The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum

The evolution of endothermy in birds and mammals was one of the most important events in the evolution of the vertebrates. Past tests of hypotheses on the evolution of endothermy in mammals have relied largely on analyses of the relationship between basal and maximum metabolic rate, and artificial selection experiments. I argue that components of existing hypotheses, as well as new hypotheses, can be tested using an alternative macrophysiological modeling approach by examining the development of endothermy during the Cenozoic. Recent mammals display a 10°C range in body temperature which is sufficiently large to identify the selective forces that have driven the development of endothermy from a plesiomorphic (ancestral) Cretaceous or Jurassic condition. A model is presented (the Plesiomorphic‐Apomorphic Endothermy Model, PAE Model) which proposes that heterothermy, i.e. bouts of normothermy (constant body temperature) interspersed with adaptive heterothermy (e.g. daily torpor and/or hibernation), was the ancestral condition from which apomorphic (derived), rigid homeothermy evolved. All terrestrial mammal lineages are examined for existing data to test the model, as well as for missing data that could be used to test the model. With the exception of Scandentia and Dermoptera, about which little is known, all mammalian orders that include small‐sized mammals (<500 g), have species which are heterothermic and display characteristics of endothermy which fall somewhere along a plesiomorphic‐apomorphic continuum. Orders which do not have heterothermic representatives (Cetartiodactyla, Perissodactyla, Pholidota, and Lagomorpha) are comprised of medium‐ to large‐sized mammals that have either lost the capacity for heterothermy, or in which heterothermy has yet to be measured. Mammalian heterothermy seems to be plesiomorphic and probably evolved once in the mammalian lineage. Several categories of endothermy are identified (protoendothermy, plesioendothermy, apoendothermy, basoendothermy, mesoendothermy, supraendothermy, and reversed mesoendothermy) to describe the evolution of endothermy during the Cenozoic. The PAE Model should facilitate the testing of hypotheses using a range of macrophysiological methods (e.g. the comparative method and the reconstruction of ancestral states).     

Cool sperm: why some placental mammals have a scrotum

Throughout the Cenozoic, the fitness benefits of the scrotum in placental mammals presumably outweighed the fitness costs through damage, yet a definitive hypothesis for its evolution remains elusive. Here, I present an hypothesis (Endothermic Pulses Hypothesis) which argues that the evolution of the scrotum was driven by Cenozoic pulses in endothermy, that is, increases in normothermic body temperature, which occurred in Boreotheria (rodents, primates, lagomorphs, carnivores, bats, lipotyphylans and ungulates) in response to factors such as cursoriality and climate adaptation. The model argues that stabilizing selection maintained an optimum temperature for spermatogenesis and sperm storage throughout the Cenozoic at the lower plesiomorphic levels of body temperature that prevailed in ancestral mammals for at least 163 million years. Evolutionary stasis may have been driven by reduced rates of germ‐cell mutations at lower body temperatures. Following the extinction of the dinosaurs at the Cretaceous–Palaeogene boundary 65.5 mya, immediate pulses in endothermy occurred associated with the dramatic radiation of the modern placental mammal orders. The fitness advantages of an optimum temperature of spermatogenesis outweighed the potential costs of testes externalization and paved the way for the evolution of the scrotum. The scrotum evolved within several hundred thousand years of the K‐Pg extinction, probably associated initially with the evolution of cursoriality, and arguably facilitated mid‐ and late Cenozoic metabolic adaptations to factors such as climate, flight in bats and sociality in primates.     

Energetics, body size, and the limits to endothermy

The scaling rate of metabolism with respect to body mass is analysed. Scaling of heat production implies that scaling also exists between temperature regulation and body mass. Most vertebrates follow a Kleiber relation down to a "critical mass, below which the scaling of metabolism must be changed to ensure the maintenance of endothermy. Such an adjustment is found interspecifically in birds and mammals, and is found intraspecifically in mammals during post-natal growth. If the Kleiber scaling relation is maintained below the critical mass, mammals and birds shiR from endothermic temperature regulation (above critical mass) to endothermy with obligatory torpor (below critical mass). If the Kleiber relation is followed to masses far below the critical mass, ectothermy results. Critical mass varies inversely with the level of energy expenditure, which therefore accounts for the fact that most mammals and birds are endotherms and most reptiles and fish are ectotherms. The same relationship permits the facultative endothermy found in some insects and plants.
The scaling relations existing among rate of metabolism, endothermy, and body mass can be written as a modification of the Kleiber relation. This analysis suggests that any organism, irrespective of phylogenetic position, can be endothermic at any body size, if its rate of metabolism is high enough, or can be endothermic with any rate of metabolism, if it is large enough. Consequently, it is difficult to distinguish minimal endothermy from inertial homoiothermy in animals having a large mass. The boundary conditions for effective endothermy are similar to the relationship described between metabolism and mass in the evolution of endothermy through a decrease in mass in the phylogeny of mammals. Even though endothermy may evolve with an increase in mass, its perfection may always require an evolutionary decrease in mass.     

