Rise Of The Mammals

Primitive forms, and then success

The first mammals, small insect eaters in the Late Triassic and Early Jurassic (see p. 450), probably hunted at night. Mammals remained small through most of the Mesozoic and they did not achieve high diversity, perhaps held in check in some way by the dinosaurs. Several lines of insectivorous, carnivorous and herbivorous forms appeared, some of them adapted to climbing trees. Most Mesozoic mammals were small, and a recent find from China proved to be an exception (Box 17.4). Nonetheless, most basal mammal groups did not outlive the Cretaceous-Tertiary mass extinction (see pp. 174-7). Three of the clades that did survive into the Tertiary were the monotremes, marsupials and placentals, the modern groups (Box 17.5).

Monotremes today are restricted to Australasia, being represented by the platypus and the echidnas. These mammals are unique in still laying eggs, as the cynodont ancestors of mammals presumably did. The young hatch out as tiny helpless creatures, and feed on their mother's milk until they are large enough to live independently.

It is often said that mammals owe everything to their teeth. The marsupials, and especially the placentals, radiated dramatically in the Tertiary, and this is often taken as a classic example of an adaptive radiation (see p. 544). It is notable that previously rather small, similar-looking animals had diversified within 10 myr to forms as disparate as bats and rats, monkeys and whales. Mammals uniquely have differentiated teeth, with incisors, canines and cheek teeth. Fishes, amphibians and reptiles have undifferentiated teeth - their teeth are pretty much identical from front to back. Differentiated teeth allow mammals to adopt a huge array of diets, and to become superefficient at biting, and especially chewing. High metabolic rates need lots of nutritious food, and chewing, moving the cheek teeth round and across the food, allows mammals to improve the efficiency of their digestive systems. Most dinosaurs (except ornithopods; see p. 457), like reptiles in general, could not chew, or at least not well - so they swallowed their food whole and probably failed to digest much of it. One thing is for sure: don't stand downwind of a dinosaur!

Marsupials: the pouched mammals_

Marsupial young are also born tiny and helpless, and have to feed on maternal milk in a

Box 17.3 The spectacular birds of Liaoning

Back in 1984, local farmers in Liaoning Province, China, began to send fossils they had found in their fields to paleontologists in Beijing and Nanjing. The fossils were all fantastically well preserved: fishes with skin, insects with color patterns, birds and dinosaurs with feathers, and early mammals with hair. The Chinese paleontologists began to publish accounts of the specimens, and they mounted organized digs to recover many tonnes of fossiliferous sediments. It seems all these ancient creatures had swum, or fallen, into ponds where fine lime muds were accumulating and locking in the cadavers before they could decay.

So far, about 20 species of birds have been named from the Liaoning sites (Zhou et al. 2003), including Confuciusornis, perhaps the best-known new genus. The most amazing specimen of Con-fuciusornis shows a male and female bird of the same species sitting side by side on the slab (Fig. 17.11). The male has long, streamer-like tail feathers, almost certainly brightly colored in life and used in sexual displays. Confuciusornis was about the size of a rook, and it is advanced over Archae-opteryx in that it has no teeth in the jaws, and its bony tail has been reduced to a nubbin of bone, or pygostyle. But the Chinese bird is still primitive in having powerful fingers and claws on its wings. Nonetheless, its feathers are like those of any modern bird, and the confuciusornithids almost certainly flapped in and out of the trees in China 125 Ma, swooping after prey and landing gracefully on the branches, just like any modern bird.

Not only birds with feathers, but dinosaurs too! Since 1995, a string of reports of small theropod dinosaurs from Liaoning have shown that many flesh-eating dinosaurs also had feathers, even though they did not fly. The feathers were presumably initially for insulation, so the theropod dinosaurs at least must have been warm-blooded. So, in the evolution of birds, feathers came first, perhaps as early as the Early Jurassic and then wings and flight came in the Late Jurassic when Archaeopteryx evolved.

Read more about the Liaoning birds and dinosaurs in Zhou et al. (2003), and at web sites linked through http://www.blackwellpublishing.com/paleobiology/.

Liaoning Fossils
Figure 17.11 Two examples of the Early Cretaceous bird Confuciusornis from Liaoning, China, showing a male (below, with long tail streamers) and a female. (Courtsey of Zhou Zhonghe.)

