Sluggish Evolution

Throughout this book, it is proposed that times of low oxygen in Earth's history stimulated new kinds of evolution but were also times of low diversity. During high-oxygen times, conversely, diversity is high but the rate of new species formation is low. This hypothesis is based on the proposal that low oxygen forces new experimentation in terms of body plan. This proposal is supported by a new comparison of oxygen levels with data on the rate of new taxon formation. Thus, we should expect to see a very low rate of new species formation during the oxygen high of the Carboniferous-early Permian. Just such a finding has recently been made. In 2005, paleontologist Matthew Powell of Johns Hopkins University compiled voluminous data on the fates of various marine invertebrates during this oxygen high. He discovered very low rates of both origination and extinction. In other words, few new taxa appeared, and those that were already present rarely went extinct. The marine world was composed of an assemblage of virtual living fossils, which are characterized by long ranges (they existed for long periods of time) and produced very few new species.

Why did this happen? Powell invoked the presence of the late Paleozoic glaciation as the cause:

The Paleozoic history of marine life was interrupted in late Paleozoic time by a conspicuous interval of sluggish diversification and low taxonomic turnover. This unique interval coincided precisely with the late Paleozoic Ice Age.

Powell went on to suggest that the cool climate was the cause of this slow interval of evolution. Yet other times of glaciation seem to contradict this. One of the greatest extinctions of all time, that of the Ordovician (the mass extinction discussed in Chapter 4), has been blamed on the glaciation by most experts, and noted paleontologist Steve Stanley has suggested that cooling is a killer and cause of mass extinction. In our different view the sluggish evolution seen during the late Paleozoic is related to the high level of oxygen.

So how did all of this relate to the group we belong to and the group most people are interested in—the vertebrates?

OXYGEN AND LAND ANIMALS—REPTILES AND THEIR EGGS

Conquest of the land by chordates, our lineage, required many major adaptations. The most pressing was a way to reproduce that allowed development of the embryo in an egg out of water. The amphibians of the Pennsylvanian and Permian presumably still laid eggs in water, and thus they could not exploit the resources of land regions that were without lakes or rivers. The evolution of what is termed the amniotic egg solved this, and it was this egg that ensured the existence of a stock of vertebrates now known as reptiles. The evolution of the amniotic egg differentiates the reptiles, birds, and mammals from their ancestral group, the amphibians. Before the end of the Mississippian Period, three great stocks of reptiles had diverged from one another to become independent groups: one that gave rise to mammals, a second to turtles, and a third to the other reptilian groups and to the birds. The fossil record shows that there are many individual species making up these three. A relatively rich fossil record has delineated the evolutionary pathway of these groups. It has also required a reevaluation of just what a "reptile" is. As customarily defined, the class Reptilia includes the living turtles, squamates, and crocodiles. Technically, reptiles can now be defined by what they are not: they are amniotes that lack the specialized characters of birds and mammals. The fossil record suggests that the "amniotes" are "monophyletic"—that they have but one common ancestor—rather than suggesting the possibility that amni-otic eggs arose independently more than once.

Reptiles are considered to be a monophyletic stock that diverged from amphibian ancestors perhaps sometime in the Mississippian Period of more than 320 million years ago. But while genetic evidence of this divergence, obtained by the "molecular clock" analysis technique, can be dated back to as long ago as 340 million years, fossils that are ascribed to the first reptiles (instead of terrestrial amphibians) have been recovered from several localities globally. Fossils of small reptiles named Hylonomus and Paleothyris have been found interred in fossilized tree stumps of early Pennsylvanian age, and it may be that the fossil record of this later appearance is more valid than the assumption of a Mississippian evolution of the group. In either case, these first reptiles were very small—only about 4 to 6 inches long.

That these small reptiles laid the first amniotic eggs is still speculation. There are no fossil eggs in the stratigraphic record until the lower Permian, and this single find remains controversial. But the pathway to the amniotic condition probably passed through an amphibian-like egg without a membrane that would reduce desiccation, which laid in moist places on land. It would have been the evolution of a series of membranes surrounding the embryo (the chorion and amnion), covered by either a leathery or a calcareous but porous egg that was required for fully terrestrial reproduction. One possibility seemingly never considered is that these first tetrapods evolved live births, so that the embryos were not born until substantial development within the female had taken place; we would love to know if any animals of this time produced live births, but that is only rarely recorded in the fossil record. One exception is the extraordinary fossil showing a female ich-thyosaur of the Jurassic that died giving live birth. We also have no record of eggs laid in water—for instance, frog and salamander eggs are so soft that they are never preserved.

