Origin of Ectothermy
We should not make too much of the claim that the evolution of endothermy flies in the face of the second law of thermodynamics, when we consider that the evolution of increasingly complex organisms in general does the same (as does the evolution of stars, cities, and so forth). Still, the existence of such thermodynamically inefficient organisms as endotherms begs explanation, especially since, unlike the problem of general evolution, it invites explanation in purely thermodynamic terms. All explanations to date have assumed that homeothermy was derived from poikilothermy, and that ectotherms gave rise to endotherms. It is the purpose of this article to examine that assumption from several angles, not precisely in the following order: 1) by attempting to define the terms; 2) by pointing to clear exceptions to the assumption; 3) by philosophical analysis of the problem and extrapolation to the general case; 4) by examining vertebrate evolution in light of the general case.
1) Definitions: Unfortunately the biological terms do not agree with the thermodynamic terms, where plants are correctly labeled endothermic and animals are always exothermic. Biological “endothermy” refers to the character that the organism’s temperature is controlled internally, rather than by its ambient, as is the case with ectotherms. Although the biological “endotherms” may be quantitatively contrasted to “ectotherms,” the fact remains that a penguin with an internal temperature of 310ºK, sitting out an Antarctic storm at 210ºK, still obtains a majority of its heat from the sun. It is only with the evolution of fur and feathers that a seemingly qualitative distinction between endotherms and ectotherms becomes possible, and of course this criterion vanishes when investigating the primitive origins of endothermy, unless we go along with the assumption (or should we say, definition) of Robert McNab (1978), that the evolution of mammalian fur preceded mammalian endothermy, in which case even fur and feathers were not always relevant criteria.
The customary terms, endothermy, and ectothermy, in fact confuse several parameters, principally, those of metabolic rate and the degree of temperature regulation. Clearly, high energy organisms have a greater potential than do less active organisms for acquiring an internal temperature substantially higher than the external temperature. But in spite of the fact that metabolism can only be quantified in terms of heat production, because heat loss must also be taken into account in determining an organism’s internal temperature, there is only a circumstantial relationship between metabolic rate and temperature regulation. The “paradox” of biological thermodynamics is that those organisms with the greatest variability in energy production, at least arithmetically, if not geometrically, are those with the least variation in temperature, while those with less variation in heat output undergo greater temperature variation. Of course this “paradox” may be explained by the differences in heat loss between the two groups, but a description of the evolution of the mechanisms of heat loss, and temperature regulation in general, is not as simple a matter.
The earlier terms, homeotherm and poikilotherm have been replaced to some extent by the later endotherm and ectotherm, but those writers who retain both term pairs tend to emphasize with the former the tendency or lack thereof of maintaining a constant temperature, and with the latter, the organism’s capacity to maintain an internal temperature substantially different from the external temperature, either through heat generation, heat loss, or prevention of heat loss. Accordingly, at least one investigator (McNab) speaks of “endothermic poikilotherms” (like tuna and marlin), and he applies “inertial homeothermy” to animals sufficiently large that they maintain a fairly constant temperature as a result of their large mass rather than a high metabolic rate. McNab introduces the term “trivial homeothermy” in reference to animals that maintain a constant temperature simply because they inhabit an environment with a constant temperature, but we submit that once removed from such environs the animal will either die or it will not: if it dies its homeothermy was not so trivial, and if it lives, it is either an endotherm or a poikilotherm. Hence, there is no such thing as trivial homeothermy, but there is certainly such a thing as obligatory homeothermy, as displayed by such thermophylic creatures as lungfish when exposed to cold, or by any other organism with a very long pedigree of high-temperature physiology. We suggest the term tropotherm to designate such tropical homeothermy, or monotherm to denote the general case of inability to survive moderate temperature fluctuations, as exemplified by some arctic and Antarctic fish which cannot survive temperatures much higher than freezing.
What we have then are two basic parameters for describing the thermal physiology of organisms: the degree of temperature and the width of temperature range at which it can survive. Survival in turn may entail various degrees of activity, including the inactivity of hibernation at one extreme, the activity of many temperate amphibians over a wide temperature range at the other extreme, and between the two extremes, the peak activity of many lizards at specialized temperatures with a sharp drop-off in activity at other than ideal temperatures. Thus on one parameter we have what we might call hyperthermy and hypothermy and on the other, monothermy and poikilothermy, avoiding the established term “homeothermy” only because it has generally been associated with hyperthermy, and so confuses the two parameters.
