Fossill Record
The table below lists various environment changes and evolutionary innovations that may be relevant to endohermy/homeothermy and/or the 7cv constraint. These innovations are grouped according to the geologic era in which they likely first arose in the mammalian lineage, and also by the type of change; changes in degree of parental care (indicated by P), in ability to elevate internal temperature (endothermy, T+), reduce temperature (torpor, T-), or maintain a more constant temperature (homeothermy, H), changes in respiratory capacity (R+ or R-), changes in neck structure (N),changes in body size(S), changes in mobility (M), changes in development, including novel organs(D), changes that required increased energy utilization (E),and other changes in behavior (B). Included are innovations in the mammalian lineage involving soft tissues or behavior which, of course, did not leave any fossilized material. Many of these innovations have been discussed in Lovegrove (2019), and the chapter or page numbers are given.
Time(mya) Era Inovation/event Type References
350 Carboniferous Elevated posture and gait D,E Lovegrove(p25)
Amniotic egg D Lovegrove(ch2), Packard(1997)
Metanephric kidney D
Keratin scales D Lovegrove(p35)
300 Early Permian Thoracic heart/lung D,R+ Hirasawa(2016)
Longer egg retention B Lauren (2005)
Increased size T+ Lovegrove(ch2)
Whiskers D
Reduced cervical ribs N, M
265 Late Permian Permian warming begins Lovegrove (ch4)
Fewer plants
Decreasing oxygen
Burrowing Botha-Brink(2017)
Rapid growth, early breeding Botha-Brink(2016)
252 Triassic P/T extinction
250 Temperature begins falling
Bony secondary palate R+ Lovegrove(p31)
Rise of reptiles Lovegrove(ch5)
Decreased size T-,E Huttenlocker(2013), Lovegrove (p60)
Nocturnal lifestyle B Lovegrove(p122)
Neocortex D Lovegrove(p131)
Loss of lumbar ribs R+
Diaphragm D.R Buchholtz (2012)
Initial 7CV constraint N Arnold
Primitive torpor T- Lovegrove(p63),Fernandez(2013)
Decreased RBC size R+ Huttenlocker(2016), Lovergrove(p56)
Heart septation R+ Poelmann (2014)
Disappearance of parietal R+ Lovegrove(p123)
foramen
Whiskers D Tooth differentiation/occlusion
advanced torpor T-
Nasal turbinates T+ Lovegrove(p89), Laass(2011)
200 Jurassic Maternal Nutrition D,E Farmer(2000)
Live birth D
Fur D,T+
Scrotum D Lovegrove(2014)
66 C/C extinction
The first amphibians (350 mya) were poorly adapted to life on land. They had moist skin that led to rapid water loss. They dragged their bodies on the ground. Their limbs extended to the side rather than downward to support their weight, and their hands and feet pointed in the wrong direction to give them much forward thrust. The bones of the limbs had no connection the vertebral column, which was not adapted to support the torso between the front and rear limbs. The undifferentiated vertebrae were not adapted for supporting the torso between the front and hind limbs. They did not have the respiratory capacity required for rapid movement on land. They had to return to the water to lay their eggs.
Innovations to address many of these deficiencies would likely require greater rates of energy generation and respiration. Animals obtain energy by breaking down (food) molecules into smaller pieces. Since chemical reactions generally increase with higher temperature, energy could be generated at a higher rate if a higher internal temperature could be reached. Early amphibians did have a way of increasing their body temperature not available to purely aquatic animals, directly exposing their bodies to the rays of the sun. But this ran the risk of drying out their moist skin.
A substantial fraction of amphibian respiration (intake of oxygen and discharge of carbon dioxide) occurs through their skin (cutaneous respiration). Some amphibians, such as the Titicaca water frog, have folds in their skin which allows more respiration by this route. However, any further increase in respiration would be limited; extensive folds of thin skin would hinder movement and invite injury and hinder respiration by limiting air flow across the skin surface.
Early amphibians may have respired through primitive lungs. However, ventilation of the respiratory surfaces was likely limited, perhaps provided by up and down movement of the floor of the mouth (buccal breathing) as in frogs.
Animals produce ammonia during the metabolism of amino acids and nucleic acids. Ammonia is highly toxic because it raises the pH. Fully aquatic organisms easily excrete ammonia through their gills. This was not available to the air-breathing stages of amphibians, who evolved the conversion of ammonia to urea, which is less toxic, and excretion through mesonephric kidneys. These processes require energy and result in water loss.