Land eggs eventually were produced, and it was here that the level of oxygen must have played a part. There is a huge tradeoff in reproduction for any land animal using an egg-laying strategy. Moisture must be conserved, so the openings of the egg must be few and small. But reducing permeability of the egg to water moving from inside to outside also reduces the movement of oxygen into the egg by diffusion. Without oxygen the egg cannot develop. The first amniotic eggs were probably produced in oxygen levels equal to or even higher than those of today. It may be no accident that the evolution of the first amniote occurred during a time of high oxygen. This leads us to a new hypothesis:

Hypothesis 6.1: Reproductive strategy is affected by atmospheric oxygen content, with higher-oxygen contents producing more rapid embryonic development. High oxygen may have allowed amniotic eggs and then live births.

Some biologists have suggested that live births could not take place in low oxygen because, at least in mammals, the placenta delivers lower levels of oxygen than are present even in arterial blood in the same mother. But this is for mammals. Reptiles have a very different reproductive anatomy. It may be that low oxygen even favors live birth. Evidence to support this comes from three lines of evidence. First, birds (egg layers) living in high-altitude habitats routinely feed at higher altitudes than the maximum altitude at which they can reproduce. The maximum altitudes of the nests of many mountainous bird species repeatedly show this pattern. The highest nests are at 18,000 feet, and higher than this the embryos will not develop successfully. While at least three factors may be involved in this limit (lowered-oxygen con tent with altitude, desiccation because of air dryness at altitude, and relatively low temperatures at greater altitude), it may be oxygen content that is most important. Second, recent experiments by John VandenBrooks from Yale University have shown that alligator eggs taken from natural clutches and raised in artificially higher-oxygen levels showed dramatically faster than normal development rates. The embryos grew some 25 percent faster than controls held at normal atmospheric oxygen levels. Increased oxygen clearly influences growth rates, at least in American alligators. Since egg contents are a tasty snack for many predators now, and surely back then, it is in the embryo's better survival interest to develop and hatch as quickly as possible. Finally, a higher proportion of reptiles at high altitudes use live births than do reptiles at lower altitudes.

At this point we can summarize and discuss the variables in land animal reproduction and try to relate these to generalizations about both oxygen levels and temperature. There are two possible strategies, egg laying or live birth. In the egg case, the eggs are either covered with a calcareous shell or a softer, more leathery shell. Today, all birds utilize calcareous eggs, while all living reptiles that lay eggs use the leathery covering. Unfortunately, there is little information about the relative oxygen diffusion rates for leathery, or parchment, eggs compared to calcareous eggs.

The utilization of egg laying or live births has important consequences for land animals. The embryos developed by the live birth method are not endangered by temperature change, desiccation, or oxygen deprivation. But the cost is the added volume to the mother, which must invariably make her more vulnerable to predation in addition to making her need more food than would be necessary for herself alone. Egg layers are not burdened with this problem but have the tradeoff of a less safe environment—the interior of an egg outside the body—that leads to enhanced embryonic death rate through predation or lethal conditions of the external environment.

The study of oxygen levels and egg morphology or reproductive strategy is in its infancy. Obvious tests include raising eggs at both high-and low-oxygen levels, for both calcareous and leathery eggs. Also, a direct study of fossil eggs themselves would be of great interest. A pre diction is that fossil eggs from times of low oxygen should show more openings than those from times of higher oxygen.