2) As mentioned above, most investigators have assumed endotherms to be derived from ectotherms, but there is little agreement on how or when the transformation took place. Many take homeothermy to be an automatic result of a high metabolism: the heat resulting from high activity leads a species to tolerate increasing temperatures, and the need for high activity requires that such organisms evolve enzymes that operate at uniform temperatures. Bernd Heinrich (1977) notes that a lack of physiological temperature specialization can only be maintained at the cost of enzyme efficiency, since only a fraction of catalytic processes may operate at any given temperature. McNab on the other hand, considers his “inertial homeothermy” to be the result of a large mass, which once attained by mammals required that when they were reduced in size during the Cretaceous, they were forced to evolve into endotherms. While few would embrace McNab’s postulate that fur and feathers predated endothermy, the notion that homeothermy preceded endothermy should not be dismissed out of hand. Heinrich writes (1977:635):
[A switch to a new body temperature] may be an evolutionary “hurdle” of greater magnitude than mere species evolution. But body temperature can be altered [in order to maintain a high temperature] relatively easily (involving presumably few genes) by changes of insulation, vascular control, postural adjustments, and escape behavior. It is probable that these parameters would be the primary targets for evolutionary response in homeotherms that must respond to thermal changes.
While Heinrich and McNab might agree on little else, they do agree on the persistence of homeothermy, and one wonders why they and all persist in ignoring tropothermy, the most persistent of all “homeothermies,” as a relevant factor in the evolution of endothermy.
There are at least two pathways of evolving to fill a new endothermic niche: 1) by way of ectothermy, which would involve alteration of both temperature requirement and improved temperature maintenance, or 2) by way of tropothermy, i.e., homeothermy, that is, through improved temperature maintenance only. It is the cross purposes of the processes of temperature alteration and temperature maintenance that presumably lead McNab to separate the evolution of homeothermy and endothermy; as he states (1978:4):
It seems unlikely that small endotherms could evolve directly from small ectotherms because the low rates of metabolism and high conductances typical of ectotherms must be simultaneously converted to the very high rates and low conductances of small endotherms. Simultaneity is important because a small ectotherm with a low conductance is disenfranchized with respect to its heat source; equally, a small endotherm with a high rate of conductance would squander heat in a hopeless attempt to maintain a constant body temperature.
So McNab’s solution to the problem that most have failed even to recognize, is to invent “inertial homeothermy” as a stepping stone to endothermy, and to postulate a comparatively late evolution of mammalian endothermy. In taking such a late development as the secondary palate as an indicator of mammalian endothermy, McNab is forced to assail Robert Bakker’s assertion that therapsids were endotherms (1978:16). Bakker suggests that the common ancestors of dinosaurs and crocodiles were warm blooded as well (1970:645):
Crocodilian circulatory and respiratory systems seem more complex than those of other reptiles–the lungs are highly subdivided and mammal-like, the heart is four chambered and a muscular diaphragm is present. The earliest, Late Triassic crocodilians were long-limbed, gracile, terrestrial, probably diurnal predators descended from semierect thecodonts (Walker, 1970). Improvements were quite possibly present in most semierect Triassic archosaurs, including the ancestors of dinosaurs.
Bakker makes a commendable leap when he seems to profess that in this case, ectotherms, crocodiles to wit, evolved from endotherms. Bakker’s insistence that a semierect posture denotes endothermy is of course anathema for McNab (1978:16): “it can be argued that the placement of the limbs under the body is a means of reducing the energy expenditure associated with the transport of a large mass, not evidence of the high rates of metabolism associated with endothermy, as suggested by Bakker.” McNab argues this point to buttress his theory that endothermy comes much later–he and Bakker are on opposite ends of the spectrum on this issue–but his point is well taken: inefficient limbs are in need of a better cardiovascular system than are efficient limbs. Accordingly, the ancestors of crocodiles would have had the greatest selective pressure to evolve complex lungs and a four-chambered heart while they were still squatters and active predators, i.e., before they ever became “long-limbed, gracile…predators.”
The energy efficiency gained by vertical limbs was more advantageous to very large reptiles and dinosaurs than to moderately sized therapsids, since the larger endotherms were in greater danger of overheating–the more efficient their limbs, the faster they could run, and the longer they could run without succumbing to the exhaustion brought on by the inevitable internal temperature rise. This goes far to explain the retention of semisprawling in monotremes–energy efficiency as effected through reduced food consumption was evidently not of sufficient advantage for mammals of a mass typical of monotremes to quickly evolve efficient limbs. Limb structure is first, a measure of adaptation to a particular environment (granted such restrictions as a marsupial pouch, for instance, which might hinder efficient quadrupedal locomotion), and second, a measure of adaptation toward efficient endothermy. It is probably useless as an indicator of incipient endothermy. Limb position is a better indication of how long a lineage has been absent from trees or cliffs than of metabolic history.
