10 Didelphimorphia (opossums)

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1 Chiroptera (bats) 1 1 Perissodactyla (horses, rhinos) Carnivora (lions, wolves) MYA c. 120 MYA c. 90 MYA MYA MYA Pholidota (pangolins) Artiodactyla (deer, pigs) 2 Cetacea (whales, dolphins) Erinaceomorpha (hedgehogs) Sericomorpha (moles, shrews) Primates (monkeys, humans) 3 Dermoptera (colugos, cobegos) Scandentia (tree shrews) Rodentia (rats, guinea pigs) 4 Lagomorpha (rabbits, hares) Xenarthra (armadillos, sloths, anteaters) Proboscidea (elephants) 6 Sirenia (manatees, dugong) Hyracoidea (hyraxes) 7 Tubulidentata (aardvark) Afrosoricida (tenrecs, golden moles) 5 Laurasiatheria (laurasiatherians) Euarchontoglires (supraprimates) Afrotheria (afrotherians) Boreoeutheria (boreoeutherians) EUTHERIA (placentals) Macroscelidea (elephant shrews) Notoricteromorphia (marsupial moles) 8 41 c. 200 MYA Dasyuromorphia (Tasmanian devil, numbat) Peramelemorphia (bandicoots) Diprotodontia (kangaroos, koala) 9 Microbiotheria (colocolo) Paucituberculata (shrew opossums) 8 METATHERIA (marsupials) 9 10 Didelphimorphia (opossums) Monotremata (equidnas, platypus) 10 Tree of Mammals showing the phylogenetic relationships among the most significant groups (28 orders). Colored boxes indicate high taxonomic ranks. Branches with thick lines indicate robust clades, and branches with thin lines less-supported clades. The number in the green circle indicates the chapter in which mammals are also included. Orange circles mark main nodes and their ages. Photographs illustrate principal clades; boxed numbers associate photographs with clades.

2 Mammals 43 Proliferation of Species after Dinosaurs Demise Pablo Vargas SUMMARY Mammals are a natural group composed of three principal clades of extant species: monotremes (oviparous), metatherians (viviparous marsupials), and eutherians (viviparous placentals). From a systematics point of view, extant mammals are subdivided into 28 orders and 134 families, unequally distributed among monotremes (1 order/2 families), marsupials (7 orders/19 families), and placentals (20 orders/113 families). Placentals are in turn divided into 3 principal clades (afrotherians, xenarthrans, and boreoeutherians), with the relationships among the 3 difficult to resolve. A strong geographical component allows for a precise biogeographical reconstruction of the most ancient groups of mammals originated in the Late Triassic and distributed mainly in Australia (monotremes, marsupials), Africa (afrotherians), South America (marsupials, xenarthrans), North America (marsupials, boreoeutherians), and Eurasia (boreoeutherians). The phylogeny of mammals also makes it possible to point out five unique characters (dentary bone, no intermediate bones in the mandibular joint, three bones in the inner ear, development of hair, and production of milk) and a tendency toward giving birth to increasingly underdeveloped young, increasing separation between the digestive and urogenital orifices, and ribs limited to the thoracic region. Although morphological and physiological characters have historically provided the basis for a natural classification reflecting the evolution of mammals, there are other convergent characters in certain groups that have not facilitated systematics; notably among them, a derived epitheliochorial placenta, hooves (former ungulates ), or the development of dentition related to the type of food (former insectivores ). In this chapter the supraspecific systematics of the 5200 extant species is analyzed in the light of morphological and molecular data, and the most important groups of extinct tetrapods in the evolutionary line of mammals are discussed. The still-enigmatic origin of elephants and whales and the evolution of Homo sapiens are also addressed in detail in this chapter. Undoubtedly, mammals are the best-known extant organisms, in spite of their great organic complexity. Because of human beings interest in learning about ourselves, and our intense study of species either phylogenetically related (apes, chimpanzees), commercially useful (cows, goats, sheep), or medically useful (mouse, rat) we have been able to understand the evolution of mammals in detail. As if this were not enough, the interesting fossil register left mainly by the bones of mammals makes a well-documented historical reconstruction possible, although not without gaps. Mammals are thought to have been one of the dominant groups on Earth since the extinction of the dinosaurs some 65 million years ago, not only because of the number of species (but see Chapter 34, Coleopterans), but also because of their size and the adaptability of What is a mammal? Mammals (from the Latin mamma [teat]) are vertebrates with constant body temperature, hair, cerebral neocortex, and, in particular, the females develop mammary glands that produce milk with which they feed their young. All extant mammals descend from a common ancestor dating back to the Late Triassic, more than 200 million years ago. Specifically, present-day mammals descend from primitive sinapsids (amniote tetrapods) that appeared in the Early Permian. Several radiations of mammals that occurred in the last 65 million years, after the mass extinction of dinosaurs, have been described. Since then, they have diversified into multiple lineages of species adapted to land, water, and air environments.