The three orders of amphibians that are extant (alive today), frogs, salamanders, and the limbless caecilians, first arose about 250 mya and represent refinement of the amphibian “lifestyle”. The lineage that evolved a suite of innovations that allowed a fully terrestrial environment to be inhabited was that of the Reptiliomorpha. One innovation was the metanephric kidney, which saved water by concentrating urea in the urine.
Predation by fishes of their aquatic eggs and larval forms limited amphibians. The evolution of the amniotic egg allowed a fully terrestrial lifestyle. Among the required innovations were internal fertilization and laying an egg with an impermeable shell to prevent dehydration before hatching, which dispensed with the larval stage. But the shell resulted in a new problem. excretion of urea would be a problem. This was solved by the evolution of excretion of uric acid into a membranous bag (the allantois). Uric acid is non-toxic and precipitates at a low concentration, so can be excreted as a paste with little water loss. Reptiles and birds excrete uric after hatching, so are particularly suited to arid regions.
Reptilomorphs also had several skeletal innovations that improved their ability to move on land. Their limbs were more directly underneath their torsos, rather than off to their sides in the early amphibians. The limb bones also made more direct connections to the rest of the skeleton than earlier amphibians.
The fossil record does reveal that early Reptilomorphs had scales. Scales slowed water loss, protected the skin, and were elaborated into claws. However, because of the scales, cutaneous respiration would have been reduced, and they would have been more dependent on lung respiration. This limitation had potential benefits. With internal respiration the respiratory surface area could increase, the distance between the respiratory surface and blood vessels could decrease, and muscles could be used to increase ventilation. Increased respiration would allow greater rates of energy production, larger size, and the possibility of endothermy.
The origin of amniotes
Mammals, birds, and reptiles are members of the Amniote clade. A clade consists of a common ancestor species and all the species (both current and extinct) that are its descendants.
As discussed above, evolution of extraembryonic structures in the amniotic egg allowed movement into terrestrial environments unavailable to amphibians. In the mammalian lineage, there are no fossilized eggs found from the time of the first amniotes. This suggests that throughout this period the eggs were non-mineralized and soft.
Background 7 has a discussion of changes in the stage of development at which eggs are laid have occurred in the evolution of amniotes.
Within the therapsids, ancestors of mammals were probably became nocturnal and lived in burrows. They developed thick filaments of keratin which acted as sensory organs (whiskers).
Perhaps the most important innovation in an ancestor that was a precursor of all current amniotes was the relocation of the heart to within the thorax (Hirasawa et al. 2015). In amphibians, the heart is located anterior to the forelimbs. In all amniotes, early development of the precursors of the heart and lungs still originated in this region mainly from cells derived from ventral lateral mesoderm (heart) and foregut (lungs), with more posterior cells becoming blood cells and vessels.
The time at which the first Amniotes arose is not very certain, but around 345 mya. Among extant amniotes, all derive from one of two branches, sauropsids, ancestors of reptiles and birds that arose about 340 mya, and the synapsids from which mammals descend, around 320 mya.
Localized tissues (eyes, brains or some muscles) can reach temperatures above the ambient temperature (partial body endothermy) in some species of fish. Whole body endothermy in any aquatic species that obtains oxygen through gills is likely impossible due the very high rate of heat loss. However, once tetrapods began breathing air, whole body endothermy became a possibility. Many eutherian mammals (those other than monotremes and marsupials) utilize a form of non-shivering thermogenesis (NST) utilizing brown adipose tissue. Grigg et al. (22) have compiled a large body of evidence suggesting this process originated prior to origin of tetrapods.
Grigg et al. (2022) looked for evidence in the fossil records of characteristics observed in extant endotherms indicating high rates of metabolism (tachy-metabolism). Six proxy characteristics of tachy-metabolism were used to suggest which extinct species were endotherms.
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In extant endotherms, microscopic examinations of slices of long bones show an irregular fibrous texture with many blood vessels (fibrolamellar bone), which is indicative of sustained fast growth, which is observed in ectotherms, if at all, as isolated regions of fast seasonal growth.
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In extant ectotherms, the maximum vertical distance between the heart and the highest point on the body is about 35 cm. This is due to the inability of low metabolism (brady-metabolism) animals to produce a high enough maximum blood pressure(MBP) to push blood any higher, in addition to overcoming the flow resistance in the blood vessels. Larger such vertical distance, rather due to posture, shape, or size was taken as evidence of endothermy.