Permian–Triassic Osteichthyes (bony fishes): diversity dynamics and body size evolution

The Permian and Triassic were key time intervals in the history of life on Earth. Both periods are marked by a series of biotic crises including the most catastrophic of such events, the end‐Permian mass extinction, which eventually led to a major turnover from typical Palaeozoic faunas and floras to those that are emblematic for the Mesozoic and Cenozoic. Here we review patterns in Permian–Triassic bony fishes, a group whose evolutionary dynamics are understudied. Based on data from primary literature, we analyse changes in their taxonomic diversity and body size (as a proxy for trophic position) and explore their response to Permian–Triassic events. Diversity and body size are investigated separately for different groups of Osteichthyes (Dipnoi, Actinistia, ‘Palaeopterygii’, ‘Subholostei’, Holostei, Teleosteomorpha), within the marine and freshwater realms and on a global scale (total diversity) as well as across palaeolatitudinal belts. Diversity is also measured for different palaeogeographical provinces. Our results suggest a general trend from low osteichthyan diversity in the Permian to higher levels in the Triassic. Diversity dynamics in the Permian are marked by a decline in freshwater taxa during the Cisuralian. An extinction event during the end‐Guadalupian crisis is not evident from our data, but ‘palaeopterygians’ experienced a significant body size increase across the Guadalupian–Lopingian boundary and these fishes upheld their position as large, top predators from the Late Permian to the Late Triassic. Elevated turnover rates are documented at the Permian–Triassic boundary, and two distinct diversification events are noted in the wake of this biotic crisis, a first one during the Early Triassic (dipnoans, actinistians, ‘palaeopterygians’, ‘subholosteans’) and a second one during the Middle Triassic (‘subholosteans’, neopterygians). The origination of new, small taxa predominantly among these groups during the Middle Triassic event caused a significant reduction in osteichthyan body size. Neopterygii, the clade that encompasses the vast majority of extant fishes, underwent another diversification phase in the Late Triassic. The Triassic radiation of Osteichthyes, predominantly of Actinopterygii, which only occurred after severe extinctions among Chondrichthyes during the Middle–Late Permian, resulted in a profound change within global fish communities, from chondrichthyan‐rich faunas of the Permo‐Carboniferous to typical Mesozoic and Cenozoic associations dominated by actinopterygians. This turnover was not sudden but followed a stepwise pattern, with leaps during extinction events.     

Daily torpor and hibernation in birds and mammals

Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (～35°) than daily heterotherms (～25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ～13°C, and the mean minimum torpor metabolic rate was ～35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.     

Ontogeny and phylogeny of endothermy and torpor in mammals and birds

Endothermic thermoregulation in small, altricial mammals and birds develops at about one third to half of adult size. The small size and consequently high heat loss in these young should result in more pronounced energetic challenges than in adults. Thus, employing torpor (a controlled reduction of metabolic rate and body temperature) during development would allow them to save energy. Although torpor during development in endotherms is likely to occur in many species, it has been documented in only a few. In small, altricial birds (4 orders) and marsupials (1 order), which are poikilothermic at hatching/birth, the development of competent endothermic thermoregulation during cold exposure appears to be concurrent with the capability to display torpor (i.e. poikilothermy is followed by heterothermy), supporting the view that torpor is phylogenetically old and likely plesiomorphic. In contrast, in small, altricial placental mammals (2 orders), poikilothermy at birth is followed first by a homeothermic phase after endothermic thermoregulation is established; the ability to employ torpor develops later (i.e. poikilothermy-homeothermy-heterothermy). This suggests that in placentals torpor is a derived trait that evolved secondarily after a homeothermic phase in certain taxa perhaps as a response to energetic challenges. As mammals and birds arose from different reptilian lineages, endothermy likely evolved separately in the two classes, and given that the developmental sequence of torpor differs between marsupials and placentals, torpor seems to have evolved at least thrice.     

