Getting to grips with this topic – the origins of the group that now dominates the vertebrate land fauna – involves a few basic facts of anatomy and some strange names for animals long extinct. We’ll try to keep the discussion simple, but bear in mind that the history of life, although fascinating, is not simple! In essence, the amazing transformation of the jaw of some reptile lineages into a mammalian-type ear is well documented, and supports the view that some reptiles evolved into mammals. The progression was unidirectional, multifaceted, and seems to have been genetically orchestrated. However, since these lineages went extinct, it is not clear that modern-day mammals evolved from reptiles.
Reptiles are cold-blooded animals: they depend on the sun for their body heat. Their legs project from the sides of their bodies (if they have legs) and their skulls have two openings, called ‘fenestrae’, behind each eye socket. In contrast to mammals, the lower jaw is made up of several bones, of which the hindmost, the articular, connects with a skull bone called the quadrate. Reptiles hear by detecting vibrations both in the air and in the ground. From the ground, vibrations reach the middle ear via the quadrate bone; from the air, vibrations arrive via the eardrum. Legless lizards and snakes have lost the eardrum of their ancestors, so they hear only through the quadrate. The middle ear has just one bone, called the stapes, or stirrup. Another difference is that reptile teeth are all cone-shaped.
Mammals are warm-blooded animals: they generate their own body heat, which they control primarily by insulation (hair and body fat) and perspiration (sweat glands). The legs issue from beneath the body and the skull has one pair of fused arches or bars under which the jaw muscles pass up to the back of the head. The lower jaw is a single bone called the dentary, articulating with a bone in the skull called the squamosal. The middle ear contains three bones, the familiar hammer, anvil and stirrup, and is more sensitive to sound than the ear of reptiles, especially at higher frequencies. On the other hand, there is no ability to detect ground-borne vibrations. The teeth have a variety of shapes – incisors, canines and molars.
Most features that distinguish mammals, such as hair, mammary glands and reproductive organs, do not readily fossilise. Among those that do are teeth (any animal name with ‘-don’ or ‘-dont’ at the end is referring to the teeth) and skull structure. The common possession of features such as hair, mammary glands, a single dentary and mammalian teeth could indicate common descent. However, a hypothetical animal that had mammary glands and, say, a reptilian jaw might also be interpreted in accordance with this view, on the basis that it evolved before the first true mammal, either along the direct line to mammals or along a side branch. An evolutionary scenario can be devised for any eventuality. Thus the echidna and the platypus – mammals in most respects but with the reptilian characteristic that their urinary, defecatory and reproductive systems end in a single duct – are interpreted as stemming from an offshoot somewhere between ‘mammaliaforms’ and true mammals. Pterodactyls, reptiles in every respect but their hair, are assumed to have acquired hair independently. Some skinks give birth to live young after nourishing them in a womb, through placentas – organs that are otherwise characteristic of mammals. All such instances challenge the assumption of ultimate common descent.
Although the number of temporal fenestrae is considered to be fundamental to the respective evolutionary groups, fossils show them appearing abruptly. Their main purpose was to provide anchorage for certain jaw muscles, and a change in the number, position, shape or size of the fenestrae entailed co-ordinated changes in musculature and skull design. Animals with one pair are termed synapsids, those with two, diapsids. Whereas all modern reptiles apart from turtles are diapsids, ancient ‘reptiles’ showed a variety of arrangements. Rather awkwardly for evolution theory, the reptiles from which mammals are supposed to have descended were synapsids, not diapsids. Modern mammals (including humans) have no obvious fenestrae at all – an indication that they do not descend from synapsid reptiles.
Once a synapsid, it seems, always a synapsid. There are no documented cases of a synapsid evolving a second pair of temporal fenestrae. Back in time, the synapsids are presumed to have evolved from tetrapods without fenestrae (anapsids). This transition is also undocumented. The earliest known anapsid is Hylonomus, from the mid Carboniferous site of Joggins, Nova Scotia. The oldest known synapsid is the pelycosaur Archaeothyris, only slightly younger than the earliest anapsid. The oldest diapsid is Petrolacosaurus, from the Upper Carboniferous. Since there are no intermediates linking these different skull designs, the fossil record suggests that the three groups anapsids, synapsids and diapsids had independent origins.
