Evolution Of Endothermy Research Articles

Thermoregulation in monotremes: riddles in a mosaic

The three extant genera of the Monotremata have evolved, probably from a pre-Cretaceous Gondwanan origin, independently of the Theria to display a variety of ancestral and derived features. A comparison of their thermoregulation reveals a diversity of physiology that might represent both plesiomorphic and apomorphic elements within this mosaic. In the tachyglossids, the echidnas Tachyglossus and Zaglossus, body temperature is often labile, rising as a result of activity and allowed to decline during inactivity. This daily heterothermy, which is not necessarily torpor, may combine with typical mammalian hibernation to provide substantial energy economy in a wide variety of often unproductive habitats. Only when incubating do free-ranging echidnas display classic mammalian thermoregulation, the facultative nature of which suggests echidna-like physiology as an example of a protoendothermic stage in the evolution of endothermy. Similarly, physiological response to heat in Tachyglossus, at least, may be plesiomorphic, relying on the cyclic loss of heat stored during activity. Tachyglossids neither exhibit a panting response nor spread saliva to facilitate evaporative cooling and Tachyglossus, though not Zaglossus, lacks functional sweat glands. By contrast, the only extant ornithorhynchid, the platypus Ornithorhynchus, does not utilise heterothermy of any kind and maintains its body temperature more tightly than several semiaquatic eutherians. Although not necessarily required, it responds to heat via sweating, but not panting or saliva spreading. The classic nature of ornithorhynchid thermoregulation stands in marked contrast to the more diverse thermoregulatory responses shown by the tachyglossids, making it difficult to determine which aspects of monotreme thermoregulation are plesiomorphic and which are apomorphic.

Reptile scale paradigm: Evo-Devo, pattern formation and regeneration.

The purpose of this perspective is to highlight the merit of the reptile integument as an experimental model. Reptiles represent the first amniotes. From stem reptiles, extant reptiles, birds and mammals have evolved. Mammal hairs and feathers evolved from Therapsid and Sauropsid reptiles, respectively. The early reptilian integument had to adapt to the challenges of terrestrial life, developing a multi-layered stratum corneum capable of barrier function and ultraviolet protection. For better mechanical protection, diverse reptilian scale types have evolved. The evolution of endothermy has driven the convergent evolution of hair and feather follicles: both form multiple localized growth units with stem cells and transient amplifying cells protected in the proximal follicle. This topological arrangement allows them to elongate, molt and regenerate without structural constraints. Another unique feature of reptile skin is the exquisite arrangement of scales and pigment patterns, making them testable models for mechanisms of pattern formation. Since they face the constant threat of damage on land, different strategies were developed to accommodate skin homeostasis and regeneration. Temporally, they can be under continuous renewal or sloughing cycles. Spatially, they can be diffuse or form discrete localized growth units (follicles). To understand how gene regulatory networks evolved to produce increasingly complex ectodermal organs, we have to study how prototypic scale-forming pathways in reptiles are modulated to produce appendage novelties. Despite the fact that there are numerous studies of reptile scales, molecular analyses have lagged behind. Here, we underscore how further development of this novel experimental model will be valuable in filling the gaps of our understanding of the Evo-Devo of amniote integuments.

Stoichiometry of endothermy: shifting the quest from nitrogen to carbon

For many animals, notably herbivores, plants are often an inadequate food source given the low content of protein and high content of C-rich material. This conception is mainly based on studies on ectotherms. The validity of this conception for endotherms is unclear given their much higher carbon requirements for maintenance energy metabolism than ectotherms. Applying stoichiometric principles, we hypothesized that endotherms can cope with diets with much higher (metabolizable) carbon to nitrogen ratios than ectotherms. Using empirical data on birds, eutherian mammals, marsupials and reptiles, we compiled and compared measurements and allometric equations for energy metabolism as well as nitrogen requirements. Our analysis supports our hypothesis that plants, and especially their leaves, are generally sufficiently rich in nitrogen to fulfil protein demands in endotherms, at least during maintenance conditions, but less so in ectotherms. This has important implications with respect to community functioning and the evolution of endothermy.