Hibernation and non-shivering thermogenesis in the Hottentot golden mole (<Emphasis Type="Italic">Amblysomus hottentottus longiceps</Emphasis>)

Although heterothermy (hibernation and torpor) is a common feature among mammals, there is debate over whether it is a derived or ancestral trait relative to endothermic homeothermy. Determination of the physiological characteristics of primitive mammals is central to understanding the evolution of endothermy. Moreover, evaluation of physiological mechanisms responsible for endothermic heat production [e.g. non-shivering thermogenesis (NST)] is key to understanding how early mammals responded to historical climate changes and colonised different geographical regions. Here we investigated the capacity for NST and heterothermy in the Hottentot golden mole, a basal eutherian mammal. NST was measured as the metabolic response to injections of noradrenalin and heterothermy by recording body temperature in free-ranging animals. We found that hibernation and torpor occurred and that the seasonal phenotypic adjustment of NST capacity was similar to that found in other placental mammals. Using phylogenetically independent contrasts, we compared measured values of NST with those obtained from the literature. This showed that all variation in NST was accounted for by differences in phylogeny and not zoogeography. These findings lend support to the observation that NST and heterothermy occur in the Afrotheria, the basal placental mammalian clade. Furthermore, this work suggests that heterothermy, rather than homeothermy is a plesiomorphic trait in mammals and supports the notion that NST mechanisms are phylogenetically ancient.     

Mitochondrial metabolism in hibernation and daily torpor: a review

Hibernation and daily torpor involve substantial decreases in body temperature and metabolic rate, allowing birds and mammals to cope with cold environments and/or limited food. Regulated suppression of mitochondrial metabolism probably contributes to energy savings: state 3 (phosphorylating) respiration is lower in liver mitochondria isolated from mammals in hibernation or daily torpor compared to normothermic controls, although data on state 4 (non-phosphorylating) respiration are equivocal. However, no suppression is seen in skeletal muscle, and there is little reliable data from other tissues. In both daily torpor and hibernation, liver state 3 substrate oxidation is suppressed, especially upstream of electron transport chain complex IV. In hibernation respiratory suppression is reversed quickly in arousal even when body temperature is very low, implying acute regulatory mechanisms, such as oxaloacetate inhibition of succinate dehydrogenase. Respiratory suppression depends on in vitro assay temperature (no suppression is evident below ~30 degrees C) and (at least in hibernation) dietary polyunsaturated fats, suggesting effects on inner mitochondrial membrane phospholipids. Proton leakiness of the inner mitochondrial membrane does not change in hibernation, but this also depends on dietary polyunsaturates. In contrast proton leak increases in daily torpor, perhaps limiting reactive oxygen species production.     

Air‐filled postcranial bones in theropod dinosaurs: physiological implications and the ‘reptile’–bird transition

Pneumatic (air‐filled) postcranial bones are unique to birds among extant tetrapods. Unambiguous skeletal correlates of postcranial pneumaticity first appeared in the Late Triassic (approximately 210 million years ago), when they evolved independently in several groups of bird‐line archosaurs (ornithodirans). These include the theropod dinosaurs (of which birds are extant representatives), the pterosaurs, and sauropodomorph dinosaurs. Postulated functions of skeletal pneumatisation include weight reduction in large‐bodied or flying taxa, and density reduction resulting in energetic savings during foraging and locomotion. However, the influence of these hypotheses on the early evolution of pneumaticity has not been studied in detail previously. We review recent work on the significance of pneumaticity for understanding the biology of extinct ornithodirans, and present detailed new data on the proportion of the skeleton that was pneumatised in 131 non‐avian theropods and Archaeopteryx. This includes all taxa known from significant postcranial remains. Pneumaticity of the cervical and anterior dorsal vertebrae occurred early in theropod evolution. This ‘common pattern’ was conserved on the line leading to birds, and is likely present in Archaeopteryx. Increases in skeletal pneumaticity occurred independently in as many as 12 lineages, highlighting a remarkably high number of parallel acquisitions of a bird‐like feature among non‐avian theropods. Using a quantitative comparative framework, we show that evolutionary increases in skeletal pneumaticity are significantly concentrated in lineages with large body size, suggesting that mass reduction in response to gravitational constraints at large body sizes influenced the early evolution of pneumaticity. However, the body size threshold for extensive pneumatisation is lower in theropod lineages more closely related to birds (maniraptorans). Thus, relaxation of the relationship between body size and pneumatisation preceded the origin of birds and cannot be explained as an adaptation for flight. We hypothesise that skeletal density modulation in small, non‐volant, maniraptorans resulted in energetic savings as part of a multi‐system response to increased metabolic demands. Acquisition of extensive postcranial pneumaticity in small‐bodied maniraptorans may indicate avian‐like high‐performance endothermy.     

