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.

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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 con- vergent 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.

U , - enough, the interesting fossil register left mainly by the organisms, in spite of their great organic complexity. bones of mammals makes a well-documented histori- Because of human beings’ interest in learning about cal reconstruction possible, although not without gaps. ourselves, and our intense study of species—either Mammals are thought to have been one of the domi- phylogenetically related (apes, chimpanzees), com- nant groups on Earth since the extinction of the dino- mercially useful (cows, goats, sheep), or medically saurs some 65 million years ago, not only because of the useful (mouse, rat)—we have been able to understand number of species (but see Chapter 34, Coleopterans), the evolution of mammals in detail. As if this were not but also because of their size and the adaptability of

What is a mammal? Mammals (from the Latin mamma [teat]) are verte- primitive sinapsids (amniote tetrapods) that appeared brates with constant body temperature, hair, cere- in the Early Permian. Several radiations of mammals bral neocortex, and, in particular, the females that occurred in the last 65 million years, after the develop mammary glands that produce milk with mass extinction of dinosaurs, have been described. which they feed their young. All extant mammals Since then, they have diversified into multiple lin- descend from a common ancestor dating back to eages of species adapted to land, water, and air the Late Triassic, more than 200 million years ago. environments. Specifically, present-day mammals descend from

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than extant species (Figure 43.1). Because the bones BOX 43.1 Morphological characters are so easily fossilized, there is a fairly ample mammal unique to mammals fossil record available. The five species of monotremes • Mandible consists of only the dentary bone. form a whole order of mammals, and are considered living fossils because they combine characteristics com- The dentary bone joins directly to the squamous • mon to the other mammals (hair, production of milk, bone of the cranium, making the mandibular joint. three bones in the ear, diaphragm, and heart with four • There are three bones in the middle ear (hammer, chambers) and to the sauropsids (laying eggs, feet with anvil, and stirrup), except in the monotremes spurs on hind legs of males, cranium tapering toward (reptilian ear). the beak-shaped snout, corneous beak). One platypus • All species develop hair to a greater or lesser degree. and four echidnas make up this ancient lineage, which • Mammary glands (derived from sebaceous glands) has survived in Australia and nearby islands in the face secrete milk, the necessary food for mammal young. of vigorous competition from placentals. Two hundred of the 275 species of marsupials are also Australian, which clearly shows that the island continent of Aus- many groups to nearly all the ecosystems on the planet. tralia has facilitated an independent and parallel evolu- Moreover, many mammal species are at the top of the tion of mammals with characteristics similar to those of trophic pyramid, making their ecological role one of su- placentals (in Australia there are few native placentals). preme interest. However, they had to wait for their evo- Standing out among the most notable paleontological lutionary moment, some 60 million years ago, for their findings is a marsupial (Sinodelphys) in a surprising impressive differentiation, even though the lineage that state of preservation, even with detectable hairs. Con- gave rise to them, starting with the therapsids, had comitant in space (China) and time (approximately appeared long before that. In fact, the extinction of the 125 Mya) with fossils, marsupials is the most ancient dinosaurs unleashed several adaptive radiations that placental found (Eomaia). Due to the wide diversity of launched a number of lineages and species of mammals placentals (some 5500 species) developed in the last 125 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 BOX 43.2 Mammals by the numbers extant. Therefore, their evolutionary tree requires a combined knowledge of the fossil record and of ex- • Number of species: some 5500 placentals, 5 tant species. The first division of mammals in the strict monotremes, and around 275 marsupials. 70% sense separates the prototherians (eotherians, allote- of mammal species are rodents rians, and monotremes) and the therians (tritubercu- • Number of genera: about 1200 lata, pantotherians, metatherians or marsupials, and • Genera with the greatest number of species: eutherians or placentals), both with extant and extinct Crocidura (about 90 species), Myotis (about 90 groups. The term mammaliaformes is used to include a species), Rhinolophus (about 65 species) clade of mammals and related extinct forms. Mamma- • Number of families: 134 (although it varies liaforms derived from the therapsids (an extinct group, depending on the author) with the exception of the mammaliaforms), which be- • Number of orders: 28 (although it varies substantially long to the synapsids (sister group to the sauropsids; depending on the author) see Chapter 44, Sauropsids). Finally, the synapsids • Orders with the greatest number of species: are considered “mammal-like reptiles” because they Rodentia (rodents) and Chiroptera (bats) include the lineage that would give rise to the mam- Origin of extant mammals: Late Triassic (about 200 maliaforms. To give an idea of their systematics, the • Mya) evolutionary line of mammals would include a hierar- chical classification of taxonomic groups nested within • Oldest fossil: Sinodelphys (China), genus of marsupial from about 125 million years ago; Eomaia more inclusive groups: the synapsids, the pelycosaurs, (China), genus of placental from about 120 million the therapsids, the cynodonts, and modern mammals. years ago To establish a timeline, it can be said that the first true mammal appeared in the Late Triassic (approximately • Longest-lived mammal: Homo sapiens (110–120 years) 220 Mya), that is, approximately 70 million years after the appearance of the first therapsids and 30 million • Largest mammal: blue whale (Balaenoptera years after the appearance of the first mammaliaforms. musculus), at 160 tons Extant mammals have been reduced to three large • Smallest mammal: bumblebee bat (Craseonycteris groups: monotremes, marsupials, and placentals (see thonglongyai ), at 2 grams Tree of Mammals), of which there are also more extinct

