Albert F. Bennett

Endothermy and activity in vertebrates.

Resting and maximal levels of oxygen consumption of endothermic vertebrates exceed those of ectotherms by an average of five- to tenfold. Endotherms have a much broader range of activity that can be sustained by this augmented aerobic metabolism. Ectotherms are more reliant upon, and limited by, anaerobic metabolism during activity. A principal factor in the evolution of endothermy was the increase in aerobic capacities to support sustained activity.

PHYLOGENETIC STUDIES OF COADAPTATION: PREFERRED TEMPERATURES VERSUS OPTIMAL PERFORMANCE TEMPERATURES OF LIZARDS

The view that behavior and physiological performance are tightly coadapted is a central principle of physiological ecology. Here, we test this principle using a comparative study of evolutionary patterns in thermal preferences and the thermal dependence of sprinting in some Australian skinks (Lygosominae). Thermal preferences (Tp) differ strikingly among genera (range 24° to 35°C), but critical thermal maxima (CTMax) (range 38° to 45°C) and optimal temperatures for sprinting (To, 32° to 35°C) vary less. Diurnal genera have relatively high Tp, To, and CTMax. In contrast, nocturnal genera have low Tp but have moderate to high To and CTMax. Both nonphylogenetic and phylogenetic (minimum‐evolution) approaches suggest that coadaptation is tight only for genera with high Tp. Phylogenetic analyses suggest that low Tp and, thus, partial coadaptation are evolutionarily derived, indicating that low thermal preferences can evolve, even if this results in reduced performance. In one instance, thermal preferences and the thermal dependence of sprinting may have evolved in opposite directions, a phenomenon we call “antagonistic coadaptation.” We speculate on factors driving partial coadaptation and antagonistic coadaptation in these skinks.

SELECTION ON LOCOMOTOR PERFORMANCE CAPACITY IN A NATURAL POPULATION OF GARTER SNAKES

Selection on locomotor performance was determined for a series of marked and recaptured individuals from a population of garter snakes (Thamnophis sirtalis fitchi) in Northern California. We measured snake length and mass, burst speed, endurance on a treadmill, and the distance crawled around a stationary circular track. Size‐corrected values (residuals) of mass and locomotor performance were generated from the scaling equations of S–V length (SVL). Randomization tests and regressions were used to determine the probability that a trait was a significant predictor of survivorship, and a nonparametric, cubic spline estimate of the fitness function was used to facilitate detection of the patterns of selection. From 275 (“cohort”) snakes measured and tested within 8 days of birth in 1985, 79 were recaptured in the spring–summer of 1986 and subsequent years. Birth SVL was the only significant (randomization P = 0.022) predictor of neonatal survival from 1985 to 1986 with directional selection favoring larger individuals. In addition to the lab‐born cohort, 382 field‐born snakes from all ages in the population were captured, tested, and released during spring–summer 1986. Similar to the 1985 cohort, the survivorship of 37 of 86 neonates from 1986 to 1987 showed no significant relationship with any residual value using any statistical test. Survivorship from 1986 to 1987 for 127 of 250 yearlings (including 32 lab‐born cohort snakes) analyzed with the randomization test showed that greater values of both speed (P = 0.007) and distance residual (P = 0.008) significantly favored survival, whereas intermediate values of mass residual (P = 0.006) were significantly more likely to survive. Univariate regressions predicting the survival of yearlings from 1986 to 1987 gave similar results to the randomization test, but in a multiple regression with yearling burst speed residual, distance capacity residual, and a quadratic term of mass residual, distance capacity residual was the least important predictor variable. For the survivorship of 37 of the 113 older snakes, greater burst speed residual significantly favored survival (randomization P = 0.001).