Towards mammal-like reptiles
According to present thinking, mammals evolved from an extinct group of ‘mammal-like’ reptiles called the therapsids, and the therapsids from a family of pelycosaurs called the sphenacodonts. Pelycosaurs, of which sphenacodonts were surprisingly early representatives, first appeared in the late Carboniferous. If you have a mental picture of a pelycosaur, it is probably of a large sail-backed animal (as illustrated below). However, the earliest pelycosaurs did not have a sail, and since the innovation arose in two separate lineages within the group, it seems likely that these remarkable excrescences were already present in the ancestral genome and were activated during development by a genetic switch. Be that as it may, therapsids first appeared in the mid Permian, and if they originated from sphenacodonts, they must have done so, at the latest, by the end of the Carboniferous (Reisz & Laurin 2004). A substantial time gap separates the two groups. There is also a substantial morphological gap, amounting to a ‘major remodelling of the global tetrapod fauna’ (Lucas 2004).
Therapsids are distinguished from pelycosaurs by:
- the absence of several skull elements
- modifications of the shoulder and pelvic girdles, associated with a more upright hindlimb posture
- larger temporal fenestrae, providing a larger area of origination for jaw adductor muscles
- larger canines and a correspondingly expanded lower jaw bone, with reduced palatal teeth
Therapsids also possessed heavy skeletons with short stout limbs, broad flat feet, a short tail, massive skull, and almost no neck. In comparison with some pelycosaurs they were lumbering animals, though the carnivorous species were smaller and had a lighter build.
Pelycosaurs were already diverse when they first appeared, indicating that they had undergone significant evolution before they made an impact on the fossil record. They inhabited what were then equatorial regions (present Europe and North America). Therapsids, by contrast, occurred mostly in the higher-latitude regions of each hemisphere (Russia and South Africa). They too show a high degree of diversity early in their history. The mountainous equatorial belt left no fossil record, but the faunas of these previously separated hemispheres, north and south, were similar. The ice caps were now melting and the interior of the supercontinent was warming. By the late Permian a few pelycosaurs were themselves beginning to migrate to more temperate climes, scratching a living alongside the therapsids. Their dwindling species and individual numbers show they were struggling, and soon afterwards pelycosaurs went extinct, victims of the events that caused mass extinctions in the late Permian across a wide range of groups. Therapsids were among the few that survived.
|Late Carboniferous (318-299 Ma)||varanopsids, ophiacodonts, sphenacodonts, edaphosaurs|
|Early Permian (299-284 Ma)||varanopsids, ophiacodonts, sphenacodonts, edaphosaurs, caseids|
|Early Permian (284-270 Ma)||varanopsids, ophiacodonts, sphenacodonts, caseids|
|Mid Permian (270-260 Ma)||varanopsids, ophiacodonts, sphenacodonts, caseids||biarmosuchians, dinocephalians, anomodonts, gorgonopsians, therocephalians|
|Late Permian (260-251 Ma)||varanopsids, caseids||biarmosuchians, anomodonts, gorgonopsians, therocephalians, cynodonts|
|Early Triassic (251-245 Ma)||anomodonts, therocephalians, cynodonts|
Therapsids are ranked as an order, with six suborders: biarmosuchians, dinocephalians, anomodonts, gorgonopsians, therocephalians, and cynodonts. Analysis of their degrees of similarity reveals clear time-progressive evolutionary patterns within the suborders. By the end of the Permian three of the six were extinct and by the end of the Triassic five were; they failed to evolve further and failed to live on unchanged. Cynodonts continued into the Jurassic. They too went extinct except insofar as one branch might have evolved into mammals whose descendants included the 19 or so orders of modern mammal. Thus the question splits into two parts: (1) did cynodonts evolve into mammals, and (2) can today’s mammals be traced back to the cynodonts?
Did cynodonts evolve into mammals?
The earliest therapsids had a typically reptilian jaw joint, where the articular in the jaw con- nected with the quadrate in the skull. During the Triassic these bones decreased in size, as the dentary jaw-bone and squamosal skull-bone became larger, moved closer together and replaced the articular-quadrate joint – thereby approaching the mammalian body plan. This was a remarkable development, but only the cynodonts showed a consistent trend of dentary enlargement; other therapsids retained their ancestral proportions (Sidor 2003). Anomodonts showed the opposite trend: decreasing dentary size and increasing size of the postdentary bones.
In some cynodonts the jaw eventually had a double hinge, articulating with the squamosal as well as the quadrate. They also had features typical of mammals, such as an array of incisor, canine and postcanine teeth, a double occipital condyle (where the skull articulated with the spine), and a secondary palate. On the other hand, a double occipital condyle is not unique to mammals; it also occurs in the extinct microsaurs and modern amphibians. The secondary palate, as in mammals, served to separate the airway from the food-processing system, and a series of fossils shows this palate evolving as initially separate plates became sutured together along the midline. But here too the situation is more complicated than fits a Darwinian world, since a secondary palate arose independently in two other therapsid lineages, the anomodonts and therocephalians (Sidor 2003). These did not evolve into mammals.