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Basic terms Allantoic placenta: Extraembryonic placenta the position of this last is controversial), and the (allantois) originating as an extension or evagination extant order Monotremata (echidnas and platypus). of the endoderm of the embryo’s primitive digestive Prototherians are characterized by being therians tube. The allantois surrounds the embryo between with the squamous bone in the posterior of the the amnion and the chorion, or is located caudally cranium joined directly to the mandible, and for to the vitelline sac. developing the flat bone on the wall of the posterior Cerebral neocortex: Neural layer that covers the temporal fossa. prefrontal lobe; developed in the more evolved Synapsids: Tetrapods forming the group of mammals areas of the mammalian cortex. These areas are and other extinct mammaliaforms. closely related to memory and intelligence. Therapsids: Synapsids that include the direct line to Epitheliochorial placenta: Type of superficial mammals. placenta in which the maternal and fetal epithelia Therians: Viviparous mammals whose females have are in contact. teats, and are grouped into an independent subclass. Evagination: Protuberance or hollow protrusion of an Trophoblast: Group of cells developed as a basic organism’s duct or cavity. part of the placenta, forming the outer layer of the Hemochorial placenta: Type of placenta in which blastocyte and providing nutrients to the embryo. the membrane surrounding the fetus (chorion) is “Ungulates”: Mammals characterized by having in intimate and direct contact with the maternal hooves. “Ungulates” have turned out to be circulatory system. polyphyletic due to the blurred definition of “Insectivores”: Mammals characterized by small a hoof and the character’s convergence. The body size, plantigrade feet, nocturnal habits, following orders used to be considered “ungulates”: and complete dentition mostly related to eating Hyracoidea, Sirenia, Proboscidea, Perissodactyla, invertebrates. They form a polyphyletic group. Artiodactyla, Cetaceae, and occasionally, Oviparity: Reproductive mechanism by which eggs Tubulidentata. are deposited in the external environment, where Viviparity: Mechanism by which animal progeny they complete their development before hatching. develops from embryos within the female’s womb. Prototherians: Oviparous mammals in a subclass Placental viviparism is undoubtedly the most consisting of the extinct orders Docodonta, advanced and appears only in mammals. Multituberculata, and Triconodonta (although

million years, most of the characteristics described in sion, in which fragmentation of chromosomes at the this chapter refer to this group of mammals. centromere allows the two parts to migrate with two arms each. This same mechanism is observed in some Characteristics of Mammal more recent groups, and with great variation in the number of chromosomes, as in the Old World shrews. Genomes Specifically, the genus Crocidura displays an increase The mammalian nuclear genome is distributed in a in chromosomes from a low number in a group of nu- variable number of chromosomes, not only among merous Palearctic and Asiatic species (2n = 22–40) to a groups, but also within a single group (Laurasiathe- high number in an Afrotropical group, also with nu- ria); for example, the diploid number (2n) ranges from merous species (2n = 42–60). Nevertheless, the most 6 chromosomes in the Indian muntjac deer (Muntiacus effective mechanism in gene duplication is polyploidy, muntjac) to 72 in the South American short-eared fox although it is much less important in mammals than in (Atelocynus microtis). Nevertheless, in spite of so much other organisms, such as plants (see Chapter 12, Angio- variation, mammals retain the X sex chromosomes sperms). For a specific example, a polyploid number that characterize females (XX), and the Y sex chromo- (tetraploid) has been described in a plains viscacha rat some that characterize males (XY). The rearrangement (Tympanoctomys barrerae), a rodent adapted to the Ar- of chromosomes and their packaging have resulted in gentine desert, which has the highest number of chro- the evolution of very different karyotypes. Many au- mosomes (2n = 102) known in mammals. A correlation thors agree that the most likely base number in mam- has been found between the number of chromosomes mals is 2x = 2n = 14, given that it appears in numerous and the vital characteristics of mammals, specifically marsupials and in placentals with ancestral characters. between a larger size of the genome and an evolution To explain the high number of chromosomes, cytoge- toward a lower basal metabolic rate and a larger cell neticists turn to multiplication via chromosome fis- size, mainly in red blood cells (erythrocytes).