The Molecular Diversity of Adaptive Convergence

Natural Selection Caught in the Act Understanding how new functions evolve has been of long-standing interest. However, the number of mutations needed to evolve a key innovation is rarely known, or whether other sets of mutations would also suffice, whether the intermediate steps are driven by natural selection, or how contingent the outcome is on steps along the way. Meyer et al. (p. 428; see the Perspective by Thompson) answer these questions for a case in which phage lambda evolved the ability to infect its host Escherichia coli through a novel receptor. This shift required four mutations, which accumulated under natural selection in concert with coevolution of the host. However, when Tenaillon et al. (p. 457) exposed 115 lines of E. coli to high temperature and sequenced them, adaptation occurred through many different genetic paths, showing parallelism at the level of genes and interacting protein complexes, but only rarely at the nucleotide level. Thus, epistasis—nonadditive genetic interaction—is likely to play an important part in the process of adaptation to this environment. Replicate Escherichia coli lines show multiple convergent adaptations via different mutations in response to high temperature. To estimate the number and diversity of beneficial mutations, we experimentally evolved 115 populations of Escherichia coli to 42.2°C for 2000 generations and sequenced one genome from each population. We identified 1331 total mutations, affecting more than 600 different sites. Few mutations were shared among replicates, but a strong pattern of convergence emerged at the level of genes, operons, and functional complexes. Our experiment uncovered a set of primary functional targets of high temperature, but we estimate that many other beneficial mutations could contribute to similar adaptive outcomes. We inferred the pervasive presence of epistasis among beneficial mutations, which shaped adaptive trajectories into at least two distinct pathways involving mutations either in the RNA polymerase complex or the termination factor rho.

THE THERMAL DEPENDENCE OF LIZARD BEHAVIOUR

Abstract New techniques were utilized to measure burst speed and distance running capacity in six species of lizards and to examine the thermal dependence of these behavioural capacities. These behaviours were repeatable among groups of animals within a species, within a group during the experiments, and among individuals of a group. Burst speeds averaged 130 to 150 m/min for active species, with some individuals exceeding 200 m/min. Total distances run during 2 min averaged 60 to 70 m in species with the greatest stamina. Thermal dependence of these behaviours was low or absent ( Q 10 ≤1.5) over the normal range of active body temperatures, and performance was not necessarily maximal at normally experienced body temperatures. These processes have much less thermal dependence than do most physiological processes and suggest adaptations to maintain functional behavioural capacity over a broad range of body temperature.

Animals and temperature: phenotypic and evolutionary adaptation.

List of contributors Preface 1. Adaptation of biological membranes to temperature: biophysical perspectives and molecular mechanisms A. Y. Gracey, J. Logue, P. E. Tiku and A. R. Cossins 2. Temperature adaptation: molecular aspects G. Di Prisco and B. Giardina 3. Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges G. N. Somero, E. Dahlhoff and J. J. Lin 4. Ecological and evolutionary physiology of stress proteins and the stress response: the Drosophila melanogaster model M. E. Feder 5. Temperature adaptation and genetic polymorphism in aquatic animals A. J. S. Hawkins 6. Phenotypic plasticity and evolutionary adaptations of mitochondria to temperature H. E. Guderley and J. St Pierre 7. Temperature and ontogeny in ectotherms: muscle phenotype in fish I. A. Johnston, V. L. A. Vieira and J. Hill 8. Ectotherm life-history responses to developmental temperature D. Atkinson 9. Testing evolutionary hypotheses of acclimation R. B. Huey and D. Berrigan 10. Experimental investigations of evolutionary adaptation to temperature J. A. Mongold, A. F. Bennett and R. E. Lenski 11. Thermal evolution of ectotherm body size: why get big in the cold? L. Partridge and V. French 12. Physiological correlates of daily torpor in hummingbirds J. E. P. W. Bicudo 13. Development of thermoregulation in birds: physiology, interspecific variation and adaptation to climate Z. A. Eppley 14. Evolution of endothermy in mammals, birds and their ancestors J. Ruben 15. The influence of climate change on the distribution and evolution of organisms A. Clarke Index.

RAPID EVOLUTION OF ESCAPE ABILITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA )

Abstract Predators are widely assumed to create selection that shapes the evolution of prey escape abilities. However, this assumption is difficult to test directly due to the challenge of recording both predation and its evolutionary consequences in the wild. We examined these events by studying natural and experimental populations of Trinidadian guppies, Poecilia reticulata, which occur in distinct high‐predation and low‐predation environments within streams. Importantly, in the last two decades several populations of guppies have been experimentally introduced from one type of predatory environment into the other, allowing measurements of the consequences of change. We used this system to test two hypotheses: First, that changes in predatory environments create phenotypic selection favoring changes in escape ability of guppies, and second, that this selection can result in rapid evolution. For the first test we compared escape ability of wild caught guppies from high‐ versus low‐predation environments by measuring survival rates during staged encounters with a major predator, the pike cichlid Crenicichla alta. We used guppies from three streams, comparing two within‐stream pairs of natural populations and three within‐stream pairs of an introduced population versus its natural source population. In every comparison, guppies from the high‐predation population showed higher survival. These multiple, parallel divergences in guppy survival phenotype suggest that predatory environment does create selection of escape ability. We tested our second hypothesis by rearing guppies in common garden conditions in the laboratory, then repeating the earlier experiments using the F2 generation. As before, each comparison resulted in higher survival of guppies descended from the high‐predation populations, demonstrating that population differences in escape ability have a genetic basis. These results also show that escape ability can evolve very rapidly in nature, that is, within 26–36 generations in the introduced populations. Interestingly, we found rapid evolutionary loss of escape ability in populations introduced into low‐predation environments, suggesting that steep fitness trade‐offs may influence the evolution of escape traits.

