| 1 | Systematics and Phylogeny of Cattle |
AlexandreHassanin
UniversitĂ© Pierre et Marie Curie and MusĂ©um national dâHistoire naturelle, Paris, France
Introduction
Systematic Position of the Genus Bos
Description of Bos Species
Bos primigenius Bojanus, 1827
Bos bison Linnaeus, 1758
Bos gaurus C.H. Smith, 1827
Bos javanicus dâAlton, 1823
Bos mutus (Przewalski, 1883)
Bos sauveli Urbain, 1937
Phylogenetic Relationships Among Species of Bovina
Classifications of the tribe Bovina based on morphology
Molecular phylogenies
Fossil Record and Biogeography
Rapid radiation and dispersal of Bovina during the Middle Pliocene
Evolution of the yakâbison lineage in the northern hemisphere
Acknowledgements
References
Introduction
Cattle belong to the subtribe Bovina, a taxonomic group represented by a single genus, Bos , which contains six wild species that were widely distributed in the Palearctic, Nearctic and Indomalayan regions during the Late Pleistocene and Holocene epochs (Plate 1): (i) Bos primigenus â aurochs (now only represented by domestic forms, humpless cattle and humped cattle or zebu); (ii) Bos bison â American bison (in the western half of North America) and European bison (reintroduced in Poland and a few adjacent countries); (iii) Bos gaurus â gaur (in India and mainland Southeast Asia); (iv) Bos javanicus â banteng (in Southeast Asia); (v) Bos mutus â yak (throughout the Tibetan Plateau); and (vi) Bos sauveli â kouprey (formerly in northern and eastern Cambodia and adjacent countries). The present classification differs from that of the IUCN (2012) by the fact that American and European bison are not considered as two separate species of the genus Bison , but are treated as two subspecies of Bos bison (see below for details).
The most fascinating aspect in the evolution of Bos is that four species have been domesticated since the Neolithic period: B. primigenius , B. mutus , B. javanicus and B. gaurus . Today, there are more than 1.5 billion cattle and zebu around the world (FAO, 2011), 14 million domestic yaks in the Tibetan Plateau and adjacent Asian highlands (Leslie and Schaller, 2009), 2.6 million Bali cattle, a domesticated banteng of Indonesia (Martojo, 2012) and more than 100,000 mithun (or gayal), a domesticated form of gaur found in the hill regions of Bangladesh, Bhutan, northeast India, Myanmar and China (Simoons and Simoons, 1968; Mondal et al., 2010). Domestic cattle provide an important part of the food supply for many of the worldâs people, either as livestock for meat or as dairy animals for milk. In many rural areas, they are still used as draught animals. Before the Neolithic period, populations of wild cattle were very successful and widely distributed across Europe, North Africa, Asia and North America (Plate 1). Today, domestic forms are present on all arable land on Earth, whereas wild species are restricted to small and isolated populations in a few countries. The aurochs, Bos primigenius , which was the ancestor of most breeds of domestic cattle, became extinct in 1627 (Van Vuure, 2005). Field scientists have not reported a living specimen of kouprey (B. sauveli ) in Southeast Asia since the 1980s, suggesting that it is also extinct (IUCN, 2012).
Despite the obvious importance of cattle in the emergence and development of human civilizations, several aspects of their evolutionary history still remain poorly understood. In this chapter, I review the systematic position of the genus Bos , give a brief description of wild species and discuss ancient and recent phylogenetic hypotheses of interspecies relationships. I also propose a biogeographic scenario explaining their past and current geographic distributions.
Systematic Position of the Genus Bos
Cattle belong to the order Cetartiodactyla (Fig. 1.1), which is the second most diversified order of large mammals after Primates (IUCN, 2012). Members of this taxonomic group were originally divided into two different orders: ArtioÂdactyla and Cetacea (e.g. Wilson and Reeder, 2005). Artiodactyls are even-toed ungulates including ruminants, pigs, hippos and camels. They were originally present on all continents, except Antarctica and Australasia, and most domestic livestock come from this group, including cattle, sheep, goats, pigs and camels. They are characterized by two main limb features: a paraxonic foot, which means that the axis of the limb support passes between the third and fourth digits; and in the ankle, the astragalus is âdouble-pulleyedâ, i.e. with a trochlea for the tibia and an opposing trochlea for the navicular, which enhances hind limb flexion and extension and allows very limited lateral rotation of the foot. Cetaceans include whales, dolphins and porpoises. All are marine animals except a few species of freshwater dolphins. The common ancestor of Cetacea acquired many adaptations for an aquatic life, such as a fusiform body, forelimbs modified into flippers, no hindlimbs or rudiments and a tail fin (fluke) used for propulsion (Muizon, 2009; Uhen, 2010).
