Thermal sensitivity of sprint-running in the lizard Sceloporus undulatus: support for a conservative view of thermal physiology

Summary The thermal sensitivity of sprint-running ability was investigated in two populations of Sceloporus undulatus that occupy thermally distinct habitats. Integration of field and laboratory data indicates that lizards inhabiting a cool, high-elevation habitat are frequently active at body temperatures that retard sprint-running velocity, which could affect adversely their ability to evade predators and to capture prey. These negative effects might be expected to select for local adaptation of thermal physiology. No differences in thermal physiology (optimal temperature for sprinting, critical thermal limits) were found, however, between lizards from the two habitats.Preferred body temperature of Sceloporus undulatus is lower than the body temperature that maximizes sprint velocity but is still well within an optimal performance range where lizards can run at better than 95% of maximum velocity. Analysis of data from other studies shows a similar concordance of preferred body temperature and temperatures that maximize sprint velocity for some, but not all lizard species studied.Low diversity of predators and high levels of food may compensate in part for the reduced sprinting ability of highelevation lizards active at low body temperatures. The lack of population differentiation supports the view that lizard thermal physiology is evolutionarily conservative.     

不同经度地区北草蜥的喜好体温和热耐受性

在外温动物热生理特征的进化理论中,“静态”和“易变”是两个持续争论的对立观点。热生理学特征的种内变异是检验此类假设的最有力证据。本研究比较了不同经度地区北草蜥的热环境和热生理特征,以检验“静态”和“易变”假设。东部沿海地区(宁德)的环境温度高于内陆地区(贵阳),与之相适应,沿海地区北草蜥的喜好体温也高于内陆地区。然而,两地区蜥蜴的上临界温度和下临界温度无显著差异。尽管这些热生理学特征的种群间变异趋势并不一致,但是喜好温度随环境温度变化而改变的结果符合“易变”假设的预测。此外,本研究表明蜥蜴的喜好体温存在沿经度方向的地理变异。     

Differences in the thermal physiology of adult Yarrow's spiny lizards (Sceloporus jarrovii) in relation to sex and body size

Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of differential selection operating on each sex. Species that exhibit SSD may also show intersexual differences in other traits, including field‐active body temperatures, preferred temperatures, and locomotor performance. For these traits, differences may be correlated with differences in body size or reflect sex‐specific trait optima. Male and female Yarrow's spiny lizards, Sceloporus jarrovii, in a population in southeastern Arizona exhibit a difference in body temperature that is unrelated to variation in body size. The observed sexual variation in body temperature may reflect divergence in thermal physiology between the sexes. To test this hypothesis, we measured the preferred body temperatures of male and female lizards when recently fed and fasted. We also estimated the thermal sensitivity of stamina at seven body temperatures. Variation in these traits provided an opportunity to determine whether body size or sex‐specific variation unrelated to size shaped their thermal physiology. Female lizards, but not males, preferred a lower body temperature when fasted, and this pattern was unrelated to body size. Larger individuals exhibited greater stamina, but we detected no significant effect of sex on the shape or height of the thermal performance curves. The thermal preference of males and females in a thermal gradient exceeded the optimal temperature for performance in both sexes. Our findings suggest that differences in thermal physiology are both sex‐ and size‐based and that peak performance at low body temperatures may be adaptive given the reproductive cycles of this viviparous species. We consider the implications of our findings for the persistence of S. jarrovii and other montane ectotherms in the face of climate warming.     

An intraspecific analysis of trade-offs in sprinting performance in a West Indian lizard species (Anolis lineatopus)

We examined whether a trade-off exists in sprinting ability among individuals within the Caribbean lizard Anolis lineatopus. Specifically, we made the following predictions: Longer-legged (relative to body size) individual lizards should sprint faster than shorter-legged lizards on a broad (5.1 cm diameter) rod. However, longer-legged lizards should also decline in sprinting performance to a greater extent than shorter-legged lizards when sprinting on rods of different diameters. To test these predictions, we examined morphology and sprinting performance in adult male, adult female and juvenile A. lineatopus. As predicted, longer-legged lizards are faster sprinters than shorter-legged lizards on the broad substrate, but they also decline more in speed between the broad and narrow (0.7 cm diameter) dowel. However, despite statistically significant morphological differences among intraspecific classes, differences in morphology did not result in differences in sprinting performance among intraspecific classes, with the exception that larger lizards run faster than smaller lizards on each dowel size.     

Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania)

The integration or coadaptation of morphological, physiological, and behavioral traits is represented by whole-organism performance traits such as locomotion or bite force. Additionally, maximum sprint speed is a good indicator of whole-organism performance capacity as variation in sprinting ability can affect survival. We studied thermal biology, morphology, and locomotor performance in a clade of Liolaemus lizards that occurs in the Patagonian steppe and plateaus, a type of habitat characterized by its harsh cold climate. Liolaemus of the lineomaculatus section display a complex mixture of conservative and flexible traits. The phylogenetically informed analyses of these ten Liolaemus species show little coevolution of their thermal traits (only preferred and optimum temperatures were correlated). With regard to performance, maximum speed was positively correlated with optimum temperature. Body size and morphology influenced locomotor performance. Hindlimbs are key for maximal speed, but forelimb length was a better predictor for sustained speed (i.e. average speed over a total distance of 1.2?m). Finally, sustained speed differed among species with different diets, with herbivores running on average faster over a long distance than omnivores.     

Quantification of correlational selection on thermal physiology,thermoregulatory behavior,and energy metabolism in lizards

Phenotypic selection is widely accepted as the primary cause of adaptive evolution in natural populations, but selection on complex functional properties linking physiology, behavior, and morphology has been rarely quantified. In ectotherms, correlational selection on thermal physiology, thermoregulatory behavior, and energy metabolism is of special interest because of their potential coadaptation. We quantified phenotypic selection on thermal sensitivity of locomotor performance (sprint speed), thermal preferences, and resting metabolic rate in captive populations of an ectothermic vertebrate, the common lizard, Zootoca vivipara. No correlational selection between thermal sensitivity of performance, thermoregulatory behavior, and energy metabolism was found. A combination of high body mass and resting metabolic rate was positively correlated with survival and negatively correlated with fecundity. Thus, different mechanisms underlie selection on metabolism in lizards with small body mass than in lizards with high body mass. In addition, lizards that selected the near average preferred body temperature grew faster that their congeners. This is one of the few studies that quantifies significant correlational selection on a proxy of energy expenditure and stabilizing selection on thermoregulatory behavior.     

Total lactate dehydrogenase activity of tail muscle is not cold-adapted in nocturnal lizards from cool-temperate habitats

The dependence of metabolic processes on temperature constrains the behavior, physiology and ecology of many ectothermic animals. The evolution of nocturnality in lizards, especially in temperate regions, requires adaptations for activity at low temperatures when optimal body temperatures are unlikely to be obtained. We examined whether nocturnal lizards have cold-adapted lactate dehydrogenase (LDH). LDH was chosen as a representative metabolic enzyme. We measured LDH activity of tail muscle in six lizard species (n = 123: three nocturnal, two diurnal and one crepuscular) between 5 and 35 °C and found no differences in LDH-specific activity or thermal sensitivity among the species. Similarly, the specific activity and thermal sensitivity of LDH were similar between skinks and geckos. Similar enzyme activities among nocturnal and diurnal lizards indicate that there is no selection of temperature specific LDH enzyme activity at any temperature. As many nocturnal lizards actively thermoregulate during the day, LDH may be adapted for a broad range of temperatures rather than adapted specifically for the low temperatures encountered when the animals are active. The total activity of LDH in tropical and temperate lizards is not cold-adapted. More data are required on biochemical adaptations and whole animal thermal preferences before trends can be established.     