3 504 CHAPTER 43 MAMMALS BOX 43.1 Morphological characters unique to mammals Mandible consists of only the dentary bone. The dentary bone joins directly to the squamous bone of the cranium, making the mandibular joint. There are three bones in the middle ear (hammer, anvil, and stirrup), except in the monotremes (reptilian ear). All species develop hair to a greater or lesser degree. Mammary glands (derived from sebaceous glands) secrete milk, the necessary food for mammal young. many groups to nearly all the ecosystems on the planet. Moreover, many mammal species are at the top of the trophic pyramid, making their ecological role one of supreme interest. However, they had to wait for their evolutionary moment, some 60 million years ago, for their impressive differentiation, even though the lineage that gave rise to them, starting with the therapsids, had appeared long before that. In fact, the extinction of the dinosaurs unleashed several adaptive radiations that launched a number of lineages and species of mammals that colonized so many ecological environments. As with all living things, the number of extinct lineages of mammals is much greater than that of those extant. Therefore, their evolutionary tree requires a combined knowledge of the fossil record and of extant species. The first division of mammals in the strict sense separates the prototherians (eotherians, alloterians, and monotremes) and the therians (trituberculata, pantotherians, metatherians or marsupials, and eutherians or placentals), both with extant and extinct groups. The term mammaliaformes is used to include a clade of mammals and related extinct forms. Mammaliaforms derived from the therapsids (an extinct group, with the exception of the mammaliaforms), which belong to the synapsids (sister group to the sauropsids; see Chapter 44, Sauropsids). Finally, the synapsids are considered mammal-like reptiles because they include the lineage that would give rise to the mammaliaforms. To give an idea of their systematics, the evolutionary line of mammals would include a hierarchical classification of taxonomic groups nested within more inclusive groups: the synapsids, the pelycosaurs, the therapsids, the cynodonts, and modern mammals. To establish a timeline, it can be said that the first true mammal appeared in the Late Triassic (approximately 220 Mya), that is, approximately 70 million years after the appearance of the first therapsids and 30 million years after the appearance of the first mammaliaforms. Extant mammals have been reduced to three large groups: monotremes, marsupials, and placentals (see Tree of Mammals), of which there are also more extinct than extant species (Figure 43.1). Because the bones are so easily fossilized, there is a fairly ample mammal fossil record available. The five species of monotremes form a whole order of mammals, and are considered living fossils because they combine characteristics common to the other mammals (hair, production of milk, three bones in the ear, diaphragm, and heart with four chambers) and to the sauropsids (laying eggs, feet with spurs on hind legs of males, cranium tapering toward the beak-shaped snout, corneous beak). One platypus and four echidnas make up this ancient lineage, which has survived in Australia and nearby islands in the face of vigorous competition from placentals. Two hundred of the 275 species of marsupials are also Australian, which clearly shows that the island continent of Australia has facilitated an independent and parallel evolution of mammals with characteristics similar to those of placentals (in Australia there are few native placentals). Standing out among the most notable paleontological findings is a marsupial (Sinodelphys) in a surprising state of preservation, even with detectable hairs. Concomitant in space (China) and time (approximately 125 Mya) with fossils, marsupials is the most ancient placental found (Eomaia). Due to the wide diversity of placentals (some 5500 species) developed in the last 125 BOX 43.2 Mammals by the numbers Number of species: some 5500 placentals, 5 monotremes, and around 275 marsupials. 70% of mammal species are rodents Number of genera: about 1200 Genera with the greatest number of species: Crocidura (about 90 species), Myotis (about 90 species), Rhinolophus (about 65 species) Number of families: 134 (although it varies depending on the author) Number of orders: 28 (although it varies substantially depending on the author) Orders with the greatest number of species: Rodentia (rodents) and Chiroptera (bats) Origin of extant mammals: Late Triassic (about 200 Mya) Oldest fossil: Sinodelphys (China), genus of marsupial from about 125 million years ago; Eomaia (China), genus of placental from about 120 million years ago Longest-lived mammal: Homo sapiens ( years) Largest mammal: blue whale (Balaenoptera musculus), at 160 tons Smallest mammal: bumblebee bat (Craseonycteris thonglongyai ), at 2 grams

4 PABLO VARGAS 505 Basic terms Allantoic placenta: Extraembryonic placenta (allantois) originating as an extension or evagination of the endoderm of the embryo s primitive digestive tube. The allantois surrounds the embryo between the amnion and the chorion, or is located caudally to the vitelline sac. Cerebral neocortex: Neural layer that covers the prefrontal lobe; developed in the more evolved areas of the mammalian cortex. These areas are closely related to memory and intelligence. Epitheliochorial placenta: Type of superficial placenta in which the maternal and fetal epithelia are in contact. Evagination: Protuberance or hollow protrusion of an organism s duct or cavity. Hemochorial placenta: Type of placenta in which the membrane surrounding the fetus (chorion) is in intimate and direct contact with the maternal circulatory system. Insectivores : Mammals characterized by small body size, plantigrade feet, nocturnal habits, and complete dentition mostly related to eating invertebrates. They form a polyphyletic group. Oviparity: Reproductive mechanism by which eggs are deposited in the external environment, where they complete their development before hatching. Prototherians: Oviparous mammals in a subclass consisting of the extinct orders Docodonta, Multituberculata, and Triconodonta (although the position of this last is controversial), and the extant order Monotremata (echidnas and platypus). Prototherians are characterized by being therians with the squamous bone in the posterior of the cranium joined directly to the mandible, and for developing the flat bone on the wall of the posterior temporal fossa. Synapsids: Tetrapods forming the group of mammals and other extinct mammaliaforms. Therapsids: Synapsids that include the direct line to mammals. Therians: Viviparous mammals whose females have teats, and are grouped into an independent subclass. Trophoblast: Group of cells developed as a basic part of the placenta, forming the outer layer of the blastocyte and providing nutrients to the embryo. Ungulates : Mammals characterized by having hooves. Ungulates have turned out to be polyphyletic due to the blurred definition of a hoof and the character s convergence. The following orders used to be considered ungulates : Hyracoidea, Sirenia, Proboscidea, Perissodactyla, Artiodactyla, Cetaceae, and occasionally, Tubulidentata. Viviparity: Mechanism by which animal progeny develops from embryos within the female s womb. Placental viviparism is undoubtedly the most advanced and appears only in mammals. million years, most of the characteristics described in this chapter refer to this group of mammals. Characteristics of Mammal Genomes The mammalian nuclear genome is distributed in a variable number of chromosomes, not only among groups, but also within a single group (Laurasiatheria); for example, the diploid number (2n) ranges from 6 chromosomes in the Indian muntjac deer (Muntiacus muntjac) to 72 in the South American short-eared fox (Atelocynus microtis). Nevertheless, in spite of so much variation, mammals retain the X sex chromosomes that characterize females (XX), and the Y sex chromosome that characterize males (XY). The rearrangement of chromosomes and their packaging have resulted in the evolution of very different karyotypes. Many authors agree that the most likely base number in mammals is 2x = 2n = 14, given that it appears in numerous marsupials and in placentals with ancestral characters. To explain the high number of chromosomes, cytogeneticists turn to multiplication via chromosome fission, in which fragmentation of chromosomes at the centromere allows the two parts to migrate with two arms each. This same mechanism is observed in some more recent groups, and with great variation in the number of chromosomes, as in the Old World shrews. Specifically, the genus Crocidura displays an increase in chromosomes from a low number in a group of numerous Palearctic and Asiatic species (2n = 22 40) to a high number in an Afrotropical group, also with numerous species (2n = 42 60). Nevertheless, the most effective mechanism in gene duplication is polyploidy, although it is much less important in mammals than in other organisms, such as plants (see Chapter 12, Angiosperms). For a specific example, a polyploid number (tetraploid) has been described in a plains viscacha rat (Tympanoctomys barrerae), a rodent adapted to the Argentine desert, which has the highest number of chromosomes (2n = 102) known in mammals. A correlation has been found between the number of chromosomes and the vital characteristics of mammals, specifically between a larger size of the genome and an evolution toward a lower basal metabolic rate and a larger cell size, mainly in red blood cells (erythrocytes).

