Testing for evolutionary trade-offs in a phylogenetic context: ecological diversification and evolution of locomotor performance in emydid turtles

The evolution of ecological trade-offs is an important component of ecological specialization and adaptive radiation. However, the pattern that would show that evolutionary trade-offs have occurred between traits among species has not been clearly defined. In this paper, we propose a phylogeny-based definition of an evolutionary trade-off, and apply it to an analysis of the evolution of trade-offs in locomotor performance in emydid turtles. We quantified aquatic and terrestrial speed and endurance for up to 16 species, including aquatic, semi-terrestrial and terrestrial emydids. Emydid phylogeny was reconstructed from morphological characters and nuclear and mitochondrial DNA sequences. Surprisingly, we find that there have been no trade-offs in aquatic and terrestrial speed among species. Instead, specialization to aquatic and terrestrial habitats seems to have involved trade-offs in speed and endurance. Given that trade-offs between speed and endurance may be widespread, they may underlie specialization to different habitats in many other groups.     

QUANTITATIVE GENETICS OF SPRINT RUNNING SPEED AND SWIMMING ENDURANCE IN LABORATORY HOUSE MICE (MUS DOMESTICUS)

We tested the hypothesis that locomotor speed and endurance show a negative genetic correlation using a genetically variable laboratory strain of house mice (Hsd:ICR: Mus domesticus). A negative genetic correlation would qualify as an evolutionary “constraint,” because both aspects of locomotor performance are generally expected to be under positive directional selection in wild populations. We also tested whether speed or endurance showed any genetic correlation with body mass. For all traits, residuals from multiple regression equations were computed to remove effects of possible confounding variables such as age at testing, measurement block, observer, and sex. Estimates of quantitative genetic parameters were then obtained using Shaw's (1987) restricted maximum-likelihood programs, modified to account for our breeding design, which incorporated cross-fostering. Both speed and endurance were measured on two consecutive trial days, and both were repeatable. We initially analyzed performances on each trial day and the maximal value. For endurance, the three estimates of narrow-sense heritabilities ranged from 0.17 to 0.33 (full ADCE model), and some were statistically significantly different from zero using likelihood ratio tests. The heritability estimate for sprint speed measured on trial day 1 was 0.17, but negative for all other measures. Moreover, the additive genetic covariance between speeds measured on the two days was near zero, indicating that the two measures are to some extent different traits. The additive genetic covariance between speed on trial day 1 and any of the four measures of endurance was negative, large, and always statistically significant. None of the measures of speed or endurance was significantly genetically correlated with body mass. Thus, we predict that artificial selection for increased locomotor speed in these mice would result in a decrease in endurance, but no change in body mass. Such experiments could lead to a better understanding of the physiological mechanisms leading to trade-offs in aspects of locomotor abilities.     

GENETIC BASIS OF ACTIVITY METABOLISM. I. INHERITANCE OF SPEED,STAMINA, AND ANTIPREDATOR DISPLAYS IN THE GARTER SNAKE THAMNOPHIS SIRTALIS

Recent conceptual advances in physiological ecology emphasize the potential selective importance of whole-animal performance. Empirical studies of locomotor performance in reptiles have revealed surprising amounts of individual variation in speed and stamina. The present study is the first in a series examining the genetic basis of variation in locomotor performance, activity metabolism, and associated behaviors in garter snakes. Maximal sprint crawling speed, treadmill endurance, and antipredator displays (Arnold and Bennett, 1984; exhibited as snakes reached exhaustion on the treadmill) were measured for approximately six offspring (presumed to be full siblings) from each of 46 wild-caught gravid garter snakes (Thamnophis sirtalis). Each character was measured on two days; all were individually repeatable. Correlations of these characters with body mass, snout–vent length, age at testing, litter size, dam mass, and dam snout–vent length were removed by computing residuals from multiple-regression equations. These residuals were used in subsequent genetic analyses. Approximate coefficients of variation of residuals were 17% for speed, 48% for endurance, and 31% for antipredator displays. Broad-sense heritabilities were significant for all characters: speed h² = 0.58; stamina h² = 0.70; antipredator display h² = 0.42. All three residual characters showed positive and statistically significant phenotypic correlations (r = 0.19–0.36). Genetic correlations (estimated and tested by restricted maximum likelihood) among residuals were positive and highly significant between speed and endurance (0.58), but nonsignificant between speed and antipredator display (0.43), and between endurance and antipredator display (0.26). All environmental correlations were nonsignificant. These data suggest that, contrary to expectations based on previous physiological studies, there may be no necessary evolutionary trade-off between speed and stamina in these animals. This tentative conclusion will have important implications for future theoretical studies of the evolution of locomotor performance and associated antipredator behaviors.     