The influence of hypoxia on the thermal sensitivity of skin colouration in the bearded dragon, Pogona vitticeps

One physiological mechanism used by reptiles to remain within thermal optima is their ability to reversibly alter skin colour, imparting changes in overall reflectance, and influencing the rate of heat gain from incident radiation. The ability to lighten or darken their skin is caused by the movement of pigment within the dermal chromatophore cells. Additionally, lizards, as ectotherms, significantly lower their preferred body temperatures when experiencing stressors such as hypoxia. This decrease in preferred temperature has been proposed to be the result of a downward adjustment of the thermal set-point, the temperature around which the body temperature is typically defended. We tested the hypothesis that lightening of the skin in lizards would be modified by hypoxia in a manner consistent with the known reduction in preferred temperatures. Skin colouration values of the dorsal skin of bearded dragons were analysed at three different levels of oxygen (20.8, 9.9 and 4.9 kPa) and at temperatures spanning the preferred temperature range (30, 32, 34, 36, 38 and 40 C). Hypoxic lizards lightened their skin at lower ambient temperatures more than normoxic ones, and in an oxygen-dependent fashion. The orchestrated adjustment of skin reflectance suggests that this physiological trait is being regulated at a new and lower set-point. Evidence from this study demonstrates that skin colouration plays a role in body temperature regulation and that the reduction in temperature set-point so prevalent in hypoxia is also manifested in this physiological trait.     

Basking behavior predicts the evolution of heat tolerance in Australian rainforest lizards

There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming. We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks, with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms’ vulnerability and potential resilience to climate change.     

The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards

Natural selection is an important driver of microevolution. Yet, despite significant theoretical debate, we still have a poor understanding of how selection operates on interacting traits (i.e., morphology, performance, habitat use). Locomotor performance is often assumed to impact survival because of its key role in foraging, predator escape, and social interactions, and shows strong links with morphology and habitat use within and among species. In particular, decades of study suggest, but have not yet demonstrated, that natural selection on locomotor performance has shaped the diversification of Anolis lizards in the Greater Antilles. Here, we estimate natural selection on sprinting speed and endurance in small replicate island populations of Anolis sagrei. Consistent with past correlational studies, long-limbed lizards ran faster on broad surfaces but also had increased sprint sensitivity on narrow surfaces. Moreover, performance differences were adaptive in the wild. Selection favored long-limbed lizards that were fast on broad surfaces, and preferred broad substrates in nature, and also short-limbed lizards that were less sprint sensitive on narrow surfaces, and preferred narrow perches in nature. This finding is unique in showing that selection does not act on performance alone, but rather on unique combinations of performance, morphology, and habitat use. Our results support the long-standing hypothesis that correlated selection on locomotor performance, morphology, and habitat use drives the evolution of ecomorphological correlations within Caribbean Anolis lizards, potentially providing a microevolutionary mechanism for their remarkable adaptive radiation.     

Spatial patterns in the size of Chinese lizards are driven by multiple factors

BackgroundFor almost two centuries, ecologists have examined geographical patterns in the evolution of body size and the associated determinants. During that time, one of the most common patterns to have emerged is the increase in body size with increasing latitude (referred to as Bergmann''s rule). Typically, this pattern is explained in terms of an evolutionary response that serves to minimize heat loss in colder climates, mostly in endotherms. In contrast, however, this rule rarely explains geographical patterns in the evolution of body size among ectotherms (e.g., reptiles).LocationChina.AimIn this study, we assembled a dataset comprising the maximum sizes of 211 lizard species in China and examined the geographical patterns in body size evolution and its determinants. Specifically, we assessed the relationship between body size and climate among all lizard species and within four major groups at both assemblage and interspecific levels.ResultsAlthough we found that the body size of Chinese lizards was larger in warmer regions, we established that at the assemblage level, size was correlated with multiple climatic factors, and that body size–climate correlations differed within the four major groups. Phylogenetic analysis at the species level revealed that no single climatic factor was associated with body size, with the exception of agamids, for which size was found to be positively correlated with temperature.Main conclusionsGeographical patterns in Chinese lizard body size are driven by multiple factors, and overall patterns are probably influenced by those of the major groups. We suggest that our analyses at two different levels may have contributed to the inconsistent results obtained in this study. Further studies investigating the effects of altitude and ecological factors are needed to gain a more comprehensive understanding of the evolution of ectotherm body size.     

