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J. exp. Biol. 160, 1-23 (1991)Printed in Great Britain © The Company of Biologists Limited 1991

THE EVOLUTION OF ACTIVITY CAPACITY

BY ALBERT F. BENNETT

Department of Ecology and Evolutionary Biology, University of California,Irvine, CA 92717, USA

Summary

The capacities of animals for activity (burst speed, maximal exertion, endur-ance) are examined in relation to their selective importance in extant populationsand the pattern of their evolution in major animal taxa.

Activity capacities have been demonstrated to be both heritable and highlyvariable in natural populations and hence susceptible to natural selection. Somefield studies have demonstrated significant positive associations between activitycapacities, particularly burst speed, and survivorship; other studies have not. Thepotential for such selection therefore clearly exists, although it may not operate inall populations.

Comparative studies of major taxa have linked endurance capacities to maximalrates of oxygen consumption; speed and exertion are correlated with capacities foranaerobic metabolism, either the catabolism of phosphagens or the production oflactic acid or octopine, depending on taxon. In vertebrates, the primitivemetabolic pattern involved the use of aerobic metabolism to support moderateswimming performance, supplemented by bursts of activity fuelled through lacticacid production. Because of much greater locomotor costs, the transition ofvertebrates onto land entailed a decrease in endurance, which was greatlyexpanded again only after the evolution of the higher rates of aerobic metabolismcharacteristic of the birds and mammals. These greater aerobic capacities mayhave been selected for thermoregulatory reasons and/or for increased activitycapacity itself.

Introduction

The animal kingdom consists of organisms of very diverse activity capacities,maxima] performance levels of which an animal is capable. Some animals arecompletely sessile, some are slow as snails, some are fleet but tire quickly, andsome possess seemingly endless stamina. Physiologists, behaviourists, ecologistsand natural historians have been interested in quantifying these activity capacities,because animal athletic abilities are of intrinsic interest and have functional andecological implications. Knowing activity capacities may, for instance, permit abiologist to identify those structures and functions that impose intrinsic limitations

Key words: aerobic metabolism, anaerobic metabolism, burst speed, cost of transport,endothermy, endurance, lactic acid, locomotion, macroevolution, maximal oxygen consump-tion, microevolution, natural selection, octopine, thermoregulation, vertebrate.

2 A. F. BENNETT

on performance, to define quantitatively the constraints within which anybehaviour must occur (e.g. locomotor performance space, Bennett, 1989) or topredict the outcome of an encounter such as that between predator and prey. Mostcommonly examined are capacities for three different types of activity: burstspeed, maximal exertion and endurance. Burst speed is the greatest velocity ananimal attains over a short distance; maximal exertion is the work output duringactivity to rapid exhaustion, usually measured as distance travelled; and endur-ance is measured as the greatest speed an animal can sustain or the length of timean activity can be sustained. Different morphological, physiological and biochemi-cal processes are thought to underlie and limit each of these different types ofbehaviour (see Bennett, 1989). Research has concentrated on defining theselimits; only now have investigations of the intermittent use of these capacitiesbegun (e.g. R. B. Weinstein and R. J. Full, in preparation). Capacities aregenerally measured as absolute, instead of size-relative, speeds or distancesbecause interactions among organisms in natural conditions depend on absoluteand not relative performance.

How did the great diversity of activity types come about in different animals andhow is it maintained? There has recently been considerable interest in andspeculation on the evolution of activity capacity (e.g. Bennett and Ruben, 1979;Arnold, 1983; Bakker, 1983; Huey and Bennett, 1986; Pough, 1989; Bennett andHuey, 1991), and it is currently one of the most fertile areas of interactive researchbetween the disciplines of evolutionary biology and comparative physiology/physiological ecology. It is a logical bridge between these fields because scenariosof natural selection in which activity capacity is crucial for survival can be relativelyeasily envisioned. These include, for example, predator-prey, reproductive orterritorial interactions in which minor differences in speed or exertion may meansuccess or failure, perhaps with fatal consequences. Such direct and decisiveselection on other physiological variables, such as rates of maintenance metab-olism or sodium excretion, is less easy to envision. Interest in the evolution ofactivity capacity has ranged from investigations on its variability and importance inextant natural populations (microevolutionary studies) to its derivation in differ-ent major taxa, such as classes or phyla (macroevolutionary studies). As such, ittouches on many fundamental issues in organismal biology and ecology. This essayexamines some data and major issues that have been studied in regard to theevolution of activity capacities.

Microevolutionary studies

... 'the race is not to the swift nor the battle to the strong... but time and chancehappeneth to them all.' (Ecclesiastes 9:11)

While scenarios of selection involving physical capacity are easy to imagine, arethey in fact real? Do minor differences in activity ability translate into differentialsurvivorship, reproduction and fitness? Or is adequacy enough? Are encounters inwhich performance capacity is important so infrequent or balanced by so many

The evolution of activity capacity 3

fother factors that selection operates only against individuals with greatly impairedcapacities, e.g. birds that cannot fly or fish that cannot swim? Do time and chance,as suggested in Ecclesiastes, outweigh athletic ability? Only empirical studies onnatural populations can answer these questions, and thereby inform speculation inboth physiological ecology and evolutionary biology on the natural significance ofactivity capacity.