5 506 CHAPTER 43 MAMMALS Subclass Prototheria (order Tachyglossa: equidnas; order Platypoda: platypus, Monotrematum) Infraclass Allotheria (multituberculates) Infraclass Tricondonta (triconodontes) Group Marsupialia (marsupials) Magnorder Australidelphia (monito del monte, kangaroos, Microbiotherium) Magnorder Ameridelphia (opossums, Borhyaenidium) Group Placentalia (placentals) Magnorder Xenarthra (toothless: armadillos, sloths, anteaters, Glyptodon) Subclass Theriiformes Infraclass Holotheria Magnorder Epitheria (epitheria) Grandorder Anagalida (rodents, lagomorphs, elephant shrew Anagole, Mimotona, Gomphos) Grandorder Ferae (carnivorans, pangolins, Creodonta, Hyaenodon) Grandorder Llipotyphia (tenrec, hedgehogs, moles, Adapisorex, Dimylus, Micropternodus) Grandorder Archonta (primates, bats, colugos, tree shrews Adapisorex, Nyctitherium, Micropternodus) Grandorder Ungulata (aardvark, perissodactyla, whales, artiodactyla, elephants, hyracoids, manatees, Meridiungulata, Palaeorycteropus, Uintautherium, Arctocyon) Figure 43.1 A synthesized taxonomic proposal of extant and extinct mammals based on the work of McKenna and Bell (1997, Classification of Mammals Above the Species Level. New York, NY: Columbia University Press), which included some 5000 species, as well as a supraspecific taxonomic treatment of 425 families and 46 orders (brown denotes a group that is extinct.) Through Homo sapiens presence in the group of vertebrates in general, and of mammals in particular, the quantified genome (amount of DNA or 2C value) has been determined for numerous placentals (657 species by the year 2013; see updates at www. genomesize.com). Today there are also completely sequenced mitochondria available (approximately 17,000 base pairs) for almost 700 species of mammals (see updates on Additionally, many ongoing projects have provided incomplete genome sequencing (draft genomes). By 2007, complete genome sequencing included the following species: human being (Homo sapiens), chimpanzee (Pan troglodytes), domestic cow (Bos taurus) (Figure 43.2), dog (Canis lupus familiaris), horse (Equus caballus), rhesus macaque (Macaca mulatta), rat (Rattus norvegicus), and mouse (Mus musculus). Six years later, approximately twenty more genomes of mammals were sequenced, a notable increase in enormous datasets that are useful for phylogenomics. The human genome has more than 20,000 coding genes too small a number to account for the complex diversity observed. The one gene one enzyme hypothesis, which dominated most of the twentieth century, is so extremely simple that it has been necessary to resort to alternative explanations such as complex gene interaction to understand the great diversity in the morphological and physiological development of mammals. To this end, complete genomes are needed. Indeed, the level of knowledge about mammalian kinship relationships is growing faster than that of most of the great groups of living things. At the beginning of the twentieth century, kinship relationships were investigated based on blood immunity tests. In the 1980s, reliable phylogenetic reconstructions were done based on polypeptides Miyamoto and Goodman sequenced eight polypeptides for 107 species in In the 1990s, cytochrome b was used to reconstruct phylogenetic relationships among cetaceans, artiodactylans, sirenids, primates, and rodents. The era of phylogenomics began in the early twenty-first century, with the goal of sequencing complete genomes of orders and families of mammals. Now, thousands of genes and millions of nucleotides are already being concatenated, but the number of species for which we have complete genomes is still too small to allow complete resolution of the mammalian tree (see Tree of Mammals).

6 PABLO VARGAS 507 Figure 43.2 The first complete genomes sequenced of mammals were those of the human being, the chimpanzee, the cow, the dog, the horse, the rhesus macaque, the rat, and the mouse. The photograph shows a Hereford cow (named after Hereford County in southwest England), which was used for the complete sequencing of the cow (Bos taurus) genome. Phylogenetic Results Contrasted with Previous Classifications From the very first classifications (Aristotle) to those of authors like Linnaeus (1758), Gregory (1910), Simpson (1945), and McKenna and Bell (1997), there has always been special interest in a classification to which human beings belong. In fact, there are three key aspects to these classifications: the first is naming the human being (Homo sapiens) as just another species in the order of Primates (Linnaeus, 1758). The second is classifying the large quantity of fossils that paleontologists have pursued in the past two centuries. The third is reconstructing the phylogeny based on DNA sequences. As a consequence, the most important goal has been to propose a combined classification of fossils and extant species based on evolutionary groups. Undoubtedly, the classification of mammals published by George Gaylord Simpson (1945) was the most significant during a large part of the twentieth century. This paleontologist, cofounder of the modern theory of evolution in the first part of the twentieth century, updated all the data on extant and fossil species. More than 50 years would have to go by before McKenna and Bell published a similar but much more complete work. Figure 43.1 shows a classification of supraspecific taxa (425 families in 46 orders) based on these authors work and further kinship results. Significant conflicts appear in the most internal nodes of mammal phylogeny based on DNA sequences (see Tree of Mammals). Phylogenomics will shed further light on large group relationships. Certainly, the position of the group of armadillos, sloths, and anteaters (Xenartha) in the branch of Eutheria is one issue of great evolutionary interest. Placement of Xenartha, Afrotheria, and Boreoeutheria in the tree of mammals is important not only because it determines systematic ranges, but also because it determines reconstruction of the key characters for placentals success in colonizing all the continents. In contrast, species delimitation and other supraspecific taxa of extant mammals are fairly well known. Nevertheless, assigning some species to particular genera, families, and especially orders continues to be a subject of debate. Among them, the old group of insectivores (former order Insectivora ) should be emphasized. It has often posed significant classification problems because of the absence of unique characters and the confusion created by recurrent evolution of some morphological traits. This has resulted in the old group of insectivores becoming a taxonomic black box. Interestingly, phylogenies have made it possible to reclassify several families of the former insectivores as follows: Erinaceidae (hedgehogs and moonrats) in the order Erinaceomorpha; Soricidae (shrews), Talpidae (moles and desmans), and Solenodontidae (solenodons) in the order Soricomorpha; Tenrecidae (Malagasy tenrecs and African otter-shrews) and Chrysochloridae (African golden moles) in the order Afrosoricida; Macroscelididae (elephant shrews) in the order Macroscelidea; and Tupaiidae (tree shrews) in the order Scandentia. DNA phylogenetics have also resolved the systematics problem of the former order of ungulates, which for many authors was another black box including hoofed mammals (see Evolution of Characters that follows). Evolution of Characters The appearance in mammals of five key characters ontogeny of the mandible, the mandibular joint, three bones in the middle ear, the development of hair, and the production of milk has always intrigued researchers. While paleontologists have been able to interpret whether the three bone characters could have been present in extinct mammals, the presence of hair and mammary glands is more difficult to reconstruct because these features are unlikely to be fossilized. Another extremely important character that is hard to trace in the development of mammals is viviparity. The presence of oviparity only in the most basal lineage (monotremes) confirms that viviparity appeared very early in the evolution of mammals and was then retained throughout their diversification (see Tree of Mammals). Marsupials belong to the group of therians along with placentals, although they still share some ancestral characters with the monotremes (the rectum and the urogenital system open jointly into a common cloaca, and there is no true placenta). Without a doubt, their most noteworthy character is the marsupium, a