Evolutionary trade‐offs in locomotor capacities in lacertid lizards: are splendid sprinters clumsy climbers?

We tested the hypothesis that an evolutionary trade‐off exists between the capacity to run on level terrain and the ability to climb inclined structures in lacertid lizards. Biomechanical and physiological models of lizard locomotor performance suggest that the morphological design requirements of a ground‐dwelling vs. scansorial life style are difficult to reconcile. This conflict is thought to preclude simultaneous evolution of maximal locomotor performance on level and inclined terrain. This notion has been corroborated by comparative studies on lizard species from other groups (Anolis, Chamaeleo, Sceloporus), but is not supported by our data on 13 species from the family Lacertidae. We found no indication of a negative association between maximal sprint speed of lizards over a level racetrack (indicative of ground‐dwelling locomotor performance), on an inclined stony surface (indicative of climbing performance over rock faces) and inclined mesh surface (indicative of clambering performance among vegetation). Moreover, morphological characteristics associated with fast sprinting capacities (e.g. long hind limbs) apparently enhance, rather than hinder climbing and clambering performance. We conclude that in our sample of lacertid lizards, the evolution of fast sprinting capacity on level terrain has not inflicted major restrictions on climbing and clambering performance.     

Thermal dependence of locomotor performance in two cool-temperate lizards

Temperate-zone ectotherms experience varying or very low ambient temperatures and may have difficulty in attaining preferred body temperatures. Thus, adaptations to reduce the thermal dependence of physiological processes may be present. We measured the optimal temperature range for sprint speed and compared it with the selected body temperatures (T _sel) of two sympatric, cool-temperate lizards: the diurnal skink Oligosoma maccanni and the primarily nocturnal gecko Woodworthia (previously Hoplodactylus) “Otago/Southland”. We also investigated whether time-of-day influenced sprint speed. Contrary to results for other reptiles, we found that time-of-day did not influence speed in either species. For each species, the optimal temperature range for sprinting and T _sel overlapped, supporting the ‘thermal coadaptation’ hypothesis. However, the optimal range of temperatures for speed is not always attainable during activity by either species, which have limited opportunities to attain T _sel in the field. The thermal sensitivity of sprint speed in these two species does not appear to have evolved to fully match their current thermal environment. More data on cold-adapted species are needed to fully understand physiological adaptation in ectotherms.     

Giant spiny-frog (<Emphasis Type="Italic">Paa spinosa</Emphasis>) from different populations differ in thermal preference but not in thermal tolerance

To examine whether different thermal environments have induced a change in thermal characteristics, we have conducted a between-population comparison on broad geographic patterns of preferred body temperature and critical thermal maximum in a giant spiny-frog Paa spinosa. We found a bimodal pattern of preferred body temperature during the day, with high preferred body temperature during the inactive diurnal period and low temperature during the active nocturnal period. There were significant differences among six populations of P. spinosa in preferred body temperatures, which decreased along a south to north gradient. Unlike preferred body temperatures, critical thermal maximum did not differ between frogs from the six localities. Although not all characteristics of thermal physiology in P. spinosa underwent parallel changes between the populations, the shift of preferred body temperatures suggests that the features of thermal physiology in the frog may change along a latitudinal gradient in response to different thermal environments.     