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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)

Magnorder Epitheria (epitheria)

Grandorder Anagalida (rodents, lagomorphs, Grandorder Archonta (primates, bats, colugos, elephant shrew Anagole, Mimotona, Gomphos) tree shrews Adapisorex, Nyctitherium, Micropternodus) Grandorder Ferae (carnivorans, pangolins, Creodonta, Hyaenodon) Grandorder Ungulata (aardvark, perissodactyla, whales, artiodactyla, elephants, Infraclass Holotheria Subclass Theriiformes Grandorder Llipotyphia (tenrec, hedgehogs, hyracoids, manatees, Meridiungulata, moles, Adapisorex, Dimylus, Micropternodus) Palaeorycteropus, Uintautherium, Arctocyon)

Figure 43.1 A synthesized taxonomic proposal of extant included some 5000 species, as well as a supraspecific and extinct mammals based on the work of McKenna and taxonomic treatment of 425 families and 46 orders (brown Bell (1997, Classification of Mammals Above the Species denotes a group that is extinct.) Level. New York, NY: Columbia University Press), which

Through Homo sapiens’ presence in the group of been necessary to resort to alternative explanations— vertebrates in general, and of mammals in particu- such as complex gene interaction—to understand the lar, the quantified genome (amount of DNA or 2C great diversity in the morphological and physiologi- value)Figure has 43.1 been determined for numerous placentals cal development of mammals. To this end, complete (657 species by the year 2013; see updates at www. genomes are needed. genomesize.com). Today there are also completely Indeed, the level of knowledge about mammalian sequenced mitochondria available (approximately kinship relationships is growing faster than that of 17,000 base pairs) for almost 700 species of mammals most of the great groups of living things. At the be- (see updates on www.ncbi.nlm.nih.gov). Additionally, ginning of the twentieth century, kinship relationships many ongoing projects have provided incomplete ge- were investigated based on blood immunity tests. In nome sequencing (draft genomes). By 2007, complete the 1980s, reliable phylogenetic reconstructions were genome sequencing included the following species: done based on polypeptides—Miyamoto and Good- human being (Homo sapiens), chimpanzee (Pan trog- man sequenced eight polypeptides for 107 species in lodytes), domestic cow (Bos taurus) (Figure 43.2), dog 1986. In the 1990s, cytochrome b was used to recon- (Canis lupus familiaris), horse (Equus caballus), rhesus struct phylogenetic relationships among cetaceans, ar- macaque (Macaca mulatta), rat (Rattus norvegicus), and tiodactylans, sirenids, primates, and rodents. The era mouse (Mus musculus). Six years later, approximately of phylogenomics began in the early twenty-first cen- twenty more genomes of mammals were sequenced, a tury, with the goal of sequencing complete genomes notable increase in enormous datasets that are useful of orders and families of mammals. Now, thousands for phylogenomics. The human genome has more than of genes and millions of nucleotides are already be- 20,000 coding genes— too small a number to account ing concatenated, but the number of species for which for the complex diversity observed. The one gene–one we have complete genomes is still too small to allow enzyme hypothesis, which dominated most of the complete resolution of the mammalian tree (see Tree twentieth century, is so extremely simple that it has of Mammals).

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ers (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 “Insectivo- ra”) should be emphasized. It has often posed significant classification problems because of the absence of unique characters and the confusion created by recur- Figure 43.2 The first complete genomes sequenced of rent evolution of some morphological traits. This has mammals were those of the human being, the chimpanzee, resulted in the old group of “insectivores” becoming a the cow, the dog, the horse, the rhesus macaque, the rat, and the mouse. The photograph shows a Hereford cow taxonomic black box. Interestingly, phylogenies have (named after Hereford County in southwest England), which made it possible to reclassify several families of the for- was used for the complete sequencing of the cow (Bos mer “insectivores” as follows: Erinaceidae (hedgehogs taurus) genome. and moonrats) in the order Erinaceomorpha; Soricidae (shrews), Talpidae (moles and desmans), and Solen- odontidae (solenodons) in the order Soricomorpha; Phylogenetic Results Contrasted Tenrecidae (Malagasy tenrecs and African otter-shrews) and Chrysochloridae (African golden moles) in the or- with Previous Classifications der Afrosoricida; Macroscelididae (elephant shrews) in From the very first classifications (Aristotle) to those the order Macroscelidea; and Tupaiidae (tree shrews) of authors like Linnaeus (1758), Gregory (1910), Simp- in the order Scandentia. DNA phylogenetics have also son (1945), and McKenna and Bell (1997), there has al- resolved the systematics problem of the former order ways been special interest in a classification to which of “ungulates,” which for many authors was another human beings belong. In fact, there are three key as- black box including “hoofed mammals” (see Evolution pects to these classifications: the first is naming the of Characters that follows). 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 paleon- Evolution of Characters tologists have pursued in the past two centuries. The The appearance in mammals of five key characters— third is reconstructing the phylogeny based on DNA ontogeny of the mandible, the mandibular joint, three sequences. As a consequence, the most important goal bones in the middle ear, the development of hair, and has been to propose a combined classification of fos- the production of milk— has always intrigued re- sils and extant species based on evolutionary groups. searchers. While paleontologists have been able to in- Undoubtedly, the classification of mammals published terpret whether the three bone characters could have by George Gaylord Simpson (1945) was the most sig- been present in extinct mammals, the presence of hair nificant during a large part of the twentieth century. and mammary glands is more difficult to reconstruct This paleontologist, cofounder of the modern theory because these features are unlikely to be fossilized. of evolution in the first part of the twentieth century, Another extremely important character that is hard to updated all the data on extant and fossil species. More trace in the development of mammals is viviparity. than 50 years would have to go by before McKenna The presence of oviparity only in the most basal lin- and Bell published a similar but much more complete eage (monotremes) confirms that viviparity appeared work. Figure 43.1 shows a classification of supraspe- very early in the evolution of mammals and was then cific taxa (425 families in 46 orders) based on these au- retained throughout their diversification (see Tree of thors’ work and further kinship results. Mammals). Marsupials belong to the group of therians Significant conflicts appear in the most internal along with placentals, although they still share some nodes of mammal phylogeny based on DNA sequences ancestral characters with the monotremes (the rectum (see Tree of Mammals). Phylogenomics will shed fur- and the urogenital system open jointly into a common ther light on large group relationships. Certainly, the cloaca, and there is no true placenta). Without a doubt, position of the group of armadillos, sloths, and anteat- their most noteworthy character is the marsupium, a

