As reported in previous blogs, the issue of New Scientist dated 27 February 2008 carried a major article on intermediate or transitional forms in nature. It was written by Donald Prothero who is Professor of Geology at Occidental College in Los Angeles and lecturer in Geobiology at the California Institute of Technology in Pasadena. The full article can be read here. In addition, his book "Evolution: What the fossils say and why it matters" was published by Columbia University Press in 2007. In this article, we consider Professor Prothero's further suggestion that: Another excellent example of a transitional sequence is the evolution of mammals from their ancestors, the synapsids. These were once called "mammal-like reptiles", but that term is no longer used because synapsids are not reptiles - the two groups evolved in parallel from a common ancestor.
Synapsids are a classification construct (i.e. clade) that includes so-called mammal-like reptiles and true mammals. The non-mammalian synapsids comprise the pelycosaurs which are regarded as primitive and the therapsids which are regarded as more advanced.
In contradistinction, the sauropsids are tetrapod animals including reptiles, dinosaurs and birds. Together, the synapsids and the sauropsids comprise the amniotes all of which are characterised by the presence of amniotic membranes surrounding the embryo either within an egg or carried within the body of the mother. These embryonic membranes distinguish amniotes from the amphibians which lay their eggs in water and generally possess a distinctive larval stage in their life history.
Prior to the 1990s, the non-mammalian synapsids were actually considered true reptiles. Nevertheless, because of the widespread adoption of a revised evolutionary classification largely based on cladistic analysis, these extinct creatures are no longer considered reptiles and are now regarded as the ancestors of mammals. Why is this? Professor Prothero gives us a clue: In this instance, we have hundreds of beautiful fossils of skulls as well as many complete skeletons that document the transition over 100 million years from the late Carboniferous to the early Jurassic ... Among the striking evolutionary changes occurring in the synapsids was in their lower jaws. Most reptiles have several bones in the lower jaw, and Dimetrodon shares this characteristic. But mammals have only a single lower jawbone, the dentary. Throughout synapsid evolution, we see the gradual reduction of the non-dentary elements of the jaw as they are crowded towards the back and eventually lost. The dentary bone, in contrast, gets larger and takes over the entire jaw. In the final stage of evolution, the dentary bone expands until it makes direct contact with the skull and develops a new articulation with it.
Accordingly, this transitional sequence is almost solely based on changes in cranial architecture which is distinctively different in reptiles and mammals. In particular, in mammals, the lower jaw comprises a single dentary bone whereas in reptiles, the lower jaw consists of many. Furthermore, it is suggested that some of these many bones eventually became the bones of the mammalian middle ear. As Professor Prothero suggests: Where did the rest of the non-dentary bones go? Most were lost, but the articular bone and the corresponding quadrate bone of the skull are now the malleus ("hammer") and incus ("anvil") bones in your middle ear. This may seem bizarre until you realise that most reptiles hear with their lower jaws, transmitting sound from this to the middle ear through the jaw articulation.
The diagram (accurately redrawn here from that shown in New Scientist) is lacking in some important details. We have Dimetrodon, a "primitive" synapsid found in Permian strata and we have the mammal Morganucodon found in the Jurassic. The reader of the New Scientist, however, has no idea what the intermediate jaws represent as they are not named. Also the suggestion that mammals are only to be found in Jurassic strata is highly misleading. For example, Adelobasileus cromptoni as well as Morganucodon itself have been found in the Triassic as the Professor himself later acknowledges.
The Professor then makes a remarkable statement (repeated in his book) that the general reader has little choice but to take at face value: "In addition, during embryonic development, the middle ear bones start in the lower jaw, and then eventually migrate to the ear."
In mammalian embryos, however, the middle ear ossicles (bones) are derived from the 1st and 2nd arch mesenchyme (i.e. embryonic connective tissue of mesodermal origin). To download a recent article  on the embryological development of middle ear bones in mammals see here.
The primitive synapsid Dimetrodon is probably the most familiar example of a pelycosaur. The reason that it is regarded as in any way mammal-like is the presence of teeth that enabled the creature to "chew" its prey and to aid ingestion. Modern-day carnivorous reptiles generally "gulp" their prey whole. Chewing demands specialised teeth and the jaw muscles to go with them. Chewing is also characteristic of animals that are primarily herbivorous. Remarkably, this is also true for some true reptiles including many dinosaur species many of which were herbivorous. For a more detailed examination of the differences between the jaws of carnivorous and herbivorous dinosaurs click here.
