costs and consequences of evolutionary temperature adaptation

Costs and consequences ofevolutionary temperature adaptationAndrew Clarke

Biological Sciences Division, British Antarctic Survey, High Cross, Madingley Road, Cambridge, UK CB3 0ET

Temperature affects everything that an organism does.

Although we have an increasingly sophisticated under-

standing of evolutionary adaptation to temperature at

the molecular level for some cellular processes, we still

know little about evolutionary temperature adaptation

in gene expression, cell-cycle control or growth, all of

which influence organism performance and fitness.

Recent studies have shown that the physiological costs

of evolutionary temperature adaptation vary with body

temperature. Here, I argue that this macroecological

pattern has powerful consequences for life-history

theory, and probably also for food-web dynamics, bio-

logical diversity and biotic response to climate change.

The relationships among evolution, temperature and

ecology are multivariate, hierarchical and complex

making evolutionary physiology at the macroecological

scale an exciting and challenging agenda for the next

decade.

Over the past few decades, significant advances have beenmade in our understanding of the evolutionary adaptationto temperature in some cellular processes and we can nowmake important generalizations concerning the molecularmechanisms involved [1–3]. Here, I present a highlypersonal view of how these recent advances affect ourunderstanding of temperature adaptation and its ecologi-cal and evolutionary consequences. My aim is twofold: firstto identify important gaps in our knowledge of evolution-ary temperature adaptation, particularly where theseimpinge on organism performance and, second, to explorethe consequences of this adaptation for ecology.

Evolutionary temperature compensation in cellular

processes

A simple conceptual model of evolutionary temperaturecompensation is given in Box 1. This model prompts twoimmediate questions: how has evolution altered physi-ology to optimize function at different temperatures, and towhat extent has full compensation been achieved?

Faced with a change in temperature, organismsattempt to maintain physiological rates by one or moreof three strategies: quantitative (changing the concen-trations of enzyme and/or reactants); qualitative (using aprotein variant with different thermal characteristics); ormodulation (modifying the protein environment to mini-mize the impact of temperature change) [4]. Important

general responses include changes in enzyme concen-tration, changes in primary structure affecting the freeenergy of activation, and modification to both membraneproperties and intracellular milieu. These adjustments aregenotypic (although, in some cases, similar changes areinduced by acclimation), and across-species comparativestudies meet the strong criteria for demonstratingadaptive evolution [5]. They are, however, usually con-cerned primarily with univariate studies of individualenzymes or proteins. These have provided powerfulinsights into the relationship between enzyme functionand organism performance [6,7]; what is needed now is toput these results in the context of the complex networkwithin which the individual components are functioning.

A typical vertebrate cell synthesizes many enzymes,which participate in upwards of 105 reactions. Because allof these reactions are affected by any daily or seasonalchange in temperature, the potential for disastrousmetabolic imbalance would seem to be enormous. In fact,individual biochemical reactions typically exhibit anarrow range of temperature sensitivities. This is due,in part, to the dependence of ligand binding and productrelease upon the breaking and formation of weak bonds,and the general similarity of the free energy changesinvolved tends to moderate against high temperaturesensitivity [4]. Also, it might be expected a priori thatnatural selection would have produced a balanced networkof metabolic interactions [8].

Faced with the complexity of metabolism, thermalphysiologists have tended to focus upon the centralimportance of ATP generation and utilization to cellularphysiology and, in particular, the influence of temperatureon ATP generation (glycolysis and the tricarboxylic acidcycle) and its utilization by proteins involved in cellularand organismal motility (actin, mysosin and tubulin). Thecentral importance of energy metabolism and locomotorability to organism function and fitness means that thesestudies are of direct relevance to life history and ecology.Our knowledge of thermal physiology is, however, limitedto a very small sub-set of proteins within the cell.Moreover, metabolic control is subtle and studies ofstructural adaptations within individual enzymes aretelling us only part of the story. A complete picture ofhow the cell responds to a thermal challenge (and hencethe whole-organism response) will come only through anunderstanding of the dynamic behaviour of the complexmetabolic systems within which those individual enzymesoperate (Box 2).Corresponding author: Andrew Clarke ([email protected]).