Locomotor capacity and foraging behaviour of kalahari lacertid lizards

Closely related lacertid lizards (Eremias, Nucras) in the Kalahari desert differ in patterns of foraging behaviour. Some species are relatively sedentary (‘sit-and-wait’) whereas others are more active (‘widely-foraging’) predators. We determined whether whole-animal locomotor capacities (cruising endurance on a treadmill, initial speed and maximum burst speed in a racetrack, and sprint endurance in a torus-shaped track) correlated with interspecific differences in foraging behaviour. Two of three widely-foraging species had greater cruising endurance, graater sprint endurance, but lower burst speed than did a sit-and-wait species. However, the two species that sprinted quickly also had limited endurance, and vice versa. Pre-feeding negatively influenced endurance but not sprint capacity. Theoretical models of foraging behaviour should recognize that ectotherms have limited endurance, that there can be a trade-off between speed and endurance, and that pre-feeding can reduce some aspects of locomotor capacity.     

Geometry and self-righting of turtles

Terrestrial animals with rigid shells face imminent danger when turned upside down. A rich variety of righting strategies of beetle and turtle species have been described, but the exact role of the shell's geometry in righting is so far unknown. These strategies are often based on active mechanisms, e.g. most beetles self-right via motion of their legs or wings; flat, aquatic turtles use their muscular neck to flip back. On the other hand, highly domed, terrestrial turtles with short limbs and necks have virtually no active control: here shape itself may serve as a fundamental tool. Based on field data gathered on a broad spectrum of aquatic and terrestrial turtle species we develop a geometric model of the shell. Inspired by recent mathematical results, we demonstrate that a simple mechanical classification of the model is closely linked to the animals' righting strategy. Specifically, we show that the exact geometry of highly domed terrestrial species is close to optimal for self-righting, and the shell's shape is the predominant factor of their ability to flip back. Our study illustrates how evolution solved a far-from-trivial geometrical problem and equipped some turtles with monostatic shells: beautiful forms, which rarely appear in nature otherwise.     

Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina,Laticaudidae)

Yellow‐lipped sea kraits (Laticauda colubrina) are amphibious in their habits. We measured their locomotor speeds in water and on land to investigate two topics: (1) to what degree have adaptations to increase swimming speed (paddle‐like tail etc.) reduced terrestrial locomotor ability in sea kraits?; and (2) do a sea krait’s sex and body size influence its locomotor ability in these two habitats, as might be expected from the fact that different age and sex classes of sea kraits use the marine and terrestrial environments in different ways? To estimate ancestral states for locomotor performance, we measured speeds of three species of Australian terrestrial elapids that spend part of their time foraging in water. The evolutionary modifications of Laticauda for marine life have enhanced their swimming speeds by about 60%, but decreased their terrestrial locomotor speed by about 80%. Larger snakes moved faster than smaller individuals in absolute terms but were slower in terms of body lengths travelled per second, especially on land. Male sea kraits were faster than females (independent of the body‐size effect), especially on land. Prey items in the gut reduced locomotor speeds both on land and in water. Proteroglyphous snakes may offer exceptional opportunities to study phylogenetic shifts in locomotor ability, because (1) they display multiple independent evolutionary shifts from terrestrial to aquatic habits, and (2) one proteroglyph lineage (the laticaudids) displays considerable intraspecific and interspecific diversity in terms of the degree to which they use terrestrial vs. aquatic habitats.     