Torpor and hibernation in a basal placental mammal, the Lesser Hedgehog Tenrec Echinops telfairi

The patterns of heterothermy were measured in Lesser Hedgehog Tenrecs, Echinops telfairi, under semi-natural conditions in an outdoor enclosure during the austral mid-winter in southwestern Madagascar. The animals were implanted with miniaturized body temperature (Tb) loggers (iButtons) that measured body temperature every 42 min for 2 months (May and June). The tenrecs entered daily torpor on all 60 consecutive days of measurement, that is, on 100% of animal days, with body temperature closely tracking ambient temperature (Ta) during the ambient heating phase. The mean minimum daily Tb of the tenrecs was 18.44 +/- 0.50 degrees C (n = 174, N = 3), and never exceeded 25 degrees C whereas, apart from a few hibernation bouts in one animal, the mean maximum daily Tb was 30.73 +/- 0.15 degrees C (n = 167, N = 3). Thus during winter, tenrecs display the lowest normothermic Tb of all placental mammals. E. telfairi showed afternoon and early evening arousals, but entered torpor before midnight and remained in torpor for 12-18 h each day. One animal hibernated on two occasions for periods of 2-4 days. We consider E. telfairi to be a protoendotherm, and discuss the relevance and potential of these data for testing models on the evolution of endothermy.

4.P1. Genetic correlation between metabolic rate and food consumption in the bank vole: Consequence for evolution of endothermy

4.P1. Genetic correlation between metabolic rate and food consumption in the bank vole: Consequence for evolution of endothermy

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

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

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

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

Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus

The evolution of endothermy is thought to have been facilitated by the advent of endothermic energy sources such as brown adipose tissue (BAT), the principal site of non-shivering thermogenesis (NST). In marsupials, heat is primarily produced through shivering and NST in skeletal muscle because BAT is either absent or appears to be non-functional. The most basal group of the eutherian lineage are the Afrotheria. Rock elephant shrews, Elephantulus myurus are amongst the smallest members of the Afrotheria and are also known to use exogenous passive heating. The aim of this study was to determine whether the reliance on passive heating compromised the capacity for thermogenesis in E. myurus. We measured the thermogenic response to noradrenalin (NA) injection in E. myurus acclimated to short photoperiod. The thermogenic response at 25 degrees C was 1.58 ml O(2) g(-1) h(-1). We used phylogenetically independent analyses to establish how this thermogenic response compared to other eutherians that display classical NST. The thermogenic response of E. myurus was not significantly different from phylogenetically independent allometric predictions. However, it is unclear whether this thermogenic response is indicative of classical NST and molecular data are required to verify the presence of BAT and UCPs in elephant shrews.

Generating Heat: New Twists in the Evolution of Endothermy

Generating Heat: New Twists in the Evolution of Endothermy

The Evolution of Endothermy and Its Diversity in Mammals and Birds

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

The Evolution of Endothermy: Role for Membranes and Molecular Activity

On the basis of the comparative approach and three models of metabolism (endothermic and ectothermic vertebrates, body mass, and mammalian development), we suggest that a few common cellular processes, linked either directly or indirectly to membranes, consume the majority of energy used by most organisms; that membranes act as pacemakers of metabolism through changes in lipid composition, altering membrane characteristics and the working environment of membrane proteins--specifically, that changes in the membrane environment similarly affect the molecular activities (specific rates of activity) of membrane-bound proteins; and that polyunsaturation of membranes increases whereas monounsaturation decreases the activity of membrane proteins. Experiments designed to test this theory using the sodium pump support this supposition. Potential mechanisms considered include fluidity, electrical fields, and related surface area requirements of lipids. In considering the evolution of endothermy in mammals, for example, if the first mammals were small, possibly nocturnal and active organisms, all these factors would favour increased polyunsaturation of membranes. Such changes (from monounsaturated to polyunsaturated membranes) would allow membranes to set the pace of metabolism in the evolution of endothermy.

The Evolution of Concepts on the Evolution of Endothermy in Birds and Mammals

Warm-blooded animals, mammals and birds, are unique not because they are endothermic in the strict sense of the term but because they use an extravagant economy: they have high energy budgets and spend a large part of their energy resources on basic maintenance. Although several advantages of endothermy are easy to indicate, mechanisms behind evolution of such a wasteful life strategy remain unclear and have been subject to intensive debate. For two decades, the aerobic capacity model has been widely recognized as a promising hypothesis and has catalyzed a new direction in ecological and evolutionary physiology--the study of correlated evolution of behavioral and morphophysiological traits. Recently, two alternative models have been proposed, both of which see evolution of high metabolic rates in birds and mammals as an element in evolution of intensive parental care. Unlike previous models, which treated individuals as static objects of fixed properties, the parental care models explicitly incorporate life histories into a evolutionary-physiology research program. The aim of this article was to outline the process of evolution of major concepts in the field, which reflects development of the paradigm of modern evolutionary physiology.