7 508 CHAPTER 43 MAMMALS The enigmatic origin of elephants (Afrotheria) The largest animals on earth (elephants) and in the ocean (whales) continue to be enigmatic due to the difficulty in reconstructing the group of extant mammals closest (sister group) to each. Phylogenetic reconstructions based on DNA sequences not only of living species but also on fossils are shedding new light on the origins of both groups. Elephants (family Elephantidae) are represented today by two African elephants (the African bush elephant Loxodonta africana and the African forest elephant Loxodonta cyclotis) and one Asian elephant (Elephas maximus). The phylogenies that have reconstructed the kinship relationships of elephants have been enriched by the sequencing of the wooly or tundra mammoth (Mammuthus primigenius) from tissues well preserved in ice; it is also a species of the family Elephantidae, which became extinct after the last glaciation. The morphological characters of the skeleton and the teeth indicate that the mammoth was more closely related to African elephants than to Asian elephants. However, the resulting tree, based on DNA sequences and the fossil record, shows a resolution in which the mammoth is closer to the Asian elephant than to African elephants, with a divergence time of 7 6 million years ago. Divergence between the African bush elephant and the forest elephant occurred some 4 million years ago. Within the family Elephantidae, these two lineages split in the last million years. An exceptional study of fossil DNA has made it possible to sequence the complete mitochondrial genome not only of these elephants, but also of an American mastodon (Mammut americanum) from a piece of tooth from 50, ,000 years ago, found in Alaska. The resulting mitogenomic study shows a separation between the elephant lineage (Elephantidae) and the mastodon lineage (family Mammutidae) near the end of the Oligocene (28 24 Mya). Nevertheless, one of the most fascinating enigmas is the relationship between the proboscideans and the rest of the living mammals. The classic hypothesis based on c. 60 MYA MYA 7 6 MYA MYA c. 4 MYA Woolly or tundra mamoth (Mammuthus primigenius) Asian elephant (Elephas maximus) African bush elephant (Loxodonta africana) African forest elephant (Loxodonta cyclotis) American mastodon (Mammut americanum) Phylogenetic tree of extinct ( ) and living proboscideans based on complete mitochondrial sequencing. morphological characters related the sirenoids (order Sirenia) directly with the proboscideans (order Proboscidea). Starting from the first molecular phylogenies, additional candidates for closest relatives have gradually appeared (aardvark, hyrax, sirenids). Determining the closest relative (sister group) would help to reconstruct the appearance of the ancestor that gave origin to elephants. However, phylogenomic reconstructions are not conclusive and posit three hypotheses: (i) hyraxes (order Hiracoidea), sister group to the proboscideans; (ii) a lineage of the orders Hiracoidea and Sirenia as the sister group to the proboscideans; and (iii) the order Sirenia, sister group to the proboscideans (classic hypothesis). The mass extinction of living things between the Cretaceous and the Tertiary (65 Mya), leading to the disappearance of dinosaurs, also caused rapid appearances and disappearances of numerous lineages of mammals, making a single reconstruction of kinship relationships difficult. Specifically, the absence of extant lineages from million years ago prevents us from reconstructing the sister group to the proboscideans. Pending the discovery of key fossils, the last phylogenies better support an ancestor of Hyracoidea and Sirenia as the closest group to elephants and their relatives. (a) (b) (c) The most recent common ancestor of (a) the African elephant (Loxodonta africana, South Africa) and (b) the Asian elephant (Elephas maximus, Thailand) diverged more than 6 million years ago. (c) The tiny Cape hyrax (Procavia capensis, South Africa) is, surprisingly, one of the closest living relatives of elephants.