But returning to the original problem, let us restate it in Heinrich’s terms (1977:623):
The available evidence indicates that the various homologous enzymes and other macromolecules common to the different forms of multicellular life can be adapted to function efficiently at any of a wide range of tissue temperatures between at least 0ºC and 45ºC. Yet, most highly mobile aerobic animals, such as birds (Dawson and Hudson 1970), mammals (Bartholomew 1972), and large flying insects (Heinrich 1974), regulate body temperature, at least while active, within a few ºC of 40-45ºC, the apparent high-temperature ceiling common to most forms of multicellular life.
The question becomes then, why have endotherms of even distantly related taxa evolved similar operating temperatures: is it due to chance, the physical properties of water, the limitations of enzyme chemistry common to separate phyla of animals, or because they all retain in their physiology the temperature that has characterized the tropics of the globe since the Ordovician? And is there any way of testing the last possibility?
The two possible pathways to endothermy proposed above can be explored in the world of nature by asking in the case of each endotherm, are its closest relatives ectotherms or tropotherms? That is, in each instance, do we have an example of a tropotherm which has extended its climate range through improved temperature control, or do we have a case where an ectotherm has returned to a tropothermic physiology and evolved temperature control mechanisms to maintain it? Whenever this question can be answered, we find that the nearest relatives are tropotherms: endothermic moths evolved from tropical moths; tuna and marlin are the wide-ranging offspring of warm water fish. As we might expect, the simpler route is always taken, which should hardly surprise us when we consider that, with little exception, until the Tertiary most of the globe was tropical. We see that once a lineage has employed the considerable evolutionary effort necessary to evolve poikilothermy, it is hardly a suitable candidate to re-evolve homeothermy, especially when tropotherms are available to fill the niche.
To present an extreme case, consider the fish adapted to polar temperatures. Hemoglobin is useless at such temperatures, and these fish have long since lost it, hence their lack of color. If the poles were to regain the temperate climate that probably characterized them in the Cretaceous, the new niche would be filled by fish of formerly temperate waters. The fish with no hemoglobin, even if they could adapt to the warmer water, would be at a great disadvantage when competing with fish with hemoglobin; the polar fish would have to re-evolve hemoglobin or go extinct, and their future would be dim indeed.
3. Within the phylum Chordata there have always been one or more lineages which progressively pressed their metabolic capacity to new levels. Single celled organisms never had need of special breathing apparatus; with their tiny size they could easily absorb sufficient oxygen from their ambient to supply their considerable metabolic needs, which were principally applied to the process of replication. With the development of multi-celled organisms the metabolic processes of cells became subservient to the needs of the organism, and lower metabolic rates were required, but with continued growth in size there came a time when gas diffusion was insufficient for oxygen supply, and various innovations resulted: a vascular system, a heart pump, hemoglobin, gills, and specialized blood cells. We stress that all these innovations were evolved by those lineages which had the highest activity rates and the highest metabolic requirements.
Ever since the evolution of specialized muscle cells then, there has presented itself an open ended ecological niche for faster, stronger, more responsive organisms, which niche can only be filled by those competitors with the highest metabolic capacity and the most complex sensory responses. Accordingly, such contestants always occupy a highly unstable niche characterized by a rapid rate of evolution. These innovators comprise the principal stock of evolutionary advancement, periodically spinning off shoots that find more stable niches with lower energy life styles (though adaptation to a lower metabolism may itself present the opportunity of radiation into previously unexploited niches).
The need for speed of Devonian fish left them perpetually starved for oxygen. The Devonian atmosphere probably had a lower percentage of oxygen than the present one, and what atmospheric oxygen was available had a low solubility rate in the hot Devonian seas. There were no ice-cold polar waters to provide oxygen to the tropics by way of bottom sea currents. Tides were slightly more frequent and quite stronger than at present, creating murkier coastal waters, more tidal pools, and stranding great numbers of coastal fish in oxygen depleted water at regular intervals. (Lest we underestimate the role of tides in early vertebrate evolution, consider that the most direct pathway to the observed estivation of Dipnoi (lungfish) is first, through surviving daily tidal strandings, then surviving from spring tide to spring tide, and only then, evolving the ability to survive from rainy season to rainy season.) The fish with the highest mortality due to suffocation (except less than 100% of course) were those that evolved lungs, and this evidently occurred in fresh water, or water with a low salinity, but lungs provided Devonian fish with such an advantage that they quickly invaded and dominated the seas. Only a few inland species remain, but Devonian fish with lungs were the ancestors of all terrestrial vertebrates and most fish.