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Evolutionary temperature compensation in organism-

level processes

Thermal physiologists have tended to concentrate oncellular processes that can be examined at the molecularlevel, but we still do not know much about evolutionarytemperature adaptation at the molecular level in import-ant organismal-level processes, such as growth. This is acomplex process, regulated by subtle controls, which ishighly sensitive to levels of resources. Thus, a simpleobservation of a slow growth rate in a polar organism, or ofa correlation between growth rate and some measure ofenvironmental temperature, cannot itself distinguishbetween a fundamental thermodynamic limitation bytemperature and resource limitation (whether continuousor seasonal) [17]. This can only be resolved by examiningthe thermodynamic characteristics of the growth processat a molecular level (Box 3). Our poor knowledge of themechanism of evolutionary temperature compensation ingrowth processes remains a major limitation to ourunderstanding of how organisms respond to temperature.

A second area of whole-organism physiology where thedistinction between rate and underlying adaptation haslong been confounded is that of respiratory demand(i.e. oxygen consumption). As with growth, the importantdistinction is between what evolution has achieved interms of capacity, and the observed rate of oxygenconsumption, which is dictated by local ecological andphysiological demands. Aerobic respiration simplyreflects the demand for ATP at the time of measure-ment; it provides no information about the extent ornature of the evolutionary adaptation of the organismto temperature [31].

Physiological costs of temperature adaptation

Just as important as the efficacy of evolutionary adap-tation is its cost. It is here that measurements ofrespiratory demand have much to contribute to ourunderstanding of temperature adaptation, because theyprovide a direct insight into the energetic costs of thatadaptation in the sense of what it costs an organism to runcomplex metabolic systems adapted to a particulartemperature.

In absolute terms, where protein variants adapted tooperate at different temperatures vary by only a few aminoacids, it costs an organism effectively no more ATP to makea molecule of one variant than it does to make another.However, energetic costs become relevant when a particu-lar variant is required in larger amounts, or is turned overfaster. The turnover of a given protein is the outcome of acomplex interaction between temperature, molecularstability and physiological function and, currently, therequirement for protein turnover cannot be predicted fromfirst principles [31]. There is strong evidence for proteindamage in organisms at their normal living temperature[32] but as yet we do not know to what extent, if any, thisvaries between polar, temperate and tropical organisms, orthe extent to which this might be mediated by variation inconstitutively expressed chaperone proteins [33,34].Recent studies indicate that, in organisms living at lowtemperatures, a greater proportion of newly synthesized

Box 1. What is temperature compensation?

The central concept underpinning temperature compensation is that

organisms should respond to a change in temperature such that they

can maintain physiological function. This leads to a straightforward

definition of thermal compensation as the maintenance of physio-

logical rate as the temperature changes [3], which can be expressed

as a simple conceptual model (Figure Ia; redrawn, with permission,

from [17]).

In Figure Ia, the filled symbols show the acute response to a change

in temperature for individuals of two hypothetical species, one

adapted to a warmer and one to a cooler environment (circles and

squares, respectively). The open symbols mark the physiological

rates at the normal environmental temperature for the two species.

These rates are similar, indicating that evolutionary temperature

adaptation has enabled the two hypothetical species to operate at the

same rate at their normal living temperatures. The horizontal line

generalizes this to a formal definition of evolutionary temperature

compensation. Whereas the two rate/temperature relationships

reflect the thermodynamic impact of temperature on an individual

organism, the open symbols represent two independent evolution-

ary optimizations. The rate/temperature relationships for individuals

have a thermodynamic explanation, albeit complex, whereas the

evolutionary outcomes for different species can only be described

statistically.