The crucial point to note is the relative sizes of the dentary and surangular bones of the lower jaw. The surangular bone is greatly reduced in the herbivore. So where does that leave us with the jaw (and the diet) of the "mammal-like" synapsids such as Dimetrodon? Although this animal is considered to have been carnivorous with large, powerful jaws, it also had two types of teeth: sharp canines and shearing teeth. It is apparent that these creatures also had the ability to "chew" their food and may be more correctly classified as omnivores. Their jaw architecture would need to accommodate the musculature required to facilitate this. A picture of the skull of Dimetrodon can be seen here.
However, not all pelycosaurs are regarded as carnivorous. It is believed that the Caseidae and the Edaphosauridae were true herbivores. A typical herbivorous pelycosaur is Edaphosaurus. The popular BBC series "Walking with Monsters"describes the carnivorous Dimetrodon attacking the herbivorous Edaphosaurus. This, of course, is speculation. What is more certain is that both Dimetrodon and Edaphosaurus were cold-blooded creatures using their sails to maximize their ability to capture heat from the sun. They are mainly distinguishable by close examination of their cranial architecture.
The other main group of non-mammalian synapsids was the therapsids which are also to be found in middle Permian strata. Therapsida consists of three major clades, the dinocephalians, the herbivorous anomodonts and the mostly carnivorous theriodonts which includes the gorgonopsids which also featured in the BBC programme "Walking With Monsters" and, more recently, the first and sixth episodes of the ITV series "Primeval".
Therapsids were small to moderate-sized animals with several mammalian skeletal characteristics, such as: fewer bones in the skull than the other reptiles, differentiated teeth (incisors, canines, and cheek teeth) and a bony palate which permitted breathing while chewing. From a skeletal perspective, the most mammal-like therapsids were the cynodonts. According to Professor Prothero: In the Triassic and early Jurassic, the protomammal story culminated in the most advanced of all the synapsids, the cynodonts. They had a mammal-like posture, a fully developed secondary palate, a large temporal opening for multiple sets of jaw muscles allowing complex chewing movements, and highly specialised molars and premolars for grinding and chewing. Some of them probably had hair. Many of the later species of cynodonts are so mammal-like that it has long been controversial as to where to draw the line between true mammals and the rest of the synapsids. The oldest fossils that palaeontologists now agree are mammals come from the late Triassic. They were shrew-sized, with a fully developed joint between the dentary bone and the skull, and three middle-ear bones. Thanks to the fossil record, we have a full picture of how they evolved from synapsids.
To suggest that we now have a full picture of how mammals evolved from synapsids is an overstatement. Thus far, we (and the Professor) have only considered aspects of mammalian skeletal characteristics that can be inferred from the direct examination of synapsid fossil remains. In particular, relative proportions of the cranial bones such as the dentary and postdentary can only indicate one aspect of this presumed transition.
An alternative view
Furthermore, not every palaeontologist would agree with Professor Prothero's evolutionary assessment of the synapsid cranial morphology. The most recent review has been written by Christian Sidor (Assistant Professor of Biology and Curator of Vertebrate Paleontology, University of Washington) in the journal Paleobiology which and entitled "Evolutionary trends and the origin of the mammalian lower jaw". The full publication can be found here.
In this article, Professor Sidor presents detailed findings based on the morphological analysis of an extensive number of fossil synapsid jaws. These included 19 pelycosaurs, six basal therapsids, 13 dinocephalians, 25 anomodonts, ten gorgonopsians, ten therocephalians and 25 cynodonts. His conclusions are as follows:
1. The lack of a well-supported phylogeny [i.e. evolutionary relationships between organisms] has exaggerated previous estimates of morphological convergence or parallelism in the synapsid fossil record. The hypothesis of multiple therapsid groups arising independently from pelycosaur-grade ancestors necessitated rampant homoplasy and are now considered untenable.
TiS Note: Homoplasy is defined as a collection of phenomena leading to similarities in character states for reasons other than inheritance from a common ancestor. These include convergence, parallelism, and reversal.