Measurement of natural selection

Two conditions must obtain for a trait to be potentially susceptible to naturalselection (Endler, 1986): the trait must be heritable, that is, have a genetic basis sothat offspring resemble parents in regard to the trait, and it must be variable withinthe population. Laboratory and pedigree studies have demonstrated that activitycapacities have both these attributes. Performance capacities such as burst speedand endurance have been found to possess significant levels of heritability [broad-sense h2 (see Falconer, 1989)=0.2-0.7] in mammals (Ryan, 1975; Langlois, 1980;Bouchard and Malina, 1983a,b; Tolley etal. 1983; Gaffney and Cunningham,1988), reptiles (van Berkum and Tsuji, 1987; Garland, 1988; Tsuji etal. 1989;Jayne and Bennett, 1990a,b; Garland et al. 1990a) and insects (Caldwell andHegmann, 1969; Curtsinger and Laurie-Ahlberg, 1981). Considerable intrapopu-lation variability in activity capacity also exists, even at birth in precocialorganisms. For example, coefficients of variation are 16, 54 and 66%, respect-ively, for burst speed, maximal exertion and endurance in newborn snakes(Thamnophis sirtalis, Jayne and Bennett, 1990b). Even among adult individuals,variability remains similarly great (e.g. Garland, 1984). Individual differences inthese capacities persist through time, even after 1 year under field conditions(Huey and Dunham, 1987; van Berkum etal. 1989; Huey etal. 1990; Jayne andBennett, 1990a), and may possess significant physiological or morphologicalcorrelates (e.g. Garland, 1984; Miles, 1987; Gleeson and Harrison, 1988; Kolok,1990). Thus, activity capacities are apparently governed by genetic factors, persistthrough time and are highly variable among individuals, factors necessary for thepotential for selection on the characters.

How then is the presence or absence of detectable natural selection on thesecharacters assayed? The following procedure has been developed in conjunctionwith R. B. Huey (University of Washington) and S. J. Arnold (University ofChicago) (see Bennett and Huey, 1991, for a more comprehensive discussion). Agroup of gravid females is collected from a natural population and permitted togive birth or lay eggs, which later hatch in the laboratory. Activity capacities (i.e.burst speed, maximal exertion, endurance) of the neonates or hatchlings aremeasured directly, along with morphological and size characters of interest. Theyoung are then released into their parental population. This population issubsequently resampled after long periods (e.g. 1 year) to determine which of theyoung survived. The survivors may be remeasured and released again, and otheranimals in the population may also be assayed. Very large sample sizes (severalhundred animals) are required for these experiments. Selection is analyzed

4 A. F . BENNETT

according to a variety of techniques (e.g. Lande and Arnold, 1983; Schluter, 1988;iJayne and Bennett, 1990ft) that ask whether the survivors are a random subsampleof the original group of animals released. If so, selection has not been detected; ifthey are not a random subsample, selection may be inferred to favour an extreme(directional selection) or the mean value (stabilizing selection) of the trait. As suchfactors as body size may induce false correlations and patterns within the data (seeBennett, 1987a), these are generally removed statistically before selection isanalyzed.

An example of such a study is our work on a natural population of garter snakes(Thamnophis sirtalis) in northern California (Jayne and Bennett, 1990a,b).Reptiles are favoured model organisms for such studies because of high localpopulation densities, low mobility and extreme precociality (Huey etal. 1983;Seigel etal. 1987). We measured burst speed, maximal exertion (as total distancecrawled under pursuit) and endurance on 275 neonatal snakes born in ourlaboratory, as well as 382 field-caught snakes (including 86 neonates), and releasedall of them into their local population. The persistence of these individuals withinthe population was determined for periods as long as 3 years. When recaptured, ananimal had its activity capacities measured again prior to release. As activitycapacity in snakes depends greatly on body size (Heckrotte, 1967; Pough, 1978;Jayne and Bennett, 1990a), we analyzed size-corrected residuals. Activity capaci-ties were significantly correlated with year-to-year survival in some age classes ofthis population (Table 1). During the first year of life, body size (length, not mass)was a significant correlate of survival (P=0.022), but none of the activity capacitytraits were significantly involved. However, for yearling animals, burst speed [bothsize-corrected and absolute (P<0.01)] and maximal exertion were positively andsignificantly associated with survivorship, and endurance was nearly so. In animals2 years of age and older, burst speed, both in absolute and in size-corrected terms,was also significantly correlated with survivorship (illustrated in Fig. 1). Theintensity of selection on these activity capacities is similar to that previouslydetermined for morphological characters under selection (Schluter, 1988). Since

Table 1. Selection on activity capacities in different age classes in a naturalpopulation of garter snakes (data from randomization tests for 1986-1987 survival

from Jayne and Bennett, 1990b)

Size-corrected trait

Burst speedMaximal exertionEndurance

Neonatal

0.2620.4630.265

Age class

Yearling

0.0070.0080.060

Older

0.0010.0840.100

Table entries are probabilities that survivors are a random subsample of the original groupreleased into the population; a low probability is consistent with the interpretation of positivedirectional selection on the trait.

The evolution of activity capacity

40-

30-

20-

10-

40-

30-

20-

10-

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B

-

-

—.