The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

We described the diet of Emydura macquarii, an omnivorous turtle from south-eastern Australia, compared its digestive performance on diets of fish or plants at two temperatures, and related how both diet and temperature affect its food selection in nature. Filamentous algae constituted 61% of the stomach content of E. macquarii. The turtles rarely fed on motile prey, but selected carrion from the lagoon bottom and terrestrial insects (Diptera, Hymenoptera and Coleoptera) trapped on the surface of the water. Digestive efficiency of E. macquarii was affected little by body temperature, in contrast to consumption rates and rates of passage which were strongly influenced by both temperature and diet. In combination, these responses resulted in a slower rate of digestion at 20°C than at 30°C. Digestive efficiency of E. macquarii on a herbivorous diet at 30°C (49%) was about half that of turtles on a carnivorous diet (91%), but they had longer transit times (118 h on the plant diet versus 70 h). Lower consumption rates and longer mean retention times in turtles fed plants compared those fed fish relate to slower digestive processing of the plant. Rapid processing and higher consumption rates of fish by E. macquarii resulted in higher energy gains compared to turtles consuming plants (almost 100 times more energy at 30°C). The laboratory results suggest that fish carrion and aquatic and terrestrial invertebrates are probably essential dietary items of E. macquarii in the wild, because its metabolic requirements cannot be met from aquatic macrophytes alone.     

Reduction in locomotor ability as a cost of reproduction in gravid snakes

Summary Recent studies suggest that lower survival among gravid squamate reptiles may be partially the result of decreased locomotor ability during gestation. In this study, we compared the speed and endurance of female garter snakes (Thamnophis marcianus), before, during, and after pregnancy. Gravid snakes had significantly lower locomotor performance than did non-gravid females, and performance varied among stages of gestation, reaching a minimum 0–6 weeks prior to parturition. Both number of offspring and relative clutch mass were inversely correlated with locomotor performance; as females increased these traits, locomotor ability decreased. If reduced locomotor performance results in greater risk of predation and/or lowered foraging ability, then natural selection (operating via differential mortality or feeding rates of gravid females) may result in important constraints on both clutch size and relative clutch mass in squamates.     

中华鳖新孵幼体的热耐受性、体温昼夜变化和运动能力的热依赖性

研究中华鳖新孵幼体的热耐受性、体温及温度对运动能力的影响 .结果表明 ,在干燥和潮湿环境下 ,选择体温分别为 2 8.0℃和 30 .3℃ ;潮湿环境下 ,临界高温和低温分别为 40 .9℃和 7.8℃ .在缺乏温度梯度的热环境中 ,水温对幼鳖体温的影响比气温更直接 ,体温和环境温度的昼夜变化相一致 ,说明幼鳖生理调温能力很弱 .在有温度梯度的热环境中 ,幼鳖能通过行为调温将体温维持到较高且较恒定的水平 ,导致体温昼夜变化不明显 .幼鳖运动能力有显著的热依赖性 ,在一定温度范围内随体温升高而增强 .体温31.5℃时 ,幼鳖的运动表现最好 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.87m、4 92m·min-1和 6 .2次·min-1.体温过高时 ,运动能力下降 .当体温为 33 .0℃时 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.30m、4.2 8m·min-1和 7.7次·min-1.     

Ontogenetic scaling of bite force in lizards and turtles

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.     

High thermal variance in naturally incubated turtle nests produces faster offspring

The effects of climate change on populations are complex and difficult to predict, and can result in mismatches between interdependent organisms or between organisms and their environment. Reptiles with temperature-dependent sex determination may be able to compensate for potential skews in offspring sex ratio caused by climate change by selecting cooler (i.e., shadier) nest sites. Although changing nest location may prevent sex ratio skews, it may also affect thermally sensitive performance traits in offspring. I tested righting, sprinting, and swimming performance in hatchling painted turtles (Chrysemys picta), produced by female turtles from five populations across the species’ geographic range, nesting in a common-garden environment. I found that speed of hatchling performance was faster in hatchlings whose mothers originated from warmer climates, and that nests with higher mean daily variation in incubation temperature produced faster hatchlings. These results suggest that the increased temperatures predicted by climate change models could result in hatchling turtles that are faster at sprinting and swimming; however, it is not yet known how these performance measures translate into fitness.     