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Large openings (foramina) where blood vessels enter bone is necessary to support the rapid sustained bone growth made possible by endothermy.
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There are no extant ectotherms that move bipedally larger than 200kg, and none larger 10kg that can move swiftly. Thus, some extinct species can be inferred to have been endotherms based on their size and evidence of bipedality.
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Estimates of stable temperatures based on the ratios of carbon and oxygen content in bone and teeth. This may not always be an indication of endothermy since large size may result in stable temperatures even in ectotherms, since the ratio of surface to volume increases with size, reducing the rate of heat loss.
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The presence of respiratory turbinates, porous bony structures in the nasal passages. In extant mammals, they help conserve heat and water.
By the early Permian, around 290 mya, there were two groups of synapsids, the Pelycosaurs, and the Therapsids, which included the ancestors of mammals. Grigg thought that some pelycosaurs could have been endothermic, based on bone histology (proxies 1 and 3) and/or because some had large sail-like structures on their backs that would have required a large MBP (proxy 2).
Grigg found some characteristics of endothermy in many species of therapsids in the late Permian. But there were cases of closely related species with none of these characteristics. Rather than de-novo endothermic processes arising in many different groups, it seems likely that some form of endothermy was inherited from ancestral species but could be readily lost if costs outweighed benefits as species encountered new environments or evolved new lifestyles.
Grigg also found evidence of endothermy in many early sauropsids, suggesting that at the origin of the Amniotes there was some endothermic mechanism(s).
Mammalian lineage innovations in response to temperature changes of the late Permian period
Starting around 265 mya temperatures rose worldwide about 16 degrees C over the next 15 million years. The initiating events for these drastic changes were large lava flows initially in China and later in Siberia, releasing large amounts of carbon dioxide, methane, and other greenhouse gases. The Siberian flows also ignited underlaying coal-bearing rocks, further increasing carbon dioxide. The initial rise in temperature melted the permafrost in polar regions, releasing methane, further increasing temperatures. There was a large die-off of both marine and plant life resulting in decreased oxygen production. These conditions resulted in the Permian-Triassic Mass Extinction (PTME).
By around 250 mya, early in the Triassic period, 80% of marine and 70% of land animal species had become extinct. All vertebrates disappeared from the equatorial regions, and elsewhere only species survived that were able to adapt to a higher range of temperatures and lower oxygen concentrations.
Around this time, several changes occurred in a subgroup of therapsids, the Eucynodonts, which were among the groups of therapsids surviving the new conditions. The therapsids that survived were generally smaller. As animals retreated away from the inhospitable conditions in the tropics and food sources decreased, smaller animals may have had an advantage. But smaller size also implies faster heat loss, so this may have given impetus for new endothermic innovations. The extreme conditions favored species that could breed faster (Botha-Brink et al. 2016). In ectothermic animals in regions with large seasonal temperature changes, growth is rapid only part of the year, and growth rings are observed during microscopic examination of cross-sections of bone. No such patterns were observed in Lystrosaurus, a therapsid genus that survived the P/T extinction, from the Karoo basin of South Africa. Lack of growth rings in bones suggest they grew at a continuously fast rate as juveniles allowing earlier breeding.
Lystrosaurus species were widespread and prevalent in the early Triassic. Their fossils are often found in burrows. This would allow them (and other therapsids) to escape the highest temperatures of the day (Lovegrove p52). Being able to retreat from the highest temperatures and dryness on the surface was particularly important in limiting water loss from their surface and respiration, in addition to that from urination. As did their amphibian ancestors, they excreted waste products from the breakdown of amino acids as urea, which has a relatively has relatively low solubility in water. In contrast. the Archosaurs(ancestors of reptiles and birds) had evolved to excrete uric acid in a semi-solid form in their feces and to have scales, resulting in little water loss. Some desert-dwelling mammals have more recently evolved the ability to excrete uric acid.
Lystrosaurus fossils have also been found in Antarctica. Antarctica in the early Triassic was attached to what is now Africa, part of the super continent Pangea. Whitney and Sidor (2020) examined the dentine of Lystrosaurus tusks from fossils from the Karoo region of South Africa (latitude of 60 degrees south at the time) and Antarctica (72 degrees south). Dentine is a continuously growing tissue. They found uniform rings possibly reflecting daily fluctuation in growth rate in fossils from the Karoo, but these uniform rings were periodically interrupted by more irregular regions in fossils from the Antarctica. They have interpreted this as evidence that in the colder region these animals used a primitive form of torpor in which their body temperature decreased to conserve resources while they waited in their burrows for better conditions on the surface.