The Evolution of Endothermy in Terrestrial Vertebrates: Who? When? Why?

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

The maximum metabolizable energy intake and the relationship with basal metabolic rate in the striped hamsterCricetulus barabensis

The maximum metabolizable energy intake (MEImax) of striped hamsterCricetulus barabensis (Pallas, 1773) was determined in gradually lowering temperature. The MEImax was gained at 0 C, 3.6 ± 0.1 kJ/(g × d) or 121.9 ± 4.9 kJ/d, which is 2.8 times the basal metabolic rate (BMR). This suggests that the actual energy budgets of striped hamsters in natural environment will keep near the upper physiological limit. As the temperature decreased, both metabolizable energy intake (MEI) and BMR increased though there was no significant correlation between the MEI and BMR or between the MEImax and BMR. However, the significant correlation between MEImax and BMR was found in nine species of rodents. Our results support the assimilation capacity model of the origin and evolution of endothermy at the interspecific level.

The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology ofAllothunnus fallai

Two significant functional differences—a more anterior and internally positioned red myoÍtomal muscle mass and modification of the red-muscle vascular supply to form counter-current heat exchangers—distinguish the tunas (tribe Thunnini) from other species in the teleost family Scombridae. Neither of these characteristics is found in the bonitos (tribe Sardini), the sister group to the Thunnini. The most recent scombrid classification places the slender tuna, Allothunnus fallai, in the tribe Sardini, but some earlier studies suggested that this species should be a member of the Thunnini. Allothunnus fallai does not possess the lateral subcutaneous arteries and veins or the lateral heat-exchanging retia typical of tunas. However, we have found that this species has a highly modified central circulation (dorsal aorta, post cardinal vein, and associated branch vessels) similar to the central heat-exchanging retia of certain tunas, an enlarged haemal arch to accommodate this structure, and the anterior, internal placement of red muscle characteristic of tunas. With these new characters, phylogenetic reconstructions based on parsimony place A. fallai as the sister taxon to the tunas, establish that it is the most basal tuna species, and support the hypothesis that the derivation of tunas from a bonito-like ancestor occurred through selection for an integrated set of characteristics affecting locomotion and endothermy. The major features of this hypothesis are as follows. (1) Selection for continuous, steady, and efficient swimming resulted in changes in body shape (the result of enlargement of the anterior myotomes, the anterior and internal shift of red muscle, and a narrowing of the caudal peduncle) which increased streamlining and led to the adoption of the thunniform swimming mode unique to the tunas. (2) Alterations in blood supply necessitated by the anterior shift in red muscle led to the interdigitation of numerous arterial and venous branches which set the stage for heat conservation. (3) The evolution of endothermy, together with thunniform swimming, contributed significantly to the ecological radiation and diversification of tunas during the Early Tertiary Period. Our studies of A. fallai thus suggest that the shift in red muscle position and changes in central circulation preceded the evolution of red-muscle endothermy. Co-evolutionary changes in red muscle quantity and distribution and in vascular specializations for heat conservation have led to different macroevolutionary trajectories among the now five genera and 14 tuna species of tunas and appear to reflect the influence of changing paleocological and paleoceanographic conditions, including cooling, that occurred in the Tertiary.