- ,

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1.0

- 0.8CO>

'E3 0.6

0.2

-0.3 -0.2 -0.1 0 0.1 0.2log size residual of burst speed

-0.3 -0.2 -0.1 0 0.1 0.2log size residual of burst speed

Fig. 1. Survival of garter snakes 2 years of age or older and burst speed capacity.(A) Size-corrected distribution of speeds of snakes released in 1986 (/V=113). (B) Size-corrected speeds (measured in 1986) of those snakes recaptured in 1987 (N=37).(C) Probability of survival as a function of size-corrected speed. The dotted lines arethe linear regression and 95 % confidence limits given by Lande and Arnold (1983); thesolid line is the cubic spline fitness function (Schluter, 1988). (From Jayne and Bennett,1990b.)

snakes in this population do not reproduce until they are 3-4 years old, someactivity capacities are associated with differential survivorship prior to repro-duction and may therefore have an impact on fitness.

Similar studies have been undertaken on natural populations of other groups ofvertebrates, with mixed results. Unpublished work (quoted in Bennett and Huey,1991) by R. B. Huey, T. Garland, J. S. Tsuji and F. H. van Berkum on fencelizards (Sceloporus occidentals) and by A. E. Dunham, R. B. Huey, K. L. Overalland R. A. Newman on canyon lizards (Sceloporus merriami) has found noevidence for selection on speed or endurance in either species. In contrast, Miles(1989) has reported a significant positive association between size-corrected burstspeed and survivorship in the tree lizard (Urosaurus ornatus). In two differentstudies involving staged behavioural encounters, individuals with greater burst.speed had greater success. Coho salmon (Oncorhynchus kisutch) with greater'speed were more successful in avoiding predation by other fish (Taylor and

6 A. F. BENNETT

McPhail, 1985) (these individuals were also larger and this result may becomplicated by size effects). Faster fence lizards were found to be sociallydominant in behavioural interactions with size-matched conspecifics (Garlandet al. 1990b). Comparative studies on taxa from different natural thermal regimesshow shifts in the thermal dependence of activity capacities consistent with thenotion of adaptive evolution in response to selection on those capacities(endurance in populations of killifish, Fundulus heteroclitus, DiMichele andPowers, 1982; burst speed in species of scincid lizards, Huey and Bennett, 1987).Several studies, therefore, have found associations between activity capacities andsurvivorship, important behaviours or temperature adaptation. These resultspoint to the significance of these capacities in evolution. However, the effects areclearly not universal, and selection for these factors may be only episodic, toodifficult to detect or simply absent in some natural populations.

Identifying the actual agents of selection on activity capacity through focalanimal observations has been suggested as an alternative approach to microevolu-tionary studies (Pough, 1989). This, however, to my mind is a secondary question,to be approached only after the likelihood of selection has been established withthe type of experiment outlined above. If selection effects are undetectable inthose observations, it is unlikely to be profitable to search for agents. Identifi-cation of such agents is highly problematic, and a series of studies on differentspecies of anuran amphibians has failed to produce correlations between activityperformance and characters thought to be related to fitness (Wells and Taigen,1984; Sullivan and Walsberg, 1985; Walton, 1988a). Studies on small numbers ofindividuals may, however, fail to detect selection even if it is occurring, because oflow statistical power and the stochastic nature of the selection event, or may missthe event if it occurs at a different age from that studied. Ideal studies of this typewould require continuous observation of very large numbers of animals in the fieldthroughout their entire lifetime, or at least until they are postreproductive. Suchstudies are generally impossible.

Macroevolutionary patternsConsiderable interest has been directed towards the evolution of activity

capacity and its metabolic and physiological support among and within differentanimal taxa. As is not uncommon in evolutionary studies, such macroevolutionaryconsiderations do not flow seamlessly from microevolutionary observations andspeculation, so these areas of thought regarding activity capacity have largelydeveloped independently of each other. Macroevolutionary studies have beendirected primarily towards the analysis of qualitative differences in metabolicpathways among different animal phyla and quantitative differences in metaboliccapacities within phyla. These differences determine rates of ATP generation andhence ability to support the skeletal muscle contraction on which activity depends.

Metabolic support of activityMost animals use aerobically based metabolism to fuel both maintenance and


iu moderate levels of activity. As activity level (e.g. speed) increases, oxygenconsumption rises to meet increased demand for ATP production. The quantitat-ive pattern of this increase depends primarily on locomotor mode (e.g. walk-ing-running, swimming) (Schmidt-Nielsen, 1972; Tucker, 1975) and not on taxon.In running animals, for instance, the patterns of speed dependence of oxygenconsumption and size-adjusted net cost of transport are very similar in insects (Fulletal. 1990), crustaceans (Herreid, 1981), reptiles (Gleeson, 1979; Walton et al.1990), mammals and birds (Taylor et al. 1982). Maximal oxygen consumption setsan upper limit on this kind of sustainable behaviour. Endurance and maximaloxygen consumption are well correlated both within and among taxa according todifferences in body size, athletic ability and body temperature (Brett, 1972;Taylor, 1982; Bennett and John-Alder, 1984; Garland, 1984; Taylor etal. 1987;Full et al. 1988). The evolution of endurance capacity is therefore intimately linkedwith, and depends on, evolutionary changes in maximal capacities to consumeoxygen.