The Late Triassic/Early Jurassic Morganucodon (‘Glamorgan tooth’, named after its find locality in south Wales) was a shrew-sized insectivore. Only the skull is well preserved, but we can hazard some assessment of whether it is related to cynodonts from the skeleton of other members of the morganucodont family. The groups are not strikingly similar. For example, the neck vertebrae of morganucodonts was essentially mammalian, they lacked lumbar ribs, the brain was comparatively large and the femur had a ball-like head which fit into the pelvis sideways, indicating a gait that was fully erect. There is also a chronological difficulty in linking the groups, since the cynodonts closest in form to the morganucodonts – either the tritylodonts or the tritheledonts (opinions differ) – appear at the same time as their presumed descendants. They cannot therefore have been directly ancestral to morganucodonts, though their own direct ancestors may have been. In either case, the cynodonts that continued the trend of increasingly mammal-like features without directly giving rise to mammals provide a strong hint that the evolution was pre-programmed. As with the secondary palate, the same characteristics were developing independently in multiple lineages. The fossils show a pattern of precisely co-ordinated, biologically complementary changes, not a random zigzag.
On balance, it would not be unreasonable to conclude that the morganucodonts did descend from the cynodonts. While their forms are discontinuous, this has to be evaluated in a context where the putative ancestral group (the cynodonts) itself encompassed a high degree of diversity. The same applies in relation to size, which can vary greatly within a genealogically united group. Morganucodonts were tiny, but some tritylodonts were also quite small. Morganucodonts and cynodonts had a similar pectoral girdle. Morganucodon also had the double jaw joint of some advanced cynodonts, but now the dentary-squamosal hinge took most of the stresses associated with biting and chewing, leaving the tiny articular-quadrate hinge free to function as a sound-conductor. It still had a composite jaw, and its cochlea was straight rather than coiled as in modern mammals, but the dentary was much enlarged. Its teeth were also characteristically mammalian.
Can today’s mammals be traced back to the cynodonts?
The most advanced mammaliaform so far known is Hadrocodium (Luo et al 2001), from the Early Jurassic. With an estimated body weight of 2 grams, it is the smallest known from the Mesozoic, though it had a very large brain for its size. It is also the earliest animal to have had a single jaw joint, as in triconodonts and present-day mammals: the middle ear was now completely separate from the mandible. This is surprisingly early, for the next animal to show this feature, Triconodon itself, was not to arise for another ‘45 million years’. Differing from its predecessors also in the lack of a postdentary trough, Hadrocodium is an enigma; it would be rash to assume that it evolved from the cynodonts.
Morganucodonts were the end of a line (Luo 2007). As with the pelycosaurs and the cynodonts, one has to take several steps back in time in order to be at an evolutionary stage where a plausible ancestor might yet be found. Not to prolong what is already a complicated discussion, suffice to say that when today’s mammal orders appeared, in the Cenozoic, they appeared suddenly, without obvious forbears. As summarised in the diagram, the numerous orders and subclasses that arose, about the same time, in the Middle Jurassic did not survive to the present day. None seem to have been ancestral to modern mammals.
Moreover, mammals were more disparate in the Mesozoic, near the presumed beginning of their evolutionary history, than they are now – certainly in terms of tooth design (regarded, like the temporal fenestrae, as a fundamental marker). As can be seen from the terminal width of the spindles representing marsupials and placentals, the number of present-day families and orders is very great, but the number of higher-level groups is much smaller. In the early Cretaceous there were nine such groups; today there are only three.
In taxonomic terms, mammals are a class, and the three modern groups of mammals are subclasses, comprising around 19 orders. Though they may be less disparate than their Mesozoic counterparts, these three subclasses are still extremely heterogeneous, so much so that, if we assume they are related, we encounter just the converse problem to the disparity in the Mesozoic. Because the Cenozoic orders include living animals, we are able to analyse their DNA and quantify the extent to which the DNA of one species differs from another. Thus, assuming that all the Cenozoic orders go back to a common ancestor, we can infer the rates at which their DNA diverged over time. These lead to the expectation that the orders must have been preceded by long evolutionary branches. This is not, however, what the fossil record reveals:
Both fossil and extant taxa demonstrate that there are few or no such lineages with a long evolutionary lag time. This discrepancy is so systemic and widespread that it cannot be explained by the difference between minimum age constraint (represented by actual fossils) and the timing of origin that can be hypothetically estimated by molecules [DNA mutation rates] in marsupial and placental evolution.