8 PABLO VARGAS 509 The enigmatic origin of whales (Laurasiatheria) The 15 species of true whales (suborder Mysticeti) belong to the group of cetaceans (order Cetacea) together with some 70 species of sperm whales, beaked whales, dolphins, orcas, and porpoises (suborder Odontoceti). The fossil record clearly shows that the cetaceans evolved from land mammals similar to present-day ungulates (order Artiodactyla), such as deer, swine, antelopes, cows, and hippopotamuses. In fact, they are so closely related to them that there are authors who include both orders in a new order (Cetartiodactyla). Note that the similarities between cetaceans and sirenids (order Sirenia) are owed to morphological convergences as a consequence of two independent conquests of the aquatic environment by mammals (see Tree of Mammals). The fossil record also shows that an ancestor of amphibian habits and similar in appearance to the present-day hippopotamus gave rise to a lineage that colonized the ocean environment, probably during the Eocene (55 34 Mya). The question is if the similarity to a hippopotamus-type ancestor would be a convergence or if the hippopotamus family (Hippopotamidae) really shares a most recent common ancestor with extant cetaceans. Paleontological studies of some fossils found recently in Pakistan and dated at around 47 million years ago, together with others found in India and dated around 48 million years ago, support both the first and the second hypothesis, depending on the type of analysis performed. Phylogenies based on morphological characters of living species and fossils support the hypothesis that there was an ancestor similar to the hippopotamus, but which did not form part of the direct evolutionary line that gave rise to the family Hippopotamidae. Moreover, the fossils of true hippopotamus appear much later (Miocene). In any case, the radiation that the cetaceans underwent million years ago (Eocene) makes a more precise reconstruction difficult. Indeed, the cetacean fossil record for this period is especially rich, and as a result the conquest of the sea is understood to have been immediately and profusely successful. Studies of comparative anatomy show that cetaceans are more specialized now than they were then. The body plan formed in the Eocene was very successful, and is associated with the rapid differentiation of more than six different lineages in this short period. (a) (b) The enormous bones of beached whales appear today on seashores. They were deposited in sedimentary soils in the same way, resulting in the numerous cetaceans fossils that are being discovered. Top: Humpback whale (Megaptera novaeangliae) skeleton on Fernandina Island (Galápagos Islands, Ecuador). Bottom: Southern minke whale (Balaenoptera bonaerensis) in Tierra de Fuego (Argentina). Future paleontological and phylogenomic studies are needed for a more precise reconstruction of the conquest of the ocean by the group of mammals that gave rise to the largest vertebrates that have ever existed. fold of skin covering the breasts and forming an epidermal pouch that functions as an incubation chamber (Figure 43.3). The young are born underdeveloped and have to crawl from the vagina to the marsupium, where they feed on milk until they complete their development. Before birth, they are retained in the maternal uterus for a long time, fed by an allantoic placenta (coming from outside the embryo) that originates as an extension or evagination of the endoderm in the embryo s primitive digestive tube. The placenta, which joins the fetus and the mother very intimately, gives the young the clear advantage of being born in a very advanced stage of development although it puts the burden of their survival on the mother before birth during the delicate gestation period. Undoubtedly, mammals provide one of the most spectacular examples of adaptive convergence. Specifically, it has been observed that marsupials isolated

9 510 CHAPTER 43 MAMMALS Figure 43.3 The kangaroo Macropus fuliginosus in Yanchep National Park, Perth, Australia. The birth of underdeveloped young carried in the marsupium allows kangaroos to flee shortly after giving birth. on the continent of Australia have arrived at the same evolutionary solutions as placental mammals on other continents. Parallelism between the wolf (Canis lupus) and the extinct Tasmanian tiger or wolf (Thylacinus cynocephalus) shows how similar characteristics converged in two predators. Another equally surprising example is that of the common hedgehog (Erinaceus europaeus) and the short-beaked echidna (Tachyglossus aculeatus). Comparison of adaptive structures among different groups of phylogenetically distant placentals has always been used as an example of evolutionary convergence. In recent centuries, extremities adapted for swimming such as the foot in seals (Phocidae), sea otters (Enhydra lutris, Mustelidae), beavers (Castor spp.), and the Pyrenean desman (Galemys pyrenaicus), and even in a monotreme, the duck-billed platypus (Ornithorhyncus anatinus) were compared to support the concept of morphological convergence (Figure 43.4). Other convergences have been detected by means of phylogenies. Armadillos, anteaters, and American sloths were formerly in the same group as pangolins and African aardvarks (order Edentata). Currently, the morphological characters of armadillos and pangolins are considered to be the result of extreme convergences, since armadillos and tree sloths (order Xenarthra) belong to a different clade from the pangolins (order Pholidota) and the aardvark (order Tubulidentata). Other morphological characters have confused taxonomists throughout history. The word ungulate refers to animals with hooves, that is, with extremities that have an enlarged finger and nail. The homology of the hoof character is extremely complex, making the term inconsistent in classification and tending to circumscribe groups that are difficult to designate taxonomically (black box). Phylogenies have served to reclassify this artificial group into the following orders: perissodactyls, artiodactyls, and cetaceans (laurasiatherians) on the one hand, and on the other, proboscideans, sirenids, hyracoids, and tubilodentata (afrotherians). Even the relationships within these two groups are not as close as would be expected (see Tree of Mammals). Molecular phylogenies also detected convergence in one more large group. The characters that defined the former group of insectivores have been very successful in the course of evolution. Indeed, independent lineages share similar characters, such as small body size, plantigrade feet, nocturnal habit, and complete dentition related to feeding on small insects and other small invertebrates. They are considered the product of ancestral (plesiomorphic) traits, since those characters have been the most successful during long evolutionary periods. Evolutionary Tendencies Mammals owe their success to certain evolutionary tendencies that have made it possible for them to be very competitive. Homeothermy already achieved (A) (B) Figure 43.4 The top photograph shows an ancestral character (horny beak) as well as a morphological convergence (feet with interdigital membranes suited for swimming) between (A) the marsupial platypus (Ornithorhyncus anatinus) and (B) the placental beaver (Castor canadensis).