Activity requiring power output in excess of that supported by oxygenconsumption is fuelled by anaerobic metabolism. Part of this may be provided byendogenous stores of ATP or muscle phosphagens (creatine or arginine phos-phate), but these are present in small quantities in comparison to metabolicdemand. Additional ATP generation is provided by catabolic anaerobic pathways.A considerable diversity of such pathways is known in the animal kingdom(Hochachka, 1980; Hochachka and Somero, 1984; Gade and Grieshaber, 1986),with a correspondingly diverse array of end products, energetic efficiencies andrates of energy production. In a highly interesting article, Gnaiger (1983) hasargued on thermodynamic grounds (challenged by Watt, 1986) that rate of poweroutput and efficiency of energy transformation cannot be optimized simul-taneously within any one of these pathways. Hence, some anaerobic pathways,those terminating in lactic acid, alanine or octopine, emphasize high rates of ATPformation and relatively low ATP yield per unit of substrate catabolized. Others,those terminating in succinate or propionate, have a greater energetic efficiency ofsubstrate use but a low capacity for power output. The former class of pathways istherefore used in fuelling short-term bursts of activity (when ATP demand exceedsaerobic ATP supply) and can be useful in enhancing activity capacity. The latterpathways are used for enduring environmental hypoxia and permit long-termsurvival in anoxia but do not contribute to activity enhancement. Lactic acidproduction is used as the principal anaerobic pathway during activity in ver-tebrates (Bennett, 1978), urochordates and echinoderms (Ruben and Parrish,1991), crustaceans (McMahon, 1981), arachnids (Prestwich. 1988). leeches (Zebeet al. 1981) and some insects (Harrison et al. 1989; activity metabolism in flyinginsects is not anaerobically supplemented). Octopine formation occurs duringintense activity in molluscs, both cephalopods (Grieshaber and Gade, 1976) andbivalves (Gade, 1981), and sipunculids (Grieshaber and Zebe, 1978). Accumu-^tion of alanopine during activity has been demonstrated in some annelids^Biegmund etal. 1985). The evolutionary antiquity of the formation of these

8 A. F. BENNETT

compounds during activity is still unknown, both because of uncertainties in tlWphylogeny of the invertebrate groups and because of lack of information on endproduct accumulation in many of them. (The literature on anaerobic productformation in invertebrates is reviewed in Gade and Grieshaber, 1986.) Theevolution of the capacity for bouts of intense activity therefore generally dependson the development of capacities for rapid formation and tolerance of highconcentrations of lactic acid or octopine. Production of the former is associatedwith rapid exhaustion, the exact physiological causation of which is still in dispute.

Evolution of activity capacities in the vertebrates

The evolution of activity capacities and their metabolic bases in the vertebrateshas engendered considerable interest and speculation. The scenarios proposed willform the basis for the ensuing discussion of the macroevolutionary development ofactivity capacity within a major taxon. This concentration of interest is not simply areflection of vertebrate self-absorption. It is due primarily to an excellentlydocumented palaeontological history, a great diversity of types and mechanisms oflocomotion exhibited by members of the group, and a very large behavioural andphysiological data base.

Ancestral condition

It is believed that the original vertebrates, the ostracoderms, were active,predatory carnivores (Jollie, 1973; Northcutt and Gans, 1983). They probablypossessed metabolic patterns, and hence activity capacities, not very differentfrom those of most modern fish (Ruben and Bennett, 1980; Ruben and Parrish,1991). These would have included aerobically supported maintenance metabolismand a modest capacity for aerobically sustained swimming. Bouts of intenseactivity would have been fuelled by anaerobic glycolysis, resulting in lactic acidformation. These assertions come from phylogenetically based studies on thecomparative activity physiology of contemporary animals. Lactic acid formationhas been shown to occur during activity in teleosts (see references in Bennett,1978), elasmobranchs (Wells and Davie, 1985), agnathans and a cephalochordate(Ruben and Bennett, 1980), and a free-swimming urochordate and an echinoderm(Ruben and Parrish, 1991). Given this pattern of trait distribution in outgroup taxaand extant vertebrates (Fig. 2), the most parsimonious assumption is its presencein the original ancestral vertebrates (Ruben and Bennett, 1980; Ruben andParrish, 1991). Likewise, maintenance levels of oxygen consumption, adjusted forbody size and temperature, are similar in extant ectothermic vertebrates andmulticellular invertebrates (reviewed by Hemmingsen, 1960) and were, therefore,probably similar in vertebrate ancestors. Maximal rates of oxygen consumption formost of the taxa relevant to such an analysis (i.e. those in Fig. 2) are unknown andtheir study would be a valuable contribution in this regard. At this point, theassumption of moderate aerobic scopes for activity by ostracoderms does not seenaunwarranted. In its qualitative aspects, therefore, the vertebrate metabolic plan

The evolution of activity capacity

Chordates

IVertebrates

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o

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tCc *cd

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Fig. 2. Phylogenetic distribution in the deuterostome lineage of lactic acid formationduring intense activity. At question is whether ancestral vertebrates (marked by theopen box) and later ostracoderms (now extinct, marked by a dagger) possessed thischaracter. Extant groups in which lactic acid formation during activity has beendemonstrated are marked with asterisks. The most parsimonious interpretation is thepresence of the character in ancestral vertebrates and ostracoderms and earlyevolution of the character within the lineage (marked by black box). References tolactate formation are given in the text; phylogeny from Maisey (1986).

appears to be an inheritance from deuterostome ancestors and not a novelinvention of the group.