OXYGEN AND LAND ANIMALS—REPTILES AND THEIR LOCOMOTION

As four-legged vertebrates emerged from their piscine ancestors, many new anatomical challenges had to be overcome. No longer was there water to support the animal's body; in air, both support and locomotion had to be accomplished by the four legs. An entirely new suite of shoulder and pelvic girdle designs had to evolve, along with the muscles necessary to allow locomotion. Equally daunting was the problem of acquiring sufficient oxygen to allow sustained exercise. Early tetrapods apparently used the same set of muscles for motion and for taking a breath, and they could not do both at the same time. Fish seem to have no problem with sustained exercise or with respiring during activity, suggesting that oxygen is not a limiting factor in daily activity. For land tetrapods this is not the case. The body plan of the earliest land tetrapods provided for a sprawling posture with legs splayed out to the sides of the body trunk. In walking or running with such a body plan, the trunk is twisted first to one side and then to the other in a sinuous fashion. As the left leg moves forward, the right side of the chest and the lungs within are compressed. This is reversed with the next step. The distortion of the chest makes "normal" breathing difficult to impossible—so each breath must be taken between steps. This process makes it impossible for the animal to take a breath when running— modern amphibians and most reptiles cannot run and breathe at the same time (the exceptions including varanids that augment respiration with gular pumping), and it is a good bet that their Paleozoic ancestors were similarly impaired. Because of this there are no reptilian marathoners and not too many long-distance sprinters. This is why reptiles and amphibians are ambush predators. They do not run down their prey. The best of the modern reptiles in terms of running is the Komodo dragon, which will sprint for no more than 30 feet when attacking prey. This is called Carrier's Constraint, after it discoverer, physiologist David Carrier.

The dilemma of not being able to breathe and move rapidly at the same time was a huge obstacle to colonizing land. The first land tetra-pods would have been at a great disadvantage to even the land arthropods, such as the scorpions, for the vertebrates would have been slow and would have needed to stop constantly to take a breath. This is why oxygen levels would have been critical. Only under high-oxygen conditions would the first land vertebrates have had any chance of making a successful living on land.

One consequence of limited respiration while moving was that the early amphibians and reptiles evolved a three-chambered heart. This kind of heart is found in most modern amphibians and reptiles and is adaptive for creatures that have the problem of inferior respiration while moving. While a lizard is chasing prey it is not breathing, and thus the fourth chamber of the heart, which would be pumping blood to the lungs, is superfluous. The three chambers are used to pump blood throughout the body, but the price that must be paid is that it takes the lizard longer to reoxygenate the blood when activity ceases.

One group of reptiles, the mammal-like reptiles or synapsids, either partially or totally solved the reptilian problem of not being able to breathe while running by changing their stance. The synapsids show an evolutionary trend of moving their legs into a position so that they were increasingly under the trunk of the body, rather than splayed out to the side as in modern lizards. This created a more upright posture and removed, or at least greatly decreased, the lung compression that accompanies the sinuous gait of lizards and salamanders. While there was still some splay of the limbs to the sides of the trunk, it was certainly less than in the first tetrapods. With the evolution of the ther-apsids in the middle Permian, the stance became even more upright.

OXYGEN AND LAND ANIMALS—REPTILES AND THEIR THERMOREGULATION

Another important variable is the nature of thermoregulation—the possibilities of endothermy (warm-bloodedness), ectothermy (coldbloodedness), and a third category that is essentially neither of the others and is associated with very large size. Warm-bloodedness

(endothermy) allows animals using it to stay at a constant, warm temperature no matter how cold it gets. However, this can work against animals in very hot climates, as it is more difficult to cool off than warm up. Cold-blooded animals match the temperature around them. They are sluggish in the cold. There is a third kind of metabolism, found in animals so big that they are largely unaffected by daily swings in temperature, such as daytime and nighttime. The very large dinosaurs presumably used this system.

Other important aspects that might be related to the environmental conditions in which the various clades evolved and then lived include the presence or absence of scales, hair, and feathers. With thermoregulation pathways, the question of whether or not dinosaurs were warm-blooded has been the most discussed and most controversial of all. The fact that each of these characteristics, thermoregulatory systems and body covering, is primarily either physiological or involves body parts that only rarely leave any fossil record (such as fur) is in large part responsible for the controversies. We know that all living mammals and birds are warm-blooded, with the former having hair and the latter feathers, just as we know that all living reptiles are coldblooded, with no hair or feathers. The status of extinct forms remains controversial. Of interest here is how oxygen concentration primarily and characteristic global temperatures secondarily affected thermoregulation or characteristic body coverings in animal stocks of the past. Let's look at each of the three stocks in more detail with this overarching question in mind.

Diapsids

Openings are used to lighten the reptile skull, and their number (or lack of) is a convenient way of differentiating the three major stocks of "reptiles." Anapsids (ancestors of the turtles) had no major openings in their skulls; synapsids (ancestors of the mammals) had one; and diapsids (dinosaurs, crocodiles, lizards, and snakes) had two. The earliest member of the diapsids is known from the latest Pennsylvanian rocks around 305 million to 300 million years ago, and it was small in size, about 8 inches in total length. From the time of their origins until the beginning of the fall of oxygen, which probably began in earnest some 260 million years ago, in the middle and late part of the Permian period, the diapsids did little in the way of diversification or specialization. They remained small and lizard-like. They gave no indication that they would be the ancestors of the largest land animals ever to appear on Earth, in the form of the Mesozoic dinosaurs. If the time of highest oxygen stimulated insects to their greatest size, the same cannot be said of the diapsids.