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The enigmatic origin of elephants (Afrotheria) The largest animals on earth (elephants) and in the Woolly or tundra mamoth † ocean (whales) continue to be enigmatic due to 7–6 MYA (Mammuthus primigenius) the difficulty in reconstructing the group of extant Asian elephant mammals closest (sister group) to each. Phyloge- 9–6.5 MYA (Elephas maximus) netic reconstructions based on DNA sequences African bush elephant not only of living species but also on fossils are c. 4 MYA (Loxodonta africana) 28–24 MYA shedding new light on the origins of both groups. African forest elephant (Loxodonta cyclotis) Elephants (family Elephantidae) are repre- c. 60 MYA sented today by two African elephants (the African American mastodon † bush elephant Loxodonta africana and the African (Mammut americanum) forest elephant Loxodonta cyclotis) and one Asian elephant (Elephas maximus). The phylogenies that have reconstructed the kinship relationships of Phylogenetic tree of extinct (†) and living proboscideans based elephants have been enriched by the sequencing of the on complete mitochondrial sequencing. wooly or tundra mammoth (Mammuthus primigenius) from tissues well preserved in ice; it is also a species morphological characters related the sirenoids (order of the family Elephantidae, which became extinct after Sirenia) directly with the proboscideans (order Probos- the last glaciation. The morphological characters of the cidea). Starting from the first molecular phylogenies, skeleton and the teeth indicate that the mammoth was additional candidates for closest relatives have gradually Figure UNB 1 more closely related to African elephants than to Asian appeared (aardvark, hyrax, sirenids). Determining the elephants. However, the resulting tree, based on DNA closest relative (sister group) would help to reconstruct sequences and the fossil record, shows a resolution in the appearance of the ancestor that gave origin to ele- which the mammoth is closer to the Asian elephant than phants. However, phylogenomic reconstructions are not to African elephants, with a divergence time of 7–6 mil- conclusive and posit three hypotheses: (i) hyraxes (order lion years ago. Divergence between the African bush el- Hiracoidea), sister group to the proboscideans; (ii) a lin- ephant and the forest elephant occurred some 4 million eage of the orders Hiracoidea and Sirenia as the sister years ago. Within the family Elephantidae, these two lin- group to the proboscideans; and (iii) the order Sirenia, eages split in the last 9–6.5 million years. An exceptional sister group to the proboscideans (classic hypothesis). study of fossil DNA has made it possible to sequence The mass extinction of living things between the Creta- the complete mitochondrial genome not only of these ceous and the Tertiary (65 Mya), leading to the disap- elephants, but also of an American mastodon (Mammut pearance of dinosaurs, also caused rapid appearances americanum) from a piece of tooth from 50,000–130,000 and disappearances of numerous lineages of mammals, years ago, found in Alaska. The resulting mitogenomic making a single reconstruction of kinship relationships study shows a separation between the elephant lineage difficult. Specifically, the absence of extant lineages from (Elephantidae) and the mastodon lineage (family Mam- 60–30 million years ago prevents us from reconstructing mutidae) near the end of the Oligocene (28–24 Mya). the sister group to the proboscideans. Pending the dis- Nevertheless, one of the most fascinating enigmas is covery of key fossils, the last phylogenies better support the relationship between the proboscideans and the rest an ancestor of Hyracoidea and Sirenia as the closest of the living mammals. The classic hypothesis based on group to elephants and their relatives.

(a) (b) (c)

The most recent common ancestor of (a) the African elephant years ago. (c) The tiny Cape hyrax (Procavia capensis, South (Loxodonta africana, South Africa) and (b) the Asian elephant Africa) is, surprisingly, one of the closest living relatives of (Elephas maximus, Thailand) diverged more than 6 million elephants.

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The enigmatic origin of whales (Laurasiatheria)

The 15 species of true whales (suborder Mysticeti) be- (a) long 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 (Cetartiodac- tyla). Note that the similarities between cetaceans and sirenids (order Sirenia) are owed to morphological convergences as a consequence of two independent (b) 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 (Hippopot- amidae) 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 Hippopot- The enormous bones of beached whales appear today on seashores. They were deposited in sedimentary soils amidae. Moreover, the fossils of true hippopotamus in the same way, resulting in the numerous cetaceans appear much later (Miocene). In any case, the radiation fossils that are being discovered. Top: Humpback whale that the cetaceans underwent 55–37 million years ago (Megaptera novaeangliae) skeleton on Fernandina Island (Eocene) makes a more precise reconstruction difficult. (Galápagos Islands, Ecuador). Bottom: Southern minke whale Indeed, the cetacean fossil record for this period is (Balaenoptera bonaerensis) in Tierra de Fuego (Argentina). especially rich, and as a result the conquest of the sea is understood to have been immediately and profusely Figure UNB 2 photos successful. Studies of comparative anatomy show that Future paleontological and phylogenomic studies cetaceans are more specialized now than they were are needed for a more precise reconstruction of the con- then. The body plan formed in the Eocene was very suc- quest of the ocean by the group of mammals that gave cessful, and is associated with the rapid differentiation rise to the largest vertebrates that have ever existed. of more than six different lineages in this short period.