The Origin and Early Radiation of Archosauriforms: Integrating the Skeletal and Footprint Record

We present a holistic approach to the study of early archosauriform evolution by integrating body and track records. The ichnological record supports a Late Permian–Early Triassic radiation of archosauriforms not well documented by skeletal material, and new footprints from the Upper Permian of the southern Alps (Italy) provide evidence for a diversity not yet sampled by body fossils. The integrative study of body fossil and footprint data supports the hypothesis that archosauriforms had already undergone substantial taxonomic diversification by the Late Permian and that by the Early Triassic archosauromorphs attained a broad geographical distribution over most parts of Pangea. Analysis of body size, as deduced from track size, suggests that archosauriform average body size did not change significantly from the Late Permian to the Early Triassic. A survey of facies yielding both skeletal and track record indicate an ecological preference for inland fluvial (lacustrine) environments for early archosauromorphs. Finally, although more data is needed, Late Permian chirotheriid imprints suggest a shift from sprawling to erect posture in archosauriforms before the end-Permian mass extinction event. We highlight the importance of approaching palaeobiological questions by using all available sources of data, specifically through integrating the body and track fossil record.     

Heterothermy in Afrotropical mammals and birds: a review

Recent years have seen a rapid increase in the number of Afrotropical endotherms known to avoid mismatches between energy supply and demand by using daily torpor and/or hibernation. Among mammals, heterothermy has been reported in 40 species in six orders, namely Macroscelidea, Afrosoricida, Rodentia, Eulipotyphla, Primates and Chiroptera. These species span a range in body mass of 7-770?g, with minimum heterothermic body temperatures ranging from 1-27°C and bout length varying from 1?h to 70 days. Daily torpor is the most common form of heterothermy, with true hibernation being observed in only seven species, Graphiurus murinus, Graphiurus ocularis, Atelerix frontalis, Cheirogaleus medius, Cheirogaleus major, Microcebus murinus and Microcebus griseorufus. The traditional distinction between daily torpor and hibernation is blurred in some species, with free-ranging individuals exhibiting bouts of > 24?h and body temperatures < 16 °C, but none of the classical behaviours associated with hibernation. Several species bask in the sun during rewarming. Among birds, heterothermy has been reported in 16 species in seven orders, and is more pronounced in phylogenetically older taxa. Both in mammals and birds, patterns of heterothermy can vary dramatically among species occurring at a particular site, and even among individuals of a single species. For instance, patterns of heterothermy among cheirogalid primates in western Madagascar vary from daily torpor to uninterrupted hibernation for up to seven months. Other examples of variation among closely-related species involve small owls, elephant shrews and vespertilionid bats. There may also be variation in terms of the ecological correlates of torpor within a species, as is the case in the Freckled Nightjar Caprimulgus tristigma.     

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.     

Temperature,metabolic power and the evolution of endothermy

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

A review of the energetics of pollination biology

Pollination biology is often associated with mutualistic interactions between plants and their animal pollen vectors, with energy rewards as the foundation for co-evolution. Energy is supplied as food (often nectar from flowers) or as heat (in sun-tracking or thermogenic plants). The requirements of pollinators for these resources depend on many factors, including the costs of living, locomotion, thermoregulation and behaviour, all of which are influenced by body size. These requirements are modified by the availability of energy offered by plants and environmental conditions. Endothermic insects, birds and bats are very effective, because they move faster and are more independent of environmental temperatures, than are ectothermic insects, but they are energetically costly for the plant. The body size of endothermic pollinators appears to be influenced by opposing requirements of the animals and plants. Large body size is advantageous for endotherms to retain heat. However, plants select for small body size of endotherms, as energy costs of larger size are not matched by increases in flight speed. If high energy costs of endothermy cannot be met, birds and mammals employ daily torpor, and large insects reduce the frequency of facultative endothermy. Energy uptake can be limited by the time required to absorb the energy or eliminate the excess water that comes with it. It can also be influenced by variations in climate that determine temperature and flowering season.     

