Viviparity is associated with larger female size and higher sexual size dimorphism in a reproductively bimodal lizard.

Squamate reptiles are central for studying phenotypic correlates of evolutionary transitions from oviparity to viviparity because these transitions are numerous, with many of them being recent. Several models of life-history theory predict that viviparity is associated with increased female size, and thus more female-biased sexual size dimorphism (SSD). Yet, the corresponding empirical evidence is overall weak and inconsistent. The lizard Zootoca vivipara, which occupies a major part of Northern Eurasia and includes four viviparous and two non-sister oviparous lineages, represents an excellent model for testing these predictions. We analysed how sex-specific body size and SSD is associated with parity mode, using body length data for nearly 14,000 adult individuals from 97 geographically distinct populations, which cover almost the entire species' range and represent all six lineages. Our analyses controlled for lineage identity, climatic seasonality (the strongest predictor of geographic body size variation in previous studies of this species) and several aspects of data heterogeneity. Parity mode, lineage and seasonality are significantly associated with female size and SSD; the first two predictors accounted for 14%-26% of the total variation each, while seasonality explained 5%-7%. Viviparous populations exhibited a larger female size than oviparous populations, with no concomitant differences in male size. The variation of male size was overall low and poorly explained by our predictors. Albeit fully expected from theory, the strong female bias of the body size differences between oviparous and viviparous populations found in Z. vivipara is not evident from available data on three other lizard systems of closely related lineages differing in parity mode. We confront this pattern with the data on female reproductive traits in the considered systems and the frequencies of evolutionary changes of parity mode in the corresponding lizard families and speculate why the life-history correlates of live-bearing in Z. vivipara are distinct. Comparing conspecific populations, our study provides the most direct evidence for the predicted effect of parity mode on adult body size but also demonstrates that the revealed pattern may not be general. This might explain why across squamates, viviparity is only weakly associated with larger size.

The functional significance of residual yolk in lizards.

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.

Allocation costs of regeneration: tail regeneration constrains body growth under low food availability in juvenile lizards.

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.

Behavioral patterns in the early-stage antipredator response change after tail autotomy in adult wall lizards.

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.

The movement dynamics of autotomized lizards and their tails reveal functional costs of caudal autotomy.

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.

Effects of incubation temperature on hatchling phenotypes in an oviparous lizard with prolonged egg retention: are the two main hypotheses on the evolution of viviparity compatible?

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 degrees C for gravid females; 34.05+/-1.07 degrees 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 degrees C). Incubation time decreased as temperature increased, following a negative exponential function. Incubation temperatures also affected the hatchlings' morphology: hatchlings incubated at 34 degrees C had shorter heads than those from other temperatures. Survival at 34 degrees 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.

Sex of incubation neighbours influences hatchling sexual phenotypes in an oviparous lizard.

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.

Variation in digestive performance between geographically disjunct populations of Atlantic salmon: countergradient in passage time and digestion rate.

European Atlantic salmon (Salmo salar) populations inhabit rivers from northern Portugal to northern Norway across a wide spectrum of environmental variability. To address whether single physical factors might lead to genetic divergence of isolated populations, we compared the digestive performances total digestibility, relative nitrogen digestibility, passage time, and digestion rate (g dry matter · h-1) - of northern (Scotland) and southern (Asturias, northern Spain) populations at three temperature regimes (5, 12, and 20° C). Total dry matter digestibilities increased directly with temperature but were similar for both populations at each of the three trials. Relative nitrogen digestibility did not differ between populations nor among temperature regimes. In contrast, passage time was significantly longer for low-than for high-latitude fish at both 5 and 20° C. When the percentage of food digested and the passage time were integrated as digestion rates (food digested per unit time), a significant population × temperature interaction consistent with a genotype × environment interaction was detected in addition to the population and temperature effects. This implies that not only is the digestive performance of the high-latitude population higher throughout the range of temperatures examined, but moreover the difference is reinforced at high temperatures, where the digestion rate of high-latitude fish was 1.6 times greater. Taken together, these two results provide preliminary evidence for countergradient variation in digestive rates of salmonids in response to variation in growth opportunity. The data support our previous work on the same two populations showing differences in growth rates, and underlie one of the possible mechnisms leading to more rapid growth of the high-latitude fish when both populations are reared in a common environment.