Molecular studies have recovered a sister-group relationship between cetaceans and hippos, indicating that Artiodactyla is paraphyletic (Irwin and Arnason, 1994; Gatesy et al., 1996; Montgelard et al. , 1997). In addition, they have shown that Ruminantia, Cetacea and HippopotÂamidae form a clade named the Cetruminantia by Waddell et al. (1999) (e.g. Shimamura et al. ,1997; Gatesy et al. , 1999; Hassanin et al., 2012). To render the classification compatible with the molecular phylogeny, Montgelard et al. (1997) proposed to place all species of Artiodactyla and Cetacea into the same order, called Cetartiodactyla. After several years of controversy between molecular biologists and morphologists, a paraxonic foot and a double-pulley astragalus were found in Eocene whales (Gingerich et al., 2001), confirming that cetaceans evolved from terrestrial cetartiodactyls.
Cattle belong to the suborder Ruminantia (Fig. 1.1), which is the most diversified group of Cetartiodactyla, with 214 species related to goats, sheep, deer, pronghorn, giraffes and chevrotains. Ruminants are herbivores, which are primarily defined by rumination, i.e. the digestion is done through a process of regurgitation, rechewing and reswallowing of foregut digesta (Mackie, 2002). Since this process greatly facilitates the digestion of plant fibres, it is clear that rumination largely explains the evolutionary success of ruminants. All ruminants are able to digest cellulose through the enzymes produced by various microorganisms (bacteria and eukaryotes, such as ciliates and fungi) that are contained in the rumen, the most developed compartment in their stomach. The ruminant stomach is composed of three other compartments: the reticulum, omasum and abomasum. The reticulum retains particles larger than 1 mm in the rumen (Zharova et al., 2011). The main function of the omasum remains little known, but it filters particles depending on their size, serves as a suction pump controlling the flow of digesta (liquid and particles) between the reticulum and abomasum, facilitates the reabsorption of water, volatile fatty acids, ammonia, sodium, potassium and carbon dioxide, and participates in fibre digestion (Hackmann and Spain, 2010). The last compartment, the abomasum, corresponds to the glandular stomach: secreting acid, its function is very similar to that of the stomach of monogastric mammals such as humans.
Ruminants have well-adapted teeth characterized by the presence of an incisiform lower canine, which is adjacent to the lower incisors, and a horny pad that replaces the upper incisors. All modern and fossil representatives of the group are diagnosed by an osteological autapomorphy, which corresponds to the fusion of the cuboid and navicular bones in the tarsus. Molecular studies have confirmed the monophyly of Ruminantia, as well as the major division between Tragulina and Pecora (Hassanin and Douzery, 2003; Matthee et al. , 2007; Hassanin et al., 2012). The infra-order Tragulina is represented by only a few species of chevrotains, which are found in tropical forests of the Old World. The infra-order Pecora contains all other families, i.e. Bovidae (see below), Cervidae (deer), Moschidae (musk deer), Giraffidae (giraffes and okapi) and Antilocapridae (pronghorn). According to the most recent estimations (Hassanin et al., 2012), Pecoran families diverged rapidly from each other at the Oligocene/Miocene boundary, between 27.6 ± 3.8 Ma and 22.4 ± 2.4 Ma. During the Early Miocene, most habitats in Western Europe and Africa were forested; whereas those of Eastern Europe, Asia and North America were more open (Prothero and Foss, 2007). The spread of open habitat grasses at the Oligocene/Miocene was promoted by a global environmental change, when the warming Late Oligocene was interrupted by a brief but deep glacial maximum at the Oligocene/Miocene boundary (Stromberg, 2005). All these paleoecological data suggest that the emergence of modern pecoran families took place in the northern hemisphere, most probably in Eastern Eurasia. Then, the families dispersed and diversified rapidly: Antilocapridae and a group of extinct Moschidae (BlastomeryÂcinae) entered into North America; Cervidae and other Moschidae stayed in Eurasia; Bovidae and Giraffidae appeared suddenly throughout the Old World (Prothero and Foss, 2007).
Cattle belong to the family Bovidae (Fig. 1.1), which is the most successful family of the suborder Ruminantia (139 species). Bovids are characterized by the structure of the horns. Present in all males and sometimes females, these consist of a permanent bone core covered by a non-branched and non-deciduous sheath of keratin. Wild representatives of the family are found on all continents except Australia, Antarctica and South America. Most older classifications recognize between five and eight subfamilies within the Bovidae (e.g. Simpson, 1945; McKenna and Bell, 1997; Wilson and Reeder, 2005), but molecular studies have concluded there exists a major divis...