Climatic drivers of latitudinal variation in Late Triassic tetrapod diversity

The latitudinal biodiversity gradient (LBG), the increase in biodiversity from the poles to the equator, is one of the most widely recognized global macroecological patterns, yet its deep time evolution and drivers remain uncertain. The Late Triassic (237–201 Ma), a critical interval for the early evolution and radiation of modern tetrapod groups (e.g. crocodylomorphs, dinosaurs, mammaliamorphs), offers a unique opportunity to explore the palaeolatitudinal patterns of tetrapod diversity since it is extensively sampled spatially when compared with other pre‐Cenozoic intervals, particularly at lower palaeolatitudes. Here, we explore palaeolatitudinal patterns of Late Triassic tetrapod diversity by applying sampling standardization to comprehensive occurrence data from the Paleobiology Database (PBDB). We then use palaeoclimatic model simulations to explore the palaeoclimatic ranges occupied by major tetrapod groups, allowing insight into the influence of palaeoclimate on the palaeolatitudinal distribution of these groups. Our results show that Late Triassic tetrapods generally do not conform to a modern‐type LBG; instead, sampling‐standardized species richness is highest at mid‐palaeolatitudes. In contrast, the richness of pseudosuchians (crocodylians and their relatives) is highest at the palaeoequator, a pattern that is retained throughout their subsequent evolutionary history. Pseudosuchians generally occupied a more restricted range of palaeoclimatic conditions than other tetrapod groups, a condition analogous to modern day reptilian ectotherms, while avemetatarsalians (the archosaur group containing dinosaurs and pterosaurs) exhibit comparatively wider ranges, which is more similar to modern endotherms, such as birds and mammals, suggesting important implications for the evolution of thermal physiology in dinosaurs.     

Simplification as a trend in synapsid cranial evolution

The prevalence and meaning of morphological trends in the fossil record have undergone renewed scrutiny in recent years. Studies have typically focused on trends in body size evolution, which have yielded conflicting results, and have only rarely addressed the question as to whether other morphological characteristics show persistent directionality over long time scales. I investigated reduction in number of skull and lower jaw bones (through loss or fusion) over approximately 150 million years of premammalian synapsid history. The results of a new skull simplification metric (SSM), which is defined as a function of the number of distinct elements, show that pronounced simplification is evident on both temporal (i.e., stratigraphic) and phylogenetic scales. Postcranial evolution exhibits a similar pattern. Skull size, in contrast, bears little relationship with the number of distinct skull bones present. Synapsid skulls carried close to their observed maximum number of elements for most of the Late Carboniferous and Early Permian. The SSM decreased in the Late Permian but, coincident with the radiation of early therapsids, the range of observed SSM values widened during this interval. From derived nonmammalian cynodonts in the Early Triassic through the earliest mammals in the Early Jurassic, both the minimum and maximum SSM decreased. Data from three representative modern mammals (platypus, opossum, and human) suggest that this trend continues through the Cenozoic. In a phylogenetic context, the number of skull elements present in a taxon shows a significant negative relationship with the number of branching events passed from the root of the tree; more deeply embedded taxa have smaller SSM scores. This relationship holds for various synapsid subgroups as well. Although commonly ascribed to the effects of long-term selection, evolutionary trends can alternatively reflect an underlying intrinsic bias in morphological change. In the case of synapsid skull bones (and those of some other tetrapods lineages), the rare production of novel, or neomorphic, elements may have contributed to the observed trend toward skeletal simplification.     