Aerobic scopes of modern fish are relatively low in comparison with those ofendothermic vertebrates or flying insects (Beamish, 1978; Bennett, 1978; Tayloret al. 1981; Bartholomew, 1981). However, fish have a considerable range ofsustainable speeds supported by these aerobic capacities and, consequently,relatively great endurance. This endurance capacity is due to the low cost ofswimming as a locomotor mode (Fig. 3): net costs of transport (mlO2

g"1 mass km"1) of swimmers are only about one-tenth those of walkers andrunners (Schmidt-Nielsen, 1972; Tucker, 1975). Hence, even limited aerobiccapacity can support a wide range of speeds, in comparison with a similarcondition in terrestrial animals (Fig. 3). Anaerobic metabolism is reserved for veryintense bursts of activity, avoiding temporal delays in the augmentation of oxygenconsumption and permitting attainment of speeds beyond those supportableaerobically. Burst speeds in fish exceed sustainable speeds by a factor of only twoor three (Table 2; see references in Beamish, 1978). In fish, therefore, the pattern^ metabolic support coupled with locomotor cost is conducive to aerobically^pported activity over a wide range of speeds and behaviours.

10 A. F. BENNETT

a.E

2-

2 4 6Speed (km h"1)

Fig. 3. Oxygen consumption as a function of speed in a fish (1.43 kg salmon,Oncorhynchus nerka, 15°C, Brett, 1965), lizard (0.87kg tegu, Tupinambis nigropunc-tatus, 35 °C, Bennett and John-Alder, 1984) and mammal (1.0 kg, slope and interceptfrom Taylor et al. 1970; maximal aerobic speed from Garland et al. 1988). Arrowsindicate the greatest aerobically sustainable speed for each animal.

Table 2. Endurance (sustainable speed) and burst speed for animals from differentgroups of vertebrates

GroupEndurance(rnrnin"1)

Burst speed(mmin"1) Ratio

FishesLizardsMammals

10-1530-4037-40

421388

108240239

2.618.52.7

Tb, body temperature.Predicted values for 100 g animals in each group are derived from general allometric equations

for mammals (Garland, 1983; Garland et al. 1988), lizards (T. Garland, personalcommunication) and fish (calculated from Tables 4 and 6 in Beamish, 1978).

Transition to the land

The transition of vertebrates from an aquatic to a terrestrial habitat entailedmajor changes in many structural and functional systems (Randall et al. 1981;Carroll, 1988). Oxygen in the aerial environment is more easily accessible becauseof its increased diffusivity and concentration (Dejours, 1981). But in spite of thisincreased accessibility, aerobic capacities were not expanded: resting and maximalrates of oxygen consumption in reptiles and amphibians are very similar to those offish of equal size and body temperature (Hemmingsen, 1960; Brett, 1972; Bennett,1978, 1982; Withers and Hillman, 1979). Paradoxically, in spite of increase^environmental oxygen availability, endurance capacities, measured as sustainat


, decreased in comparison with values measured in fish. Sustainable walkingspeeds of salamanders are less than Smmin"1 (Full, 1986; Feder, 1986; Else andBennett, 1987; Full et al. 1988), less than one-tenth those of fish swimming(Table 2). Sustainable speeds of reptiles are greater (Table 2), but still far belowthose of fish (Fig. 3). This decrement in endurance is the result of greatly increasedlocomotor costs in the terrestrial environment. Net costs of transport are nearly 10times greater in terrestrial walkers and runners than in swimmers of equal bodysize (Schmidt-Nielsen, 1972; Tucker, 1975). The biomechanics underlying thisdifference are still not fully understood. It may relate to the costs of sequentialacceleration and deceleration of limbs and vertical displacement of centre of mass(Alexander, 1977), but the equality of locomotor costs of snakes and limbedreptiles (Walton et al. 1990) suggests that such explanations are less than complete,as snake locomotion has neither of these features. Factors involving the rate ofcycling of skeletal muscle contraction may be of greater importance (Full et al.1990; Kram and Taylor, 1990). In any event, greatly increased locomotor costscoupled with a lack of increment in aerobic capacity meant that limits of endurancewere reached at much lower speeds and levels of exertion than in their aquaticancestors (Fig. 3; Bennett, 1985).

How was capacity for burst speed affected by the transition to land? Data onburst speed capacities of amphibians are scant: tiger salamanders (Ambystomatigrinum) attain peak running speeds of only about lOmmin"1 (Else and Bennett,1987; Shaffer et al. 1991), slow in comparison to fish (Table 2). Burst locomotorperformance of anuran amphibians is generally measured as jump distance (e.g.Zug, 1978), which is not directly comparable to other measurements reportedhere. Lizards are capable of running at 10-30 times sustainable speeds for shortbursts (Table 2; Bennett, 1982; Garland, 1982, personal communication), speedsthat are substantially greater than those of fish. These bursts of activity are fuelledby ATP or creatine phosphate catabolism and anaerobic glycolysis and lactic acidformation, the capacity for which is very great in lizards (Bennett and Licht, 1972)and some amphibians (Bennett and Licht, 1974). In comparison to fish, a muchgreater portion of the total behavioural repertoire of these amphibians and reptilesis thus accessed only by anaerobic metabolism (Table 2). Activity capacities ofthese terrestrial tetrapods are consequently short on endurance, but their maximalexertion and burst speed can be very great. Their behaviour is typically limited torather slow movements, punctuated with periods of very intense bouts of activityof short duration.