Zhe-Xi Luo, Nature 450:1012 (2007)
Nor can the discrepancy be dismissed as due to the incompleteness of the fossil record. The number of Mesozoic mammalian and mammaliaform genera known to science has tripled in the last thirty years, but the most persistent gaps continue to be those around the base of the Cenozoic groups and those surrounding the marsupial and placental subclasses as a whole.
In short, today’s mammals cannot be traced back to the cynodonts. Impressive – indeed, wonderful – though the series is that shows reptiles evolving into mammaliaforms, it does not validate the dogma that all organisms compose a single evolutionary tree.
Evidence of genetic control
The ‘rise of mammals’ in the fossil record is a striking phenomenon. No mammals are known from the Palaeozoic. Apart from amphibians, all the tetrapods that flourished at that time were reptiles. One branch of synapsid reptiles, the cynodonts, became progressively more mammal-like, and possibly one branch of cynodonts evolved into morganucodonts, which were even more mammal-like. The Late Jurassic saw the radiation of several groups which may reasonably be called mammals, but their origin is obscure, and apart from the monotremes – represented only by the echidna and the platypus – none of them survived to the present day. The Cretaceous saw the radiation of the marsupials and placentals, the latter diversifying spectacularly in the Cenozoic.
We can draw the following conclusions:
- Some of the evolution we see is large-scale. Hearing systems change from those designed to pick up ground as well as air-borne vibrations to those designed to pick up primarily air-borne vibrations. They become less sensitive to ground vibrations and more sensitive to high-frequency sound. The same animals also acquire a more upright gait and various other progressively more mammal-like modifications.
- The evolution appears to be ‘directed’. Complex changes to the lower jaw and associated soft body parts (muscles, internal ear organisation) and concomitant changes in the post-cranial skeleton and tissues appear to be orchestrated towards a pre-determined end.
- Not all reptiles evolved in this direction. No modern-day group of reptiles did, nor did most ancient reptiles. Even among the therapsids, all but one of the six suborders retained their ancestral proportions. Anomodonts showed an opposite trend of decreasing dentary size and increasing post-dentaries.
Natural selection acting upon chance mutations therefore does not seem the power at work. As, in the vast majority of cases, selection did not result in reptiles becoming more mammal-like, one might question whether it was the mechanism at all. Furthermore, ‘there is a paradox when matching an evolutionary mechanism based on single, small changes in discrete characters to a long term, large evolutionary change in very many, fully integrated characters.’ (Kemp p. 133) Darwinian theory postulates single, small, random changes; what we see is synchronous, inter-related and inter-dependent changes, affecting the whole organism. Darwinism cannot account for the evolution, paradoxically, because the scale of it is too great, not too small.
Concerted interrelated changes of the phenotype, reflecting changes in hugely complex genetic systems, are best viewed as the result of those systems having been pre-programmed to change. This is supported by what is arguably the most devastating of evidences against the Darwinian hypothesis, the phenomenon of convergence. Convergence is where the same feature occurs in two or more related lineages whose common ancestor did not have that feature. How, one asks, can the same biological structure arise through a process of random mutation more than once?
Here are a number of examples (some of which have already been mentioned). In relation to developments before the therapsids:
- Lathanosuchid reptiles had features characteristic of early anapsids, except that they had a pair of lower temporal fenestrae. Thus either their ‘anapsid’ characteristics evolved independently of true anapsids or their synapsid-like fenestrae evolved independently of synapsids. Similar anomalies sabotage attempts to fit the late Permian millerettids into a neat scheme where anapsid tetrapods in the Carboniferous branched into synapsids and diapsids.
- By contrast, captorhinids and protorothyridids had no temporal fenestrae but in most other supposedly fundamental respects were similar to diapsids.
- Accompanying the full range of fenestral arrangements that were present soon after the first appearance of terrestrial animals there appeared a bewilderingly diverse array of tetrapod body designs. Some tetrapods propelled themselves by lateral undulation of the vertebral column, later forms, increasingly, by a combination of lateral undulation and limb-driven locomotion. The latter arose independently within several groups (Rieppel & Reisz 1999). There were also convergences in respect of skull roof pattern, the mandible, the axial skeleton and limb design (ibid).