This conceptual model defines a theoretical outcome for

evolutionary temperature adaptation, against which we can

compare what organisms actually do. However, this simple

idealized outcome is unlikely to be seen in nature, because all

biology is characterized by variability. A more realistic descrip-

tion is shown in Figure Ib, where the compensation plot (shaded

area) has both slope and bandwidth. The slight slope empha-

sizes that there might be fundamental thermodynamic con-

straints that make perfect compensation impossible to achieve

in the real world. The bandwidth emphasizes that, in any one

thermal habitat, there will be variation in physiological rates

associated with ecology, lifestyle and phylogeny.

A null model?The simple conceptual model (Figure Ia) defines what we might

expect to be the outcome of perfect evolutionary temperature

compensation. In recent years, powerful insights have been gained

in ecology through the construction of null models. This suggests

that an alternative hypothesis is that of no adaptation. The problem is

defining such a null model. Apart from the theoretical objection that

an organism exhibiting no temperature adaptation would not

survive, any construction of a meaningful null model of the effect

of temperature on physiological rate in the absence of compensation

is hindered by our lack of knowledge of the underlying processes. A

null model for temperature compensation is thus currently imposs-

ible to construct, and we are forced to compare our observations of

the real world with a conceptual model of perfect temperature

compensation.

Figure I.

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protein is degraded than in those living at warmertemperatures [35].

One way to examine the energetic consequences oftemperature adaptation is thus to look at the overall costsof existence, which comprises the sum of all processes thatare necessary to maintain viability, but excludes reproduc-tion, growth or activity. Recent comparative studies ofmarine ectotherms have shown that these costs varysignificantly with temperature (Box 4). Resting metab-olism comprises the ATP demand of many differentprocesses, and thus represents the cost of living aparticular lifestyle at a given temperature [31].

We cannot yet determine whether the higher restingmetabolism of tropical organisms is an inevitable conse-quence of living at higher temperatures, or whether theoverall relationship in Box 4 reflects the outcome ofselection on other factors, such as seasonality of resourceavailability, aerobic scope, or thermal flexibility. Onepossible fundamental constraint on the scaling of whole-organism power output is mitochondrial function. Recentwork has suggested a strong thermal dependence on ATPgeneration in mitochondria isolated from fish living atdifferent temperatures [43,44]. This suggests that, in spiteof changes in mitochondrial structure and composition,

evolution has not produced mitochondria that can syn-thesize ATP as rapidly in polar organisms as in tropicalones. One response to this constraint is to increase themitochondrial volume density which, in polar fish, can bevery high [45,46].

Ecological constraints: temperature, energetics and life

history

The macroecological-scale variation in the cost of existencein marine ectotherms provides a clear indication of theimportance of physiological constraints in ecology at theglobal scale [47]. Three aspects of the relationship betweenresting metabolic rate and temperature merit discussionin relation to life history and ecology, namely the slope,variance and the influence on aerobic scope.

The slope indicates that the cost of living is significantlylower in ectothermic marine organisms living at lowtemperatures than in those living in the tropics. Thismeans that, all else being equal, a polar marine organismneeds significantly less food to stay alive than does asimilar tropical organism; it also means that polarorganisms can withstand longer periods of starvation.Indeed, many polar marine invertebrates cease feedingcompletely for several months during winter [48].

Box 2. The challenge of physiological complexity

Studies of evolutionary temperature adaptation have concentrated

almost exclusively on selected individual proteins. A typical

vertebrate cell, however, synthesizes .104 different proteins,

which are involved in .105 interactions, and even a simplified

model of the more important pathways of metabolism is complex.

Although selection in a competitive food-limited environment will

have led to the evolution of efficient metabolic pathways [9], until

recently we have lacked the formal tools to explore this

analytically.

Recent studies with microbes have shown that temperature

acclimation results in restructuring of the genome [10]; at present

we have no idea how general this response is, or what the

implications might be for metazoan cellular physiology. At the

proteome level, important insights into the structure of metabolic

networks have come from analyzing interactions between proteins

[11]. A recent study of the core metabolic network of 43 different

organisms ranging from archaea to metazoans has shown that the

probability that a given substrate participates in a particular

number of reactions follows a power law distribution (Figure I).