All the teleosts evolved from air breathing fish; the swim bladder evolved from the lung. The evolution of the lung was partly the result of hot water, but gills were effective cooling organs, and the replacement of gills with lungs left the bigger fish susceptible to overheating. The teleost retention of juvenile gills can be explained as a response to changing conditions: an adaptation to cooler waters; but such a target niche could only be exploited at the expense of a previously warmer physiology. While lungs evolved as a response to a warm habitat, the same lungs evolved into a swim bladder as a response to an abandonment of those warmer waters. The first stage of diminished dependence on lungs–that displayed by the holostenes–was adaptation toward a lower metabolic rate, and this must have been the result of competition with the other descendents of fish with lungs: aquatic reptiles and birds. Thus the holostene-teleost lineage presents a major example of metabolic high achievers (obligatory air-breathing fish) spinning off somewhat less active dropouts from the metabolic competition.
Lungfish still exhibit the voracious appetite of their Devonian ancestors; in fact they chew their food! This typically mammalian trait has probably continued without interruption from the lungfish down to the mammals. The sharks provide a still clearer picture of the appetite and metabolism, as well as the temperature requirements of some of the most primitive surviving jawed fish. It is no accident that we find the most dangerous man-eaters among the most primitive fish.
The first amphibians were more like crawling sharks than like frogs. The cardio-respiratory advances made by the ancestors of frogs and salamanders were made while they were still ferocious predators with supreme metabolic requirements. While the amphibian lineage on the top of the food chain evolved into reptiles, those at the bottom reverted to more docile, passive lifestyles, with progressively lower metabolic and aerobic requirements. All amphibians are able to breathe through their skin and internal mouth surface, which trait was acquired by a single lineage with a very low oxygen intake but which still retained lungs. Two points must be taken into consideration of the development of dermal respiration: the smaller the organism, and the lower its metabolic requirements, the more effective is the function. Dermal respiration is not so much a supplement to as a replacement for lung breathing. Accordingly, when neither gills nor lungs provide enough oxygen, if the organism is small and has low metabolic requirements, dermal respiration may become a significant factor in oxygen acquisition and survival, especially if predators are waiting for the little amphibians to surface. Skin breathing is of negligible advantage, on the other hand, for large, predatory amphibians, of the sort that provided the ancestral stock for reptiles. We are quite safe in assuming that the evolution of dry reptilian skin did not involve the sacrifice of dermal respiration, but rather involved the dessication of fish-like scales. By the same token, mammals did not derive their glandular skins from anything like reptilian or amphibian skin, but from the same moist fish-like scales from which the amphibians and reptiles derived their skins.
Mud-burrowing amphibians lost their lungs altogether and took to competing with earthworms. The adaptation to niches with short oxygen supply pre-adapted amphibians to enduring hypothermia and hibernation. At low temperatures metabolic rates are greatly diminished, hemoglobin ceases to release oxygen, and oxygen supplied by gas diffusion is sufficient to sustain life. But more to the point, amphibians provide the most striking and undeniable case of reverse metabolic evolution: like the teleosts, they abandoned a strict dependence on pulmonary respiration.
As the earlier quote of Bakker’s asserted, the ancestors of the crocodilians were agile predators which evolved bird-like digestive and cardio-respiratory systems. The most primitive reptiles had inherited the carnivorous niche once occupied by ferocious amphibians with which primitive high energy amphibians could not compete–only amphibians with low energy lifestyles could survive the age of reptiles. The evolution of the amniotic egg–an egg that could survive in the relative safety of dry land contributed greatly toward reproductive efficiency, but had no bearing on the adult reptiles’ dependence on water. This was a function of metabolism, and the higher the metabolic need, the more water was required for predator and prey alike. The fully terrestrial behavior exhibited by desert lizards was only made possible by a great reduction in food intake and energy expenditure, accompanied by highly efficient conservation of body fluids. This naturally entails a dry skin, with no chance of cooling by perspiration.