10 PABLO VARGAS 511 Human evolution 40, , , , ,000 70,000 Early Homo sapiens Colonization by neanderthals Asian colonization by H. sapiens 10,000 60,000 The appearance of Homo sapiens in Africa and the gradual colonization of all continents. (Dates in years; updated from Burenhult 2010, Die ersten Menschen, wiki/early_human_migrations) The study of human evolution (hominization) has a starting point at the separation of the lineage of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) from the lineage that gave rise to the genus Homo 7 5 million years ago. Numerous lineages in the evolutionary line of Homo (hominins) have gone extinct. Hominins form a subtribe of erect hominids that includes Homo and other genera that appeared approximately in the following order: Sahelanthropus 7 5 million years ago, Orrorin about 6 million years ago, Ardipithecus million years ago, Australopithecus 4 million years ago, and Paranthropus between 2.6 and 1.1 million years ago. The fossil record shows there was a notable differentiation of these hominins in the past 7 million years, due to their successful adaptation to bipedalism in the African savannahs followed by a major extinction of genera and species around 2.8 million years ago, due to Africa s progressive desertification. A number of characteristics were crucial to the evolutionary success of hominins: cranial capacity, rectilinear spine, widening of the pelvis, opposing thumb, acute vision, less specialized dentition, vocal anatomy specialized for phonation, legs adapted to bipedalism, and social behavior. All these characters are in a very tiny percentage of genes making up only 0.23% of the differences between the genomes of bonobos and humans. In fact, when the complete Homo sapiens genome was sequenced in 2003, the one gene one enzyme hypothesis, which had reigned for most of the twentieth century, fell defeated in favor of an explanation of morphological and physiological diversity also related to gene interactions. It seems that the appearance of Homo is linked to the shift to carnivorism from the predominant herbivorism of forms such as Paranthropus. Thanks to the efforts of paleontologists in the last 50 years, numerous fossil remains of some 12 species of Homo that appeared and disappeared approximately in the following sequence (analytical taxonomy): H. habilis ( Mya in eastern Africa), H. erectus (2 0.3 Mya in Africa and Eurasia), H. rudolfensis (1.9 Mya in Kenya), H. ergaster ( Mya in eastern Africa), H. georgicus ( Mya in the Caucasus), H. cepranensis (0.8 Mya in Italy), H. antecessor ( Mya in western Europe), H. heidelbergensis ( Mya in Europe and Africa, H. rhodesiensis ( Mya in Zambia), H. neanderthalensis ( Mya in Europe and east Asia), H. floresiensis ( Mya in Indonesia), and H. sapiens (0.25 Mya to the present, over the entire world). Given that H. sapiens is the only living species of the genus, reconstructing the kinship relationships among species is primarily in the hands of paleontologists. In contrast, reconstruction of H. sapiens lineages is addressed mainly by methods that range from physical anthropology to linguistics, passing through population genetics, phylogenomics, biogeography, and phylogeography, among other disciplines. During the past 25 years, phylogeography has specifically had a decisive influence on the level of understanding of H. sapiens evolutionary history. Phylogeography has made reconstruction of human evolution possible based on genetic haplotypes and the analysis of lineage relationships in a geographic framework (map below) (see Chapter 55, Analysis of Genetic Variation and Intraspecific Phylogenies). Making use of the genetic characteristics (molecular markers) of H. sapiens, lineage relationships can be reconstructed with some independence using regions of mitochondrial DNA (mitochondria are inherited exclusively from the mother), the human Y chromosome (inherited exclusively 35,000 from the father), and the nuclear genome (biparental). In any case, agreement between anthropological, population genetics, phylogeographic, and linguistic data has provided the most interesting results. In a now classic study, Cavalli-Sforza and colleagues (1988) compared a cladistic tree of all world languages with a genetic tree using ethnicities from the entire world. The results showed a high congruence; some incongrui Continued on next page

11 512 CHAPTER 43 MAMMALS Human evolution (continued) ties were explained by historic events related to invasions of humans to new territories and language imposition. The body of knowledge obtained on H. sapiens has led researches to suggest: a first migration out of Africa 90,000 years ago through northeast Africa toward Eurasia; a migratory episode related with an ecological catastrophe and the resulting mass extinction of numerous lineages of humans around 70,000 years ago; a first colonization of Australia around 70,000 years ago over the Torres Strait, followed by a predominant isolation due to a rising sea level; a final colonization of Europe some 40,000 years ago implied the subsequent extinction of H. neanderthalensis (the last individuals found in southern Europe (Gibraltar), which is dated back to 28,000 years ago); several colonizations of America over the Bering Strait beginning 30,000 40,000 years ago; independent domestication of animals and plants on different continents between 10,000 and 6000 years ago, which led to independent settlements and a population s growth explosions; a subsequent colonization of Polynesia and New Zealand only about 1500 years ago, stemming from a previous colonization of southeast Asia; and a high level of genetic diversification among African ethnicities compared to a low genetic diversity in other ethnicities on other continents (Europe, America, Asia). Other specific hypotheses continue to be submitted for analysis, among which the following stand out: extinction of H. neanderthalensis from competition and without significant genetic interchange with H. sapiens; intellectual development linked to duplication and to certain transposons located at strategic positions on the genome; adaptation of the predominant blood group O in native Americans to resistance to syphilis, but not to gastric ulcers produced by Helicobacter pylori; processes of domestication of livestock (sheep, goats, cattle) related to lactose tolerance; predominance of the Rh factor in the first human groups of Europe; tolerance to malaria in African ethnicities through sickle cell anemia and strains of the human immunodeficiency virus (HIV); continuous transmission of viruses between humans and the Old World animals (less in the New World), which facilitated recurrent acquisition of antibodies and thus competitive human colonization; sexual dimorphism due to female neotenic morphological features related to sexual attractiveness; and scant genetic diversity in native Europeans, but rapid development of external adaptive characters, such as the loss of melanin related to better transformation of provitamin into vitamin D. Finally, it is worth pointing out that the old concept of human races was defined by human perception of superficial characters (skin color, eye color, nose shape, hair type), which are actually determined by a very few genes and influenced by rapid climatic changes (glaciations, desertifications). That has led to an erroneous historical perception of particular human races because the greatest diversity is retained in humans of the continent of Africa. The erroneous definition of human races was interpreted based on morphological features related to a few genes (color of eyes, skin, hair, etc.). For that reason some were surprised that most genetic diversity was found in African ethnicities rather than in that of all other ethnicities. In the photographs, from left to right, children of Bubi, Oromo, Mediterranean, Central European, and Chinese ethnicities. long ago by other ancestors of vertebrates such as the lineage of Aves and hair were useful in successfully colonizing the coldest environments. Perfecting the eye, not only on land but also in aquatic environments, also unleashed an adaptive race between mammalian predators and prey, as well as between mammals and birds, which became the most competitive animals on land and in the air. Mammals show a considerable reduction