In other words, metabolic networks are scale-free networks [12].

They also exhibit so-called small-world behaviour, in that any two

substrates (nodes) can be connected by relatively few links. The

modal number of links is 3, and this number is similar in all 43 taxa

examined, suggesting that the basic structure of the metabolic

network is similar in all organisms [12].

The dominance of the network structure by a few highly

connected hubs provides a rigorous framework for the observation

that selection pressure on the primary structure is related to the

contribution of that protein to overall fitness [13]. Not all enzymes

are under equal selection pressure and we do not know whether

the evolutionary adaptations observed in those enzymes studied

so far are typical of all cellular enzymes. Neither do we yet

understand the balance between whole-cell homeostatic processes

and evolutionary adjustment to individual enzymes in achieving

compensation for temperature.

There is continuing debate over whether evolutionary or

stochastic processes led to the structure we observe in metabolic

networks [14–16]. In terms of thermal physiology, the next step

is to determine the robustness of the metabolic network to

physiological challenge and, particularly, the boundary conditions

for variation in the thermal characteristics of individual links to

maintain network integrity and function in the face of temperature

change.

Figure I. Connectivity distributions for metabolic substrates. P(k) is the prob-

ability of a given metabolite participating in k reactions. Note the logarithmic

transformation. Data shown are combined data for 43 organisms from three

domains (archaea, bacteria and eukaryotes). The power law is PðkÞ < k2u;

appearing as a straight line on a double logarithmic plot, as here. For these

data, u ¼ 25:7 under natural logarithm transformation. Redrawn, with per-

mission, from [12].


Ln (k)

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A temperature-related latitudinal variation in restingmetabolic costs will also lead, all else being equal, to higherecological growth efficiencies at lower temperaturessimply because, for any given amount of food consumedor reserves utilized, a greater proportion can be directed atgrowth, as less is lost in maintenance. The extent to whichthis is realized will be influenced by absolute rates ofenergy intake, but first-order analyses of available datahave supported the predicted trend in the production:bio-mass (P:B) ratio [49]. A recent study of marine copepods[50] has also indicated higher growth efficiencies at lowertemperatures.

The macroecological-scale variation in cost of living formarine ectotherms (Box 4) and the associated variation ingrowth efficiency [49] mean that a given trophic level in a

tropical food web will degrade a greater proportion ofbiologically fixed energy than will a similar biomass at thesame trophic level in a comparable polar food web. Coupledwith the strong latitudinal variation in the seasonality ofenergy input, and in the proportion of endotherms athigher levels in the community, this means that both ratesand patterns of energy flux will differ markedly betweenpolar, temperate and tropical food webs. Although thiscould limit the number of trophic levels, there is littleconvincing evidence for any link between energy flow andfood-web structure, with the exception of the undoubtedlyextreme case of the highly oligotrophic lakes in the DryValleys of Antarctic [51]. We have yet to explore theimplications of macroecological-scale variations in theenergetics of individuals to food-web dynamics or stability.

Temperature-related variation in metabolic costs alsohas implications for reproductive investment. Factorssuch as detoxification in organisms inhabiting pollutedenvironments, or the production of heat-shock proteins inthermally stressful habitats [52] increase maintenancecosts and thereby reduce investment in growth orreproduction [53]. Latitudinal patterns in maintenancecosts have, however, received little attention in thiscontext. A preliminary study of the deep-water shrimpPandalus borealis has suggested that, across the widelatitudinal range of its distribution, there is a balancebetween annual reproductive output, metabolic costs andlongevity, leading to lifetime reproductive effort beinginvariant with latitude [54]. Furthermore, many high-latitude organisms have slow growth rates and extendedlife times; it is an intriguing but currently untestedpossibility that this might balance the lower restingmetabolism to equalize lifetime maintenance costs acrosslatitudes and thermal environments.

