Selective breeding for high endurance running increases hindlimb symmetry

Comparative studies provide correlational evidence of morphological adaptations for high locomotor performance, such as the classical indicators of cursoriality in mammals, long limbs and high metatarsal/femur ratios. More recently, enlarged femoral condyles have been suggested as an adaptation for high endurance running in the genus Homo. Asymmetry of locomotor appendages should adversely affect locomotor abilities, but this has not been studied in a rigorous evolutionary context. We used experimental evolution to test for morphological adaptations associated with high voluntary wheel running in selectively bred lines of mice. Surprisingly, the classical indicators of cursoriality had not evolved in concert with high activity levels. Instead, high runners had larger femoral condyles and reduced directional asymmetry of hindlimb bones. We hypothesize that greater limb symmetry and larger femoral heads are general adaptations associated with sustained, high-speed locomotion.     

Trade-off between pre and post-copulatory traits depends on locomotor activity in male Tribolium castaneum beetles

Locomotor performance is an indicator of dynamic exercise; thus, it is a central trait in many animal behaviours. Although higher locomotor endurance may increase male reproductive success (e.g., in mate searching and male–male contests), investment in other male reproductive traits (e.g., male attractiveness and sperm competition) may be decreased through energy consumption due to higher activity levels. Here, I investigated male attractiveness, mating success, and paternity success using males of the red flour beetle Tribolium castaneum selected for higher (H) and lower (L) locomotor endurance. Although there was no difference in male attractiveness between the selection regimes, H males had significantly higher mating success than L males. Conversely, L males had significantly higher paternity success than H males. Therefore, there was a trade-off between mating success and paternity success among the selection regimes, suggesting that locomotor endurance affects male reproduction in T. castaneum, and individual variation of locomotor endurance may be maintained within a population.     

Locomotor performance and social dominance in male Anolis cristatellus

The proximal mechanisms determining social dominance are not well understood. We used the highly territorial lizard A. cristatellus to test two main hypotheses: (1) that male social dominance is associated with locomotor abilities; (2) that locomotor abilities (maximal performance), as measured in the laboratory, are correlated with behaviour in the field. In the field, we recorded locomotor behaviours and assertion displays, then characterized microhabitat use and thermal relations. In the laboratory, we measured maximum sprint running speed, endurance and morphometric characters, and assessed dominance by pairing males of similar body size in an experimental arena. In 72 of 77 interactions, one lizard (the ‘winner’) was unequivocally determined to be dominant over the other (the ‘loser’). Winners performed more assertion displays than losers before capture and also had higher endurance in laboratory tests. Although contestants were matched for snout-vent length, winners had significantly deeper and wider heads. However, we found no significant differences in field locomotor behaviours, perch or thermal characteristics, head length, or maximal sprint speed. Our findings support those of previous studies, and extend them in several ways. This is the first demonstration that assertion displays in the field are related to both locomotor performance and laboratory-assessed social dominance. Locomotor performance may directly affect social dominance by allowing some males to perform better in dyadic interactions. Alternatively, both locomotor performance and social dominance may be linked to a common underlying mechanism, such as variation in hormone levels, which are known to affect aggression, locomotor performance and morphology.     

Lizard threat display handicaps endurance

Honest-signalling theory asserts that threat displays reliably advertise attributes that influence fighting success. Endurance, as measured by treadmill performance, predicts the outcome of agonistic interactions among lizards. If threat displays in lizards function to advertise endurance capacity then variation in threat displays should correlate with endurance. I tested this prediction for the duration of threat posturing in male side-blotched lizards (Uta stansburiana) and examined whether threat displays act as quality handicaps, reliable signals that expend the attribute that is advertised. Individual variation in the duration of threat posturing correlated with endurance, while an experimental reduction of endurance diminished the duration of threat posturing. As expected of a quality handicap, endurance fell below baseline after display production. A restriction of aerobic metabolism can account for this effect. In threat posturing, lateral compression of the thorax may interfere with respiration or with circulation, limiting aerobic metabolism and causing a compensatory increase in anaerobic metabolism, thereby generating lactate and diminishing locomotor capacity. Concentrations of lactate measured after display production were higher than baseline, consistent with the proposed mechanism. By restricting aerobic metabolism, the threat posture can act as a quality handicap, simultaneously advertising and expending the endurance capacity of displaying lizards.     

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.     

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.     

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.     

Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards

Abstract. A reduction in the locomotor capacity of gravid females is considered to be a cost of reproduction if it leads to an increased risk of mortality. In this study, we measured the change in endurance between gravid and postgravid female side-blotched lizards ( Uta stansburiana ) as a test of the cost of reproduction. We also altered reproductive investment in some females by direct ovarian manipulation (yolkectomy), which decreased reproductive burden by 30%. Regardless of experimental treatment, all females had lower endurance when gravid. Endurance was 28% lower in gravid females from the yolkectomy treatment and 31% lower in the unmanipulated females relative to postoviposition females. The experimental reduction in clutch mass resulted in a 21% increase in endurance of gravid yolkectomy females relative to control females. Postovipositional endurance was significantly higher in the yolkectomized females than unmanipulated females, which suggests that the cost of reproduction carries over to postoviposition performance. Unmanipulated females exhibited a significant negative association between endurance and size-specific burden. Endurance was not correlated with clutch size or size-specific burden in the yolkectomy females. Survivorship to the second clutch was higher in the yolkectomy females. The results from a logistic regression showed the probability of survival to the second clutch was significantly and positively associated with endurance after controlling for the effects of treatment. Our analyses demonstrated that the decrement in performance associated with current reproductive investment represents a cost of reproduction expressed as diminished locomotor performance and lowered survivorship to the next clutch.     

The effects of temperature and inter-individual variation on the locomotor performance of juvenile turtles

The effects of temperature on aquatic and terrestrial locomotor performance, including measures of burst speed, endurance, and righting response, the inter-individual correlation between measures of locomotor performance, and the temporal repeatability of performance were assessed in juvenile western painted turtles, Chrysemys picta bellii. Locomotor performance increased as temperature increased, with Q ₁₀ values ranging from 1.33 to 1.98 for burst speed and 2.28 to 2.76 for endurance measures. Righting response performance also increased with temperature. Aquatic and terrestrial measures of locomotor performance were highly correlated; however, righting response was not correlated with any other measure of performance. Measures of terrestrial locomotor performance were highly repeatable over the entire 30-week study period, whereas aquatic locomotor performance was only repeatable through week 12. The righting response was repeatable over a 6-week study period. Both the interindividual variation and temperature effects on locomotor performance likely influences the survival of turtles, especially juveniles, by affecting the length of time turtles are exposed to potential predators and their ability to escape.     

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.     

Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.     

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.     

Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis

Differences in predation intensity experienced by organisms can lead to divergent natural selection, driving evolutionary change. Western mosquitofish (Gambusia affinis) exhibit larger caudal regions and higher burst-swimming capabilities when coexisting with higher densities of predatory fish. It is hypothesized that a trade-off between steady (constant-speed cruising; important for acquiring resources) and unsteady (rapid bursts and turns; important for escaping predators) locomotion, combined with divergent selection on locomotor performance (favouring steady swimming in high-competition scenarios of low-predation environments, but unsteady swimming in high-predation localities) has caused such phenotypic divergence. Here, I found that morphological differences had a strong genetic basis, and low-predation fish required less hydromechanical power during steady swimming, leading to increased endurance. I further found individual-level support for cause-and-effect relationships between morphology, swimming kinematics and endurance. Results indicate that mosquitofish populations inhabiting low-predation environments have evolved increased steady-swimming abilities via stiffer bodies, larger anterior body/head regions, smaller caudal regions and greater three-dimensional streamlining.     

Metabolic rate and endurance capacity in Australian varanid lizards (Squamata: Varanidae: Varanus)

In ecomorphological and ecophysiological studies, locomotor performance is often considered to be an intermediate step between the form of an organism and its environment. We examined this premise by measuring morphology, physiology and circular track endurance in the closely related group of Australian varanid lizards. Body size, body mass and relative body proportions were poor indicators of endurance. Body mass was not correlated with endurance and size-free lower forelimb length had only a weak relationship with endurance. Instead, maximal metabolic rate was positively correlated with endurance capacity in varanids. A comparison of varanids with other groups of lizards supported this result as varanids showed both elevated maximal metabolic rate and elevated endurance scores when compared with similar sized non-varanid lizards. There was support for a strong association between endurance with foraging mode and climate. Varanid species with higher endurance tended to be widely foraging and from xeric climates, while sit-and-wait and mesic species showed reduced endurance.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 664–676.     