We have alluded vaguely to the evolving climatic conditions underlying vertebrate evolution, and of course, a detailed understanding of Mesozoic climates would be greatly desirable for purposes of discussing the evolution of homeothermy if such were available. Unfortunately a good deal of what is surmised is based on suppositions of vertebrate homeothermy; for example, the temperature of Cretaceous temperate zones inhabited by dinosaurs can best be determined by knowing whether such dinosaurs were warm or cold-blooded. Tertiary climates may be more accurately correlated to modern climatic zones by correlating fossil remains of pollen and the like to closely related surviving species. But to avoid interdependence between evolution and paleoclimatology we must base the latter solely on the geologic evidence, and a very brief summary of the conclusions based on that evidence is called for (Encyclopedia Britannica, 1985, v.16, p.528):
In the last 600,000,000 years the Earth’s climate, on a planetary scale, generally has been much warmer than it is today. At such times there are no ice caps near the poles, the polar seas are open, and there are no glaciers on even the highest mountain ranges. Instead, temperate conditions prevail beyond the Arctic Circle. This picture of a relatively warm, ice-free planet applies for perhaps 95 percent of the geological past. Ice caps are anomalous in this framework of reference, and their presence has indicated past and present ice ages. There were several of these…cold aberrations during the history of the Earth; the first two occurred about 570,000,000 and 280,000,000 years ago. The third began about 3,000,000 years ago, bringing on a sequence of cold and relatively warm spasms known as the Pleistocene Ice Age.
The Infra-Cambrian (c. 570,000,000 years ago), Permo-Carboniferous (c. 280,000,000 years ago), and Pleistocene (c. 3,000,000 years ago to the present) ice ages are exceptional in the geological history of the Earth. There is no evidence of any glacial phenomena between the mid-Permian and late Miocene (a span of 250,000,000 years), when mountain glaciers are first indicated in Alaska; similarly, glaciation was rare or absent from Early Cambrian to mid Carboniferous times (again, about 250,000,000 years). Glaciers are anomalous on Earth, even in polar latitudes.
The “normal” climate of geological times was comparatively warm, with few extremes of temperature. Polar latitudes were cool-temperate, with open seas, and a reduced albedo (index of reflection of radiation from the Earth’s surface) in the absence of snow or ice. Mid-latitudes were subtropical or warm-temperate, although the tropics do not appear to have been warmer than the modern equatorial zone. [p. 530]
Global climatic variation is no doubt a function of many factors, including the configuration of wandering continents and changing seas and ocean currents, the principal factor probably being the presence of mountain ranges, but probably one important factor is atmospheric variation, possibly including the fluctuating content of carbon dioxide and oxygen in the air, but more probably depending on a variable total atmospheric mass. The consensus is that there was no free oxygen in the atmosphere prior to two billion years ago, and that its introduction was brought about by the evolution of algae. The deposition of organic matter during the Carboniferous might indicate a lowering of atmospheric carbon dioxide and thus to a lower atmospheric density, which may well have contributed to the cooling of the Permian. The Tertiary cooling that led to the Pleistocene ice ages was certainly a gradual process, as proven by the fully climate adapted flora and fauna of the present age.
Till this point we have emphasized the supremacy of the high-energy vertebrates and the secondary derivative status of the low-energy offshoots, without specific reference to the temperature tolerances, i.e., the thermal behavior of either, the evolution of which is a function of the various lineages’ metabolic rates and other inherited traits and the climates in which they evolve. The question becomes then, as mammal-like reptiles or other high energy reptiles and their low-energy relatives found themselves confronted with a cooling Permian climate, how could their warm-blooded physiologies cope? The contrast is sharp between the strategies available to the two groups. Energy consumers could stoke the fire by increasing food intake, grow larger, or even evolve insulation. Energy conserving lineages had no such options, but relied on outside heat sources, evolving behavioral responses to optimize solar intake, and evolving a heat sensing organ that enabled them to locate the warmest places available with the least expenditure of energy.
The evolution of the pineal eye, the heat sensing organ that evidently evolved in the lineage ancestral to the snakes and lizards and the tuatara, and hence evolved early in the Permian, was the survival strategy of a reptile with a limited food supply in a cooling climate. In other vertebrates, including agnatha, the pineal gland is present, and its primary purpose has probably always been as a temperature sensing organ, but it is not at all apparent how this organ could evolve into a sensitive prey detecting device without having first evolved some useful intermediate function that aided the survival of early reptiles. Such an intermediate function would simply be an extension of the heat sensing function, albeit heat detection which gradually became more sensitive until it could detect heat sources from a distance. Such an organ is of particular value to a low energy tropotherm finding itself in a sometimes cool environment. Once fine tuned, this infrared detection could easily be transferred to detecting other warm-blooded reptiles, and once these evolved into ectotherms, to detecting the surviving warm-blooded vertebrates–mammals and birds. As mentioned, when the saurid and rhynchocephalian lineages diverged, the pineal eye (or at least, some fine-tuned infrared detector) was well developed, and whether it was used at that time for detecting suitable environmental temperatures or for detecting prey, its existence requires that either the heat seekers were tropotherms or that they hunted tropotherms.
