THE EVOLUTION OF ENDOTHERMY: TESTING THE AEROBIC CAPACITY MODEL

One of the most important events in vertebrate evolution was the acquisition of endothermy, the ability to use metabolic heat production to elevate body temperature above environmental temperature. Several verbal models have been proposed to explain the selective factors leading to the evolution of endothermy. Of these, the aerobic capacity model has received the most attention in recent years. The aerobic capacity model postulates that selection acted mainly to increase maximal aerobic capacity (or associated behavioral abilities) and that elevated resting metabolic rate evolved as a correlated response. Here we evaluate the implicit evolutionary and genetic assumptions of the aerobic capacity model. In light of this evaluation, we assess the utility of phenotypic and genetic correlations for testing the aerobic capacity model. Collectively, the available intraspecific data for terrestrial vertebrates support the notion of a positive phenotypic correlation between resting and maximal rates of oxygen consumption within species. Interspecific analyses provide mixed support for this phenotypic correlation. We argue, however, that assessments of phenotypic or genetic correlations within species and evolutionary correlations among species (from comparative data) are of limited utility, because they may not be able to distinguish between the aerobic capacity model and plausible alternatives, such as selection acting directly on aspects of thermoregulatory abilities. We suggest six sources of information that may help shed light on the selective factors important during the evolution of high aerobic metabolic rates and, ultimately, the attainment of endothermy. Of particular interest will be attempts to determine, using a combination of mechanistic physiological and quantitative-genetic approaches, whether a positive genetic correlation between resting and maximal rates of oxygen consumption is an ineluctable feature of vertebrate physiology.     

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.     

Genetic variances and covariances of aerobic metabolic rates in laboratory mice

The genetic variances and covariances of traits must be known to predict how they may respond to selection and how covariances among them might affect their evolutionary trajectories. We used the animal model to estimate the genetic variances and covariances of basal metabolic rate (BMR) and maximal metabolic rate (MMR) in a genetically heterogeneous stock of laboratory mice. Narrow-sense heritability (h²) was approximately 0.38 ± 0.08 for body mass, 0.26 ± 0.08 for whole-animal BMR, 0.24 ± 0.07 for whole-animal MMR, 0.19 ± 0.07 for mass-independent BMR, and 0.16 ± 0.06 for mass-independent MMR. All h² estimates were significantly different from zero. The phenotypic correlation of whole animal BMR and MMR was 0.56 ± 0.02, and the corresponding genetic correlation was 0.79 ± 0.12. The phenotypic correlation of mass-independent BMR and MMR was 0.13 ± 0.03, and the corresponding genetic correlation was 0.72 ± 0.03. The genetic correlations of metabolic rates were significantly different from zero, but not significantly different from one. A key assumption of the aerobic capacity model for the evolution of endothermy is that BMR and MMR are linked. The estimated genetic correlation between BMR and MMR is consistent with that assumption, but the genetic correlation is not so high as to preclude independent evolution of BMR and MMR.     

动物内温性进化研究进展

对动物内温性进化的研究进行了较为系统的论述,包括内温性动物概念的由来、特点和起源的选择因子。内温性起源的选择因子包括8个模型：热生态位扩展模型、恒温与代谢效率模型、降低个体大小模型、姿势改变模型、增加脑大小模型、有氧呼吸能力模型、双亲行为模型和同化能力模型。其中后3个模型较为重要。有氧呼吸能力模型认为,选择提高支持物理运动的最大呼吸能力,而增加的静止代谢作为其相关反应而得以进化。该假说得到种内研究数据的支持,而种问的数据并小完全支持。双亲行为模型是指在鸟兽类中,内温性是对双亲行为选择的结果,因为内温性为双亲控制抚育温度提供了保证。同化能力模型认为,在鸟类和兽类中内温性进化由以下两个因素所推动：①子代出生后双亲行为加强;②为支持每日总体能量高速消耗所需,动物内脏器官能力增强而导致的较高维持消耗。     

Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy

According to the aerobic capacity model, endothermy in birds and mammals evolved as a correlated response to selection for an ability of sustained locomotor activity, rather than in a response to direct selection for thermoregulatory capabilities. A key assumption of the model is that aerobic capacity is functionally linked to basal metabolic rate (BMR). The assumption has been tested in several studies at the level of phenotypic variation among individuals or species, but none has provided a clear answer whether the traits are genetically correlated. Here we present results of a genetic analysis based on measurements of the basal and the maximum swim- and cold-induced oxygen consumption in about 1000 bank voles from six generations of a laboratory colony, reared from animals captured in the field. Narrow sense heritability (h2) was about 0.5 for body mass, about 0.4 for mass-independent basal and maximum metabolic rates, and about 0.3 for factorial aerobic scopes. Dominance genetic and common environmental (= maternal) effects were not significant. Additive genetic correlation between BMR and the swim-induced aerobic capacity was high and positive, whereas correlation resulting from specific-environmental effects was negative. However, BMR was not genetically correlated with the cold-induced aerobic capacity. The results are consistent with the aerobic capacity model of the evolution of endothermy in birds and mammals.     