The most pressing question is whether or not this group was warm-blooded.

Anapsids

The lineage that ultimately gave rise to turtles was very successful during the late Pennsylvanian but less so into the Permian. Anapsids did evolve into giant forms, including cotylosaurs and the even larger pareiosaurs. These were armored giants, surely slow moving and herbivores that lived right until the end of the Permian. Other anapsids were small and more lizard-like. It is very likely that the gigantic size of the earlier Permian anapsids was allowed by high oxygen. All modern anapsids use ectothermy; they are cold-blooded. Presumably the ancient forms used this system as well, but that is still controversial.

Synapsids

The third group of amniotes from this time, the synapsids, or mammal-like reptiles, are known in their most primitive form from Pennsylvanian rocks, and these ancestors of mammals had a lizard-like small shape and mode of life in all probability. It is assumed that these early synapsids were cold-blooded. They in turn gave rise to two great and largely temporally successive stocks, the pelycosaurs (or finbacks, like the early Permian Dimetrodon) and their successors, the therapsids (the lineage giving rise to mammals). It is this latter group that is also called the mammal-like reptiles.

Unlike the diapsids, the synapsids diversified during the oxygen high and at its peak became the largest of all land vertebrates. In the

Reconstruction of the synapsid reptile Dimetrodon. The large fin was probably for thermoregulation, and thus is evidence that this group was not warmblooded.

latter part of the Pennsylvanian the pelycosaurs probably looked and acted like the large monitor lizards or iguanas of today. By the end of the Pennsylvanian some attained the size of today's Komodo dragon, and they may have been fearsome predators. By the beginning of the Permian Period, some 300 million years ago, the pelycosaurs made up at least 70 percent of the land vertebrate fauna. And they diversified in terms of feeding as well; three groups were found: fish eaters, meat eaters, and the first large herbivores. Both predators and prey (for this group evolved both predatory and herbivorous species) could attain a size of 12 feet in length, and some, such as Dimetrodon, had a large sail on its back that would have made it appear even larger.

The sail present on both carnivores and herbivores of the late Pennsylvanian and early Permian is a vital clue to the metabolism of the pelycosaurs: it was a device used to rapidly heat the animal in the morning hours. By positioning the sail so as to catch the morning sun, both predators and prey could warm their large bodies quickly, allowing rapid movement. The animal that first attained warm internal temperature would have been the winner in the game of predation or escape, and hence natural selection would have promoted these sails. But the larger clue from the presence of sails is that during the oxygen high, the ancestors of the mammals had not yet evolved warm-bloodedness.

So when did warm-bloodedness first appear? That revolutionary breakthrough must have happened among the successors to the pely-cosaurs, the therapsids. We must note as well that the late Pennsylva-

nian and early Permian, while a time of oxygen high, was a period of temperature low. There was a great glaciation during this interval and much of the polar regions of both hemispheres would have been covered in ice, both continental and sea ice.

The transition from the pelycosaurs to the therapsids is poorly known because of few fossiliferous deposits of the critical age. The gap in our knowledge of the synapsid fossil record extends from perhaps 285 million years ago to around 270 million years ago with some few exceptions in two main regions, the Russian area around the Ural Mountains and the Karoo region of South Africa. The record in the Karoo begins with glacial deposits perhaps as much as 270 million years in age, and then there is a continuous record right into the Jurassic (199 million to 145 million years ago), giving an unparalleled understanding of this lineage of animals.

The therapsids split into two groups, a dominantly carnivorous group and an herbivorous group. By about 260 million years ago the ice was gone in South Africa, but we can assume that the relatively high latitude of this part of the supercontinent Pangea (about 60 degrees South latitude) remained cool. It was still a time of high oxygen, certainly higher than now, but that was changing. As the Permian period progressed, oxygen levels dropped. Seemingly two great radiations of therapsids occurred, among both carnivores and herbivores. From perhaps 270 million to 260 million years ago the dominant land animals were the dinocephalians, and these great bulky beasts reached astounding size, not dinosaur-sized but certainly exceeding the size of any land mammal today save, perhaps, the elephant, and some of the largest of the dinocephalians certainly must have weighed as much as elephants. Moschops, for instance, a common genus from South Africa, was 10 feet in length, with an enormous head and front legs longer than the back. This was an enormous animal, the biggest yet on the Earth. But it was graceless in construction, being bulky, and surely awkward. No fast running here, or any deep thoughts, if the tiny size of its brain case is any indication. It was hunted by a group of nearly equally-sized carnivores, also lumbering and slow in all probability.