Is physiological performance optimized by thermoregulatory behavior?: a case study of the eastern fence lizard,Sceloporus undulatus

Eastern fence lizards (Sceloporus undulatus) exhibit a distinct thermal preference that might be related to the thermal optimum for physiological performance. Sprint speed and treadmill endurance of S. undulatus were insensitive to body temperature in the ranges of 28–38°C and 25–36°C, respectively. Both locomotor and digestive performances are optimized at the preferred body temperature of S. undulatus, but thermoregulatory behavior is more closely related to the thermal sensitivity of digestive performance than that of locomotor performance.     

SPEED AND STAMINA TRADE-OFF IN LACERTID LIZARDS

Abstract.— Morphological and physiological considerations suggest that sprinting ability and endurance capacity put conflicting demands on the design of an animal's locomotor apparatus and therefore cannot be maximized simultaneously. To test this hypothesis, we correlated size‐corrected maximal sprint speed and stamina of 12 species of lacertid lizards. Phylogenetically independent contrasts of sprint speed and stamina showed a significant negative relationship, giving support to the idea of an evolutionary trade‐off between the two performance measures. To test the hypothesis that the trade‐off is mediated by a conflict in morphological requirements, we correlated both performance traits with snout‐vent length, size‐corrected estimates of body mass and limb length, and relative hindlimb length (the residuals of the relationship between hind‐ and forelimb length). Fast‐running species had hindlimbs that were long compared to their forelimbs. None of the other size or shape variables showed a significant relationship with speed or endurance. We conclude that the evolution of sprint capacity may be constrained by the need for endurance capacity and vice versa, but the design conflict underlying this trade‐off has yet to be identified.     

Concordance between locomotor morphology and foraging mode in lacertid lizards

Foraging behaviors exist along a continuum from highly sedentary, ambush foraging, to more continuous searching, or active foraging. Foraging strategies, or modes, are defined based upon locomotor behaviors (e.g. percent time moving, moves per minute). In lizards, traits correlated with ambush and active foraging have been of interest for some time; however, general patterns of correlated evolution between locomotor morphology and locomotor behavior have only recently begun to be quantified. In this study, variation in hindlimb morphology is investigated in a model group of lizard species that vary between active foraging and more sedentary (or mixed) foraging mode. Canonical variates analysis reveals that the two active foraging species occupy similar regions of the morphospace, while the two more sedentary species occupy different regions. The active foraging species have a narrow pelvis with shorter tibia and femora. The more sedentary species have a wide pelvis, long tibia and femora, and slightly longer metatarsals. Phylogenetic patterns of trait variation were examined through ancestral character state reconstruction and show morphological shifts in concert with foraging mode in these species. The observed shifts in locomotor morphology are discussed in light of published data on sprint speed and endurance in these species. Together, the data show that linking morphological variation to variation in stride length and stride frequency is critical to understanding the evolution of locomotor performance. Much more stride length and frequency data are needed among ambush, mixed, and active foraging species because these parameters, and their morphological components, are likely correlated with variation in food acquisition mode.     

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.     

Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running

The hypothalamic-pituitary-adrenal (HPA) axis is important in regulating energy metabolism and in mediating responses to stressors, including increasing energy availability during physical exercise. In addition, glucocorticoids act directly on the central nervous system and influence behavior, including locomotor activity. To explore potential changes in the HPA axis as animals evolve higher voluntary activity levels, we characterized plasma corticosterone (CORT) concentrations and adrenal mass in four replicate lines of house mice that had been selectively bred for high voluntary wheel running (HR lines) for 34 generations and in four nonselected control (C) lines. We determined CORT concentrations under baseline conditions and immediately after exposure to a novel stressor (40 min of physical restraint) in mice that were housed without access to wheels. Resting daytime CORT concentrations were approximately twice as high in HR as in C mice for both sexes. Physical restraint increased CORT to similar concentrations in HR and C mice; consequently, the proportional response to restraint was smaller in HR than in C animals. Adrenal mass did not significantly differ between HR and C mice. Females had significantly higher baseline and postrestraint CORT concentrations and significantly larger adrenal glands than males in both HR and C lines. Replicate lines showed significant variation in body mass, length, baseline CORT concentrations, and postrestraint CORT concentrations in one or both sexes. Among lines, both body mass and length were significantly negatively correlated with baseline CORT concentrations, suggesting that CORT suppresses growth. Our results suggest that selection for increased locomotor activity has caused correlated changes in the HPA axis, resulting in higher baseline CORT concentrations and, possibly, reduced stress responsiveness and a lower growth rate.