More like those of birds and monotremes, and less like those of temperate amphibians, most reptilian eggs, in order to remain viable, cannot sustain cold temperatures. The notion that the long road to endothermy entailed first the evolution of eggs that required warmth (unlike the adult reptile forms), and then adults that required warm internal temperatures, highlights the absurdity of the view that obtains till the present, for there could hardly be imagined a more disadvantageous trait for a cold-blooded animal than to have eggs (which formerly required no special heat) evolve the necessity of special temperatures. Far more tenable is the notion that reptilian tropotherms evolved toward ectothermy at a faster pace than did their embryonic forms, where developmental rates of various tissues are precisely controlled and are highly temperature dependent. True enough, amphibians along with their eggs, having little selection of water temperatures available, did evolve eggs with the ability to survive variable temperatures, even suspending development when temperatures dropped below critical thresholds, but the notion that this was the primitive condition of reptilian stock flies in the face of the climatic evidence, and requires a leap of faith in the inherent survival advantage of eggs that must keep warm to remain viable. That is, one must postulate some advantage gained that required warm eggs when crossing the terrestrial threshold, so much so that the enormous disadvantage of evolving such vulnerable eggs became minor by comparison. The burden of proof lies therefore with any who defend the status quo.
So called “cold-blooded” vertebrates have been characterized by the trait of being slow growing, and of having no genetic mechanisms for arresting growth after reaching determined limits of size. According to the prevailing view such mechanisms were only necessitated after the evolution of rapid growth rates enabled by high metabolic rates enabled by efficient heart-lung systems. The fact is, some of the most primitive vertebrates, like lung fish, for example, have relatively rapid early growth rates as well as arrested growth rates once maximum size is attained, and we are justified in supposing that it is the starvation rations of typical ectotherms that limit their growth rates, and which over time have rendered their original growth limiting mechanisms first irrelevant, and then non-functional. In the world of natural selection, a slow growing vertebrate is likely to die of causes other than a mechanically unmanageable size. Others have noted that all the surviving orders of reptiles have reduced in size from the “age of reptiles” till the present. We may pertinently ask, why? Is it because their life spans have decreased (greater predation?), or their growth rates have decreased (were they more successful feeders anciently?), or because they really do have maximum size controlling mechanisms? (True, a part of this size reduction may be attributed to the disappearance of dinosaurs–constituting a reduction in size of both the reptiles’ predators and their prey–but the mere ability to respond to such an altered ecosystem presupposes existing growth control mechanisms.) If their growth rates have decreased it must have been because their metabolic rates have decreased as a result of their reduced food intake, so that in any case, the more primitive reptiles were more like birds and mammals in their physiological behavior. Typical ectothermic behavior is thus seen to be a response to competition over time with endotherms: the lower their diet requirements, the less directly they compete with endotherms. In other words, by diverting to lower metabolic rates, ectotherms avoid competition with endotherms. And progressive specialization in starvation diets would predict a decrease in size of ectotherms in the same way that restricted diets tend to reduce the size of endotherms–island stranded grazers, for example, in the case of pygmy elephants and rhinos.
Monotremes and marsupials operate on the average at temperatures several degrees lower than placentals, which fact dovetails with the prevailing view that mammalian physiology has steadily climbed in temperature from a primitive, cold-blooded, reptilian condition. But such a view again ignores the climatic evidence, presupposing that mammalian evolution occurred primarily in the temperate zones of Tertiary like climates, and that the reptilian stock ancestral to mammals had already become ectothermically adapted to a cool Permian climate. This view requires that tetrapods evolved from a hot, Carboniferous physiology to a heterothermic physiology in the Lower Permian, and to an endothermic physiology quickly enough during the Permian to allow for a survival advantage of fur before the evolution of marsupials and placentals. Unless, of course, we allow for McNab’s furry poikilotherms. A better explanation for the lower temperatures of monotremes and marsupials is to be had in recognizing the southern temperate geology of these primitive mammals. Their physiological behavior has come to terms with the climate of Gondwana, their trail leading through the present continents of South America, Antarctica, and Australia. Having the highest metabolic rates, the birds have most closely retained the tropothermic temperature, followed by the placental mammals, while marsupials have lowered their operating temperatures a little, and the monotremes have even evolved hibernation.