12 PABLO VARGAS 513 in the number of bones with respect to ancient saurians, but they have a larger encephalic cavity. The stirrup of the ear was already present in tetrapods, but the hammer and anvil bones of the inner ear are unique to mammalians. The presence of a mandible consisting only of the dentary bone is used to identify a vertebrate fossil as a mammal or not. In fact, the intermediate bones between the mandible and the cranium present in other tetrapods went on to form part of the ear in mammals. The tegumentary tissues proximal to the dentary bone gave rise to dentition, which gradually became specialized depending on diet and other functions, to the point of highly developed structures like the canine teeth of saber-tooth tigers or the tusks of elephants. Nevertheless, the most important evolutionary tendency within mammals was the evolution of the placenta. Although there is no doubt as to its unique (synapomorphic) character in mammals, the two types of placenta do not appear to have had a single origin. Specifically, the epitheliochorial (superficial) and hemochorial (intimate) placentas have appeared and disappeared many times throughout the evolutionary history of mammals. If one assumes that the ancestral placenta was epitheliochorial, since it is present in marsupials, then a change to a hemochorial placenta occurred in the most basal lineages of placentals, to later appear as an epitheliochorial placenta in independent groups such as the lemuriformes (lemurs), moles of North America (Scalopus), and in the broad group that includes cetaceans, hippopotamuses, ruminants, swine, and perissodactyls. Therefore, this is a convergence (parallelism) that has occurred at least three times in the evolution of mammals. This is interpreted as a strong tendency toward developing a more efficient secondary epitheliochorial placenta. Specifically, the contact between the uterine epithelium and the trophoblast remains primary; however, this stage is not followed by an invasive phase and is therefore more superficial. The contact not being as intimate as in a hemochorial placenta makes the alimentary function of this secondary placenta more efficient (flow rate by exchange surfaces). Some other evolutionary tendencies inferred from kinship relationships between monotremes, marsupials, and placentals are: birth of increasingly underdeveloped young, well-separated digestive and urogenital openings, and ribs increasingly limited to the thoracic region. Biogeography and Biodiversity Many biogeographers think that most land organisms of a certain size have remained in the territories where they originated. This has been especially true for the large groups of mammals, which are primarily distributed over different continents. Indeed, following the specific works of P. L. Sclater for birds and of A. de Candolle for plants, A. R. Wallace defined six biogeographic regions in 1876 based on the overall distribution of mammals (see Chapter 47, Biogeography). The principal distribution of the 28 orders is shown in Table Although the Australian Region includes the most ancient groups (monotremes and marsupials) 5 orders and 18 families of endemic marsupials the number of orders and families is comparatively low, since there are few native terrestrial placentals (Figure 43.5). In contrast, there is a more or less equal distribution of large groups of placentals on the other four continents. The Nearctic region (North America) is home Figure 43.5 The wallaby (Macropus parma, left) and the koala (Phascolarctos cinereus, right) belong to the same order of marsupials (Diprotodontia).

13 514 CHAPTER 43 MAMMALS TABLE 43.1 More recent taxonomic proposal at a suprageneric level, including 134 families and 28 orders that circumscribes the 5200 extant species of mammals Note the agreement with the Tree of Mammals. Geographical distributions of orders are indicated when restricted to one or two continents. Subclass Prototheria Order Monotremata (Australia, New Guinea) Family Tachyglossidae (echidnas) Family Ornithorhynchidae (platypus) Subclass Theria Infraclass Metatheria (marsupials) Order Didelphimorphia (America) Family Didelphidae (opossums) Order Paucituberculata (America) Family Caenolestidae (Incan shrew-opossums, shrew-opossum, paucituberculates) Order Microbiotheria (America) Family Microbiotheriidae (monito del monte) Order Diprotodontia (Australia, Asia) Family Phascolarctidae (koalas) Family Vombatidae (wombats) Family Phalangeridae (cuscus and brushtail possums) Family Potoroidae (betongs, potoroos and kangaroo rats) Family Macropodidae (kangaroos and wallabies) Family Burramyidae (pigmy possums) Family Pseudocheiridae (ring-tailed possums) Family Petauridae (opossums and gliding marsupials) Family Tarsipedidae (honey possum) Family Acrobatidae (feathertail glider and feather-tailed possum) Order Peramelemorphia (Australia, New Guinea) Family Peramelidae (bandicoots) Family Peroryctidae (spiny bandicoots) Order Dasyuromorphia (Australia) Family Thylacinidae (Tasmanian tiger, extinct) Family Myrmecobiidae (numbat) Family Dasyuridae (Tasmanian devil, marsupial cats, marsupial mice, marsupial rats) Order Notoryctemorphia (Australia) Family Notoryctidae (marsupial moles) Infraclass Eutheria (placentals) Order Macroscelidea (Africa) Family Macroscelididae (elephant shrews) Order Afrosoricida (Africa) Family Tenrecidae (tenrecs) Family Chrysochloridae (golden mole) Order Tubulidentata (Africa) Family Orycteropodidae (aardvarks) Order Hyracoidea (Africa) Family Procaviidae (hyraxes or dassies) Order Sirenia Family Dugongidae (dugongs) Family Trichechidae (manatees) Order Proboscidea (Africa, Asia) Family Elephantidae (elephants) Order Xenarthra (America) Family Bradypodidae (three-toed sloths) Family Megalonychidae (two-toed sloths) Family Dasypodidae (armadillos) Family Myrmecophagidae (anteater) Order Lagomorpha Family Ochotonidae (pikas) Family Leporidae (rabbits, hares) Order Rodentia Family Aplodontiidae (mountain beaver) Family Sciuridae (squirrels) Family Beaveridae (true beavers) Family Geomyidae (pocket gophers, gophers) Family Heteromyidae (kangaroo rats) Family Dipodidae (gerbils) Family Muridae (rats, mice, voles) Family Anomaluridae (false flying squirrels) Family Pedetidae (Cape spring-hare) Family Ctenodactylidae (comb rats) Family Gliridae (dormice) Family Bathyergidae (mole rats) Family Hystricidae (Old World porcupines) Family Petromuridae (dassie rats) Family Thryonomyidae (cane rats) Family Erethizontidae (New World porcupines) Family Chinchillidae (chinchillas, viscachas) Family Dinomyidae (pacaranas) Family Caviidae (guinea pigs) Family Hydrochaeridae (capybaras) Family Dasyproctidae (agouties) Family Agoutidae (pacas) Family Ctenomyidae (tuco-tucos) Family Octodontidae (degus) Family Abrocomidae (chinchilla rats) Family Echimyidae (spiny rats, tree rat) Family Capromyidae (hutias) Family Myocastoridae (coypu)