Box 17.4 Mammal eats dinosaur shock!

A common view about the mammals of the Mesozoic is that they were all rather small, and that this was because the dinosaurs preyed on them and prevented any becoming large. Two new mammals from the mid-Cretaceous of China have turned this idea over: one was as big as a dog, the other as big as a cat, and one of them had just eaten a dinosaur - admittedly a baby dinosaur only 140 mm long.

The new fossils come from the classic localities around Liaoning, China, that have produced so many spectacular fossils of dinosaurs, birds (see Box 17.3), salamanders, fishes, insects and plants. Yaoming Hu, a graduate student at the American Museum of Natural History in New York and his colleagues from China described two new species, Repenomamus giganticus and R. robustus, both based on excellent skeletons (Hu et al. 2005), 1.0 and 0.4 m in length, respectively. Repenomamus is a triconodont, a group known otherwise mainly from isolated jawbones, and thought before to have specialized in eating insects. One specimen of R. robustus had the remains of a baby Psittaco-surus, a ceratopsian dinosaur (see p. 457), torn into chunks inside its rib cage, in the region of the stomach (Fig. 17.12).

"This is a good man-bites-dog story", commented paleontologist Kevin Padian, when the discovery was announced. Read a review of Mesozoic mammals in Luo (2007), and find out more about Repenomamus, and see color images, at http://www.blackwellpublishing.com/paleobiology/.

Repenomamus Robustus
Figure 17.12 The dog-sized triconodont mammal, Repenomamus, from the mid-Cretaceous of Liaoning, China: (a) reconstruction of this mammal eating a small Psittacosaurus, and (b) specimen showing Psittacosaurus bones inside the rib cage. (Courtesy of Hu Yaoming.)

Box 17.5 Classification of mammals

Modern mammals fall into three groups - the monotremes, marsupials and placentals - characterized by their breeding modes. Various primitive groups are omitted.

Class MAMMALIA

Subclass MONOTREMATA

• Females lay eggs, and newborn young grow in pouch

• Early Cretaceous to Recent

Subclass METATHERIA (marsupials and extinct relatives)

• Young are born live, but continue development in pouch

• Late Cretaceous to Recent

Subclass EUTHERIA (placentals and extinct relatives)

• Young are born live at an advanced stage, having been nourished by a placenta while in the womb. Main orders only are listed

• Mid-Cretaceous to Recent Infraclass AFROTHERIA

Order PROBOSCIDEA (elephants)

• Eocene to Recent Infraclass XENARTHRA

Order EDENTATA (armadillos, tree sloths, anteaters)

• Paleocene to Recent Infraclass LAURASIATHERIA

Superorder BOREOEUTHERIA Order LIPOTYPHLA ("insectivores": hedgehogs, moles, shrews)

• Paleocene to Recent Order CHIROPTERA (bats)

• Eocene to Recent

Order ARTIODACTYLA (pigs, hippos, camels, cattle, deer, giraffes, antelopes)

• Eocene to Recent

Order CETACEA (whales and dolphins)

• Eocene to Recent

Order PERISSODACTYLA (horses, rhinos, tapirs)

Order CARNIVORA (dogs, bears, cats, hyaenas, seals)

• Paleocene to Recent Superorder EUARCHONTOGLIRES

Order PRIMATES (monkeys, apes, humans)

• Paleocene to Recent

Order RODENTIA (mice, rats, squirrels, porcupines, beavers)

• Paleocene to Recent

Order LAGOMORPHA (rabbits and hares)

• Eocene to Recent

Diprotodon
Figure 17.13 Extinct marsupials: (a) the sabretooth Thylacosmilus from South America, and (b) the giant herbivore Diprotodon from Australia. (Based on Gregory 1951.)

pouch for many months, but egg laying has been abandoned. The oldest marsupial fossils come from the mid-Cretaceous of North America. The group radiated successfully in South America during the Tertiary, and included several lines of insectivores, carnivores and herbivores, many of which were remarkably like unrelated placental mammals elsewhere. Some forms were dog-like, and Thylacosmilus (Fig. 17.13a) independently evolved all the characters of the placental saber-toothed cats of Europe and North America.