Temperature,metabolic power and the evolution of endothermy

Endothermy has evolved at least twice, in the precursors to modern mammals and birds. The most widely accepted explanation for the evolution of endothermy has been selection for enhanced aerobic capacity. We review this hypothesis in the light of advances in our understanding of ATP generation by mitochondria and muscle performance. Together with the development of isotope‐based techniques for the measurement of metabolic rate in free‐ranging vertebrates these have confirmed the importance of aerobic scope in the evolution of endothermy: absolute aerobic scope, ATP generation by mitochondria and muscle power output are all strongly temperature‐dependent, indicating that there would have been significant improvement in whole‐organism locomotor ability with a warmer body. New data on mitochondrial ATP generation and proton leak suggest that the thermal physiology of mitochondria may differ between organisms of contrasting ecology and thermal flexibility. Together with recent biophysical modelling, this strengthens the long‐held view that endothermy originated in smaller, active eurythermal ectotherms living in a cool but variable thermal environment. We propose that rather than being a secondary consequence of the evolution of an enhanced aerobic scope, a warmer body was the means by which that enhanced aerobic scope was achieved. This modified hypothesis requires that the rise in metabolic rate and the insulation necessary to retain metabolic heat arose early in the lineages leading to birds and mammals. Large dinosaurs were warm, but were not endotherms, and the metabolic status of pterosaurs remains unresolved.     

Locomotor activity of mice divergently selected for basal metabolic rate: a test of hypotheses on the evolution of endothermy

The aerobic capacity model postulates that high basal metabolic rates (BMR) underlying endothermy evolved as a correlated response to the selection on maximal levels of oxygen consumption () associated with locomotor activity. The recent assimilation capacity model specifically assumes that high BMR evolved as a by‐product of the selection for effective parental care, which required long‐term locomotor activity fuelled by energy assimilated from food. To test both models, we compared metabolic and behavioural correlates in males of laboratory mice divergently selected on body mass‐corrected BMR. elicited by running on the treadmill did not differ between selection lines, which points to the lack of genetic correlation between BMR and . In contrast, there was a positive, genetic correlation between spontaneous long‐term locomotor activity, food intake and BMR. Our results therefore corroborate predictions of the assimilation capacity model of endothermy evolution.     

The evolution of endothermy in terrestrial vertebrates: Who? When? Why?

Avian and mammalian endothermy results from elevated rates of resting, or routine, metabolism and enables these animals to maintain high and stable body temperatures in the face of variable ambient temperatures. Endothermy is also associated with enhanced stamina and elevated capacity for aerobic metabolism during periods of prolonged activity. These attributes of birds and mammals have greatly contributed to their widespread distribution and ecological success. Unfortunately, since few anatomical/physiological attributes linked to endothermy are preserved in fossils, the origin of endothermy among the ancestors of mammals and birds has long remained obscure. Two recent approaches provide new insight into the metabolic physiology of extinct forms. One addresses chronic (resting) metabolic rates and emphasizes the presence of nasal respiratory turbinates in virtually all extant endotherms. These structures are associated with recovery of respiratory heat and moisture in animals with high resting metabolic rates. The fossil record of nonmammalian synapsids suggests that at least two Late Permian lineages possessed incipient respiratory turbinates. In contrast, these structures appear to have been absent in dinosaurs and nonornithurine birds. Instead, nasal morphology suggests that in the avian lineage, respiratory turbinates first appeared in Cretaceous ornithurines. The other approach addresses the capacity for maximal aerobic activity and examines lung structure and ventilatory mechanisms. There is no positive evidence to support the reconstruction of a derived, avian-like parabronchial lung/air sac system in dinosaurs or nonornithurine birds. Dinosaur lungs were likely heterogenous, multicameral septate lungs with conventional, tidal ventilation, although evidence from some theropods suggests that at least this group may have had a hepatic piston mechanism of supplementary lung ventilation. This suggests that dinosaurs and nonornithurine birds generally lacked the capacity for high, avian-like levels of sustained activity, although the aerobic capacity of theropods may have exceeded that of extant ectotherms. The avian parabronchial lung/air sac system appears to be an attribute limited to ornithurine birds.     