2. Despite the striking differences between the lower jaws of basal synapsids [i.e. pelycosaur] and mammals, jaw evolution within synapsids was predominantly conservative [emphasis added]. Except for dicynodont anomodonts, most therapsids do not acquire substantial morphological novelty in their lower jaw structure.
3. When comparing the dentary and postdentary bones with overall jaw length, the trends in body-size are not sufficient to explain the reduction of the postdentary bones in synapsid evolution. Importantly, when compared with other synapsid subgroups, cynodonts are characterized by smaller-than-predicted postdentary areas.
4. Selection acting to decrease the size of the postdentary bones, and thereby improving high-frequency hearing, is still the most tenable mechanism for the evolution of the mammalian lower jaw. However, this mechanism by itself has difficulty explaining the converse pattern in anomodont therapsids (i.e. decreasing the size of the dentary and increasing the size of the postdentary bones).
5. These conclusions, in combination with those of recent studies on long-term patterns of limb and cranial evolution, suggest that morphological trends within synapsids should be re-investigated within a quantitative and phylogenetic framework.
In other words, the most detailed recent study suggests that there is little supporting evidence for the transition sequence proposed by Professor Prothero. But this is just the beginning of the problem when one considers the emergence of mammalian characteristics in the fossil record.
When is a mammal a mammal?
According to T.S. Kemp who wrote the most current definitive text book entitled "The Origin and Evolution of Mammals" [OEM] published by Oxford University Press in 2005: The formal definition of Mammalia is simple as far as the living mammals are concerned, because of the large number of unique characters they possess. However, the fossil record makes the situation a good deal less clear cut [OEM page 1].Kemp discusses the difficulty in assigning mammal-likeness to organisms that do not possess many relevant features. For example, pelycosaurs have very few mammalian characters, just a small temporal fenestra [a small opening usually covered with membrane] in the skull and an enlarged canine tooth in the jaw. Furthermore, Kemp goes on to suggest: An arbitrary decision is made about which characters to select as defining characters, and therefore which particular node on the stem lineage to label Mammalia. Characters deemed appropriate are those reflecting the evolution of the fundamental mammalian biology [emphasis added]. The essence of mammalian life is to be found in their endothermic [warm-blooded] temperature physiology, greatly enlarged brain, dentition capable of chewing food, highly agile, energetic locomotion, and so on. The organisms that achieved this grade of overall organisation are deemed to be Mammalia, and consequently those characters that they possess are the defining characters of the group [OEM page 2]
Of these attributes, only certain skeletal characteristics can be presented as evidence from the fossil record, but as Kemp has already indicated there are many other significant features of mammals. These include: (1) the possession of a relatively huge brain and highly sensitive sense organs, (2) characteristic growth and development patterns, (3) endothermic temperature physiology with high metabolic rates, insulation and high respiratory rates, (4) turbinal bones and a secondary palate, and (5) precise osmoregulatory and chemoregulatory mechanisms.
1. The brain
According to Kemp, there is little consensus about the evolution of the brain within the cynodonts, the most mammal-like of all the synapsids. Some have suggested that the brain of the cynodont was still very small compared to mammals, although others think that there may have been some enlargement. However, Kemp goes on: What is beyond dispute, however, is that the earliest mammals themselves did have significantly enlarged brains ... the brain size in Mesozoic mammals lay within the lower part of the size range of the brains of living mammals. This represents an overall increase of some four or more times the volume of basal amniote brains, and presumably involved the evolution of the neocortex, the complex, six layered surface of the cerebral hemispheres that is one of the most striking of all mammalian characters [OEM page 120].
2. Growth and development
The pattern of growth of amniotes other than mammals is described as indeterminate. This is because it is continuous throughout life and there is no absolute adult size. In addition, this pattern of growth is associated with successive replacements of each tooth (polyphyodonty) providing an increased size and number of teeth concomitant with growth. In mammals, however, growth is described as determinate. There is rapid growth in the juvenile ending in a mature adult size. Growth does not continue unabated and this unique characteristic of mammals is also associated with what is technically described as diphyodont tooth replacement. For example, as in humans, milk teeth are shed to be replaced (once) with a permanent adult dentition. According to Kemp: It is not until the basal mammal Morganucodon that the combination of determinate growth and diphyodonty is known to have evolved ... The incisors, canines, and anterior postcanines are replaced once, and posterior postcanines are added sequentially at the back, not replaced, and therefore can properly be referred to as molar teeth. Given its correlation with growth pattern, it is assumed by this stage that lactation had evolved [OEM page 121].