Additional evidence of torpor, the regulated lowering of metabolic rate and body temperature, in a vertebrate during this period was also found in South Africa. A complete fossilized carnivorous therapsid, Trinaxodon, was found curled up in a fetal posture next with an intact amphibian fossil. This has been taken as evidence that the Trinaxodon must have been in a dormant state since it did not attack the amphibian. Both then would have died when the burrow flooded.
Lovegrove argues that after the earliest uses of torpor, it further evolved, initially in the tropics, in tandem with innovations in endothermy to better adapt to daily temperature fluctuations. Hibernation in response to seasonal cold weather evolved later. However, once a lineage stopped using the more evolved forms of torpor because of a new environment or lifestyle, it was unlikely to be recovered, with the possible exception of some species of mole rat. In Exploration 1 and elsewhere, I argue that the necessity of homeothermy during some stages of development has also placed some restriction on the use of torpor.
In present day mammals, there is an inverse relationship between metabolic rate and the size of red blood cells. Mammals with high metabolic rates, such as rabbits, have the smallest red blood cells. This results in a larger surface to volume ratio in the smaller cells for faster transfer of respiratory gases.
In growing bones, there are tiny tunnels through which blood flows. The diameter of the tunnels set an upper limit on the size of red blood cells, since otherwise, they would not pass through. These tunnels can still be observed (and measured) in fossils. The size of tunnels in Therapsids in smaller after the P/T extinction than before, likely indicating a higher metabolic rate (Huttenlocker and Farmer 2016). This trend towards smaller tunnels has continued in the mammalian lineage up to the present.
Olivier et al. (2017) estimated metabolic rates from bone blood vessel tunnel measurements in three dicynodonts, a sister clade of the eucynodonts in the early Triassic. They were about twice the size of those of modern ectotherms and a quarter of that of modern birds and mammals. They infer that even at this early time endothermy, the ability to maintain a temperature above the ambient, was occurring in a common ancestor of these and the related eucynodonts.
Modern mammals and birds, with even smaller red blood cells, also have a large hearts relative to body size. It thus appears that over the last 250 million years there has been a trend of relatively larger hearts to better deliver oxygen to the tissues.
Inovations during a period of decreasing temperatures (early Triassic)
Around the time of the Permian/Triassic extinction, global temperatures were very elevated for several million years, before returning to "normal temperatures over 10-15 million years. The advantages in increased activity that higher temperatures (in non-tropical regions) allowed, with decreasing ambient temperatures, could only be maintained from innovations that increased energy utilization and resulted in increased endothermy. These innovations also included changes in internal organs (heart, lungs, liver, and kidneys), which themselves required additional energy utilization. Elevated internal temperatures were also made possible by innovations reducing heat loss.
The vertebrae of the neck in the mammalian lineage still had ribs in the early Triassic, but had become more distinct in shape and length of ribs from those of the thorax during this period. The vertebrae of the neck had protuberances on their dorsal side that allowed attachment for muscles connected to the torso that helped suspend the neck and allow the head to be more mobile. It is from sometime in this period (Early Triassic) that the number of neck vertebra was constrained to be 7 in the mammalian lineage.
A bony secondary palate allows simultaneous breathing and eating, thought to be important in endothermy. In cynodonts, as in mammals it develops from the maxilla, unlike in dicynodonts, where it develops from the premaxilla (King 1988).
Linked to the increased energy requirements, drastic changes in the respiratory and circulatory system occurred between the early therapsids and the first mammals. These involved changes in both the structure and location of major organs. In the first tetrapods, the lungs and heart were in what in amniotes became a distinct neck. Muscles located anteriorly to the lungs helped ventilate the lungs, presumably by contracting the “neck” by pulling on its ribs. The heart was a linear structure with blood entering from the anterior end and exiting at the posterior end. In mammals, the lungs are enclosed in the thorax and largely ventilated by a muscular organ, the diaphragm, located posterior to the lungs. Like the lungs and heart, cells that give rise to the diaphragm and their associated nerves arise in the neck region and migrate to the thorax during the organogenesis period of development. The heart also evolved into a more complicated 4-chambered structure.