Evolution of higher metabolic rates in birds and mammals

This pattern of activity capacities of the terrestrial ectothermic vertebrates wasfundamentally altered during the evolution of the mammals and birds. Enduranceincreased substantially in these lineages. Maximal sustainable speeds of mammalsare 6-7 times greater than those of lizards of equal size and body temperature

Sable 2, Fig. 3; Bennett, 1982; T. Garland, personal communication). Sustainedpping flight characteristic of birds is beyond the aerobic capabilities of modern

12 A . F. BENNETT

reptiles (Bennett and Ruben, 1979). Burst speed, however, has apparentlybeen greatly modified: maximal speeds of lizards and mammals of equal size arenot significantly different (Table 2; Garland, 1982, personal communication).

What is responsible for these differences in activity capacity? Most approachesto this question have restricted themselves to comparisons of mammals andreptiles, usually lizards. Such comparisons are made because of their similarity ofbody form and relative ease of measurement (in comparison to birds) of functionalcapacities during activity. These approaches implicitly assume that metabolic andperformance traits that are widely shared among extant reptilian taxa arerepresentative of the ancestral condition from which mammals evolved. Eventhough endothermy was evolved completely independently in the two lines,mammalian and avian systems appear highly convergent in many of theirmetabolic aspects (compare allometric equations for many such variables inCalder, 1984). Mammals may, therefore, potentially serve as adequate models insuch comparisons for both endothermic taxa. In mammals and birds, both basaland maximal levels of oxygen consumption and aerobic scopes are approximately6-10 times greater than those of extant reptiles of the same body mass andtemperature (Bartholomew and Tucker, 1963; Brett, 1972; Bennett, 1978, 1982;Taylor et al. 1981). Net costs of walking and running are equal in mammals andreptiles (Bakker, 1972; Gleeson, 1979; Bennett and John-Alder, 1984), so thegreater aerobic scope of the former affords a much greater range of sustainablespeeds that can be maintained without supplementary anaerobic metabolism(Table 2, Fig. 3). Capacities for anaerobic metabolism, both anaerobic scope andanaerobic capacity (Bennett and Licht, 1972), are rather similar in mammals andreptiles (Bennett, 1978, 1982; Ruben and Battalia, 1979), as are activities ofglycolytic enzymes (Bennett, 1972a) and myofibrillar ATPase (Gleeson et al.19806) in saurian and mammalian muscle. Hence, the lack of divergence in burstspeed and maximal exertion capacities of the two groups is not particularlysurprising.

What structural and functional modifications underlie the evolution of greateraerobic capacity in birds and mammals? Virtually all aspects of oxygen-transport-ing systems have been increased, quantitatively and sometimes qualitatively.Pulmonary surface area and diffusing capacity have been gTeatly increased in theevolution of the alveolar and parabronchial lungs (Perry, 1983), as has theventilatory apparatus itself, to permit high levels of pulmonary ventilation duringactivity (Ruben et al. 1987; Carrier, 1987). Oxygen-carrying capacity and oxygen-affinity of the blood have been greatly increased (Bennett, 1973; Pough, 1979).Complete structural separation of the cardiac ventricles has occurred and maximalcardiac output has increased greatly (Gleeson et al. 1980a). Activities of mitochon-drial enzymes have increased substantially (Bennett, 1972a; Else and Hulbert,1981). Else and Hulbert (1981) undertook a quantitative examination of thedifferences in aerobic capacities of the 'reptilian and mammalian machines'. Theyconcluded that the increments in aerobic capacity in the latter were duenumber of different factors, including relatively larger internal organs


mitochondrial volume and surface area. Taylor and Weibel (1981) haveargued that all portions of the oxygen transporting and utilizing apparatus shouldhave similar maximal flux capacities, that is that there should be no particularlimiting element in the chain and that no part should possess excess transportcapacity. If such parity were maintained, the augmentation of all the elements ofoxygen transport would have had to have evolved in concert and simultaneously.Given their diverse nature and probable diverse genetic control, this synchroniz-ation seems unlikely. Withers and Hillman (1988) have inferred a cardiovascularlimitation on maximal oxygen consumption in anuran amphibians; a similarrestriction in this or another element of the system may possibly have occurred inprimitive reptiles. Probably the evolution of increased aerobic capacities in birdsand mammals involved the sequential improvement in whatever aspect of thesystem formed its most limiting element at any particular time.

Where in the mammalian and avian lineages did high metabolic rates andendothermy appear? Are they inventions within the classes Mammalia and Avesor did they develop in groups ancestral to these? Since most characters relating tooxygen consumption and thermoregulation do not fossilize, there has been muchheat but little light generated from very indirect evidence about the metaboliccondition of mammal-like reptiles and dinosaurs. Bennett and Ruben (1986)proposed the following criteria for evaluating a character presumably associatedwith endothermy in extinct organisms: it must not be present in any extantectotherm and it must have a clear and direct association with high metabolic rate.Further, the presence of such characters in sister taxa suggests ancestral inheri-tance. Reviewing the evidence, Bennett and Ruben (1986) concluded that thetherapsid ancestors of mammals probably possessed high aerobic capacities andmay have been well on the path to endothermy prior to the evolution of mammalsper se. This conclusion was based on two lines of evidence. First, cynodonttherapsids possessed elaborate turbinal bones in the nasal cavity, indicative of theconditioning of extensive volumes of ventilated air. These are not present in anyectothermic vertebrate and are directly associated with capacities for high levels ofoxygen uptake. Second, all physiological and morphological features related tohigh levels of oxygen consumption and endothermy are shared by the mammaliansister taxa Prototheria (monotremes) and Theria (marsupials and placentals).These groups diverged fairly early in mammalian evolution and remain distinct inmany features of their reproduction, endocrinology and neurology. The pos-session of so many diverse systems related to high levels of oxygen consumptionand endothermy (e.g. diaphragm, four-chambered heart, hair) is due either tounprecedented levels of convergence or ancestral inheritance.