Transition from ectothermy to endothermy: the development of metabolic capacity in a bird (Gallus gallus)

The evolution of endothermy is one of the most significant events in vertebrate evolution. Adult mammals and birds are delineated from their early ontogenetic stages, as well as from other vertebrates, by high resting metabolic rates and consequent internal heat production. We used the embryonic development of a bird (Gallus gallus) as a model to investigate the metabolic transition between ectothermy and endothermy. Increases in aerobic capacity occur at two functional levels that are regulated independently from each other: (i) upregulation of gene expression; and (ii) significant increases in the catalytic activity of the main oxidative control enzymes. Anaerobic capacity, measured as lactate dehydrogenase activity, is extremely high during early development, but diminishes at the same time as aerobic capacity increases. Changes in lactate dehydrogenase activity are independent from its gene expression. The regulatory mechanisms that lead to endothermic metabolic capacity are similar to those of ectotherms in their response to environmental change. We suggest that the phylogenetic occurrence of endothermy is restricted by its limited selective advantages rather than by evolutionary innovation.     

NATURAL SELECTION ON THERMOGENIC CAPACITY OF HIGH-ALTITUDE DEER MICE

Adaptive explanations that rely on physiological arguments are common, but tests of hypotheses about the significance of whole-animal physiological performance (e.g., aerobic capacities) are rare. We studied phenotypic selection on the thermogenic capacity (i.e., maximal rate of oxygen consumption [VO₂max] elicited via cold exposure) of high-altitude (~3800 m) deer mice (Peromyscus maniculatus). A high VO₂max equates to a high capacity for heat production and should favor survival in the cold environments prevalent at high altitude. Strong directional selection favored high VO₂max, at least in one year. The selection for increased VO₂max is consistent with predictions derived from incorporating our physiological data into a biophysical model. During another year, we found weak evidence of selection for decreased body mass. Nonlinear selection was not significant for any of the selection episodes we studied. The strong directional selection for VO₂max that we observed suggests that—given ample genetic variation—aerobic metabolism and perhaps endothermy may have evolved rapidly on the geological time scale.     

Testing the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy

The origin of endothermy is a puzzling phenomenon in the evolution of vertebrates. To address this issue several explicative models have been proposed. The main models proposed for the origin of endothermy are the aerobic capacity, the thermoregulatory and the parental care models. Our main proposal is that to compare the alternative models, a critical aspect is to determine how strongly natural selection was influenced by body temperature, and basal and maximum metabolic rates during the evolution of endothermy. We evaluate these relationships in the context of three main hypotheses aimed at explaining the evolution of endothermy, namely the parental care hypothesis and two hypotheses related to the thermoregulatory model (thermogenic capacity and higher body temperature models). We used data on basal and maximum metabolic rates and body temperature from 17 rodent populations, and used intrinsic population growth rate (R(max)) as a global proxy of fitness. We found greater support for the thermogenic capacity model of the thermoregulatory model. In other words, greater thermogenic capacity is associated with increased fitness in rodent populations. To our knowledge, this is the first test of the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy.     

The quantitative genetics of maximal and basal rates of oxygen consumption in mice

A positive genetic correlation between basal metabolic rate (BMR) and maximal (VO(2)max) rate of oxygen consumption is a key assumption of the aerobic capacity model for the evolution of endothermy. We estimated the genetic (V(A), additive, and V(D), dominance), prenatal (V(N)), and postnatal common environmental (V(C)) contributions to individual differences in metabolic rates and body mass for a genetically heterogeneous laboratory strain of house mice (Mus domesticus). Our breeding design did not allow the simultaneous estimation of V(D) and V(N). Regardless of whether V(D) or V(N) was assumed, estimates of V(A) were negative under the full models. Hence, we fitted reduced models (e.g., V(A) + V(N) + V(E) or V(A) + V(E)) and obtained new variance estimates. For reduced models, narrow-sense heritability (h(2)(N)) for BMR was <0.1, but estimates of h(2)(N) for VO(2)max were higher. When estimated with the V(A) + V(E) model, the additive genetic covariance between VO(2)max and BMR was positive and statistically different from zero. This result offers tentative support for the aerobic capacity model for the evolution of vertebrate energetics. However, constraints imposed on the genetic model may cause our estimates of additive variance and covariance to be biased, so our results should be interpreted with caution and tested via selection experiments.     

Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy

The underlying assumption of the aerobic capacity model for the evolution of endothermy is that basal (BMR) and maximal aerobic metabolic rates are phenotypically linked. However, because BMR is largely a function of central organs whereas maximal metabolic output is largely a function of skeletal muscles, the mechanistic underpinnings for their linkage are not obvious. Interspecific studies in birds generally support a phenotypic correlation between BMR and maximal metabolic output. If the aerobic capacity model is valid, these phenotypic correlations should also extend to intraspecific comparisons. We measured BMR, M(sum) (maximum thermoregulatory metabolic rate) and MMR (maximum exercise metabolic rate in a hop-flutter chamber) in winter for dark-eyed juncos (Junco hyemalis), American goldfinches (Carduelis tristis; M(sum) and MMR only), and black-capped chickadees (Poecile atricapillus; BMR and M(sum) only) and examined correlations among these variables. We also measured BMR and M(sum) in individual house sparrows (Passer domesticus) in both summer, winter and spring. For both raw metabolic rates and residuals from allometric regressions, BMR was not significantly correlated with either M(sum) or MMR in juncos. Moreover, no significant correlation between M(sum) and MMR or their mass-independent residuals occurred for juncos or goldfinches. Raw BMR and M(sum) were significantly positively correlated for black-capped chickadees and house sparrows, but mass-independent residuals of BMR and M(sum) were not. These data suggest that central organ and exercise organ metabolic levels are not inextricably linked and that muscular capacities for exercise and shivering do not necessarily vary in tandem in individual birds. Why intraspecific and interspecific avian studies show differing results and the significance of these differences to the aerobic capacity model are unknown, and resolution of these questions will require additional studies of potential mechanistic links between minimal and maximal metabolic output.     

Energy assimilation, parental care and the evolution of endothermy

The question of the selection forces which initiated the evolution of endothermy in birds and mammals is one of the most intriguing in the evolutionary physiology of vertebrates. Many students regard the aerobic capacity model as the most plausible hypothesis. This paper presents an alternative model, in which the evolution of endothermy in birds and mammals was driven by two factors: (i) a selection for intense post-hatching parental care, particularly feeding offspring, and (ii) the high cost of maintaining the increased capacity of the visceral organs necessary to support high rates of total daily energy expenditures.     

The evolution of endothermy and its diversity in mammals and birds

Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.     

The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure

Several mutually incompatible theories exist about how and why endothermy evolved in mammals and birds. Some take the primary function to have been thermoregulation, selected for one adaptive purpose or another. Others take the high aerobic metabolic rate to have been primary. None of these theories is incontrovertibly supported by evidence, either from the fossil record of the synapsid amniotes or from observations and experiments on modern organisms. Furthermore, all are underpinned by the tacit assumption that endothermy must have evolved in a stepwise pattern, with an initial adaptive function followed only later by the addition of further functions. It is argued that this assumption is unrealistic and that the evolution of endothermy can be explained by the correlated progression model. Each structure and function associated with endothermy evolved a small increment at a time, in loose linkage with all the others evolving similarly. The result is that the sequence of organisms maintained functional integration throughout, and no one of the functions of endothermy was ever paramount over the others. The correlated progression model is tested by the nature of the integration between the parts as seen in living mammals, by computer simulations of the evolution of complex, multifunctional, multifactorial biological systems, and by reference to the synapsid fossil record, which is fully compatible with the model. There are several potentially important implications to be drawn from this example concerning the study of the evolution of complex structure and the new higher taxa that manifest it.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 147 , 473–488.     

Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice

The aerobic capacity model postulates that high basal metabolic rates (BMR) associated with endothermy evolved as a correlated response to the selection on maximum, peak metabolic rate Vo2max. Furthermore, the model assumes that BMR and Vo2max are causally linked, and therefore, evolutionary changes in their levels cannot occur independently. To test this, we compared metabolic and anatomical correlates of selection for high and low body mass-corrected BMR in males of laboratory mice of F18 and F19 selected generations. Divergent selection resulted in between-line difference in BMR equivalent to 2.3 phenotypic standard deviation units. Vo2max elicited by forced swimming in 20 degrees C water was higher in the low BMR than high BMR line and did not differ between the lines when elicited by exposure to heliox at -2.5 degrees C. Moreover, the magnitude of swim- and heliox-induced hypothermia was significantly smaller in low BMR mice, whereas their interscapular brown adipose tissue was larger than in high BMR mice. Our results are therefore at variance with the predictions of aerobic capacity model. The selection also resulted in correlated response in food consumption (C) and masses of metabolically active internal organs: kidneys, liver, small intestine, and heart, which fuel maximum, sustained metabolic rate (SusMR) rather than Vo2max. These correlated responses were strong enough to claim the existence of positive, genetic correlations between BMR and the mass of viscera as well as C. Thus, our findings support the suggestion that BMR evolved as a correlated response to selection for SusMR, not Vo2max. In functional terms BMR should therefore be interpreted as a measure of energetic costs of maintenance of metabolic machinery necessary to sustain high levels of energy assimilation rate.     