We have three salient criteria to deal with in tracing the thermal evolution of vertebrates: 1) their metabolic history, represented by a main stock of generally improving peak capacity which gave rise to various offshoots of diminishing metabolic rates; 2) the global climatic history which has placed periodic constraints and impetus on the physiological evolution of vertebrates; and 3) the various physiological and morphological responses of vertebrates to climatic variation as determined largely by their metabolic capacity. We must begin to separate the peak metabolic history of vertebrates, as exhibited principally by their respiratory capabilities, from their thermal histories, which are a function of their resting energy capacity, climate, and their temperature controlling ability. Having done so, we will recognize that bone growth patterns, however significant they may be in determining growth rates and the minimum metabolic rates necessary for sustaining those growth rates, are largely irrelevant to the question of the thermal behavior of the vertebrate in question. The peak metabolic capacity of a typical endotherm is generally tens of times greater than its resting rate, the rate germain to its potential growth rate. Peak metabolic rates comparable to the rest rates of hummingbirds were already to be found among Silurian and Devonian vertebrates, if we can take the sharks and lungfish as being typical of their first progenitors.
While it may be that surviving agnatha have a history of cold physiology spanning hundreds of millions of years, many ectotherms have evolved cold tolerant physiologies since the cretaceous, while they have maintained low energy physiologies since the Carboniferous in the case of surviving amphibians, and since the Permian in the case of surviving reptilian lineages. The ancestry of birds and mammals has been of steadily increasing peak metabolism since at least the Devonian, and of high temperature physiology since the Ordovician, but there is no compelling evidence for the assumption that resting metabolic rates have increased much in the ancestral stock of “warm-blooded” vertebrates since the Mesozoic.
The foregoing discussion automatically renders superfluous the controversy over whether any or all of the dinosaurs were warm-blooded, as this thesis upstages Bakker’s contention that the common ancestors of dinosaurs and crocodilians were already warm-blooded. In our view, ectotherms are exceptional, having evolved from high energy vertebrates, and having competed with each other for two hundred million years to see who could survive on the lowest rations. All dinosaurs were very high energy consumers, as required by the simple physics–the kinematics and thermodynamics of their size and skeletature, and their ability to evolve flight. (They even discuss the question of fur on Pterosaurs as though it were relevant to determining the metabolism of a flying creature in a warm climate!) Current notions of their being slow moving predators and fugitives are as untenable as the old notion that brontosaurus was a snorkeler. So for the mathematically competent paleontologists it came as no surprise that the first fossilized dinosaur heart discovered turned out to be bird-like rather than lizard-like: it was after all, fast-running dinosaurs that evolved the efficient air cooling system that the birds were able to make use of when evolving flight.
There is inherent in every species the capacity for evolving toward a higher or a lower metabolism in responding to the available food supply or numerous other factors. It is precisely for such a ubiquitous option that we may be confident that there have always been high energy vertebrates since long before the evolution of lungs, and that these have been followed by successively higher energy vertebrates till the extinction of dinosaurs. The Komodo Dragon gives us some slight indication of the general direction of upper metabolic evolution: without competition from already established high energy vertebrates even a low energy vertebrate (though high for a reptile) can become a stalking predator, dangerous to man and beast. The same tendency has been at work since the Ordovician, constantly providing lineages of high metabolism, as well as drop-outs with lower energy requirements.
To summarize our arguments for the continuity of high energy vertebrates, i.e., tropotherms, and for the contention that ectotherms have evolved secondarily, they are as follows:
1) Vertebrate improvements relating to metabolic capacity have been in progress since the Ordovician.
2) Some of the most primitive fish have some of the highest metabolic rates.
3) In the cases of Teleost and Amphibian evolution, the surviving lineages are of undeniably lower metabolic rates than their ancestors, Crocodilians are of almost certainly lower rates than their predecessors, and the other reptilian lineages are very probably of lower metabolic rates than their ancestors.
4) Inefficient locomotion (e.g., that of kangaroos) requires greater metabolic output than does more efficient locomotion (e.g., that of quadrupeds). Likewise, every other character that has at some time been taken as an indicator of incipient homeothermy can be better explained as an improvement toward more efficient homeothermy, e.g., homeotherms gain a greater survival advantage in evolving fur than do ectotherms.
5)There is always the potential in any species to evolve toward a higher metabolic rate, hence, high energy niches tend to filled, and that by already adapted high energy organisms.
6) Alteration of physiological operating temperature constitutes a formidable adaptive barrier.
7) Evolving improved temperature control and evolving different operating temperatures are mutually exclusive adaptations. Hence, it is simpler for a tropotherm than for an ectotherm to evolve endothermy.