fold of skin covering the breasts and forming an epi- bryo’s primitive digestive tube. The placenta, which dermal pouch that functions as an incubation cham- joins the fetus and the mother very intimately, gives ber (Figure 43.3). The young are born underdeveloped the young the clear advantage of being born in a very and have to crawl from the vagina to the marsupium, advanced stage of development—although it puts the where they feed on milk until they complete their de- burden of their survival on the mother before birth velopment. Before birth, they are retained in the mater- during the delicate gestation period. nal uterus for a long time, fed by an allantoic placenta Undoubtedly, mammals provide one of the most (coming from outside the embryo) that originates as an spectacular examples of adaptive convergence. Spe- extension or evagination of the endoderm in the em- cifically, it has been observed that marsupials isolated

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(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 Figure 43.3 The kangaroo Macropus fuliginosus in evolutionary periods. Yanchep National Park, Perth, Australia. The birth of underdeveloped young carried in the marsupium allows kangaroos to flee shortly after giving birth. Evolutionary Tendencies Mammals owe their success to certain evolutionary on the continent of Australia have arrived at the same tendencies that have made it possible for them to be evolutionary solutions as placental mammals on other very competitive. Homeothermy—already achieved continents. Parallelism between the wolf (Canis lupus) and the extinct Tasmanian tiger or wolf (Thylacinus cyn- (A) ocephalus) 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). Com- parison 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 (B) 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 homol- ogy of the hoof character is extremely complex, making the term inconsistent in classification and tending Figure 43.4 The top photograph shows an ancestral to circumscribe groups that are difficult to designate character (horny beak) as well as a morphological conver- taxonomically (black box). Phylogenies have served gence (feet with interdigital membranes suited for swimming) to reclassify this artificial group into the following between (A) the marsupial platypus (Ornithorhyncus anatinus) orders: perissodactyls, artiodactyls, and cetaceans and (B) the placental beaver (Castor canadensis).

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Human evolution The study of human evolution (hominization) has a start- orism of forms such as Paranthropus. Thanks to the ef- ing point at the separation of the lineage of chimpanzees forts of paleontologists in the last 50 years, numerous (Pan troglodytes) and bonobos (Pan paniscus) from the fossil remains of some 12 species of Homo that ap- lineage that gave rise to the genus Homo 7–5 million peared and disappeared approximately in the following years ago. Numerous lineages in the evolutionary line sequence (analytical taxonomy): H. habilis (2.5–1.4 Mya of Homo (hominins) have gone extinct. Hominins form in eastern Africa), H. erectus (2–0.3 Mya in Africa and a subtribe of erect hominids that includes Homo and Eurasia), H. rudolfensis (1.9 Mya in Kenya), H. ergaster other genera that appeared approximately in the follow- (1.9–1.25 Mya in eastern Africa), H. georgicus (1.8–1.6 ing order: Sahelanthropus 7–5 million years ago, Orrorin Mya in the Caucasus), H. cepranensis (0.8 Mya in Italy), about 6 million years ago, Ardipithecus 5.5–4.5 million H. antecessor (0.8–0.35 Mya in western Europe), H. years ago, Australopithecus 4 million years ago, and heidelbergensis (0.6–0.25 Mya in Europe and Africa, H. Paranthropus between 2.6 and 1.1 million years ago. rhodesiensis (0.3–0.12 Mya in Zambia), H. neanderthal- The fossil record shows there was a notable differentia- ensis (0.23–0.024 Mya in Europe and east Asia), H. flo- tion of these hominins in the past 7 million years, due to resiensis (0.10–0.012 Mya in Indonesia), and H. sapiens their successful adaptation to bipedalism in the African (0.25 Mya to the present, over the entire world). Given savannahs followed by a major extinction of genera and that H. sapiens is the only living species of the genus, species around 2.8 million years ago, due to Africa’s reconstructing the kinship relationships among species progressive desertification. A number of characteristics is primarily in the hands of paleontologists. In contrast, were crucial to the evolutionary success of hominins: reconstruction of H. sapiens lineages is addressed cranial capacity, rectilinear spine, widening of the pelvis, mainly by methods that range from physical anthropol- opposing thumb, acute vision, less specialized dentition, ogy to linguistics, passing through population genetics, vocal anatomy specialized for phonation, legs adapted phylogenomics, biogeography, and phylogeography, to bipedalism, and social behavior. All these charac- among other disciplines. During the past 25 years, phy- ters are in a very tiny percentage of genes making up logeography has specifically had a decisive influence only 0.23% of the differences between the genomes of on the level of understanding of H. sapiens’ evolutionary bonobos and humans. In fact, when the complete Homo history. Phylogeography has made reconstruction of sapiens genome was sequenced in 2003, the one gene– human evolution possible based on genetic haplotypes one enzyme hypothesis, which had reigned for most of and the analysis of lineage relationships in a geographic the twentieth century, fell defeated in favor of an expla- framework (map below) (see Chapter 55, Analysis of nation of morphological and physiological diversity also Genetic Variation and Intraspecific Phylogenies). Making related to gene interactions. use of the genetic characteristics (molecular markers) of It seems that the appearance of Homo is linked to H. sapiens, lineage relationships can be reconstructed the shift to carnivorism from the predominant herbiv- with some independence using regions of mitochondrial DNA (mitochondria are inherited exclusively from the mother), the human Y chro- 35,000 mosome (inherited exclusively 30,000 from the father), and the nu- 40,000 clear genome (biparental). In any case, agreement between 100,000 70,000 anthropological, population 125,000 genetics, phylogeographic, and linguistic data has pro- 200,000 vided the most interesting results. In a now classic study, 10,000 Cavalli-Sforza and colleagues 1500 (1988) compared a cladistic 60,000 1500 tree of all world languages with a genetic tree using eth- Early Homo sapiens nicities from the entire world. Colonization by neanderthals The results showed a high Asian colonization by H. sapiens congruence; some incongrui- The appearance of Homo sapiens in Africa and the gradual colonization of all continents. (Dates in years; updated from Burenhult 2010, Die ersten Menschen, http://en.wikipedia.org/ wiki/Early_human_migrations) Continued on next page

