hatching time and, because the temperature selected by pregnant females is much higher than average temperatures recorded in natural nests of
Z. vivipara, egg retention considerably shortens incubation time, according to predictions of the cold-climate hypothesis. Our experimental results indicate that the two main hypotheses on the evolution of viviparity are compatible in our study model.
The thermal environment during development influences many aspects of the phenotype of hatchling reptiles. We hypothesized that temperature should differentially affect early incubation stages, in ...which differentiation dominates over growth, and late incubation stages, characterized by high growth rates. To test this idea, we incubated eggs of wall lizard (Podarcis muralis) under three regimes with the same mean temperature (29 °C), one constant and two variable with opposite sequences: first cold (25 °C) and then hot (32 °C), and vice versa. Hatchlings incubated at high temperature during the initial period had shorter hindlimbs and tails than those incubated under the other two temperature regimes and shorter heads than those incubated initially at low temperature. Thus, temperature experienced by embryos during the early external incubation period produced similar phenotypic responses compared to those reported in previous studies for the same constant temperature applied over the whole incubation period. Because female wall lizards select lower body temperatures during pregnancy, an increase of intrauterine retention would extend the time of exposure of developing embryos to suitable temperatures. Diminution of body temperature during pregnancy is contrary to the expected pattern under the hypothesis that egg retention has evolved to accelerate development, as proposed by the cold-climate model for evolution of viviparity in squamates, and the results of the present study support the alternative hypothesis of developmental optimization as a special case of the broader maternal manipulation view.
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