In Australia, the marsupials diversified even more, after reaching that continent in the Eocene by traveling across a much warmer Antarctica, which then linked the southern tip of South America with Australia. Once there, the Australian marsupials radiated to parallel placental mammals in functions and body forms, except of course for the unique kangaroos. In the Pleistocene, there were abundant and diverse faunas of large marsupials, including giant kangaroos and the hippopota mus-sized herbivorous Diprotodon (Fig. 17.13b).

Palaeogeography and diversification of the placentals

Placental mammals produce young that are retained in the mother's womb much longer than is the case in marsupials, and they are nourished by blood passed through the placenta. The oldest is the mid-Cretaceous Eomaia from Liaoning in China. Many fossil placental mammals have been reported from the Late Cretaceous, but most are rather incomplete, and sometimes their classification has been controversial.

Mammalogists have struggled for two or more centuries to understand the relationships of the major groups of living placentals - are cattle related to horses, bats to monkeys, whales to seals? Some morphological evidence was found to show that, for example, rabbits and rodents are sister groups, elephants are closely related to the enigmatic African hyraxes and the aquatic sirenians, but many other supposed relationships were hotly disputed. Now, however, everything seems to have been resolved (Box 17.6).

Some time early in the Late Cretaceous, the placental mammal clade split into four. First to split off were the Afrotheria, and that clade continued to evolve in Africa. Then the Xen-arthra became isolated in South America. The Boreoeutheria remained in the northern hemisphere and split there into Laurasiatheria and Euarchontoglires. So the split into placentals in Africa, South America and Laurasia (North America-Europe-Asia) seems to have been central to the diversification of the group, and it ties perhaps with the split of major continents through the mid-Cretaceous, with the South Atlantic splitting South America from Africa, and with other oceans separating those southern continents from North America, Europe and Asia.

Placentals in southern continents

The Afrotheria ("African mammals") are known best by the elephants. The African and Indian elephants of today (Proboscidea) are a sorry remnant of a once-diverse group. Early elephant relatives such as Moeritherium (Fig. 17.15a) were small hippo-like animals that

Box 17.6 Mammals, morphology and molecules

The classification of living placental mammals has long been mysterious. We know what a whale or a bat or a primate is, but how do these major orders relate to each other? The techniques of molecular phylogeny estimation (see pp. 133-4) have revealed the answer.

The story began when Mark Springer and colleagues (1997) discovered the Afrotheria, a clade consisting of African animals, linking the elephants (Proboscidea), hyraxes and sirenians with the aardvarks (Tubulidentata), tenrecs and golden moles. The last three groups had all been assigned various positions in the classification of mammals, but their genes show they shared a common ancestor with the elephant - hyrax - sirenian group. After 1997, everything else fell into place (Fig. 17.14). The South American placentals, the edentates, formed a second major group, the Xenarthra. And the remaining mammalian orders formed a third major clade, the Boreoeutheria ("northern mammals"), split into Laurasiatheria (insectivores, bats, artiodactyls, whales, perissodactyls, carnivores) and Euarchontoglires (primates, rodents, rabbits). So, in the course of 2 or 3 years, several independent teams of molecular biologists solved one of the outstanding puzzles in the tree of life (e.g. Springer et al. 2003; Asher 2007).

But why had this proved to be such a phylogenetic puzzle? Some suggest that the major splits among placental mammals happened very rapidly, and there was no time for shared morphological characters to become fixed. But the morphologists are fired up to find such characters: if the Afrotheria is really a clade, then there must be some obscure anatomic feature shared among them all! The hunt goes on.

Read a review of Afrotheria in Tabuce et al. (2008), and find out more about the search for morphological characters of the clade at http://www.blackwellpublishing.com/paleobiology/.

Marsupials Southern Continents
Figure 17.14 Cladogram of the major orders of placental mammals based on molecular evidence. The four deep splits among modern orders happened in the Late Cretaceous, but modern placentals did not become diverse until after the extinction of the dinosaurs.

Figure 17.15 Afrotheres and xenarthrans: (a, b) skulls of the Eocene proboscidean Moeritherium

(a) and the Miocene proboscidean Deinotherium

(b); and (c, d) Pleistocene edentates from Argentina, Glyptodon (c) and Mylodon (d). (Based on Gregory 1951.)

