Evolution of mammals

Restoration of Thrinaxodon, a member of the cynodont group which includes the ancestors of mammals.
Further information: Evolutionary history of life

The evolution of mammals from synapsids (mammal-like "reptiles") was a gradual process which took approximately 70 million years, beginning in the mid-Permian. By the mid-Triassic, there were many species that looked like mammals, and the first true mammals appeared in the early Jurassic. The earliest known marsupial, Sinodelphys, appeared 125 million years ago in the early Cretaceous, around the same time as Eomaia, the first known eutherian (member of placentals' "parent" group); and the earliest known monotreme, Teinolophos, appeared two million years later. After the Cretaceous-Tertiary extinction wiped out the non-avian dinosaurs (birds are generally regarded as the surviving dinosaurs) and several other mammalian groups, placental and marsupial mammals diversified into many new forms and ecological niches throughout the Tertiary, by the end of which all modern orders had appeared.

From the point of view of phylogenetic nomenclature, mammals are the only surviving synapsids. The synapsid lineage became distinct from the sauropsid ("reptile") lineage in the late Carboniferous period, between 320 and 315 million years ago,[1] and were the most common and largest land vertebrates of the Permian period.[2] But in the Triassic period a previously obscure group of sauropsids, the archosaurs, became the dominant vertebrates and one archosaur group, the dinosaurs, dominated the rest of the Mesozoic era. These changes forced the Mesozoic mammaliforms ("nearly mammals") into nocturnal niches, and may have contributed greatly to the development of mammalian traits such as endothermy, hair and a large brain. Later in the Mesozoic mammals spread into other ecological niches, for example aquatic, gliding and even preying on dinosaurs.

Most of the evidence consists of fossils. For many years fossils of Mesozoic mammals and their immediate ancestors were very rare and fragmentary, but since the mid 1990s there have been many important new finds, especially in China. The relatively new techniques of molecular phylogenetics have also shed light on some aspects of mammalian evolution by estimating the timing of important divergence points for modern species. When used carefully, these techniques often, but not always, agree with the fossil record.

Although mammary glands are the signature feature of modern mammals, little is known about the evolution of lactation, and virtually nothing is known about the evolution of another distinctive feature, the neocortex region of the brain. Most study of the evolution of mammals centers around the development of the middle ear bones from components of the ancestral amniote jaw joint. Other much-studied aspects include the evolution of erect limb posture, a bony secondary palate, fur and hair, and warm-bloodedness.

Contents

Definition of "mammal"

Living mammal species can be identified by the presence in females of mammary glands which produce milk.

Mammalian and non-mammalian jaws. In the mammal configuration, the quadrate and articular bones are much smaller and form part of the middle ear. Note that in mammals the lower jaw consists of only the dentary bone.

Other features are required when classifying fossils, since mammary glands and other soft-tissue features are not visible in fossils. Paleontologists therefore use a distinguishing feature that is shared by all living mammals (including monotremes) but is not present in any of the early Triassic therapsids ("mammal-like reptiles"): Mammals use two bones for hearing that all other amniotes use for eating. The earliest amniotes had a jaw joint composed of the articular (a small bone at the back of the lower jaw) and the quadrate (a small bone at the back of the upper jaw). All non-mammalian amniotes use this system including lizards, crocodilians, dinosaurs (and their descendants the birds), and therapsids. But mammals have a different jaw joint, composed only of the dentary (the lower jaw bone which carries the teeth) and the squamosal (another small skull bone). And in mammals the quadrate and articular bones have become the incus and malleus bones in the middle ear.[3][4]

Mammals also have a double occipital condyle; they have two knobs at the base of the skull which fit into the topmost neck vertebra, and other vertebrates have a single occipital condyle.[3] But paleontologists use only the jaw joint and middle ear as criteria for identifying fossil mammals, as it would be confusing if they found a fossil that had one feature but not the other (e.g. a mammalian jaw and ear but a non-mammalian single occipital condyle).

Due to the incremental changes in transitional fossils, it has been said

We may again ask the question, What is a mammal? Where we draw the line between reptile and mammal has no biological significance. It is purely a matter of convenience. There are two obvious choices, both immediately following a period of rapid evolution that make as definite a break as we can hope to find.[5]

The ancestry of mammals

Here is a very simplified "family tree" - the text below describes some of the uncertainties and areas of debate.