The presence or absence of endothermy in dinosaurs has been a topic ofconsiderable discussion and sometimes acrimonious debate over the past twodecades (see references in Thomas and Olson, 1980; Czerkas, 1986; Bakker,1986). Both proponents and opponents have elaborate arguments and counter-

Puments too long and involved to be repeated here. I point out, however, thatle of the characters proposed in support of dinosaur endothermy meet the

14 A . F. BENNETT

aforementioned criteria of absence in all extant ectotherms and a clear andassociation with high metabolic rates. Further, as the birds are a monophyleticgroup, no extant endothermic sister taxon exists from which ancestral inheritanceof endothermy can be inferred. I therefore personally consider the contention ofdinosaur endothermy unproved.

Selective factors in the evolution of higher metabolic rate

What occasioned the evolution of increased aerobic capacity in the mammalianand avian lineages? Given the difficulty in determining selective factors onmorphology, physiology and performance in extant populations (see microevol-utionary section above), it is probably foolhardy to attempt it for unknownorganisms now extinct that lived in poorly understood environments. Two factors,however, have been suggested as major selective advantages. The first is metabolicthermoregulation. Body temperatures of birds and mammals are both higher andmore constant than those of most ectothermic vertebrates. High body tempera-tures are suggested to have been favoured to maximize catalytic capacity ofthermally dependent rate processes (Heinrich, 1977; Hochachka and Somero,1984; Bennett, 1987ft). Constancy of temperature presumably also favoursstability of those processes and homeostasis in general, although these purportedadvantages are more nebulous and the logic behind them often circular. Theevolution of endothermic homeothermy in these lineages required the elevation ofmaintenance rates of aerobic metabolism. Placing an insulatory layer on avertebrate ectotherm does not confer significant homeothermy, as Cowles (1958)demonstrated directly by outfitting lizards with mink coats. Increased insulation,above that afforded by the reptilian integument, is necessary for homeothermy, atleast in small endotherms, but is in itself not sufficient to produce it. Increments inmaintenance metabolic rate occurred independently in both avian and mammalianlineages, converging on very similar levels in the two groups, when differences inbody temperature are taken into account (equations in Peters, 1983; Calder, 1984).It is important to note that this metabolic increment is fundamentally differentfrom that in other 'endothermic' animals, which elevate heat production byskeletal muscle contraction (e.g. insects, Kammer, 1981; tunas, Stevens and Neill,1978; brooding pythons, Hutchison et al. 1966) or modified skeletal muscle tissue(e.g. billfish heater muscle, Block, 1987). The high rates of maintenancemetabolism of birds and mammals are not myogenically based; they are generatedprimarily by visceral organs and the central nervous system. In humans, nearly70% of resting metabolic rate is accounted for by the metabolism of the heart,kidneys, brain, liver and intestines, even though they constitute only 7 % of bodymass (Aschoff et al. 1971). Skeletal muscle tissue can produce high levels of heat inthe cold or during activity, but is largely uninvolved in the production of the highbasal metabolic rate of birds and mammals.

A difficulty in explaining the evolution of increased aerobic capacity onthermoregulatory grounds alone is its energetic cost. Maintenance metabolic ratemust be increased very substantially above reptilian levels before signified


pBmeothermy and high body temperatures can be achieved. Basal metabolic ratesof birds and mammals exceed those of extant reptiles of equal size and bodytemperature by a factor of 6-10, and this differential is substantially greater atlower ambient temperatures (Dawson and Bartholomew, 1956; Bennett andDawson, 1976). Minor increments (e.g. a doubling) in maintenance metabolicrates would not have been effective in establishing homeothermy or raising bodytemperature, but would have added substantially to energetic demands of field-active animals with little apparent benefit. The problem for the thermoregulatoryexplanation of the evolution of high metabolic rate lies in justifying intermediatestages in selective terms, presumptive adaptive valleys between adaptive peaks.Even if the final goal of endothermic homeothermy is worthwhile in terms offitness, the condition cannot evolve unless all intermediate stages also confersequentially greater fitness benefits. In a character as complex as endothermictemperature regulation, involving so many physiological systems, it is highlydoubtful that it could have developed in its entirety without many intermediatestages. The problem becomes even more complex if ancestral animals had thecapacity for behavioural thermoregulation of high body temperatures, as do manyextant reptiles. In this case the benefits of high and relatively constant temperaturewould already have been available without increased metabolic cost. Oneargument has been advanced (Crompton et al. 1978; Taylor, 1980) that endo-thermy evolved in the mammalian line in response to nocturnality, whenbehavioural thermoregulation at high temperature is precluded. This argumentloses force, however, if endothermy was already present in the reptilian ancestorsof these nocturnal mammals (see above, Bennett and Ruben, 1986).