Figure 17.15 Afrotheres and xenarthrans: (a, b) skulls of the Eocene proboscidean Moeritherium

(a) and the Miocene proboscidean Deinotherium

(b); and (c, d) Pleistocene edentates from Argentina, Glyptodon (c) and Mylodon (d). (Based on Gregory 1951.)

probably fed on lush plants in the ponds and rivers of Africa. Later, many lines of proboscideans diverged, distinguished by an astonishing array of tusks, which are modified incisor teeth. Some had tusks in the upper jaw (as in modern elephants), others had tusks in the lower jaw, and others had tusks in both as in Deinotherium (Fig. 17.15b). The Pleistocene mammoths were abundant in cold northern ice age climates, but died out as the ice retreated 10,000 years ago.

Among the other afrotheres, the hyraxes and sirenians are close relatives of proboscideans. The aardvark (Tubulidentata), as well as golden moles and tenrecs, seem to form a second afrothere group.

The Xenarthra, or edentates ("no teeth"), are a peculiar South American group. They include modern armadillos, tree sloths and anteaters, as well as their remarkable ancestors, known especially from the Pliocene and Pleistocene. There were giant armadillos such as Glyptodon (Fig. 17.15c), and giant ground sloths such as Mylodon (Fig. 17.15d) that reached a length of 6 m and fed on coarse leaves from the treetops. The ground sloths survived in South America until 11,000 years ago, and their subfossil remains include clumps of reddish hair and caves full of unrotted dung that occasionally ignites spontaneously.

The "northern" placentals

The Laurasiatheria include about half of modern placental mammals, and they are as diverse as shrews, bats, cattle, whales and lions. The Lipotyphla (sometimes Insectivora) is composed of dozens of species of hedgehogs, moles and shrews, all small animals with long snouts that feed on insects. The oldest Lipotyphla are Paleocene in age, and for the most part the fossil forms probably looked like the modern ones. One exception is the giant spiny hedgehog Deinogalerix, which was 0.5 m long.

Next in the cladogram (see Fig. 17.14) are the Chiroptera, or bats, a diverse group today of some 1000 species. The earliest bats such as Icaronycteris from the Eocene (Fig. 17.16a) show the typical wing structure in which the flight membrane is supported on four fingers of the hand that spread out. The feet turn backwards, and Icaronycteris could have hung upside down. It also had large eyes and the ear region was modified for echolocation. Icaronycteris, like most modern bats, hunted insects at night, using its large eyes to pick up movements, and sending out high-pitched

Hesperocyon Skeleton
(b)
Hesperocyon Skeleton

paddle-like hand

paddle-like hand

Figure 17.16 Diverse laurasiatherians: (a) the Eocene bat Icaronycteris; (b) the small four-toed artiodactyl Messelobunodon, showing the complete skeleton and a mass of chopped plant material in the stomach area, from the oil shale deposit of Messel, Germany; (c) the Pleistocene giant Irish deer Megaloceros; (d) the middle Eocene whale Ambulocetus; (e) the late Eocene whale Basilosaurus; (f) the Miocene horse Neohipparion; (g) the Pleistocene sabre-toothed cat Smilodon; (h) the Eocene dog Hesperocyon; and (i) the Miocene "seal" Allodesmus. (a, based on Jepsen 1970; b, courtesy of Jens Franzen; c, e-i, based on Gregory 1951; d, based on Thewissen et al. 1994.)

squeaks to detect its prey by the echoes they made.

The next clade is perhaps a little unexpected. Much evidence links whales and artio-dactyls, the even-toed ungulates (larger plant eaters), as a clade called Cetartiodactyla. Whales and artiodactyls, for example, share a similar pulley-like ankle joint (do whales have ankles?) - not now, but the early forms did (see below). The artiodactyls arose in the Eocene (Fig. 17.16b), and the group includes pigs, hippos, camels, cattle, deer, giraffes and antelopes, all with an even number of toes (two or four). Pigs and hippos share ancestors in the Oligocene, at the same time as vast herds of oreodonts fed on the spreading grasslands of North America. Oreodonts are related to the camels and the ruminants. The first camels were long-limbed and lightly built North American animals: it was only later that camels moved to Africa and the Middle East and evolved adaptations for living in conditions of drought.