Tetrapods
      |
      +-- Amphibians 
      |
      `--Amniotes
             |
             +-Sauropsids
             |
             `-Synapsids
                    |
                    `-Pelycosaurs
                           |
                           `-Therapsids
                                  |
                                  `-Mammals

Amniotes

The first fully terrestrial vertebrates were amniotes - their eggs had internal membranes which allowed the developing embryo to breathe but kept water in. This allowed amniotes to lay eggs on dry land, while amphibians generally need to lay their eggs in water (a few amphibians, such as the Surinam toad, have evolved other ways of getting round this limitation). The first amniotes apparently arose in the late Carboniferous from the ancestral reptiliomorphs.

Within a few million years two important amniote lineages became distinct: mammals' synapsid ancestors and the sauropsids, from which lizards, snakes, crocodilians, dinosaurs and birds are descended.[1] The earliest known fossils of all these groups date from about 320 to 315M years ago. Unfortunately it is difficult to be sure about when each of them evolved, since vertebrate fossils from the late Carboniferous are very rare, and therefore the actual first occurrences of each of these types of animal might have been considerably earlier.[6]

Synapsids

The original synapsid skull structure has one hole behind each eye, in a fairly low position on the skull (lower right in this image).

Synapsid skulls are identified by the distinctive pattern of the holes behind each eye, which served the following purposes:

Early Permian terrestrial fossils indicate that one synapsid group, the pelycosaurs, were the most common land vertebrates of their time and included the largest land animals of the time.[2]

Therapsids

Therapsids descended from pelycosaurs in the middle Permian and took over their position as the dominant land vertebrates. They differ from pelycosaurs in several features of the skull and jaws, including larger temporal fenestrae and incisors which are equal in size.[7]

The therapsids went through a series of stages, beginning with animals which were very like their pelycosaur ancestors and ending with some which could easily be mistaken for mammals:[8]

Therapsid family tree

(simplified from [7]; only those which are most relevant to the evolution of mammals are described below)

Therapsids
  | 
  +--Biarmosuchia
  |
  `--+--Dinocephalia
     |
     +--Neotherapsida
          |
          +--Anomodonts
          |      |
          |      `--Dicynodonts
          |
          `--+--Theriodontia
                    |
                    +--Gorgonopsia
                    |
                    `--+--Therocephalia
                       | 
                       `--Cynodontia
                              .
                              . . . (Mammals, eventually)

Only the dicynodonts, therocephalians and cynodonts survived into the Triassic.

Biarmosuchia

The Biarmosuchia were the most primitive and pelycosaur-like of the therapsids.

Dinocephalians

Dinocephalians ("terrible heads") were large, some as large as a rhinoceros, and included both carnivores and herbivores. Some of the carnivores had semi-erect hindlimbs, but all dinocephalians had sprawling forelimbs. In many ways they were very primitive therapsids, for example they had no secondary palate and their jaws were rather "reptilian".[10]

Theriodonts

The theriodonts ("beast teeth") and their descendants had jaw joints in which the lower jaw's articular bone tightly gripped the skull's very small quadrate bone. This allowed a much wider gape, and one group, the carnivorous gorgonopsians ("gorgon faces"), took advantage of this to develop "sabre teeth". But the theriodont's jaw hinge had a longer term significance - the much reduced size of the quadrate bone was an important step in the development of the mammalian jaw joint and middle ear.

The gorgonopsians still had some primitive features: no bony secondary palate (but other bones in the right places to perform the same functions); sprawling forelimbs; hindlimbs which could operate in both sprawling and erect postures. But the therocephalians ("beast heads"), which appear to have arisen at about the same time as the gorgonopsians, had additional mammal-like features, e.g. their finger and toe bones had the same number of phalanges (segments) as in early mammals (and the same number that primates have, including humans).[11]

Cynodonts

The cynodonts, a theriodont group which also arose in the late Permian, include the ancestors of all mammals - one sub-group, the trithelodonts, is widely regarded as the most likely to contain mammals' ancestor. Cynodonts' mammal-like features include: further reduction in the number of bones in the lower jaw; a secondary bony palate; cheek teeth with a complex pattern in the crowns; the brain filled the endocranial cavity.[12]