In other words, there is no fossil evidence for the emergence of determinate growth and diphyodonty until the first true mammal appears in the fossil record. This fact is omitted in Professor Prothero's article.
3. Temperature physiology
According to Kemp: Nothing is more fundamental to the life of mammals than their endothermic temperature physiology, if only because it entails a 10-fold increase in daily food requirements. Such a huge cost must be balanced by an equally large benefit for endothermy to have evolved and been maintained. Yet surprisingly there is no consensus about exactly how, why, or when endothermy evolved in the course of the evolution of the mammals. The fact that the birds share a virtually identical mode of endothermic temperature physiology with the mammals adds little elucidation: the same contentious issues apply to them. The problem arises because of the complex nature of endothermy. It has two distinct primary functions in modern mammals, and it also involves a considerable array of structures and processes, including a regulating system for the high metabolic rate, variable conductivity of the skin by use of hair and cutaneous capillaries, neurological mechanisms for bringing about panting and shivering, and so on [OEM pages 121 and 122].In endotherms, body temperature must be controlled with extreme accuracy. This is done by maintaining a body temperature which is significantly higher than the environment and is accomplished by a high metabolic rate together with the possession of insulation. In addition, it is necessary to have fine control of heat loss by vasodilation or vasoconstriction of the skin capillaries. Emergency measures must be in place under extreme conditions. These include the ability to pant, sweat or shiver. According to Kemp: The adaptive significance of a constant body temperature is hard to describe succinctly because it so permeates the total biological organisation of a mammal [OEM page 122].Needless to say, there have been various hypotheses regarding the timing of the appearance of endothermy in synapsids although according to Kemp they do not stand up to close scrutiny. The best evidence would be the discovery of insulation such as fur. Professor Prothero suggests that some synapsids "probably had hair"but this is no more than wishful thinking. Unfortunately for him, the fossil record does not provide the necessary evidence. According to Kemp: ... as yet no mammal like reptile has been shown by direct fossil evidence to have possessed a pelt [OEM page 126].
4. Turbinal bones and a secondary palate
In modern mammals, the turbinal bones inside the nasal cavity play an important role in endothermy. These very thin bones are covered in epithelium serving two functions, namely, chemoreception and an acute sense of smell and to warm and humidify air. Turbinal bones have never been found in any mammal-like reptile although, in some cases, fine bony ridges could be sites of attachment for putative cartilaginous turbinals. In addition, the presence of a secondary palate in some synapsids might indicate endothermy although it is also present in modern crocodiles to assist a semi-aquatic lifestyle.
5. Osmoregulation and chemoregulation
Mammals are able to regulate their internal chemical environment which is achieved mainly by the ability of the kidney tubule to create hyperosmotic urine. By concentrating the urine, a mammal can use soluble urea as its prime nitrogen-excreting molecule without excessive water loss. This mechanism adjusts the balance between reabsorbtion and secretion and is under precise hormonal control to maintain plasma at optimal composition.
Taken together, all of these facets of mammalian life present a vastly more complex picture than that presented in Professor Prothero's New Scientist article. The problem is summed up by Kemp as follows: Seen in this light, there is no identifiable, single key adaptation or innovation of mammals because each and every one of the processes and structures is an essential part of the whole organism's organisation. To regard for example endothermy, or a large brain, or juvenile care as somehow more fundamental is arbitrarily to focus on one point in an interdependent network of causes and effects. Endothermy is necessary for maintained elevated levels of aerobic activity, but the activity itself is simultaneously essential for collecting enough food to sustain the high metabolic rate. The large brain causes high levels of learning and social behaviour, but the latter are necessary for the parental care that allows the offspring time to develop the large brain in the first place. Lactation is on the one hand necessary for mammalian development, yet on the other can only exist by virtue of the high metabolic rates and efficient food collection. Which has ontological priority [OEM page 133]?