Most artiodactyls today are ruminants, animals that pass their food into a forestom-ach, regurgitate it (chew the cud) and swallow it again. The multiple digestive process allows ruminants to extract all the nourishment from their plant food, usually grass, and to pass limited waste material (compare the homogenous excrement of cattle with the fibrous undigested droppings of horses, which do not ruminate). Ruminants became successful after the mid-Miocene, when a great variety of deer, cattle and antelopes appeared. These animals usually have horns or antlers, seen in spectacular style in the Irish deer Megaloceros (Fig. 17.16c). The headgear is used in all cases for displays and fights between males seeking to establish territories and win mates.

The whales, Cetacea, evolved from a raccoon-sized artiodactyls that fed on aquatic plants along the edges of streams and ponds (Thewissen et al. 2007) - the oldest whale Ambulocetus (Fig. 17.16d) still has fully developed limbs, and these show the pulleylike ankle bone of artiodactyls. By the late Eocene, whales such as Basilosaurus (Fig. 17.16e) had become very large, at lengths of 20 m or more. Basilosaurus had a long thin body, like a mythical sea serpent, and a relatively small skull armed with sharp teeth. It was probably a fish eater, like the toothed whales today. The baleen whales, the biggest of all modern whales, arose later, and they owe their success to their ability to filter vast quantities of small crustaceans, krill, from polar seawaters.

The second major ungulate group, the Perissodactyla, consisting of horses, rhinos and tapirs, all have an odd number of toes -one or three. The horses provide a classic example of evolution (see p. 543). The first horse, Hyracotherium, was a small woodland-living animal that had four fingers and three toes, and low teeth used for browsing on leaves. During the Oligocene and Miocene, horses became adapted to the new grasslands that were replacing the forests, and they became larger, lost toes and evolved deep-rooted cheek teeth for grinding tough grass (Fig. 17.16f).

Tapirs and rhinoceroses are probably related. Eocene and Oligocene rhinos were modest-sized, running animals, not much different from some of the early horses. Tapirs later became a rare group, restricted to Central and South America and Southeast Asia. The rhinoceroses flourished for a while, producing monsters such as the Oligocene Indricothe-rium, the largest land mammal of all time: 5.5 m tall at the shoulder and weighing 15 tonnes.

The Carnivora - cats, dogs, hyenas, weasels and seals - are characterized by sharp cheek teeth (carnassials) used for tearing flesh. The cats have a long history during which dagger-toothed and saber-toothed forms evolved many times. The sabertooths such as Smilo-don (Fig. 17.16g) preyed on large, thick-skinned herbivores by cutting chunks of flesh from their bodies. The saber-toothed adaptations evolved independently in some South American marsupials (cf. Fig. 17.13a). Early dogs such as Hesperocyon (Fig. 17.16h) were light, fast-moving animals, close to the ancestry of modern dogs and bears. Some carnivores related to raccoons and weasels entered the sea during the Oligocene, and gave rise to the seals, sealions and walruses. Early forms such as Allodesmus (Fig. 17.16i) had broad, paddle-like limbs and fed on fish.

The monkey-rabbits_

The second boreoeutherian clade (see Fig. 17.14) is the Euarchontoglires, a mouthful that is made from a combination of the group names Archonta and Glires, and it means something like "true primate-treeshrew rodent-rabbits". The name tells the whole story!

Rats and rabbits, representing the Rodentia and Lagomorpha, belong to one group (Glires), and they shared an ancestor with buck teeth and a propensity for breeding. Rodents are the largest group, consisting of over 1700 species of mice, rats, squirrels, porcupines and beavers. They owe their success to their powerful gnawing teeth: the front incisors are deep-rooted and grow continuously, so that they can be used to grind wood, nuts and husks of fruit. The oldest rodents, such as Paramys (Fig. 17.17a) already had the front grinders, and this ability to chew materials ignored by other animals triggered several phases of rapid radiation. Beavers, porcupines and cavies radiated in the Miocene. The cavies include a giant Pliocene guinea pig that weighed 1 tonne, and was the size of a small car (Rinderknecht & Blanco 2008); why the South American rodents became so large is hard to understand. Rabbits and their relatives (Lagomorpha) have never been as diverse as the rodents. Fossil forms in the Oligocene have elongate hindlimbs used in jumping.

Primates, consisting of monkeys, apes and humans, are part of a larger clade, Archonta, which also includes the rare treeshrews and flying lemurs (dermopterans) - but it is the primates that have attracted most attention.

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