8) Competition with endotherms and with other ectotherms generally drives ectotherms into progressively lower metabolic behavior.
9) The climate of most of the globe has been warm most of the time. Hence, tropotherms have always been available to fill high energy niches without altering their operating temperatures.
Arguments for the prevailing view of ectothermic primacy may be summarized as follows:
1) Ectotherms are of primitive skeletal anatomy; i.e., those living vertebrates with the lowest metabolic rates are those that have evolved least in the fossil record.
2) The morphological evolution of the higher vertebrates may be recapitulated with confidence through the classes of fishes, amphibians, and reptiles; i.e., the anatomy of modern ectotherms may be inferred to have been the anatomy of the ancestors of endotherms, as seen even in their embryonic development.
3) Peak metabolic rates have certainly improved over time, leading to those of modern birds and mammals.
4) There is some correlation between peak and resting metabolic rates.
5) Internal temperatures generally increase in conjunction with increased metabolic rates in the evolutionary ladder of vertebrate classes.
6) Recent studies have indicated that many ectotherms are incapable of breathing and running simultaneously, which if true, strongly suggests that this was the primitive condition of tetrapods.
7) There are no high energy “ectotherms” extant.
We answer these points as follows:
1) Once ectothermic behavior is acheived, evolutionary rates decrease due to decreased competition and lower reproductive rates.
2) The physiology of extinct lines–especially their resting metabolic rates–cannot be extrapolated from their morphology. Lungfish and sharks should be given no less weight than other ectotherms in reconstructing that physiology. The present condition of ectotherms is further illusory in that they have survived because of their decreasing metabolism while competing with those high energy tetrapods that evolved into dinosaurs, birds, and mammals.
3) Peak metabolic rates are of uncertain bearing on resting rates, which have been potentially sufficient for the temperature needs of vertebrates throughout reconstructed climatic conditions.
4) While some quantitative relationships have been established between maximum and minimum metabolic rates in anurans, these cannot be extrapolated with any confidence to extinct groups of obviously much higher maximum rates. That is, the ratio of maximum to minumum rates of tropotherms has certainly increased since the Devonian, e.g., between lungfish and hummingbirds.
5) The current distribution of thermal behavior across vertebrate classes can hardly be taken to represent the historical one in light of the climatic history of the globe, especially considering the short span of the Permian in which cold-blooded reptilians are supposed to have evolved.
6) Clearly, lungfish have no need of breathing while they swim rapidly, and it is conceivable that limbs evolved and a population of amphibians adapted to a low energy niche before evolving efficient terrestrial respiration. While anaerobic locomotion is not intrinsically incompatible with our thesis, considering the many marine mammals and even aquatic birds that engage in such activity, the hypothesis that the reptilian stock ancestral to birds, mammals, and lizards was unable to run and breathe simultaneously is hardly compatible with our hypothesis. Just as crocodiles are not likely to have evolved a four-chambered heart while exhibiting their modern behavior, neither were early tetrapods likely to have evolved a three-chambered heart while not capable of sustained locomotion.
Lizards are less limited by their cardiorespiratory potential than by their impoverishment of red blood cells, but the consequent shortage of oxygen carrying capacity is still adequate to the low dietary intake. The weak link, then, even in a lizard’s peak metabolic capacity is its food intake, not its respiratory capacity, since its heart and lungs had long since evolved a greater capability than it is presently able to make use of, as its ectothermy is only secondarily derived from a former high energy physiology. A lack of stamina in lizards has probably become an advantage–when forced to stay motionless at regular intervals lizards increase their abilitiy to escape detection, so that once faced with avian predation, saurids may well have encountered a situation where those lineages with the least aerobic capacity had the best chance of survival.
7) Considering the minimal advantage insulation provides tropical vertebrates, one might well ask, why have no high energy reptiles survived till the present. In fact this question is inconsequential in the wake of the overriding question, why did no dinosaurs survive the K/T catastrophe? Like modern mammals, modern reptiles have radiated to fill the vacuum left by the dinosaur extinction. Modern reptiles, in many forms, the cacti of the animal kingdom, returned from their desert diaspora to repopulate the tropics. All high energy reptiles disappeared with the end of the Cretaceous.
While no certainty can be obtained in reconstructing the metabolic history of vertebrates, the preponderance of arguments is on the side of the derivative status of ectothermy, rather than of endothermy, as has so long been taken for granted. Ectotherms are as likely to evolve into endotherms as ratites are likely to re-evolve flight. Like island-stranded featherless birds, ectotherms are physiologically stranded on a comparative evolutionary dead end.
No mention of coelecanths?