There is no doubt that the so-called synapsid transition leading to the emergence of mammals is regarded by neo-Darwinists as the best evidence that the fossil record has to offer. Nevertheless, the speculations based upon fossil material cannot and do not begin to address the origin of the unique genetic, structural, biochemical and physiological characteristics that define all mammals. We suggest that teachers and students at least reflect upon these other fundamental aspects of mammalian life when considering the supposed emergence of mammals from the synapsids.
Postscript: When is a reptile a reptile?
As mentioned at the beginning of this article, non-mammalian synapsids were once regarded as true reptiles. Nevertheless, this is no longer the case. In chapter 13 entitled "Mammalian Explosion" in his book, the Professor writes as follows: Of the transitional series that we have examined between major groups of vertebrates, one of the best documented is the transition from primitive amniotes to mammals via the synapsids, formerly known as the "mammal-like reptiles." As we explained previously, however, the synapsids that evolve into mammals are not reptiles and never had anything to do with the lineage that leads to reptiles. Both the earliest true reptiles (Westlothiana from the Early Carboniferous) and the earliest synapsids (Protoclepsydrops from the Early Carboniferous and Archaeothyris form [sic] the Middle Carboniferous) are equally ancient, demonstrating that their lineages diverged at the beginning of the Carboniferous. Older precladistic interpretations had synapsids evolving from a paraphyletic waste-basket of primitive amniotes known as the "anaspid [sic] reptiles". This idea is now completely discredited, and anyone who still uses the obsolete and misleading term mammal like reptiles clearly doesn't know much about the current understanding of vertebrate evolution [from Donald R. Prothero (2007) Evolution: What the Fossils Say and Why It Matters New York: Columbia University Press p.271].
There are several reasons why these creatures are no longer considered reptiles (although they are most often still described as such). As we have indicated in this article, the reasons include the relative sizes of the dentary and post-dentary bones in the lower jaw and the type of teeth. In particular, it is suggested that the presence of a single temporal fenestra (hole) in the skull behind each eye is indicative of the mammalian condition. Living reptiles such as snakes and crocodiles are characterised by a diapsid situation which is the presence of two openings in the skull, namely, the lower and the upper temporal fenestrae. The lower temporal fenestra of diapsids is the equivalent of the single fenestra of synapsids.
The Professor is dogmatic: ... anyone who still uses the obsolete and misleading term mammal like reptiles clearly doesn't know much about the current understanding of vertebrate evolution.In addition, he has suggested: Older precladistic interpretations had synapsids evolving from a paraphyletic waste-basket of primitive amniotes known as the "anaspid [sic] reptiles"
We believe that the Professor has confused two terms here. Anaspids (meaning "without shields") were actually ancient jawless fish. In fact, he uses this term earlier in the book [pages 208 and 209] to describe such fish found in Silurian strata. To make matters worse, in the index of the book [page 373], he also confuses "anaspid" with the term "anapsid". As far as we know there were no "anaspid reptiles". Presumably what he meant was "anapsid reptiles". If this is the case, his description of the anapsida is totally misleading.
An anapsid reptile does not possess any fenestra in its skull. The Professor suggests that the anapsida were primitive and an evolutionary dead-end or "waste-basket". This is definitely not the case. Living examples of anapsid reptiles are the turtles, tortoises and terrapins.
To complicate matters even further, there was also a euryapsid condition with a single opening equivalent to the upper temporal fenestra of the diapsids. Examples of extinct reptiles with euryapsid skulls were the plesiosaurs and ichthyosaurs. As far as we know, there are no living examples. Likewise, as far as we know, there are no living examples of reptiles with synapsid skulls but that is not to say that they didn't exist.
Furthermore, in mammals, the temporal fenestra has been drastically modified (for an overview, see here). While the location of the fenestra is still visible in the mammalian skull, it is no longer an opening.
So what makes a reptile a reptile? If the decision is just based on the presence or absence of one or two skull fenestra, we have a variety of options; there are living and extinct reptiles that possess none, one or two. If it is based on the relative proportions of the dentary and post-dentary bones in the lower jaw, we also have a variety of options. Non-mammalian synapsids were represented by carnivorous and herbivorous species as were the dinosaurs. So why are pelycosaurs, for example, not reptiles? The answer to this problem seems to be the absolute necessity to identify mammalian ancestry within a Darwinian framework.