The maximum power that an organism can generaterelates directly to its lifestyle and ecology. Maximumpower is typically expressed either as a factorial scope (theratio of maximum to resting metabolic rate) or as theabsolute scope for activity (the arithmetic differencebetween maximum and resting metabolic rate). Currentevidence suggests that the factorial aerobic scope oforganisms with similar ecology does not vary withtemperature, although data for ectotherms are scarce[37]. Because resting metabolic rate does vary withtemperature (Box 4), the absolute metabolic scope (theamount of ATP available for physiological work, such asactivity) will also vary with temperature. Although livingat low temperatures is cheap, providing a buffer againststarvation, highly energetic lifestyles are only possible inwarmer water.

In linear space, the between-species variance in the costof living increases dramatically from the poles to thetropics (Box 4). One factor contributing to this variance islifestyle; it has been shown clearly for fish that taxa withmore active lifestyles tend to have higher resting metabolicrates [36,38]. The plot does, however, suggest that there isa greater range of life histories available in the tropicsthan in the poles. It would be premature to extrapolatefrom this to tropical and polar ecology in general, becausethere is more to life history than temperature andenergetics. Nevertheless, the central role of energetics in

Box 3. The growth rate paradox

One might expect a priori that, being crucial to fitness, growth rate

would exhibit a strong degree of evolutionary temperature compen-

sation. Comparative studies have suggested that, under favourable

circumstances, the growth rate of some polar taxa can approach

those of temperate or even tropical taxa of similar size and ecology

(reviewed in [18]).

Experimental analyses of both marine and terrestrial organisms

have shown that within-species latitudinal clines in growth rate are

determined genetically and serve to offset the effects of temperature

on growth rate [19–21] (for an exception, see [22]). Cell-cycle time

might also show a similar evolutionary adjustment [23]. These two

sets of studies demonstrate clearly that: (i) populations are often

locally adapted; and (ii) evolutionary adaptation can offset the rate-

limiting effect of low temperature on growth rate. However,

whenever ectotherm growth rates are plotted at the macroecological

scale, there is usually a positive correlation between growth and

environmental temperature [24,25]. We are therefore faced with an

apparent paradox in that physiological or genetic studies of related

taxa indicate clearly that evolution can adjust the molecular

processes underpinning whole-organism growth rate to offset the

rate-limiting effects of temperature, but, on a macroecological scale,

growth rate varies with measures of environmental temperature in a

sufficiently robust manner to be used as a predictor in physiological

or ecosystem models [26].

This emphasizes the importance of distinguishing capacity (the

rate at which an organism can work, which indicates the extent of

evolutionary temperature adaptation) and the rate realized in the

field (which does not); a simple correlation between field growth rate

and temperature tells us nothing about evolutionary temperature

adaptation. The explanation for this apparent paradox is that growth

rates in the wild are frequently constrained by resource limitation

(both absolute and temporal) such that the underlying capacity for

growth is either never realized, or only attained for short periods of

time.

An example of seasonal resource limitation comes from the

venerid bivalve genus Protothaca, where a latitudinal cline in growth

rate is caused by a progressive decrease towards higher latitudes

(and hence colder temperatures) in the number of days during which

an individual can feed [27]. Growth rate might also be influenced by

variations in digestion or growth conversation efficiencies [28], and

there is also the complex question of tradeoffs, whereby rapid growth

incurs ecological costs [29] or where a balance must be struck

between different energetic sinks such as growth, reproduction or

maintenance [30]. We still therefore have no broad-scale under-

standing of the extent to which evolution has achieved full

compensation for temperature in the complex process of growth,

and we are still some way from achieving a macroecological-scale

picture of how individual growth rate interacts with either the

environment or ecology.




ecology and its potential role in determining somemacroecological patterns suggest that this pattern isworth further investigation.

Can we generalize between marine and terrestrial

organisms?