The dinocephalians and their carnivore predators were hit by a great extinction, still very poorly understood, of some 260 million years ago, the same time, it turns out, that oxygen levels began to plummet. The immediate successors in terrestrial dominance of the dinocephalians, the dicynodonts, were the dominant herbivores of the time from 260 million to 250 million years ago. They in turn were almost eliminated from the planet in the Permian extinction, which will be described in more detail in the next chapter. The dicynodonts were hunted by three groups of carnivores, all therapsids: the gorgonopsians, which died out at the end of the Permian; the slightly more diverse therocephalians; and the cynodonts, which ultimately evolved into mammals during the Triassic. We will return to these groups—and their horrific fate—in more detail in the next chapter.

OXYGEN AND LAND ANIMALS—REPTILES AND THEIR SIZE

The rise of atmospheric oxygen to unprecedented values of over 30 percent in the Carboniferous-early Permian was accompanied by the evolution of insects of unprecedented size. The giant dragonflies and others of the late Carboniferous through the early Permian were the largest insects in Earth's history. Perhaps it is just coincidence but most specialists agree that the high oxygen would have enabled insects to grow larger, since the insect's respiratory system requires diffusion of oxygen through tubes into the interior of the body and in times of higher oxygen, more of this vital gas could penetrate into ever-larger-bodied insects. So if insects got larger as oxygen raised, what about vertebrates? New data acquired by French anatomist Michel Laurin can be used to test this question. Indeed, it does seem that body size in various late Paleozoic reptilian lineages do track oxygen levels.

Laurin's published data were compared to the oxygen levels given in the Berner curves (like so much discovered while writing this book, this information is simultaneously being published in the scientific literature). Laurin looked at a sample of animals from the anapsids and synapsids. He used a measure of body length and a measure of skull size to evaluate animal size, for specific time horizons between the late Mississippian and the end of the Permian, from about 320 million years ago until about 250 million years ago. Then I did a simple regression analysis of mean size and oxygen levels. Indeed, mean skull size closely tracks oxygen levels, increasing and decreasing in close correspondence with atmospheric oxygen levels for the time periods for which size data is available. As oxygen levels rose in the late Carboniferous, so too did the size of the reptiles increase and, as oxygen began to drop in the mid-Permian, we see size beginning to trend downward. Thus, like insects, it appears that at least these groups of land vertebrates changed size in response to the oxygen available at any given time.

The mammal-like reptiles also seem to show this trend (according to vertebrate paleontologist Christian Sidor of the University of Washington), although the quantitative data (measured in the way that Laurin measured the sizes of earlier land vertebrates) are not yet available. Nevertheless, it is clear that the largest therapsids of all time, the dinocephalians of the middle Permian, evolved at the peak of oxygen abundance. As oxygen began to drop in the mid-Permian, successive taxa assigned to various therapsid groups and, most importantly, the dicynodonts, showed a trend toward smaller skull sizes. While some relatively large forms still lived in the latest Permian—the genus Dicynodon and even the carnivorous gorgonopsians come to mind— by this time many of the dicynodonts were smaller. The latest Permian taxa, Cistecephalus, Diictodon, and a few others, were very small. The late Permian-early Triassic genus Lystrosaurus is smaller in the Triassic than it is in the Permian, and the various cynodonts of the late Permian and early Triassic are all small in size. There are a few giants in the Triassic—Kannemeyeria and Tritylodon are examples—but in general the therapsids of the Triassic are much smaller than those of the Permian. A recent paper by University of Washington paleontologist Christian Sidor has confirmed the drop in size of Triassic forms compared to their Permian ancestors. Thus, once again, we see there is a strong correlation between terrestrial animal size and oxygen levels, in this case from the latest Permian into the Triassic. In high oxygen tetra-pods grew large, and then they grew smaller as oxygen levels diminished.

We have come to a time of about 260 million years ago. It was the end of the long Paleozoic Era, and in the last 10 million years of its nearly 300-million-year-long history all hell would break loose—literally, as the next chapter shall recount.

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