14 PABLO VARGAS 515 TABLE 43.1 (continued ) Order Scandentia (Asia) Family Tupaiidae (tree shrews, bamboo squirrels) Order Dermoptera (southeast Asia) Family Cynocephalidae (colugos, cobegos) Order Primates Family Daubentoniidae (aye-aye) Family Lemuridae (true lemurs) Family Lepilemuridae (sportive lemurs) Family Galagidae (bushbabies) Family Lorisidae (lorises) Family Cheirogaleidae (dwarf lemurs, mouse lemurs) Family Indriidae (ring-tailed lemurs, wooly lemurs) Family Tarsiidae (tarsiers, spectral tarsier) Family Cercopithecidae (Old World monkeys) Family Hominidae (hominids) Family Hylobatidae (gibbons) Family Callitrichidae (titi monkeys, tamarins) Family Cebidae (marmosets, capuchin monkeys) Order Soricomorpha Family Soricidae (shrews) Family Talpidae (moles, desmans) Family Solenodontidae (solenodons) Order Erinaceomorpha Family Erinaceidae (hedgehogs) Order Cetacea Family Balaenopteridae (blue rorqual, humpback whale) Family Eschrichtiidae (gray whale) Family Balaenidae (right and bowhead whales) Family Neobalaenidae (pigmy whale) Family Physeteridae (sperm whale) Family Ziphiidae (ziphids) Family Platanistidae (Ganges and Indus dolphins) Family Delphinidae (dolphins) Family Monodontidae (narwhal, beluga whale) Family Phocoenidae (porpoises) Order Artiodactyla Family Suidae (pigs, boars) Family Tayassuidae (peccaries, hogs) Family Hippopotamidae (hippopotamuses) Family Camelidae (camels, llamas) Family Tragulidae (mouse-deer) Family Giraffidae (giraffe, okapi) Family Moschidae (musk deer) Family Cervidae (deer, elk) Family Antilocapridae (pronghorns) Family Bovidae (goats, antelopes) Order Pholidota (Africa, Asia) Family Manidae (pangolins) Order Carnivora Family Felidae (cats, lynxes) Family Viverridae (genets, civets) Family Herpestidae (mongoose, ichneumon) Family Hyaenidae (hyenas, aardwolf) Family Canidae (wolves, foxes) Family Ursidae (bears) Family Otariidae (sea wolves, sea lions) Family Phocidae (seals, sea elephants) Family Odobenidae (walrus) Family Mustelidae (otters, martens) Family Procyonidae (raccoons, coatis) Order Perissodactyla Family Equidae (horses, zebras) Family Tapiridae (tapirs) Family Rhinocerotidae (rhinoceros) Order Chiroptera Family Pteropodidae (flying foxes, fruit bats) Family Emballonuridae (bats) Family Craseonycteridae (bumblebee bat) Family Rhinopomatidae (mouse-tailed bat) Family Nycteridae (hollow-faced bats) Family Megadermatidae (false vampires) Family Rhinolophidae (horseshoe bats) Family Phyllostomidae (New World leaf-nosed bats) Family Mormoopidae (naked-back bats, moustached bats) Family Noctilionidae (fisherman bats) Family Mystacinidae (New Zealand short-tailed bats) Family Molossidae (free-tailed bats) Family Myzopodidae (sucker-footed bats) Family Thyropteridae (disc-winged bats) Family Furipteridae (smokey bat, thumbless bat) Family Natalidae (funnel-eared bats) Family Vespertilionidae (common bats)

15 516 CHAPTER 43 MAMMALS Figure 43.6 Giraffa camelopardis angolensis in Etosha National Park (Namibia). The giraffe (Giraffidae camelopardis) and the okapi (Okapia johnstoni) form the family Giraffidae, which is endemic to Africa. to 10 orders, but only two endemic families. The Neotropical region (Central America and South America) has 12 orders, of which 3, and 22 families, are endemic. The Palearctic region (Europe, most of Asia, and North Africa) is without a doubt the most extensive and has 14 orders, but only 2 endemic families. The Ethiopian region (almost all of Africa, Madagascar, and Arabia) is much richer, not only for the number of orders (15) but also for the high levels of endemism shown by 2 orders and 17 families (Figure 43.6). Finally, the Oriental region (southeast Asia and nearby islands) is host to 13 native orders (2 of them endemic) and 5 endemic families. Undoubtedly, the four last glaciations have determined the current distribution of mammals, particularly in the Nearctic and Palearctic regions. This geographical structuring of taxa provides biological support for the theory of continental drift. With few exceptions, the phylogeny of the groups of taxonomic orders supports a divergence of lineages specific to each one of the four ancient main continents. Profound diversification of mammals from the most recent common ancestor of placentals distributed over the supercontinent of Pangaea coincides with further drifting of continents during the Jurassic. First of all, in the Cretaceous, the Boreoeutheria mammals (Laurasiatheria + Euarchontoglires) in Laurasia and the Atlantogenata mammals (Afrotheria + Xenarthra) in Gondwana were separated (although see unresolved Xenartha in the Tree of Mammals). Toward the end of the Cretaceous there was another separation of continents and of groups of mammals in Laurasia, resulting in Laurasiatheria (Eurasia) and Euarchontoglires (North America). In the Southern Hemisphere, there was a parallel separation resulting in Xenarthra (South America) and Afrotheria (Africa). More recent phylogenomic analyses suggest a simultaneous separation of Boreoeutheria, Xenarthra, and Afrotheria some 120 million years ago, with Boreoeutheria then separating into Laurasiatheria and Euarchontoglires some millions of years later. This basal pattern of vicariance is, as expected, less robust when reconstructing kinship relationships of most recent lineages of mammals. For example, predominant geographical isolation affected the evolution of shrews (Crocidura) in the Paleartic (Europe and Asia) differently from that of African species. It has been proposed that Africa was independently colonized from the Paleartic on several occasions in the last 7 million years, making use of the three continents proximity. Similarly, the effects of the most recent glaciations, especially the Last Glacial Maximum (about 21,000 years ago), forced some species to disperse rapidly (Figure 43.7). For example, the broad distribution of some species connecting the Nearctic and Palearctic regions, such as the wolf (Canis lupus) or the brown bear (Ursus arctos), is interpreted as due to very recent land bridges after the most recent glaciations. Some lineages of land mammals have been able to overcome ocean barriers for long-distance dispersal that continue to be a mystery. In fact, colonization of oceanic islands by land mammals is very infrequent. The venomous Canarian shrew (Crocidura canariensis) was discovered in 1984, and it has been posited that its presence in a semi- Figure 43.7 The Daubenton s bat (Myotis daubentonii) is distributed in the Palearctic region. In contrast to many groups of mammals, the order Chiroptera has managed to colonize all continents (except Antarctica) due to their ability to fly.