The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai

Two significant functional differences—a more anterior and internally positioned red myoItomal muscle mass and modification of the red-muscle vascular supply to form counter-current heat exchangers—distinguish the tunas (tribe Thunnini) from other species in the teleost family Scombridae. Neither of these characteristics is found in the bonitos (tribe Sardini), the sister group to the Thunnini. The most recent scombrid classification places the slender tuna, Allothunnus fallai, in the tribe Sardini, but some earlier studies suggested that this species should be a member of the Thunnini. Allothunnus fallai does not possess the lateral subcutaneous arteries and veins or the lateral heat-exchanging retia typical of tunas. However, we have found that this species has a highly modified central circulation (dorsal aorta, post cardinal vein, and associated branch vessels) similar to the central heat-exchanging retia of certain tunas, an enlarged haemal arch to accommodate this structure, and the anterior, internal placement of red muscle characteristic of tunas. With these new characters, phylogenetic reconstructions based on parsimony place A. fallai as the sister taxon to the tunas, establish that it is the most basal tuna species, and support the hypothesis that the derivation of tunas from a bonito-like ancestor occurred through selection for an integrated set of characteristics affecting locomotion and endothermy. The major features of this hypothesis are as follows. (1) Selection for continuous, steady, and efficient swimming resulted in changes in body shape (the result of enlargement of the anterior myotomes, the anterior and internal shift of red muscle, and a narrowing of the caudal peduncle) which increased streamlining and led to the adoption of the thunniform swimming mode unique to the tunas. (2) Alterations in blood supply necessitated by the anterior shift in red muscle led to the interdigitation of numerous arterial and venous branches which set the stage for heat conservation. (3) The evolution of endothermy, together with thunniform swimming, contributed significantly to the ecological radiation and diversification of tunas during the Early Tertiary Period. Our studies of A. fallai thus suggest that the shift in red muscle position and changes in central circulation preceded the evolution of red-muscle endothermy. Co-evolutionary changes in red muscle quantity and distribution and in vascular specializations for heat conservation have led to different macroevolutionary trajectories among the now five genera and 14 tuna species of tunas and appear to reflect the influence of changing paleocological and paleoceanographic conditions, including cooling, that occurred in the Tertiary.

Evolution of the Cholecystokinin and Gastrin Peptides and Receptors1

The intestinal hormone, cholecystokinin (CCK), and the stomach hormone, gastrin, form a simple two member family of peptides with much to offer students of hormone and receptor evolution. They share a common carboxyl-terminal tetrapeptide sequence, which is the bioactive site of each peptide and is also antigenic, making heterologous biological and immunological assays feasible. Current evidence indicates that CCK evolved in chordate ancestors and that gastrin-like peptides that separately regulate stomach functions evolved from an ancestral CCK at the level of the divergence of tetrapods from fish. This tentative conclusion may require modification when the two separate CCK- and gastrin-like peptides recently identified in the dogfish shark are characterized further. The CCK-X receptor appears to be ancestral to the CCK-A and CCK-B receptors identified in amniotes. The evolution of gastrin and of CCK-A and -B receptors may have played roles in the evolution of the stomach and the evolution of endothermy in vertebrate phylogeny.

Evolution of the Cholecystokinin and Gastrin Peptides and Receptors

The intestinal hormone, cholecystokinin (CCK), and the stomach hormone, gastrin, form a simple two member family of peptides with much to offer students of hormone and receptor evolution. They share a common carboxyl-terminal tetrapeptide sequence, which is the bioactive site of each peptide and is also antigenic, making heterologous biological and immunological assays feasible. Current evidence indicates that CCK evolved in chordate ancestors and that gastrin-like peptides that separately regulate stomach functions evolved from an ancestral CCK at the level of the divergence of tetrapods from fish. This tentative conclusion may require modification when the two separate CCK- and gastrin-like peptides recently identified in the dogfish shark are characterized further. The CCK-X receptor appears to be ancestral to the CCK-A and CCK-B receptors identified in amniotes. The evolution of gastrin and of CCK-A and -B receptors may have played roles in the evolution of the stomach and the evolution of endothermy in vertebrate phylogeny.

Energy assimilation, parental care and the evolution of endothermy.

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

Mechanisms underlying the cost of living in animals.

The cost of living can be measured as an animal's metabolic rate. Basal metabolic rate (BMR) is factorially related to other metabolic rates. Analysis of BMR variation suggests that metabolism is a series of linked processes varying in unison. Membrane processes, such as maintenance of ion gradients, are important costs and components of BMR. Membrane bilayers in metabolically active systems are more polyunsaturated and less monounsaturated than metabolically less-active systems. Such polyunsaturated membranes have been proposed to result in an increased molecular activity of membrane proteins, and in this manner the amount of membrane and its composition can act as a pacemaker for metabolism. The potential importance of membrane acyl composition in metabolic depression, hormonal control of metabolism, the evolution of endothermy, as well as its implications for lifespan and human health, are briefly discussed.