Thermal plasticity of diving behavior, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus

Locomotion is a common measure of performance used in studies of thermal acclimation because of its correlation with predator escape and prey capture. However, for sedentary animals such as freshwater turtles, we propose that diving behavior may be a more ecologically relevant measure of performance. Increasing dive duration in hatchling turtles reduces predator exposure and therefore functions as an ecological benefit. Diving behavior is thermally dependent, and in some species of freshwater turtles, it is also reliant on aquatic respiration. This study examined the influence of thermal acclimation on diving behavior, aquatic respiration, and locomotor performance in the endangered, bimodally respiring Mary River turtle Elusor macrurus. Diving behavior was found to partially acclimate at 17 degrees C, with turtles acclimated to a cold temperature (17 degrees C) having a significantly longer dive duration than hatchlings acclimated to a warm temperature (28 degrees C). This increase in dive duration at 17 degrees C was not a result of physiological alterations in metabolic rate but was due instead to an increase in aquatic oxygen consumption. Increasing aquatic oxygen consumption permitted cold-acclimated hatchlings to remain submerged for significantly longer periods, with one turtle undertaking a dive of over 2.5 d. When burst-swimming speed was used as the measure of performance, thermal acclimation was not detected. Overall, E. macrurus demonstrated a partial ability to acclimate to changes in environmental temperature.     

Nasal anatomy of trionychid turtles

Two trionychid turtles, Trionyx ferox and Lissemys punctata, have similar and distinctive nasal cavities. Most of the parts of the nasal cavities are similar to those in other turtles, but the intermediate regions have many more small ridges and shallow sulci than do those of other turtles; these form a highly complex and distinctive pattern that varies in minor details. In turtles generally, a relatively large intermediate region appears to be correlated with strongly aquatic habits, which supports the interpretation that the vomeronasal epithelium of that region functions in olfaction in an aquatic environment.     

Thermal biology and locomotor performance of the Andean lizard Liolaemus fitzgeraldi (Liolaemidae) in Argentina

Ectotherms thermoregulate to maintain their body temperature within the optimal range needed for performing vital functions. The effect of climate change on lizards has been studied as regards the sensitivity of locomotor performance to environmental temperatures. We studied thermoregulatory efficiency and locomotor performance for Liolaemus fitzgeraldi in the Central Andes of Argentina. We determined body temperature, micro-environmental temperatures and operative temperatures in the field. In the laboratory, we measured preferred temperatures and calculated the index of thermoregulatory efficiency. We estimated the thermal sensitivity of locomotion by measuring sprint speed (initial velocity and long sprint) and endurance at five different body temperatures. Body temperature was not associated with either micro-environmental temperature, nor did it show differences with preferred temperatures. Thermoregulatory efficiency was moderate (0.61). Initial velocity and long sprint trials showed differences at different temperatures; however, endurance did not. Moreover, the optimal temperatures for the performance trials showed no significant differences among themselves. We conclude that Liolaemus fitzgeraldi has thermal sensitivity in locomotor performance with respect to body temperature and that it is an eurythermic lizard that experiences a large variation in body temperature and that has thermal flexibility in the cold.     

Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs

The importance of studying individual variation in locomotor performance has long been recognized as it may determine the ability of an organism to escape from predators, catch prey or disperse. In ectotherms, locomotor performance is highly influenced by ambient temperature (T _a), yet several studies have showed that individual differences are usually retained across a T _a gradient. Less is known, however, about individual differences in thermal sensitivity of performance, despite the fact that it could represent adaptive sources of phenotypic variation and/or additional substrate for selection to act upon. We quantified swimming and jumping performance in 18 wild-caught tropical clawed frogs (Xenopus tropicalis) across a T _a gradient. Maximum swimming velocity and acceleration were not repeatable and individuals did not differ in how their swimming performance varied across T _a. By contrast, time and distance jumped until exhaustion were repeatable across the T _a gradient, indicating that individuals that perform best at a given T _a also perform best at another T _a. Moreover, thermal sensitivity of jumping endurance significantly differed among individuals, with individuals of high performance at low T _a displaying the highest sensitivity to T _a. Individual differences in terrestrial performance increased with decreasing T _a, which is opposite to results obtained in lizards at the inter-specific and among-individual levels. To verify the generality of these patterns, we need more studies on individual variation in thermal reaction norms for locomotor performance in lizards and frogs.     