THE EVOLUTION OF FORM AND FUNCTION: MORPHOLOGY AND LOCOMOTOR PERFORMANCE IN WEST INDIAN ANOLIS LIZARDS

I tested biomechanical predictions that morphological proportions (snout–vent length, forelimb length, hindlimb length, tail length, and mass) and maximal sprinting and jumping ability have evolved concordantly among 15 species of Anolis lizards from Jamaica and Puerto Rico. Based on a phylogenetic hypothesis for these species, the ancestor reconstruction and contrast approaches were used to test hypotheses that variables coevolved. Evolutionary change in all morphological and performance variables scales positively with evolution of body size (represented by snout–vent length); size evolution accounts for greater than 50% of the variance in sprinting and jumping evolution. With the effect of the evolution of body size removed, increases in hindlimb length are associated with increases in sprinting and jumping capability. When further variables are removed, evolution in forelimb and tail length exhibits a negative relationship with evolution of both performance measures. The success of the biomechanical predictions indicates that the assumption that evolution in other variables (e.g., muscle mass and composition) did not affect performance evolution is probably correct; evolution of the morphological variables accounts for approximately 80% of the evolutionary change in performance ability. In this case, however, such assumptions are clade-specific; extrapolation to taxa outside the clade is thus unwarranted. The results have implications concerning ecomorphological evolution. The observed relationship between forelimb and tail length and ecology probably is a spurious result of the correlation between these variables and hindlimb length. Further, because the evolution of jumping and sprinting ability are closely linked, the ability to adapt to certain microhabitats may be limited.     

Chasing the Patagonian sun: comparative thermal biology of Liolaemus lizards

The importance of the thermal environment for ectotherms and its relationship with thermal physiology and ecology is widely recognized. Several models have been proposed to explain the evolution of the thermal biology of ectotherms, but experimental studies have provided mixed support. Lizards from the Liolaemus goetschi group can be found along a wide latitudinal range across Argentina. The group is monophyletic and widely distributed, and therefore provides excellent opportunities to study the evolution of thermal biology. We studied thermal variables of 13 species of the L. goetschi group, in order to answer three questions. First, are aspects of the thermal biology of the L. goetschi group modelled by the environment or are they evolutionarily conservative? Second, have thermal characteristics of these animals co-evolved? And third, how do the patterns of co-evolution observed within the L. goetschi group compare to those in a taxonomically wider selection of species of Liolaemus? We collected data on 13 focal species and used species information of Liolaemus lizards available in the literature and additional data obtained by the authors. We tackled these questions using both conventional and phylogenetically based analyses. Our results show that lizards from the L. goetschi group and the genus Liolaemus in general vary in critical thermal minimum in relation to mean air temperature, and particularly the L. goetschi group shows that air temperature is associated with critical thermal range, as well as with body temperature. Although the effect of phylogeny cannot be ignored, our results indicate that these thermal biology aspects are modelled by cold environments of Patagonia, while other aspects (preferred body temperature and critical thermal maximum) are more conservative. We found evidence of co-evolutionary patterns between critical thermal minimum and preferred body temperature at both phylogenetic scales (the L. goetschi group and the extended sample of 68 Liolaemus species).     

Do ectotherms partition thermal resources? We still do not know

Partitioning of the niche space is a mechanism used to explain the coexistence of similar species. Ectotherms have variable body temperatures and their body temperatures influence performance and, ultimately, fitness. Therefore, many ectotherms use behavioral thermoregulation to avoid reduced capacities associated with body temperatures far from the optimal temperature for performance. Several authors have proposed that thermal niche partitioning in response to interspecific competition is a mechanism that allows the coexistence of similar species of ectotherms. We reviewed studies on thermal resource partitioning to evaluate the evidence for this hypothesis. In almost all studies, there was insufficient evidence to conclude unequivocally that thermal resource partitioning allowed species coexistence. Future studies should include sites where species are sympatric and sites where they are allopatric to rule out alternative mechanisms that cause differences in thermal traits between coexisting species. There is evidence of conservatism in the evolution of most thermal traits across a wide range of taxa, but thermal performance curves and preferred temperatures do respond to strong selection under laboratory conditions. Thus, there is potential for selection to act on thermal traits in response to interspecific competition. Nevertheless, more stringent tests of the thermal resource partitioning hypothesis are required before we can assess whether it is widespread in communities of ectotherms in nature.     