Multi-chambered burrows have been found, containing as many as 20 skeletons of the Early Triassic cynodont Trirachodon; the animals are thought to been drowned by a flash flood. The complex, shared burrows indicate that these animals were capable of complex social behaviors.[13]

Triassic takeover

The catastrophic Permian-Triassic mass extinction killed off about 70 percent of terrestrial vertebrate species, and the majority of land plants. As a result:[14]

But the cynodonts lost out to a previously obscure group of sauropsids, the archosaurs (which include the ancestors of crocodilians, dinosaurs and birds). This reversal of fortunes is often called the "Triassic takeover". Several explanations have been offered for it, but the most likely is that the early Triassic was predominantly arid and therefore archosaurs' superior water conservation gave them a decisive advantage (all known sauropsids have glandless skins and excrete uric acid, which requires less water to keep it sufficiently liquid than the urea which mammals excrete and presumably therapsids excreted).[15][8] The Triassic takeover was gradual - in the earliest part of the Triassic cynodonts were the main predators and lystrosaurs were the main herbivores, but by the mid-Triassic archosaurs dominated all the large carnivore and herbivore niches.

But the Triassic takeover may have been a vital factor in the evolution of cynodonts into mammals. The cynodonts' descendants were only able to survive as small, mainly nocturnal insectivores.[12] As a result:

From cynodonts to true mammals

Many uncertainties

While the Triassic takeover probably accelerated the evolution of mammals, it made life more difficult for paleontologists because good fossils of the nearly-mammals are extremely rare, mainly because they were mostly smaller than rats:

In fact it was said as recently as the 1980s that all the Mesozoic fossils of mammals and near-mammals could be contained in a few shoeboxes - and they were mostly teeth, which are the most durable of all tissues.[20] Since then, the number of Mesozoic fossil mammals has increased, from 116 genera known in 1979 to about 310 in 2007, with an increase in quality such that "at least 18 Mesozoic mammals are represented by nearly complete skeletons".[21]

As a result:

So the evolution of mammals in the Mesozoic is full of uncertainties, although there is no room for doubt that true mammals did first appear in the Mesozoic.

Mammals or mammaliformes?

One result of these uncertainties has been a change in the paleontologists' definition of "mammal". For a long time a fossil was considered a mammal if it met the jaw-ear criterion (the jaw joint consists only of the squamosal and dentary; and the articular and the quadrate bones have become the middle ear's malleus and incus). But more recently paleontologists have usually defined "mammal" as the last common ancestor of monotremes, marsupials and placentals and all of its descendants. So they had to define another clade mammaliformes to accommodate all the animals which are more mammal-like than cynodonts but less closely related to monotremes, marsupials and placentals.[22] Although this now appears to be the majority approach, some paleontologists have resisted it because: it simply moves most of the problems into the new clade without solving them; the clade mammaliformes includes some animals with "mammalian" jaw joints and some with "reptilian" (articular-to-quadrate) jaw joints; and the newer definition of "mammal" and "mammaliformes" depend on last common ancestors of both groups which have not yet been found.[20] Despite these objections, this article follows the majority approach and treats most of the cynodonts' Mesozoic descendants as mammaliformes.

Family tree - cynodonts to mammals

(based on Mammaliformes - Palaeos)

--Cynodonts
    |
    `--Mammaliformes
         |
         +--Allotheria
         |    |
         |    `--Multituberculates
         |
         `--+--Morganucodontidae
            |
            `--+--Docodonta
               |
               `--+--Hadrocodium
                  |
                  `--Symmetrodonta
                       |
                       |--Kuehneotheriidae
                       |
                       `--Mammals

Multituberculates

Skull of the multituberculate Ptilodus

Multituberculates (named for the multiple tubercles on their "molars") are often called the "rodents of the Mesozoic" but this is an example of convergent evolution rather than meaning that they are closely related to the Rodentia. At first sight they look like mammals: their jaw joints consists of only the dentary and squamosal bones, and the quadrate and articular bones are part of the middle ear; their teeth are differentiated, occlude and have mammal-like cusps; they have a zygomatic arch; the structure of the pelvis suggests that they gave birth to tiny helpless young, like modern marsupials. And they lived for over 120 million years (from mid Jurassic, about 160M years ago, to early Oligocene, about 35M years ago), which would have made them the most successful mammals ever. But a closer look shows that they are very different from modern mammals:[22]

Morganucodontidae and other transitional forms had both types of jaw joint: dentary-squamosal (front) and articular-quadrate (rear).