As regards the therapsids:
- Phalanges are the bones that form the fingers and toes, with the ‘phalangeal formula’ being the number of such bones in each appendage counting from the first to the fifth digit. Ideally, reptiles have the formula 2-3-4-5-4, mammals 2-3-3-3-3. In therapsids the formula varied, and in a manner that was ‘extremely complex’ (Rubidge & Sidor 2001). Appearing multiple times in the course of their history, the mammalian phalangeal formula has proved resistant to tracing evolutionary relationships.
- A bony secondary palate evolved in therapsids independently three times, in dicynodonts, therocephalians and cynodonts, each time in a different way (Sidor 2003b).
- The specialised ‘leaf-shaped’ teeth of the anomodont Suminia arose independently in at least five lineages of herbivores: iguanid lizards, ornithischian and prosauropod dinosaurs, pareiasaurs and caseid pelycosaurs (Rybczynski & Reisz 2001).
- Propaliny, the ability of the upper jaw to slide backwards and forwards over the lower jaw, arose ‘perhaps as many as seven times’ within non-mammalian synapsids (ibid).
- Trithylodonts and tritheledonts had different combinations of mammalian and non-mammalian characters. Since they cannot both have been ancestral to mammals, some of their mammalian characters must have arisen independently (Kemp p 76).
- The double occipital condyle, while distinctive of mammals, is also found in modern amphibians and the extinct microsaurs.
Even the mammalian middle ear (MME) had more than one origin:
- The middle ear of the recently discovered triconodont Yanoconodon (Luo et al 2007), classified as a true mammal, surprisingly shows the ‘pre-mammalian’ condition where the middle ear bones were still connected to the mandible. Thus, either the MME structure was present in the common ancestor of monotremes, triconodonts, marsupials and placentals, and triconodonts ‘re-evolved’ the more primitive condition, or the MME was absent in the common ancestor and evolved separately in monotremes, marsupials and placentals.
- The same arrangement whereby sound is transmitted to the inner ear via an eardrum, stapes and other cartilaginous and ossified structures arose independently in frogs, squamates, crocodiles, birds and turtles (Müller & Tsuji 2007).
- A different arrangement whereby sound was transmitted to the inner ear via an eardrum, stapes and other cartilaginous structures arose as early as the Permian in the reptile Macroleter (ibid).
And so the story goes on, convergence after convergence:
- Castorocauda was a Middle Jurassic docodont with a broad, scaly tail for swimming, just like that of the modern but unrelated beaver. It is also, incidentally, the oldest fossil mammaliaform with preserved fur.
- Volaticotherium, representing another previously unknown mammal order from the Middle Jurassic, had the membrane and elongate limbs of a glider, convergent to today’s placental ‘flying’ squirrels and marsupial sugar gliders. Gliding arose no fewer than seven times amongst the mammals, Volaticotherium being an eighth such instance (Meng et al 2006).
- Haldanodon, a docodont from the Late Jurassic, possessed many of the specialisms characteristic of modern, but unrelated, semi-aquatic moles (desmans).
- Fruitafossor, an enigmatic mammal from the Late Jurassic, perfectly imitates two extreme specialisations of teeth and jaw that previously were thought to be unique to the South American xenarthrans (anteaters, armadillos and sloths).
These examples are not an exhaustive compendium, and any one of them would be grounds for questioning the belief that chance mutations drove macroevolution. In total they may be considered a devastating refutation of the idea.
This article is part of a series discussing the prime fossil evidence behind the belief that fish evolved into human beings. Such evidence is supposed to include the transition from reptiles to mammals via mammal-like reptiles. The relevant fossils, however, show the following:
- The reptiles involved in this alleged transition were synapsids and thus unlike modern reptiles, which are diapsids.
- There are no documented transitions across the anapsid/synapsid/diapsid boundaries.
- It is possible, but not likely on present evidence, that one branch of early reptile, the pelycosaurs, evolved into mammal-like reptiles.
- There was no general trend among reptiles to become more mammal-like (hence, obviously, there are still many kinds of reptile today). Even among the six orders of therapsids, only one – the cynodonts – became progressively more mammal-like. Most were fairly stable in the relevant characters, while the anomodonts showed a progression away from the mammalian state.
- It seems likely that the cynodonts were ancestral to the morganucodonts, representing the next mammal-like grade on from the cynodonts, although it is not clear precisely which group of cynodonts continued in this direction.
- The morganucodonts were not the ancestors of modern mammals.
- No Mesozoic group can be identified as the ancestors of modern mammals.
- Numerous ‘convergences’ confound all attempts to link reptiles and mammals into a single evolutionary tree.
We will consider how the same developments can be understood within a recolonisation scenario in a separate article.
Evolution in the genome
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