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Human evolution (continued) ties were explained by historic events related to in- and without significant genetic interchange with H. vasions of humans to new territories and language sapiens; imposition. • intellectual development linked to duplication and to certain transposons located at strategic positions on The body of knowledge obtained on H. sapiens has led the genome; researches to suggest: • adaptation of the predominant blood group O in native • a first migration out of Africa 90,000 years ago Americans to resistance to syphilis, but not to gastric through northeast Africa toward Eurasia; ulcers produced by Helicobacter pylori; • a migratory episode related with an ecological catas- • processes of domestication of livestock (sheep, goats, trophe and the resulting mass extinction of numerous cattle) related to lactose tolerance; lineages of humans around 70,000 years ago; • predominance of the Rh– factor in the first human • a first colonization of Australia around 70,000 years groups of Europe; ago over the Torres Strait, followed by a predominant • tolerance to malaria in African ethnicities through sickle isolation due to a rising sea level; cell anemia and strains of the human immunodeficiency • a final colonization of Europe some 40,000 years ago virus (HIV); implied the subsequent extinction of H. neander- • continuous transmission of viruses between humans thalensis (the last individuals found in southern and the Old World animals (less in the New World), Europe (Gibraltar), which is dated back to 28,000 which facilitated recurrent acquisition of antibodies and years ago); thus competitive human colonization; • several colonizations of America over the Bering • sexual dimorphism due to female neotenic Strait beginning 30,000–40,000 years ago; morphological features related to sexual attractiveness; • independent domestication of animals and plants on and different continents between 10,000 and 6000 years • scant genetic diversity in native Europeans, but rapid ago, which led to independent settlements and a development of external adaptive characters, such as population’s growth explosions; the loss of melanin related to better transformation of • a subsequent colonization of Polynesia and New provitamin into vitamin D. Zealand only about 1500 years ago, stemming from a Finally, it is worth pointing out that the old concept of previous colonization of southeast Asia; and human races was defined by human perception of super- • a high level of genetic diversification among African ficial characters (skin color, eye color, nose shape, hair ethnicities compared to a low genetic diversity in other ethnicities on other continents (Europe, type), which are actually determined by a very few genes America, Asia). and influenced by rapid climatic changes (glaciations, de- sertifications). That has led to an erroneous historical per- Other specific hypotheses continue to be submitted for ception of particular human races because the greatest analysis, among which the following stand out: diversity is retained in humans of the continent of Africa. • extinction of H. neanderthalensis from competition

The erroneous definition of human races was interpreted based than in that of all other ethnicities. In the photographs, from on morphological features related to a few genes (color of left to right, children of Bubi, Oromo, Mediterranean, Central eyes, skin, hair, etc.). For that reason some were surprised that European, and Chinese ethnicities. most genetic diversity was found in African ethnicities rather

long ago by other ancestors of vertebrates such as the unleashed an adaptive race between mammalian preda- lineage of Aves—and hair were useful in successfully tors and prey, as well as between mammals and birds, colonizing the coldest environments. Perfecting the eye, which became the most competitive animals on land not only on land but also in aquatic environments, also and in the air. Mammals show a considerable reduction