Controls on body size during the Late Permian mass extinction event

This study examines the morphological responses of Late Permian brachiopods to environmental changes. Quantitative analysis of body size data from Permian–Triassic brachiopods has demonstrated significant, directional changes in body size before, during and after the Late Permian mass extinction event. Brachiopod size significantly reduced before and during the extinction interval, increased for a short time in more extinction‐resistant taxa in the latter stages of extinction and then dramatically reduced again across the Permian/Triassic boundary. Relative abundances of trace elements and acritarchs demonstrate that the body size reductions which happened before, during and after extinction were driven by primary productivity collapse, whereas declining oxygen levels had less effect. An episode of size increase in two of the more extinction‐resistant brachiopod species is unrelated to environmental change and possibly was the result of reduced interspecific competition for resources following the extinction of competitors. Based on the results of this study, predictions can be made for the possible responses of modern benthos to present‐day environmental changes.     

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.     

TURBINATES IN THERAPSIDS: EVIDENCE FOR LATE PERMIAN ORIGINS OF MAMMALIAN ENDOTHERMY

The structure and function of the nasal conchae of extant reptiles, birds, and mammals are reviewed, and the relationships to endothermy of the mammalian elements are examined. Reptilian conchae are relatively simple, recurved structures, which bear primarily sensory (olfactory) epithelium. Conversely, the conchae, or turbinates, of birds and mammals are considerably more extensive and complex, and bear, in addition, nonsensory (respiratory) epithelium. Of the mammalian turbinates, only the exclusively respiratory maxilloturbinal has a clear functional relationship with endothermy, as it reduces desiccation associated with rapid and continuous pulmonary ventilation. The other mammalian turbinates principally retain the primitive, olfactory function of the nasal conchae. The maxilloturbinates are the first reliable morphological indicator of endothermy that can be used in the fossil record. In fossil mammals and mammallike reptiles, the presence and function of turbinates are most readily revealed by the ridges by which they attach to the walls of the nasal cavity. Ridges for olfactory turbinals are located posterodorsally, away from the main flow of respiratory air, whereas those of the respiratory maxilloturbinals are situated in the anterolateral portion of the nasal passage, directly in the path of respired air. The maxilloturbinal is also characterized by its proximity to the opening of the nasolacrimal canal. Posterodorsal ridges, for olfactory turbinals, have long been recognized in many mammallike reptiles, including early forms such as pelycosaurs. However, ridges for respiratory turbinals have not been identified previously in this group. In this paper, the presence of anterolateral ridges, which most likely supported respiratory turbinals, is reported in the primitive therocephalian Glanosuchus and in several cynodonts. The presence of respiratory turbinals in these advanced mammallike reptiles suggests that the evolution of “mammalian” oxygen consumption rates may have begun as early as the Late Permian and developed in parallel in therocephalians and cynodonts. Full mammalian endothermy may have taken as much as 40 to 50 million yr to develop.     

The “minimal boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review

According to the concept of the “minimal boundary curve for endothermy”, mammals and birds with a basal metabolic rate (BMR) that falls below the curve are obligate heterotherms and must enter torpor. We examined the reliability of the boundary curve (on a double log plot transformed to a line) for predicting torpor as a function of body mass and BMR for birds and several groups of mammals. The boundary line correctly predicted heterothermy in 87.5% of marsupials (n = 64), 94% of bats (n = 85) and 82.3% of rodents (n = 157). Our analysis shows that the boundary line is not a reliable predictor for use of torpor. A discriminate analysis using body mass and BMR had a similar predictive power as the boundary line. However, there are sufficient exceptions to both methods of analysis to suggest that the relationship between body mass, BMR and heterothermy is not a causal one. Some homeothermic birds (e.g. silvereyes) and rodents (e.g. hopping mice) fall below the boundary line, and there are many examples of heterothermic species that fall above the boundary line. For marsupials and bats, but not for rodents, there was a highly significant phylogenetic pattern for heterothermy, suggesting that taxonomic affiliation is the biggest determinant of heterothermy for these mammalian groups. For rodents, heterothermic species had lower BMRs than homeothermic species. Low BMR and use of torpor both contribute to reducing energy expenditure and both physiological traits appear to be a response to the same selective pressure of fluctuating food supply, increasing fitness in endothermic species that are constrained by limited energy availability. Both the minimal boundary line and discriminate analysis were of little value for predicting the use of daily torpor or hibernation in heterotherms, presumably as both daily torpor and hibernation are precisely controlled processes, not an inability to thermoregulate.