The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia

Vertebrate ectotherms may deal with changes of environmental temperatures by behavioral and/or physiological mechanisms. Reptiles inhabiting tropical highlands face extreme fluctuating daily temperatures, and extreme values and intervals of fluctuations vary with altitude. Anolis heterodermus occurs between 1800 m to 3750 m elevation in the tropical Andes, and is the Anolis species found at the highest altitude known. We evaluated which strategies populations from elevations of 2200 m, 2650 m and 3400 m use to cope with environmental temperatures. We measured body, preferred, critical maximum and minimum temperatures, and sprint speed at different body temperatures of individuals, as well as operative temperatures. Anolis heterodermus exhibits behavioral adjustments in response to changes in environmental temperatures across altitudes. Likewise, physiological traits exhibit intrapopulation variations, but they are similar among populations, tended to the “static” side of the evolution of thermal traits spectrum. The thermoregulatory behavioral strategy in this species is extremely plastic, and lizards adjust even to fluctuating environmental conditions from day to day. Unlike other Anolis species, at low thermal quality of the habitat, lizards are thermoconformers, particularly at the highest altitudes, where cloudy days can intensify this strategy even more. Our study reveals that the pattern of strategies for dealing with thermal ambient variations and their relation to extinction risks in the tropics that are caused by global warming is perhaps more complex for lizards than previously thought.     

Influence of photoperiod and temperature on testicular recrudescence and body growth in the lizards, Lacerta sicula and Lacerta muralis

Annual testicular cycles in the lizards Lacerta sicula and L. muralis appear to be regulated by the interaction between seasonal changes in body temperature and an endogenous rhythmicity in thermal responsiveness. Photoperiodism does not appear to be an important factor; i.e. testicular activity does not appear to be regulated by daylength.
Following testicular regression in July, the lizards are refractory to sexual stimulation by high temperatures (i.e. normal preferred levels) for about five months. High temperatures accelerate gonadal regression and prevent recrudescence during late summer. Reduced temperatures stimulate testicular enlargement and spermatid formation during the autumn; this recrudescence can be blocked by treatment with testosterone. Very low temperatures suppress gonadal activity during mid-winter.
Maintenance of lizards at constant high temperatures (33°C) starting in July suppresses testicular recrudescence until December. Also, testicular collapse occurs in lizards transferred to high temperatures after recrudescence has started. The gonads are stimulated by exogenous gonadotropins at 33°C during the fall indicating that high temperatures reduce circulating levels of gonadotropins.
The refractoriness to high temperatures is "spontaneously" terminated during midwinter (December) under a wide range of photo-thermal conditions. Low temperatures may accelerate the termination of refractoriness. Thereafter, high temperatures stimulate, and are required for the final development of the testes and accessory sexual structures. Thus, the increase in body temperature following hibernation times the onset of breeding in the spring.
Temperature also has a marked influence on appetite and growth, independent of photo-period. Weight gains are greater at 33° than at 20°C. At 33° there is a tendency for abdominal fat bodies to enlarge but with little hepatic growth; whereas, the reverse occurs at 20°C.     

Reptilian viviparity in cold climates: testing the assumptions of an evolutionary hypothesis

Viviparity (live-bearing) in reptiles often is interpreted as an adaptation to cold climates. This hypothesis relies on (i) body temperatures of gravid females being higher than soil (nest) temperatures; (ii) embryonic development being accelerated by this temperature difference; and (iii) survivorship of hatchlings being increased if eggs hatch before the advent of cold weather in autumn. I gathered data to test these assumptions, using eight species of scincid lizards in a high-elevation area of southeastern Australia. Due to behavioural thermoregulation, body temperatures of gravid lizards average ca. 7°C higher than soil (nest) temperatures. Oviparous female lizards retain eggs in utero for ca. 50% of development. Laboratory studies show that a temperature increase from 17°C (mean nest temperature) to 24°C (mean lizard temperature) reduces incubation periods of eggs by >40 days in heliothermic species, and <20 days in a thigmothermic species. In the field, soil temperatures drop to lethally low levels shortly after the usual time of hatching. Simple calculations show that without the acceleration of development caused by uterine retention, eggs could not hatch prior to the onset of these low temperatures in the field. These results support the major assumptions of the “cold climate hypothesis” for the evolution of reptilian viviparity.