Morganucodontidae

The Morganucodontidae first appeared in the late Triassic, about 205M years ago. They are an excellent example of transitional fossils, since they have both the dentary-squamosal and articular-quadrate jaw joints.[23] They were also one of the first discovered and most thoroughly studied of the mammaliformes, since an unusually large number of morganucodont fossils have been found.

Docodonts

Reconstruction of Castorocauda. Note the fur and the adaptations for swimming (broad, flat tail; webbed feet) and for digging (robust limbs and claws).

The most notable member of the docodonts is Castorocauda ("beaver tail"), which lived in the mid Jurassic about 164M years ago and was first discovered in 2004 and described in 2006. Castorocauda was not a typical docodont (most were omnivores) and not a true mammal, but it is extremely important in the study of the evolution of mammals because the first find was an almost complete skeleton (a real luxury in paleontology) and it breaks the "small nocturnal insectivore" stereotype:[24]

Hadrocodium

Hadrocodium skull. The jaw joint is fully mammalian (squamosal-dentary only) and farther forward than in earlier transitional forms.

The consensus family tree above shows Hadrocodium as an "aunt" of true mammals, while symmetrodonts and kuehneotheriids are more closely related to true mammals. But fossils of symmetrodonts and kuehneotheriids are so few and fragmentary that they are poorly understood and may be paraphyletic.[25] On the other hand there are good fossils of Hadrocodium (about 195M years ago in the very early Jurassic) and they have some important features: [26]

The earliest true mammals

This part of the story introduces new complications, since true mammals are the only group which still has living members:

Family tree of early true mammals

(based on Mammalia: Overview - Palaeos; X marks extinct groups)

--Mammals
    |
    +--Australosphenida
    |    |
    |    +--Ausktribosphenidae X
    |    |
    |    `--Monotremes
    |
    `--+--Triconodonta X
       |
       `--+--Spalacotheroidea X
          |
          `--Cladotheria
               |
               |--Dryolestoidea X
               |
               `--Theria
                    |
                    +--Metatheria
                    |
                    `--Eutheria

Australosphenida and Ausktribosphenidae

Ausktribosphenidae is a group name that has been given to some rather puzzling finds which:[27]

Australosphenida is a group which has been defined in order to include the Ausktribosphenidae and monotremes. Asfaltomylos (mid- to late Jurassic, from Patagonia) has been interpreted as a basal australosphenid (animal which: has features shared with both Ausktribosphenidae and monotremes; lacks features which are peculiar to Ausktribosphenidae or monotremes; also lacks features which are absent in Ausktribosphenidae and monotremes) and as showing that australosphenids were wide-spread throughout Gondwanaland (the old Southern hemisphere super-continent).[29]

But recent analysis of Teinolophos suggests Teinolophos (about 115M years ago) was a "crown group" (advanced and relatively specialised) monotreme, so the basal (most primitive) monotremes must have appeared considerably earlier; that some alleged Australosphenids were also "crown group" monotremes (e.g. Steropodon); and that other alleged Australosphenids (e.g. Ausktribosphenos, Bishops, Ambondro, Asfaltomylos) are therefore more closely related to and possibly members of the Therian mammals (group that includes marsupials and placentals, see below).[30]

Monotremes

The earliest known monotreme is Teinolophos, which lived about 123M years ago in Australia. Recent analysis suggest that it was not a basal (primitive, ancestral) monotreme but a full-fledged platypus, and therefore that the platypus and echidna lineages diverged considerably earlier and that basal monotremes were even earlier.[30]

Monotremes have some features which may be inherited from the original amniotes:

Unlike in other mammals, female monotremes do not have nipples and feed their young by "sweating" milk from patches on their bellies.