Sprint Speeds of Juvenile Scorpions: Among Family Differences and Parent Offspring Correlations

Sprinting from predators is an important part of the defensive repertoire of some scorpions. This study examined sprint speed in juvenile scorpions and its relation to sprint speed of the mothers. Sprint speeds of juvenile scorpions, Centruroides vittatus, were determined by repeated trials on a small racetrack. Speeds were repeatable across trials within individuals and differed among individuals. There were marked among family differences in juvenile sprint speeds. Juvenile sprint speeds were correlated with maternal sprint speeds. Although the effect of common maternal environment may inflate the measures of heritability to an unknown extent, these results suggest that sprint may respond to natural selection and there is an underlying genetic basis to observed performance differences among scorpions.     

Incubation Temperature Effects on Hatchling Performance in the Loggerhead Sea Turtle (Caretta caretta)

Incubation temperature has significant developmental effects on oviparous animals, including affecting sexual differentiation for several species. Incubation temperature also affects traits that can influence survival, a theory that is verified in this study for the Northwest Atlantic loggerhead sea turtle (Caretta caretta). We conducted controlled laboratory incubations and experiments to test for an effect of incubation temperature on performance of loggerhead hatchlings. Sixty-eight hatchlings were tested in 2011, and 31 in 2012, produced from eggs incubated at 11 different constant temperatures ranging from 27°C to 33°C. Following their emergence from the eggs, we tested righting response, crawling speed, and conducted a 24-hour long swim test. The results support previous studies on sea turtle hatchlings, with an effect of incubation temperature seen on survivorship, righting response time, crawling speed, change in crawl speed, and overall swim activity, and with hatchlings incubated at 27°C showing decreased locomotor abilities. No hatchlings survived to be tested in both years when incubated at 32°C and above. Differences in survivorship of hatchlings incubated at high temperatures are important in light of projected higher sand temperatures due to climate change, and could indicate increased mortality from incubation temperature effects.     

Consequences of metamorphosis for the locomotor performance and thermal physiology of the newt Triturus cristatus

During metamorphosis, most amphibians undergo rapid shifts in their morphology that allow them to move from an aquatic to a more terrestrial existence. Two important challenges associated with this shift in habitat are the necessity to switch from an aquatic to terrestrial mode of locomotion and changes in the thermal environment. In this study, I investigated the consequences of metamorphosis to the burst swimming and running performance of the European newt Triturus cristatus to determine the nature and magnitude of any locomotor trade-offs that occur across life-history stages. In addition, I investigated whether there were any shifts in the thermal dependence of performance between life-history stages of T. cristatus to compensate for changes in their thermal environment during metamorphosis. A trade-off between swimming and running performance was detected across life-history stages, with metamorphosis resulting in a simultaneous decrease in swimming and increase in running performance. Although the terrestrial habitat of postmetamorphic stages of the newt T. cristatus experienced greater daily fluctuations in temperature than the aquatic habitat of the larval stage, no differences in thermal sensitivity of locomotor performance were detected between the larval aquatic and postmetamorphic stages. The absence of variation across life-history stages of T. cristatus may indicate that thermal sensitivity may be a conservative trait across ontogenetic stages in amphibians, but further studies are required to investigate this assertion.     

The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii

We described the diet of Emydura macquarii, an omnivorous turtle from south-eastern Australia, compared its digestive performance on diets of fish or plants at two temperatures, and related how both diet and temperature affect its food selection in nature. Filamentous algae constituted 61% of the stomach content of E. macquarii. The turtles rarely fed on motile prey, but selected carrion from the lagoon bottom and terrestrial insects (Diptera, Hymenoptera and Coleoptera) trapped on the surface of the water. Digestive efficiency of E. macquarii was affected little by body temperature, in contrast to consumption rates and rates of passage which were strongly influenced by both temperature and diet. In combination, these responses resulted in a slower rate of digestion at 20 degrees C than at 30 degrees C. Digestive efficiency of E. macquarii on a herbivorous diet at 30 degrees C (49%) was about half that of turtles on a carnivorous diet (91%), but they had longer transit times (118 h on the plant diet versus 70 h). Lower consumption rates and longer mean retention times in turtles fed plants compared those fed fish relate to slower digestive processing of the plant. Rapid processing and higher consumption rates of fish by E. macquarii resulted in higher energy gains compared to turtles consuming plants (almost 100 times more energy at 30 degrees C). The laboratory results suggest that fish carrion and aquatic and terrestrial invertebrates are probably essential dietary items of E. macquarii in the wild, because its metabolic requirements cannot be met from aquatic macrophytes alone.