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in the number of bones with respect to ancient saurians, liochorial placenta. Specifically, the contact between the but they have a larger encephalic cavity. The stirrup of uterine epithelium and the trophoblast remains pri- the ear was already present in tetrapods, but the ham- mary; however, this stage is not followed by an invasive mer and anvil bones of the inner ear are unique to mam- phase and is therefore more superficial. The contact not malians. The presence of a mandible consisting only of being as intimate as in a hemochorial placenta makes the dentary bone is used to identify a vertebrate fossil the alimentary function of this secondary placenta more as a mammal or not. In fact, the intermediate bones be- efficient (flow rate by exchange surfaces). tween the mandible and the cranium present in other Some other evolutionary tendencies inferred from tetrapods went on to form part of the ear in mammals. kinship relationships between monotremes, marsupi- The tegumentary tissues proximal to the dentary bone als, and placentals are: birth of increasingly underde- gave rise to dentition, which gradually became special- veloped young, well-separated digestive and urogeni- ized depending on diet and other functions, to the point tal openings, and ribs increasingly limited to the tho- of highly developed structures like the canine teeth of racic region. saber-tooth tigers or the tusks of elephants. Nevertheless, the most important evolutionary tendency within mammals was the evolution of the pla- Biogeography and Biodiversity centa. Although there is no doubt as to its unique (sy- Many biogeographers think that most land organisms napomorphic) character in mammals, the two types of of a certain size have remained in the territories where placenta do not appear to have had a single origin. Spe- they originated. This has been especially true for the cifically, the epitheliochorial (superficial) and hemo- large groups of mammals, which are primarily distrib- chorial (intimate) placentas have appeared and disap- uted over different continents. Indeed, following the peared many times throughout the evolutionary history specific works of P. L. Sclater for birds and of A. de of mammals. If one assumes that the ancestral placenta Candolle for plants, A. R. Wallace defined six biogeo- was epitheliochorial, since it is present in marsupials, graphic regions in 1876 based on the overall distribu- then a change to a hemochorial placenta occurred in the tion of mammals (see Chapter 47, Biogeography). The most basal lineages of placentals, to later appear as an principal distribution of the 28 orders is shown in Ta- epitheliochorial placenta in independent groups such ble 43.1. Although the Australian Region includes the as the lemuriformes (lemurs), moles of North America most ancient groups (monotremes and marsupials)—5 (Scalopus), and in the broad group that includes ceta- orders and 18 families of endemic marsupials—the ceans, hippopotamuses, ruminants, swine, and peris- number of orders and families is comparatively low, sodactyls. Therefore, this is a convergence (parallelism) since there are few native terrestrial placentals (Figure that has occurred at least three times in the evolution 43.5). In contrast, there is a more or less equal distribu- of mammals. This is interpreted as a strong tendency tion of large groups of placentals on the other four con- toward developing a more efficient secondary epithe- tinents. 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).

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

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TABLE 43.1 (continued )

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

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nata mammals (Afrotheria + Xenarthra) in Gondwana were separated (although see unresolved Xenartha in the Tree of Mammals). Toward the end of the Creta- ceous there was another separation of continents and of groups of mammals in Laurasia, resulting in Laura- siatheria (Eurasia) and Euarchontoglires (North Amer- ica). In the Southern Hemisphere, there was a parallel separation resulting in Xenarthra (South America) and Afrotheria (Africa). More recent phylogenomic analy- ses 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 pro- posed 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 Figure 43.6 Giraffa camelopardis angolensis in Etosha ago), forced some species to disperse rapidly (Figure National Park (Namibia). The giraffe (Giraffidae camelopardis) 43.7). For example, the broad distribution of some spe- and the okapi (Okapia johnstoni) form the family Giraffidae, cies connecting the Nearctic and Palearctic regions, which is endemic to Africa. 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 to 10 orders, but only two endemic families. The Neo- mammals have been able to overcome ocean barriers tropical region (Central America and South America) for long-distance dispersal that continue to be a mys- has 12 orders, of which 3, and 22 families, are endemic. tery. In fact, colonization of oceanic islands by land The Palearctic region (Europe, most of Asia, and North mammals is very infrequent. The venomous Canarian Africa) is without a doubt the most extensive and has shrew (Crocidura canariensis) was discovered in 1984, 14 orders, but only 2 endemic families. The Ethiopian and it has been posited that its presence in a semi- 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 Orien- tal 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, par- ticularly 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. Pro- found diversification of mammals from the most recent common ancestor of placentals distributed over the Figure 43.7 The Daubenton’s bat (Myotis daubentonii) supercontinent of Pangaea coincides with further drift- is distributed in the Palearctic region. In contrast to many ing of continents during the Jurassic. First of all, in the groups of mammals, the order Chiroptera has managed to Cretaceous, the Boreoeutheria mammals (Laurasiathe- colonize all continents (except Antarctica) due to their ability ria + Euarchontoglires) in Laurasia and the Atlantoge- to fly.