Of course these features are not visible in fossils, and the main characteristics from paleontologists' point of view are:[27]

Theria

Theria ("beasts") is a name applied to the hypothetical group from which both metatheria (which include marsupials) and eutheria (which include placentals) descended. Although no convincing fossils of basal therians have been found (just a few teeth and jaw fragments), metatheria and eutheria share some features which one would expect to have been inherited from a common ancestral group:[32]

Therian form of crurotarsal ankle. Adapted with permission from Palaeos

Tribosphenic molars have been found in fossils from Madagascar, which indicates that therian mammals are at least 167 million years old.[34]

Metatheria

The living Metatheria are all marsupials ("animals with pouches"). A few fossil genera such as the Mongolian late Cretaceous Asiatherium may be marsupials or members of some other metatherian group(s).[35][36]

The oldest known marsupial is Sinodelphys, found in 125M-year old early Cretaceous shale in China's northeastern Liaoning Province. The fossil is nearly complete and includes tufts of fur and imprints of soft tissues.[37]

Didelphimorphia (common opossums of the Western Hemisphere) first appeared in the late Cretaceous and still have living representatives, probably because they are mostly semi-arboreal unspecialized omnivores.[38]

The best-known feature of marsupials is their method of reproduction:

Palate of thylacine, showing one of the paired palatal fenestrae (top left) which are a signature feature of marsupials.

Although some marsupials look very like some placentals (the thylacine or "marsupial wolf" is a good example), marsupial skeletons have some features which distinguish them from placentals:[40]

Marsupials also have a pair of marsupial bones (sometimes called "epipubic bones"), which support the pouch in females. But these are not unique to marsupials, since they have been found in fossils of multituberculates, monotremes, and even eutherians - so they are probably a common ancestral feature which disappeared at some point after the ancestry of living placental mammals diverged from that of marsupials.[41][42] Some researchers think the epipubic bones' original function was to assist locomotion by supporting some of the muscles that pull the thigh forwards.[43]

Eutheria

Main article: Eutheria

The living Eutheria ("true beasts") are all placentals. But the earliest known eutherian, Eomaia, found in China and dated to 125M years ago, has some features which are more like those of marsupials (the surviving metatherians):[44]

Eomaia also has a Meckelian groove, a primitive feature of the lower jaw which is not found in modern placental mammals.

These intermediate features are consistent with molecular phylogenetics estimates that the placentals diversified about 110M years ago, 15M years after the date of the Eomaia fossil.

Eomaia also has many features which strongly suggest it was a climber, including: several features of the feet and toes; well-developed attachment points for muscles which are used a lot in climbing; and a tail which is twice as long as the rest of the spine.

Placentals' best-known feature is their method of reproduction:

It has been suggested that the evolution of placental reproduction was made possible by retroviruses which:[45]

From a paleontologist's point of view, eutherians are mainly distinguished by various features of their teeth.[46]

Expansion of ecological niches in the Mesozoic

There is still some truth in the "small, nocturnal insectivores" stereotype but recent finds, mainly in China, show that some mammaliforms and true mammals were larger and had a variety of lifestyles. For example:

Repenomamus sometimes preyed on young dinosaurs


Evolution of major groups of living mammals

There are currently vigorous debates between traditional paleontologists ("fossil-hunters") and molecular phylogeneticists about how and when the true mammals diversified, especially the placentals. Generally the traditional paelontologists date the appearance of a particular group by the earliest known fossil whose features make it likely to be a member of that group, while the molecular phylogeneticists suggest that each lineage diverged earlier (usually in the Cretaceous) and that the earliest members of each group were anatomically very similar to early members of other groups and differed only in their genes. These debates extend to the definition of and relationships between the major groups of placentals - the controversy about Afrotheria is a good example.

Fossil-based family tree of placental mammals

Here is a very simplified version of a typical family tree based on fossils, based on Cladogram of Mammalia - Palaeos. It tries to show the nearest thing there is at present to a consensus view, but some paleontologists have very different views, for example:[51]

For the sake of brevity and simplicity the diagram omits some extinct groups in order to focus on the ancestry of well-known modern groups of placentals - X marks extinct groups. The diagram also shows the following:

--Eutheria
    |
    +--Xenarthra (Paleocene)
    |  (armadillos, anteaters, sloths)
    |
    `--+--Pholidota (early Eocene)
       |  (pangolins)
       |
       `--Epitheria (late Cretaceous)
          | 
          |--(some extinct groups) X
          |
          `--+--Insectivora (late Cretaceous)
             |  (hedgehogs, shrews, moles, tenrecs)
             |
             `--+--+--Anagalida
                |  |  |
                |  |  +--Zalambdalestidae X (late Cretaceous) 
                |  |  |
                |  |  `--+--Macroscelidea (late Eocene)
                |  |     |  (elephant shrews)
                |  |     |
                |  |     `--+--Anagaloidea X
                |  |        |
                |  |        `--Glires (early Paleocene)
                |  |             | 
                |  |             +--Lagomorpha (Eocene)
                |  |             |  (rabbits, hares, pikas)
                |  |             |
                |  |             `--Rodentia (late Paleocene)
                |  |                (mice & rats, squirrels,
                |  |                 porcupines)
                |  |           
                |  `--Archonta
                |       |
                |       |--+--Scandentia (mid [Eocene])
                |       |  |  (tree shrews)
                |       |  |
                |       |  `--Primatomorpha
                |       |       |
                |       |       +--Plesiadapiformes X
                |       |       |
                |       |       `--Primates (early Paleocene)
                |       |          (tarsiers, lemurs, monkeys,
                |       |            apes, humans)
                |       |
                |       `--+--Dermoptera (late Eocene)
                |          |  (colugos)
                |          |
                |          `--Chiroptera (late Paleocene)
                |             (bats)
                |
                `--+--Ferae (early Paleocene)
                   |  (cats, dogs, bears, seals)
                   |
                   `--Ungulatomorpha (late Cretaceous)
                        |
                        +--Eparctocyona (late Cretaceous)
                        |  |
                        |  +--(some extinct groups) X
                        |  |
                        |  `--+--Arctostylopida X (late Paleocene)
                        |     |
                        |     `--+--Mesonychia X (mid Paleocene)
                        |        | (predators / scavengers,
                        |        |  but not closely related 
                        |        |  to modern carnivores)
                        |        |
                        |        `--Cetartiodactyla 
                        |           |
                        |           +--Cetacea (early Eocene)
                        |           |  (whales, dolphins, porpoises)
                        |           |
                        |           `--Artiodactyla (early Eocene)
                        |              (even-toed ungulates:
                        |               pigs, hippos, camels,
                        |               giraffes,  cattle, deer)
                        |
                        `--Altungulata
                             |
                             +--Hilalia X
                             |
                             `--+--+--Perissodactyla (late Paleocene)
                                |  |    (odd-toed ungulates:
                                |  |     horses, rhinos, tapirs) 
                                |  |
                                |  `--Tubulidentata (early Miocene)
                                |     (aardvarks)
                                |
                                `--Paenungulata ("not quite ungulates")
                                     |
                                     +--Hyracoidea (early Eocene)
                                     |  (hyraxes)
                                     |
                                     `--+--Sirenia (early Eocene)
                                        |  (manatees, dugongs)
                                        |
                                        `--Proboscidea (early Eocene)
                                           (elephants)

This family tree contains some surprises and puzzles. For example:

Family tree of placental mammals according to molecular phylogenetics

Molecular phylogenetics uses features of organisms' genes to work out family trees in much the same way as paleontologists do with features of fossils - if two organisms' genes are more similar to each other than to those of a third organism, the two organisms are more closely related to each other than to the third.

Molecular phylogeneticists have proposed a family tree which is very different from the one with which paleontologists are familiar. Like paleontologists, molecular phylogeneticists have different ideas about various details, but here is a typical family tree according to molecular phylogenetics:[52][53] Note that the diagram shown here omits extinct groups, as one cannot extract DNA from fossils.

--Eutheria
   |
   +--Atlantogenata ("born round the Atlantic ocean")
   |    |
   |    +--Xenarthra (armadillos, anteaters, sloths)
   |    |
   |    `--Afrotheria
   |       |
   |       +--Afroinsectiphilia 
   |       |   (golden moles, tenrecs, otter shrews)
   |       |
   |       +--unnamed
   |       |    |
   |       |    +--Macroscelidea (elephant shrews)
   |       |    |
   |       |    `--Tubulidentata (aardvarks)
   |       |
   |       `--Paenungulata ("not quite ungulates")
   |            |
   |            +--Hyracoidea (hyraxes)
   |            |
   |            +--Proboscidea (elephants)
   |            |
   |            `--Sirenia (manatees, dugongs)
   |
   `--Boreoeutheria ("northern true / placental mammals")
        |
        +--Laurasiatheria
        |    |
        |    +--Erinaceomorpha (hedgehogs, gymnures)
        |    |
        |    +--Soricomorpha (moles, shrews, solenodons)
        |    |
        |    +--Cetartiodactyla 
        |    |  (cetaceans and even-toed ungulates)
        |    |
        |    `--Pegasoferae
        |         |
        |         +--Pholidota (pangolins)
        |         |
        |         +--Chiroptera (bats)
        |         |
        |         +--Carnivora (cats, dogs, bears, seals)
        |         |
        |         `--Perissodactyla (horses, rhinos, tapirs).
        |
        `--Euarchontoglires
             |
             +--Glires
             |    | 
             |    +--Lagomorpha
             |    |  (rabbits, hares, pikas)
             |    |
             |    `--Rodentia (late Paleocene)
             |        (mice & rats, squirrels, porcupines)
             |            
             `--Euarchonta
                  |
                  |--Scandentia (tree shrews)
                  |
                  |--Dermoptera (colugos)
                  |
                  `--Primates 
                     (tarsiers, lemurs, monkeys, apes)