How these changes occurred is still largely mysterious. Despite their new locations, many of the components making up these systems still arise in the neck region in the embryo. Buchholtz et al. (2012) theorized that the 7cv constraint is due to the fact that some of muscle precursors and nerves of the diaphragm first arise anterior to the cervical/thoracic boundary.
Starting in the Middle Triassic, species in the mammalian lineage became smaller (mostly <1 kg), and would remain so throughout the Mesozoic Era. Maintaining a high temperature above ambient would require less energy utilization in smaller animals, but would make the problem of heat loss more important. Small size bodies means that eggs were small, and thus the hatchlings were small and subject to rapid heat loss. This demanded even higher energy expenditures to insure their rapid growth. The Parental Care Model of Farmer (2000) postulates that increased endothermy was driven (at least in part) by increased expenditure of energy in the care of offsprings (transfer of heat to developing eggs) and foraging and nest building to support their rapid growth.
By the Late Triassic (~225mya) the ancestors of mammals had adapted to a nocturnal lifestyle, possibly to escape the dominant reptiles. This allowed them to hide and conserve energy during the day. Many innovations then allowed them to be more efficient during nighttime activity, including improved or altered senses and increases in the complexity of the brain. More diverse lifestyles only became widespread after ~66mya, when the dinosaurs became extinct.
The eyes became adapted to night rather than day vision. There was an increase in the density of the rod cells that distinguish light from dark and less of the cones that provide color discrimination. 2 of the 4 opsins that allow color discrimination were lost (one kind was “reinvented” by primates much later).
An animal hunting or foraging for food during the day can move towards the target once it is seen. At night, visual signals need to be integrated with the other senses, including the senses of touch, smell, and sound in navigating the terrain and finding targets. The neocortex of the brain developed to provide a map of the night world. Increased brain size put additional demands on energy production.
The olfactory bulb of the brain became enlarged and sound perception increased, as two bones that formerly were part of the jaw became components of the inner ear.
Since many of these innovations involve soft parts of the body, we can only very roughly estimate when they occurred from skeletal changes accompanied them. Around 230 mya, ribs disappeared from the neck and lumbar region. This makes sense in the neck region if there was no longer a need to support ventilation of the lungs. Loss of cervical ribs also allowed for a more flexible neck and increased mobility of the head. Loss of ribs from what became the lumbar region allowed for expansion of the abdomen during contraction of the rib cage produced by the diaphragm.
In the mammalian lineage, innovations also occurred that not only increased endothermy, but also better retained body heat, the foremost of which was fur. Small holes in the snouts of cynodonts (~250 mya) has been suggested to be sensory hairs (whiskers). The oldest examples of fossils with evidence of a thick covering of hairs are from about 165 mya. However, since these include both mammals and mammaliaforms, fur is likely to have first appeared much earlier.
In addition to species becoming extinct due to temperature shifts for ecological reasons (loss of habitat or food source, new predators etc.) some species may have become extinct because critical molecular systems failed to change enough to function adequately at the higher temperatures. In Exploration 2, I discuss how a property of biological systems, called sloppiness, may have determined which species survived these conditions.
Fish and amphibians in addition to being ectotherms (have body temperatures close to ambient), cannot seek out environmental conditions to the same extent as amniotes. For examples, many reptiles must sun themselves to achieve greater activity levels. Extreme variations in temperatures could have driven changes in behavior. Many amniotes regulate temperature by changes in behavior, spending some time in burrows, hollows of trees, etc. This behavior allows different activities to be performed over different and narrower ranges of temperatures. For sloppy systems, operating over a smaller range of temperatures may allow the parameters of the some of the components to change considerably without the system stop functioning. The system would be less sensitive to mutational changes, favoring survival of the organism. This intra-system freedom would then allow for more linkages between systems to occur and thus lead to more complex behavior adapted to the changing environment.
In the evolution of ever more complex organisms and behavior, the number of genes in animals has not greatly increased. Rather, each gene product became more complex with more direct interaction with other products as well as more complex expression patterns. This direct interaction often involves post-translational modification of the protein. More complex expression appears to be due to some genes becoming responsive to increased numbers of transcription factors, which are proteins that when they bind to DNA near a gene affect its expression. Thus, more systems became more linked, not only in the sense that they both were operating in a single organism, organ, or cell, but between which there are physical interactions on the molecular level. Such linkages could, however, limit the range of temperatures over which each system could function, which could render homeothermic behavior not only useful, but necessary.