Terrestrial plants and animals are exposed to a thermalenvironment that changes far more rapidly, and over agreater daily and seasonal range, than are aquatic

organisms. Does this mean that the evolutionary adjust-ments seen in terrestrial organisms are similar to those inmarine organisms, but just more difficult to detect? Ordoes the different thermal environment require a funda-mentally different evolutionary response? For example,has the terrestrial environment selected for a moreeurythermal physiology, which is perhaps more expensiveto maintain, or is the contribution from phenotypicplasticity greater? And does the difference in the physics

Box 4. Basal metabolism: the cost of evolutionary temperature adaptation.

The cost of living in marine ectotherms is related to both temperature

and ecology [36]. Where comparisons are undertaken between taxa of

similar ecology, the relationship with environmental temperature is

positive and monotonic (Figure Ia) [37]. When data for fish of all life

styles are included, these exhibit a generally higher resting metabolism,

and a significantly greater variance, much of which resting metabolism

is associated with ecology: fish with more active lifestyles tend to have

higher costs of living [36,38].

This relationship was first described for routine metabolism in

crustacean zooplankton [39], and has been shown for other groups of

marine invertebrates [40]. It is probable that a similar relationship

underlies the metabolism of terrestrial organisms, but this is difficult to

discern against the more complex thermal environment of terrestrial

habitats and no comparable macroecological-cale analyses are cur-

rently available. One global-scale study across prokaryote and

eukaryote taxa has however postulated a single temperature depen-

dence for all organisms [41], although this remains somewhat

controversial.

The between-species relationship between resting metabolic rate and

temperature is the result of many independent evolutionary optimiz-

ations (Box 1), and can only be described statistically. The Arrhenius plot

(Figure Ib) is thus just one of several statistical models that provide an

adequate fit to the resting metabolism data. At present, we have a

working explanation for neither the slope nor elevation of this

relationship. All we can say is that one or more aspect of resting

metabolism is far more expensive at warmer temperatures than at lower

ones. The overall slope of this relationship exhibits a lower temperature

sensitivity than that typically observed for individual biological

reactions or acute whole-organism responses [36].

Current estimates thus suggest that the costs of staying alive for

tropical marine ectotherms exceed those for comparable polar taxa by

roughly an order of magnitude. These extra physiological costs have

powerful ecological consequences in that they must be met through

similarly enhanced food consumption. Probable candidates for higher

existence costs at warmer temperatures include protein turnover,

osmoregulation and maintenance of mitochondrial proton balance, all

of which are important consumers of ATP [42].

Figure I. The cost of living in ectotherms. (a) Resting metabolism in teleost fish

(mmol oxygen gas h21, scaled to a wet mass of 50 g using a mass exponent of

0.78), as a function of the temperature at which the fish lives. Open circles

show data for six taxa of similar activity and lifestyle [37]. Filled circles are all

other data [36]. (b) All data for teleost fish, fitted with an Arrhenius statistical

model. Redrawn, with permission, from [36], including data from [37].


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of oxygen supply as a gas or in aqueous solution affecthow organisms respond to temperature? At present, wedo not know the answer to any of these questions, butwe should perhaps take care when generalizing betweenland and sea.

Possible macroecological consequences

The potential links between physiology and macroecologyare many and varied [55], but, as yet, most of these are onlystarting to be explored. I therefore discuss a singleexample (the relationship between temperature and thecost of living) in the hope that this will help defineinteresting questions and identify future avenues forresearch. This relationship is confined to ectotherms, andso far demonstrated clearly only for aquatic taxa, althoughresting metabolic rate has also been shown to vary, albeitonly slightly, in mammals [56]. Large-scale patterns inecological energetics have now started to enter macro-ecological thinking. For example, arguments based aroundmetabolic energy have been used to explain macro-ecological patterns in body size [57] and energy availabilityhas emerged as one of the leading hypothesies forexplaining global patterns of biological diversity [58,59]although (at least for animals) the precise mechanistic linkbetween energy and diversity is far from clear. Analternative hypothesis has proposed that a mechanistictemperature dependence of metabolic rate [41] predictsglobal patterns of biological diversity [60]. This is one ofthe first macroecological hypotheses to take explicitaccount of global-scale patterns in resting metabolicrate, although the explanation for the underlyingrelationship between cost of living and temperatureis very different from that advanced here (Box 4) andelsewhere [31].