Here are the most significant of the many differences between this family tree and the one familiar to paleontologists:

The grouping together of the Afrotheria has some geological justification. All surviving members of the Afrotheria originate from South American or (mainly) African lineages – even the Indian elephant, which diverged from an African lineage about 7.6 million years ago.[54]. As Pangaea broke up Africa and South America separated from the other continents less than 150M years ago, and from each other between 100M and 80M years ago.[55][56] The earliest known eutherian mammal is Eomaia, from about 125M years ago. So it would not be surprising if the earliest eutherian immigrants into Africa and South America were isolated there and radiated into all the available ecological niches.

Nevertheless these proposals have been controversial. Paleontologists naturally insist that fossil evidence must take priority over deductions from samples of the DNA of modern animals. More surprisingly, these new family trees have been criticised by other molecular phylogeneticists, sometimes quite harshly:[57]

Timing of placental evolution

Recent molecular phylogenetic studies suggest that most placental orders diverged about 100M to 85M years ago, but that modern families first appeared in the late Eocene and early Miocene.[61]

Some paleontologists object that no placental fossils have been found from before the end of the Cretaceous - for example Maelestes gobiensis, from about 75M years ago, is a eutherian but not a true placental.[62] Many Cretaceous fossil sites contain well-preserved lizards, salamanders, birds, and mammals, but not the modern forms of mammals. It is likely that they simply did not exist, and that the molecular clock runs fast during major evolutionary radiations.[63] On the other hand there is fossil evidence from 85 million years ago of hoofed animals which may be ancestors of modern ungulates.[64]

Fossils of the earliest members of most modern groups date from the Paleocene, a few date from later and very few from the Cretaceous, before the extinction of the dinosaurs. But some paleontologists, influenced by molecular phylogenetic studies, have used statistical methods to extrapolate backwards from fossils of members of modern groups and concluded that primates arose in the late Cretaceous.[65] However statistical studies of the fossil record confirm that mammals were restricted in size and diversity right to the end of the Cretaceous, and rapidly grew in size and diversity during the Early Paleocene.[66][67]

Evolution of mammalian features

Jaws and middle ears

See also Evolution of mammalian auditory ossicles

Hadrocodium, whose fossils date from the early Jurassic, provides the first clear evidence of fully mammalian jaw joints and middle ears, in which the jaw joint is formed by the dentary and squamosal bones while the articular and quadrate move to the middle ear, where they are know as the incus and malleus. Curiously it is usually classified as a member of the mammaliformes rather than a as a true mammal.

One analysis of the monotreme Teinolophos suggested that this animal had a pre-mammalian jaw joint formed by the angular and quadrate bones and that the typical mammalian middle ear evolved twice independently, in monotremes and in therian mammals, but this idea has been disputed.[68] In fact 2 of the suggestion's authors co-authored a later paper which reinterpreted the same features as evidence that Teinolophos was a full-fledged platypus, which means it would have had a mammalian jaw joint and middle ear.[30]

Milk production (lactation)

It has been suggested that lactation's original function was to keep eggs moist. Much of the argument is based on monotremes (egg-laying mammals):[69][70][71]

Hair and fur

The first clear evidence of hair or fur is in fossils of Castorocauda, from 164M years ago in the mid Jurassic.