Anaerobic metabolism during activity in lizards

SummaryA new technique developed for the determination of total lactate production in small animals was used to evaluate the role of anaerobiosis during activity at different temperatures in lizards. Measurements on six species of small lizards indicate little interspecific variation or thermal effect in resting lactate levels (0.35 mg lactate/g body weight) or maximal lactate levels achieved at exhaustion (1.4 mg lactate/g). Normally activeAnolis in captivity had a lactate content of 0.5 mg lactate/g. Rates of lactate formation were most rapid during the first 30 sec of activity and had a low thermal dependence (Q10=1.1–1.3 above 20 °C). The lactate formed during activity persists for long periods; e.g., for 30 to 60 min between 20 and 37 °C inAnolis carolinensis (Fig. 1). Recovery rate generally increases with temperature. Muscle lactate concentrations peak at the end of activity, but liver and blood lactate are not maximal until 10 and 30 min, respectively, after activity (Fig. 2). The decrease in the blood lactate is shown to be a poor estimator of total recovery. An estimated 80–90% of the total energy utilized during initial vigorous activity comes from anaerobic sources. Because of its low thermal dependence, anaerobiosis permits high levels of activity in lizards at all body temperatures without requiring high levels of aerobic resting metabolism.

EVOLUTIONARY ADAPTATION TO TEMPERATURE. I. FITNESS RESPONSES OF ESCHERICHIA COLI TO CHANGES IN ITS THERMAL ENVIRONMENT

We used bacteria to study experimentally the process of genetic adaptation to environmental temperature. Replicate lines of Escherichia coli, founded from a common ancestor, were propagated for 2,000 generations in 4 different thermal regimes as 4 experimental groups: constant 32, 37, or 42°C (thermal specialists), or a daily alternation between 32 and 42°C (32/42°C: thermal generalists). The ancestor had previously been propagated at 37°C for 2,000 generations. Adaptation of the groups to temperature was measured by improvement in fitness relative to the ancestor, as estimated by competition experiments. All four experimental groups showed improved relative fitness in their own thermal environment (direct response of fitness). However, rates of fitness improvement varied greatly among temperature groups. The 42°C group responded most rapidly and extensively, followed by the 32 and 32/42°C groups, whose fitness improvements were indistinguishable. The 37°C group, which experienced the ancestral temperature, had the slowest and least extensive fitness improvement. The correlated fitness responses of each group, again relative to the common ancestor, were measured over the entire experimental range of temperatures. No necessary tradeoff between direct and correlated responses of fitness was apparent: for example, the improved fitness of the 42°C group at 42°C was not accompanied by a loss of fitness at 37°C or 32°C. However, the direct fitness responses were usually greater than the correlated responses, judged both by comparing direct and correlated responses of a single group at different temperatures and by comparing direct and correlated responses of different groups at a single temperature. These comparisons indicate that the observed adaptation was, in fact, largely temperature specific. Also, the fitness responses of the generalist group across a range of temperatures were less variable than those of the thermal specialist groups considered as whole.

Coadaptation: A Unifying Principle in Evolutionary Thermal Biology*

Over the last 50 yr, thermal biology has shifted from a largely physiological science to a more integrated science of behavior, physiology, ecology, and evolution. Today, the mechanisms that underlie responses to environmental temperature are being scrutinized at levels ranging from genes to organisms. From these investigations, a theory of thermal adaptation has emerged that describes the evolution of thermoregulation, thermal sensitivity, and thermal acclimation. We review and integrate current models to form a conceptual model of coadaptation. We argue that major advances will require a quantitative theory of coadaptation that predicts which strategies should evolve in specific thermal environments. Simply combining current models, however, is insufficient to understand the responses of organisms to thermal heterogeneity; a theory of coadaptation must also consider the biotic interactions that influence the net benefits of behavioral and physiological strategies. Such a theory will be challenging to develop because each organism’s perception of and response to thermal heterogeneity depends on its size, mobility, and life span. Despite the challenges facing thermal biologists, we have never been more pressed to explain the diversity of strategies that organisms use to cope with thermal heterogeneity and to predict the consequences of thermal change for the diversity of communities.