A phenology of the evolution of endothermy in birds and mammals

Recent palaeontological data and novel physiological hypotheses now allow a timescaled reconstruction of the evolution of endothermy in birds and mammals. A three‐phase iterative model describing how endothermy evolved from Permian ectothermic ancestors is presented. In Phase One I propose that the elevation of endothermy – increased metabolism and body temperature (T_b) – complemented large‐body‐size homeothermy during the Permian and Triassic in response to the fitness benefits of enhanced embryo development (parental care) and the activity demands of conquering dry land. I propose that Phase Two commenced in the Late Triassic and Jurassic and was marked by extreme body‐size miniaturization, the evolution of enhanced body insulation (fur and feathers), increased brain size, thermoregulatory control, and increased ecomorphological diversity. I suggest that Phase Three occurred during the Cretaceous and Cenozoic and involved endothermic pulses associated with the evolution of muscle‐powered flapping flight in birds, terrestrial cursoriality in mammals, and climate adaptation in response to Late Cenozoic cooling in both birds and mammals. Although the triphasic model argues for an iterative evolution of endothermy in pulses throughout the Mesozoic and Cenozoic, it is also argued that endothermy was potentially abandoned at any time that a bird or mammal did not rely upon its thermal benefits for parental care or breeding success. The abandonment would have taken the form of either hibernation or daily torpor as observed in extant endotherms. Thus torpor and hibernation are argued to be as ancient as the origins of endothermy itself, a plesiomorphic characteristic observed today in many small birds and mammals.     

An experimental test of the thermoregulatory hypothesis for the evolution of endothermy

The thermoregulatory hypothesis proposes that endothermy in mammals and birds evolved as a thermoregulatory mechanism per se and that natural selection operated directly to increase body temperature and thermal stability through increments in resting metabolic rate. We experimentally tested this hypothesis by measuring the thermoregulatory consequences of increased metabolic rate in resting lizards (Varanus exanthematicus). A large metabolic increment was induced by feeding the animals and consequent changes in metabolic rate and body temperature were monitored. Although metabolic rate tripled at 32 degrees C and quadrupled at 35 degrees C, body temperature rose only about 0.5 degrees C. The rate of decline of body temperature in a colder environment did not decrease as metabolic rate increased. Thus, increasing the visceral metabolic rate of this ectothermic lizard established neither consequential endothermy nor homeothermy. These results are inconsistent with a thermoregulatory explanation for the evolution of endothermy.     

Evolution and consequences of endothermy in fishes

Regional endothermy, the conservation of metabolic heat by vascular countercurrent heat exchangers to elevate the temperature of the slow-twitch locomotor muscle, eyes and brain, or viscera, has evolved independently among several fish lineages, including lamnid sharks, billfishes, and tunas. All are large, active, pelagic species with high energy demands that undertake long-distance migrations and move vertically within the water column, thereby encountering a range of water temperatures. After summarizing the occurrence of endothermy among fishes, the evidence for two hypothesized advantages of endothermy in fishes, thermal niche expansion and enhancement of aerobic swimming performance, is analyzed using phylogenetic comparisons between endothermic fishes and their ectothermic relatives. Thermal niche expansion is supported by mapping endothermic characters onto phylogenies and by combining information about the thermal niche of extant species, the fossil record, and paleoceanographic conditions during the time that endothermic fishes radiated. However, it is difficult to show that endothermy was required for niche expansion, and adaptations other than endothermy are necessary for repeated diving below the thermocline. Although the convergent evolution of the ability to elevate slow-twitch, oxidative locomotor muscle temperatures suggests a selective advantage for that trait, comparisons of tunas and their ectothermic sister species (mackerels and bonitos) provide no direct support of the hypothesis that endothermy results in increased aerobic swimming speeds, slow-oxidative muscle power, or energetic efficiency. Endothermy is associated with higher standard metabolic rates, which may result from high aerobic capacities required by these high-performance fishes to conduct many aerobic activities simultaneously. A high standard metabolic rate indicates that the benefits of endothermy may be offset by significant energetic costs.