Crucial to our understanding of large-scale patterns ofdiversity is the structure of geographical range. In thiscontext, it has long been recognized that there is a matchbetween the physiology of an organism and the thermalcharacteristics of its habitat; this is simply an expressionof local adaptation (for a recent thorough study of plants ona continental scale, see [61]). Many organisms with rangesthat extend over a significant latitudinal extent alsoexhibit clines in physiological performance. Statisticaldescriptions of thermal niche are useful [62] and climate-matching approaches have proved invaluable in palaeo-climate reconstruction [63]. There are now many examplesof organism distribution shifting in response to climaticchange in ways that would be predicted from simplethermal physiology, both since the last glacial maximum[63] and under recent climate change [64–67]. Althoughthese observations are intuitively reasonable, we still lacka general model for how thermal physiology and climateinteract to determine biogeography [68], although someimportant advances are emerging from studies of Droso-phila serrata in Australia [69,70].

To understand geographical ranges, and how thesechange, we need to understand what determines theborders of the distribution of an organism. Although thereare a few well documented cases of at least one boundary tothe distribution of a particular organism being set bythermal responses [71], we do not know precisely what

processes set the boundary to the geographical range of aspecies [71,72]. For example, in the rocky intertidal zone,the upper boundaries to vertical distributions are typicallyset by tolerance to physical factors and lower boundariesby biotic interactions [73]; limits to geographical range areless well understood and probably involve both physicaland biological factors. Recent studies have demonstratedclearly the important roles of energetics and the cost ofliving in determining range limits in intertidal organisms[74,75] and they might also influence abundance structurewithin the range [76]. In spatially structured populations,gene flow from core sites can lead to suboptimal adaptationin peripheral populations, which could limit the ability ofthat organism to shift geographical range in response tothe movement of climatic zones [38].

Although the broad features of distributional changescan often be explained in terms of a generalized thermalniche, no organism lives in an ecological vacuum, andrecent experimental work has demonstrated clearly theimportance of competitive interaction in modifying theresponse to a change in thermal environment [77–79].This work has led to a strong debate [80], but the emergingpicture is that, although ecophysiological and climatespace models are valuable in describing the adaptivematch between organism and habitat, the boundaries togeographical ranges are typically set by other factors,including competitive interactions and suboptimal phys-iological performance caused by the inability to capturesufficient resources or the need to divert greater amountsof energy to defense, repair or maintenance [53].

Periods of climate change in geological history havetypically involved mean rates of change in temperaturethat are orders of magnitude slower than those that manycurrent organisms experience either daily or seasonally[81]. We are still refining the temporal details of historicalextinctions, and it remains possible that the crucialfeatures for extinction were short bouts of very rapidclimate change rather than the overall mean rate. Never-theless, the patterns of extinction point clearly toecological processes at work, and not simply the thermaldeath of individuals [82]. Rapid climate change is increas-ingly recognized as an important factor in evolutionaryhistory, and it is possible that such change could induce aswitch between different stable or metastable states, oroften catastrophic collapse of ecosystem structure, just asmuch as gradual environmental change [81]. Crucial todetermining how climate change drives either back-ground, regional or mass extinctions will be an under-standing of organism thermal physiology and how thisaffects ecosystem dynamics.