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desert connection is due to a long-distance dispersal chrome b sequences do not imply a cause-and-effect re- event from Africa reaching the western Canary Islands lationship between cytochrome b and speciation—this (about 100 km distance) in the Pleistocene. The docu- gene is not necessarily involved in speciation—but may mented record for the farthest long-distance dispersal be useful as an indicator of speciation. The case is made by land mammals belongs to the ancestor of eight spe- that genetic change is not always accompanied by mor- cies of rice rats (genera Oryzomys, Nesoryzomis, Megao- phological change, so that in these cases taxonomists ryzomys) endemic to the Galápagos Islands, whose an- cannot see that a new species has been produced. These cestor had to cross a distance of almost 1000 km from morphologically difficult-to-detect species are called the nearest continent, South America (see Chapter 48, cryptospecies. Molecular phylogenetics helps at this Evolution on Islands). point. It is clear that recognition of such species based solely on genetic changes conflicts with traditional mammal taxonomy, which is based on morphology. It Differentiation and Speciation has been calculated that more than 2000 mammal cryp- The differentiation of mammals into species (almost tospecies would have to be described and added to the 6000) is certainly impressive, although less spectacu- 5200 species that are currently recognized. Therefore, lar than that of other groups of vertebrates such as genetic separation between populations would drive birds (approximately 10,000 species). The fossil record speciation, whether species are morphologically identi- shows a great accumulation of mammal bones from fied by humans (taxonomists) or not. The Genetic Spe- the beginning of the Tertiary. One of the most impor- cies Concept has coexisted with the Biological Species tant mass extinctions of all time (Cretaceous) was para- Concept for most of the twentieth century; according doxically an ally, allowing for the expansion of mam- to the latter, the driving force for speciation is repro- mals after some of their lineages survived and began ductive isolation (reproductive barriers). In any case, to initiate processes of radiation. This unleashing of mammal researchers (mammalogists) consider these an active process of divergence and ecological specia- two concepts together with some others (see Chapter tion in a short period of time (adaptive radiation) also 46, Speciation) to determine which ones best explain occurred in later geological periods in almost all of the process of speciation in each case. the most important groups of mammals. An example Contrary to what many biologists think, mammals among marsupials are the American opossums, which also hybridize. There are classic sporadic cases of hy- diversified into five main lineages adapted to different brids between horses and donkeys (mules) or between ecological environments in Central America in about tigers and lions (tigons and ligers), which imply com- 15 million of years (65–50 Mya). Cetaceans experi- plete isolation and no fertility. It must be taken into ac- enced a radiation between 55 and 37 million years ago count that unless hybridization between populations is (Eocene), when six whale families split and the body interrupted, the process of speciation is more difficult plane seen today became established (see Box The enig- to achieve. But how can isolation processes be detected matic origin of whales). The differentiation of the more on the evolutionary tree of mammals? By considering than 1000 species of bats in the last 60 million years in- that the mechanisms acting in the present could also dicates clear success in mammals’ conquest of the air. have acted in the past, one can gain understanding of In much more recent periods (<7 Mya), the Old World significant phylogenetic signals. Many authors sur- shrews of the genus Crocidura differentiated into more mise that the resolution of the relationships between than 50 species, which resulted in one of the most ex- the three large clades of placentals (Afrotheria, Xen- plosive radiations of mammals. arthra, and Boreoeutheria) will not have support, re- The mechanisms of such an evolutionary success gardless of the larger sampling of genes and species. are related to genome characteristics, acquisition of To date, DNA sequences of over 30 megabases (= 30 the placenta, and the capacity for evolutionary change millions of base pairs) have been obtained for the phy- when environmental conditions change. For mammals, logenomic reconstruction of mammals. However, the as for many other groups of organisms, the accumula- kinship relationships among the three clades remain tion of genetic changes in two isolated populations can unresolved. This has been interpreted as the result of result in the genetic isolation of two lineages and forma- an evolutionary process, rather than lack of molecular tion of two species over time. Authors who defend the characters with reliable phylogenetic signal. Specifi- Genetic Species Concept argue that the key point is the cally, it is understood that a rapid process of speciation amount of time necessary for enough genetic changes took place in a group of early placentals in 2–4 million to accumulate. Some authors go further and suggest years. Incipient species diverging from the placental a speciation estimate: a speciation event in mammals ancestor could have continued hybridizing for a long can be measured when differences in cytochrome b se- period of time without becoming genetically isolated, quences exceed 5% between two monophyletic groups which would make it difficult to reconstruct a cladoge- of populations. Nevertheless, differences between cyto- netic process for mammals at deep levels.

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Principal Questions Remaining Hallström, B. M. and Janke, A. 2008. Resolution • Is the group Xenarthra (armadillos, sloths, among major placental mammal interordinal anteaters) sister to either Afrotheria or relationships with genome data imply that Boreoeutheria? speciation influenced their earliest radiations. BMC Evolutionary Biology 8: e162. • Do whales share a most recent common ancestor Kemp, T. S. 2005. The Origin and Evolution of Mammals. with hippopotamuses? Oxford, UK: Oxford University Press. • What is the closest living relative of elephants? Murphy, W. J. and Eizirik, E. 2009. Placental mammals (Eutheria). In, The Timetree of Life (Hedges, S. B. and Basic Bibliography Kumar, S., eds.), pp. 471–474. Oxford, UK: Oxford Benton, M. J. and Harper, D. A. T. 2009. Introduction University Press. to Paleobiology and the Fossil Record. Oxford, UK: Rose, K. D. 2006. The Beginning of the Age of Mammals. Wiley-Blackwell. Baltimore, MD: The Johns Hopkins University Press.

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