A second explanation suggested for the evolution of increased metabolic rates inthe mammalian and avian lineages is the increased capacity for aerobicallysupported activity (Regal, 1978; Bennett and Ruben, 1979). Increased levels ofmaximal oxygen consumption directly expand the range of levels of sustainableexertion and the behaviours that depend on them (e.g. Fig. 3). Animals withgreater aerobic limits have greater endurance in a variety of different activitiesthat may influence fitness, such as prey pursuit, predator avoidance, territorymaintenance and courtship. It is relatively easy to visualize a direct benefit inselective terms to such increased endurance capacity, particularly in animals, suchas reptiles, that have limited aerobic capabilities and must otherwise dependheavily on anaerobic metabolism, with its ensuing exhaustion, to support vigorousactivity. Ancestral animals in both the mammalian and avian lineages seem to havebeen progressively more capable of vigorous activity, as shown by general skeletalrearrangements, such as a change in limb suspension and reduction of skeletalmass (Romer, 1966; Olson, 1971; Kemp, 1982; Carroll, 1988). The expansion ofaerobic capacities to support endurance-related behaviours is, thus, plausible in itsprogressive accrual of benefits during its evolution (i.e. no apparent adaptivevalleys) and is also in accord with general palaeobiological patterns of the groupsi question.

The difficulty for the 'aerobic capacity' (Taigen, 1983) theory of the evolution of

16 A. F. BENNETT

endothermy is explaining the concomitant rise in maintenance metabolic rate w i^that of maximal oxygen consumption (Bennett and Ruben, 1979). If increasedaerobic capacity during activity were the only consideration, it seems that a moresatisfactory solution would have been to expand maximal aerobic rates withoutincreasing maintenance rates. Thereby, the animals could benefit from bothincreased endurance and low maintenance costs, the latter being characteristic ofectothermy (Bennett and Dawson, 1976; Pough, 1983). A general linkage betweenmaximal and maintenance aerobic metabolic rates was proposed to explainincrements in the latter as the former is increased (Bennett and Ruben, 1979). Inall groups of vertebrates, even within individual poikilotherms at different bodytemperatures, maximal oxygen consumption exceeds maintenance by an averagefactor of approximately 10. The physiological basis of this linkage is unclear,especially as maximal rates are largely myogenically based and maintenance ratesare not. This factorial difference is not fixed or absolute, and comparisons amongdisparate species of similar body size can show differences in maximal rateswithout similar differences in maintenance rates (e.g. Bennett, 1972b, 1978;Ruben, 1976; Taylor et al. 1987). In phylogenetically controlled comparisons,which are inherently more reliable (Felsenstein, 1985; Huey, 1987), significantpositive correlations between these factors occur among groups of anuranamphibians (Taigen, 1983; Walton, 1988£>). Such correlations have not been foundwithin species (Pough and Andrews, 1984; Garland and Else, 1987; Garland et al.1987). Thus, this association remains a generality, without a firm mechanisticexplanation or intraspecific correlational basis. Two factors, however, bear furtherinvestigation. First, all previous studies refer to phenotypic correlations amongmetabolic rates. Genetic correlations may have very different patterns and linktraits evolutionarily without obvious phenotypic associations (Arnold, 1987).Examinations of the genetic relationships between maximal and maintenancelevels of oxygen consumption would prove helpful in understanding theirassociation. Second, the relationship between intraspecific and interspecificcorrelation and its relationship to the analysis of evolutionary pattern is justbeginning to be analyzed (Emerson and Arnold, 1989). Further theoretical andexperimental studies on these general associations would also be valuable.

In summary, both explanations for the evolution of high metabolic ratesassociated with endothermy have positive features and difficulties. Perhaps acombination of thermoregulatory and activity capacity factors were involvedsimultaneously or sequentially. The early stages of its evolution may have beendominated by selection for increased endurance, and its later stages by selectionfor homeothermy. Unifactorial explanations for the evolution of any complexcharacter are almost certainly incomplete.

Future directionsUnderstanding the evolution of such complex characters as activity capacities, i

both their mechanistic bases and adaptive significance, is a fundamental goal 1


ppganismal biology. In the studies cited above, an excellent beginning has beenmade, both conceptually and experimentally, in addressing the issues. In myopinion, we would benefit from further studies on the operation of selection onthese characters in natural populations of diverse taxa, followed by studiesattempting to quantify locomotor behaviour under field conditions and to identifyselective agents. The bridge between microevolutionary studies on extant popu-lations and diversification of capacities among higher taxa is a difficult one tobuild, but one well worth the attempt. Comparative studies on differentpopulations within a species or among congeneric species with diverse activitycapacities may be useful in uncovering the physiological and morphological bases,and perhaps the ecological determinants, of activity capacity. Experimentalmanipulations, where feasible, of such factors as food or mate availability orpredation may be particularly useful in examining their influence as agents ofselection. Choice of appropriate experimental groups will obviously be crucial tothe success of these studies. Analysis of ancient historical pattern, for instance theselective causation and mechanism of the evolution of endothermy, will probablyalways remain speculative. However, the use of phylogenetically based analysesand the future availability of new analytical techniques may help to resolve someof the major questions in this area.

I thank R. J. Full, R. B. Huey and J. A. Ruben for critically reading andcommenting on the manuscript and S. M. Reilly for help preparing the figures.Supported by NSF Grants DCB88-20128 and BSR90-18054.

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