From 1955 onwards some scientists have interpreted the foramina (passages) in the maxillae (upper jaws) and premaxillae (small bones in front of the maxillae) of cynodonts as channels which supplied blood vessels and nerves to vibrissae (whiskers), and suggested that this was evidence of hair or fur.[72][73] But foramina do not necessarily show that an animal had vibrissae - for example the modern lizard Tupinambis has foramina which are almost identical to those found in the non-mammalian cynodont Thrinaxodon.[9][74]

Erect limbs

The evolution of erect limbs in mammals is incomplete - living and fossil monotremes have sprawling limbs. In fact some scientists think that the parasagittal (non-sprawling) limb posture is a synapomorphy (distinguishing characteristic) of the Boreosphenida, a group which contains the Theria and therefore includes the last common ancestor of modern marsupials and placentals - and therefore that all earlier mammals had sprawling limbs.[75]

Sinodelphys (the earliest known marsupial) and Eomaia (the earliest known eutherian) lived about 125M years ago, so erect limbs must have evolved before then.

Warm-bloodedness

"Warm-bloodedness" is a complex and rather ambiguous term, because it includes some or all of the following:

Since we can't know much about the internal mechanisms of extinct creatures, most discussion focuses on homeothermy and tachymetabolism.

Modern monotremes have a lower body temperature and more variable metabolic rate than marsupials and placentals.[76] So the main question is when a monotreme-like metabolism evolved in mammals. The evidence found so far suggests Triassic cynodonts may have had fairly high metabolic rates, but is not conclusive.

Respiratory turbinates

Modern mammals have respiratory turbinates, convoluted structures of thin bone in the nasal cavity. These are lined with mucous membranes which warm and moisten inhaled air and extract heat and moisture from exhaled air. An animal with respiratory turbinates can maintain a high rate of breathing without the danger of drying its lungs out, and therefore may have a fast metabolism. Unfortunately these bones are very delicate and therefore have not yet been found in fossils. But rudimentary ridges like those which support respiratory turbinates have been found in Triassic therapsids such as Thrinaxodon and Diademodon, which suggests that they may have had fairly high metabolic rates. [77] [78][72]

Bony secondary palate

Mammals have a secondary bony palate which separates the respiratory passage from the mouth, allowing them to eat and breathe at the same time. Secondary bony palates have been found in the more advanced cynodonts and have been used as evidence of high metabolic rates.[72][73][79] But some cold-blooded vertebrates have secondary bony palates (crocodilians and some lizards), while birds, which are warm-blooded, do not have them.[9]

Diaphragm

A muscular diaphragm helps mammals to breathe, especially during strenuous activity. For a diaphragm to work, the ribs must not restrict the abdomen, so that expansion of the chest can be compensated for by reduction in the volume of the abdomen and vice versa. The advanced cynodonts have very very mammal-like rib cages, with greatly reduced lumbar ribs. This suggests that these animals had diaphragms, were capable of strenuous activity for fairly long periods and therefore had high metabolic rates.[72][73] On the other hand these mammal-like rib cages may have evolved to increase agility.[9] But the movement of even advanced therapsids was "like a wheelbarrow", with the hindlimbs providing all the thrust while the forelimbs only steered the animal, in other words advanced therapsids were not as agile as either modern mammals or the early dinosaurs.[80] So the idea that the main function of these mammal-like rib cages was to increase agility is doubtful.

Limb posture

The therapsids had sprawling forelimbs and semi-erect hindlimbs.[81][73] This suggests that Carrier's constraint would have made it rather difficult for them to move and breathe at the same time, but not as difficult as it is for animals such as lizards which have completely sprawling limbs.[82] But cynodonts (advanced therapsids) had costal plates which stiffened the rib cage and therefore may have reduced sideways flexing of the trunk while moving, which would have made it a little easier for them to breathe while moving .[83] These facts suggest that advanced therapsids were significantly less active than modern mammals of similar size and therefore may have had slower metabolisms.

Insulation (hair and fur)

Insulation is the "cheapest" way to maintain a fairly constant body temperature. So possession of hair of fur would be good evidence of homeothermy but would not be such strong evidence of a high metabolic rate.[84] [85]

The first clear evidence of hair or fur is in fossils of Castorocauda, from 164M years ago in the mid Jurassic;[24] arguments that advanced therapsids had hair are unconvincing.

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Bibliography

External links