Concluding remarks

The study of thermal ecology has reached an importantpoint in its development. We have sufficient understand-ing of temperature adaptation in a few key cellularprocesses for general principles to have emerged. Forecologists, the most important areas of ignorance are thoseaspects of physiology with a direct impact on organismfunction and fitness. The next stage is to examine otherimportant cellular processes, and to relate these univari-ate studies to the rapidly developing field of the dynamical




behaviour of complex metabolic systems (Box 5). Theemerging concepts of limitation by mitochondrial poweroutput and aerobic scope combine to provide a new andstriking picture of ecological consequences: for anectotherm, living at low temperatures is cheap but forthe more energetic lifestyles a warm body is a prerequisite.

Arguments centred on per capita energy intake haverecently entered the ecological literature in several areas,including population abundance structure, optimal bodysize, the dynamics of food webs and assemblage diversity[47,57,60,83]. Maintenance costs comprise a significantfraction of per capita energy intake and an importantchallenge is to incorporate into these arguments themacroecological pattern in the cost of evolutionarytemperature adaptation [Box 5].

At small scales, we already have a working under-standing of molecular mechanisms and how these relate toecology; we can also see clear links between physiology andecology at the very largest scales. The problem is theintermediate scale: we find it difficult to understand howcommunities work [84] and we still cannot integratephysiology and ecology at the community scale [51]. Wecan see macroecological patterns that appear to relate totemperature (e.g. diversity at the global scale) and we see

how cellular physiology relates to individual organisms.What we cannot do is link this to how the range of anorganism is determined, or to the role of ecologicalphysiology at the assemblage scale. The problem ismultivariate, hierarchical and complex. What is becomingknown as evolutionary physiology [85] is an urgent andchallenging agenda for the next decade.

AcknowledgementsThe development of the ideas here benefited from many discussions withIan Boyd, Steven Chown, Pete Convey, Alistair Crame, Bill Detrich, Guidodi Prisco, Joe Eastman, Stuart Egginton, Ian Johnston, Kevin Gaston,John Montgomery, Lloyd Peck, Hans-Otto Portner and Bruce Sidell. IanBoyd, Pete Convey Lloyd Peck and four referees provided constructivecriticism of the article.

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Box 5. Outstanding questions and future directions

Although a coherent picture is emerging of the molecular changes

involved in the evolutionary adaptation of enzymes to temperature,

relatively few enzymes and important cellular processes have been

examined. We now have a broad understanding of the manner in

which some key enzymes involved in ATP generation and the

function of some contractile proteins compensate for changes in

temperature. ATP is, however, utilized in a complex array of cellular

processes, for many of which we know little about their response to a

change in temperature.

If we are to make significant advances in our understanding of the

impact of temperature on organismal function, we must focus on

those processes that are most crucial to the interaction between the

organism and its environment; in this context the most important

cellular processes are: gene function (transcription rate and

accuracy, role of promoter genes, message turnover and proces-

sing); protein synthesis (translation rate and accuracy, post-transla-

tional modification, and protein transport) and degradation;

mitochondrial power output and resting proton leak; cell-cycle

control; ion transport and cellular homeostasis; and chaperone

proteins (especially constitutive expression). The first four are

important components of organism growth, and the latter two

influence how cells respond to an external physiological challenge.

The thermal behaviour of these cellular systems must also be set in

the context of the complex metabolic network within which they sit.

Rapid progress is being made in understanding the topological

structure of metabolic networks and this is posing fundamental

questions as to how metabolism originated and has evolved. The

important questions in terms of organismal function concern the

sensitivity of the metabolic network to physiological challenge, and

its robustness and resilience to such challenges.

Finally, there is an urgent need to incorporate physiological

thinking into ecology at the global scale. Important questions include

the consequences of macroecological scale variability in the cost of

living for diversity, and the role of energetics in determining the

structure of geographic ranges. Species borders are influenced by

thermal physiology but are often set by factors including compe-

tition; simple climate-matching techniques are necessary but not

sufficient for understanding how organisms react to climate change.

Given the rate at which climate is now changing, understanding

these links is particularly urgent.




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costs and consequences of evolutionary temperature adaptation

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