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Home , Babirusa, Chacoan peccary, Common warthog, Domestic pig, Giant forest hog, Hexaprotodon

Animal Science Publications Science

1998 Systematics and of the A. Ruvinsky University of New

M. F. Rothschild Iowa State University, [email protected]

Follow this and additional works at: https://lib.dr.iastate.edu/ans_pubs Part of the Commons, Animal Sciences Commons, Genetics Commons, and the Molecular Genetics Commons The ompc lete bibliographic information for this item can be found at https://lib.dr.iastate.edu/ ans_pubs/413. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html.

This Book Chapter is brought to you for free and open access by the Animal Science at Iowa State University Digital Repository. It has been accepted for inclusion in Animal Science Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Systematics and Evolution of the Pig

Abstract According to the traditional classification system the Artiodactyla (eventoed ), to which the pig belongs, has a complicated and diversified . It is comprised of about ten families with approximately 88 genera and more than 200 . In addition, recent investigations of mammalian phylogeny show a certain degree of similarity between Artiodactyla and (), even though they are not deeply nested within the artiodactyl . Cetacea appear to be more closely related to the members of the suborder Ruminantia, than to the two other traditionally defined suborders, and Suiformes (Graur and Higgins, 1994). The limited molecular genetic studies of artiodactyls have shown good agreement with the basic structure of their phylogeny supported by morphological data (Novacek, 1992). Current estimates indicate that the common ancestor for artiodactyla (including Cetacea) may have existed around 65 million ago (MYA) (Graur and Higgins, 1994). It seems likely that future molecular genetic research will provide additional evidence of the phylogenetic structure of this mammalian group.

The ubors derTylopoda (camelids) consists of two genera: of the Old World and American . These species have a number of very distinctive differences with other representatives of Artiodactyla. They lack typical hoofs, have a with three compartments which is very different from , and differences exist in the structure and functioning of the placenta, extra embryonic tissues and sexual organs. Many adaptations of these are unique and are absent in other Artiodactyla. It has even been suggested that camels and llamas should be considered as a separate order (Bannikov, 1980). Whether or not this is acceptable, a reasonable level of similarity between camelid species does exist and the molecular data from restriction site patterns in ribosomal DNA seem to support their common origin (Semorile et al., 1994). A common ancestor for the pig and lived approximately more than 50 MYA Qermann et al., 1995).

The ubors der Ruminantia is certainly the most advanced and numerous group in the order Artiodactyla. It includes six families, of which the largest are Cervidae () and (oxen). These two most recent suborders are represented worldwide and were enormously successful and competitive during the last 20-25 million years. The most important features that appeared during the evolution of the suborder Ruminantia were changes in the digestive physiology and morphology of the digestive organs. This made them able to ferment with increased efficiency. The se timated time of divergence between the Ruminantia and Suiformes was about 55-60 MYA (Graur and Higgins, 1994).

Disciplines Agriculture | Animal Sciences | Genetics | Molecular Genetics

Comments This is a chapter from Ruvinsky, A. and M. F. Rothschild. 1998. Systematics and evolution of the pig. In: Genetics of the Pig, M. Rothschild and A. Ruvinksy (Eds.). CABI Press. pp. 1-16. Posted with permission.

This book chapter is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/ans_pubs/413 Systematics and Evolution of the Pig

A. Ruvinsky1 and M.F. Rothschild2 1 Department ofAnimal Sc ience, University of New England, Armidale 2351, NSW, Australia; 2Department of Animal Science, 225 Kildee Hall, Iowa State University, Ames, L4 50011, USA

Introduction 2 Taxonomy and Phylogeny of the Suborder Suiformes 3 Family 3 Family Tayassuidae 3 Phylogenetic relationships 4 Taxonomy and Phylogeny of the Family 4 Systematics 4 Subfamily Babyrousinae 6 Subfamily Phacochoerinae 7 Subfamily 7 Concluding remarks 8 Taxonomy of the Sus 9 Introductory remarks 9 Sus scrofa 9 Sus salvanius 11 Sus verrucosus 11 Sus barbatus 11 Sus cekbensis 12 Sus philippensis 12 Sus cebifrons 12 Interrelationships of the species in the genus Sus 12 Conclusions 14 Acknowledgements 14 References 15

©CAB INTERNATIONAL 1998. The Genetics of the Pig (eds M.F. Rothschild and A. Ruvinsky) A. Ruvinsky and M.F. Rothschi!dl

Introduction

According to the traditional classification system the order Artiodactyla (even­ toed ungulates), to which the pig belongs, has a complicated and diversified taxonomy. It is comprised of about ten families with approximately 88 genera and more than 200 species. In addition, recent investigations of mammalian phylogeny show a certain degree of similarity between Artiodactyla and Cetacea (whales), even though they are not deeply nested within the artiodactyl phylo­ genetic tree. Cetacea appear to be more closely related to the members of the suborder Ruminantia, than to the two other traditionally defined suborders, Tylopoda and Suiformes (Graur and Higgins, 1994). The limited molecular genetic studies of artiodactyls have shown good agreement with the basic structure of their phylogeny supported by morphological data (Novacek, 1992). Current estimates indicate that the common ancestor for artiodactyla (including Cetacea) may have existed around 65 million years ago (MYA) (Graur and Higgins, 1994). It seems likely that future molecular genetic research will pro­ vide additional evidence of the phylogenetic structure of this mammalian group. The suborderTylopoda (camelids) consists of two genera: camels of the Old World and American llamas. These species have a number of very distinctive differences with other representatives of Artiodactyla. They lack typical hoofs, have a stomach with three compartments which is very different from ruminants, and differences exist in the structure and functioning of the placenta, extra embryonic tissues and sexual organs. Many adaptations of these animals are unique and are absent in other Artiodactyla. It has even been suggested that camels and llamas should be considered as a separate order (Bannikov, 1980). Whether or not this is acceptable, a reasonable level of similarity between camelid species does exist and the molecular data from restriction site patterns in ribosomal DNA seem to support their common origin (Semorile et al., 1994). A common ancestor for the pig and camel lived approximately more than 50 MYA Qermann et al., 1995). The suborder Ruminantia is certainly the most advanced and numerous group in the order Artiodactyla. It includes six families, of which the largest are Cervidae (deer) and Bovidae (oxen). These two most recent suborders are represented worldwide and were enormously successful and competitive during the last 20-25 million years. The most important features that appeared during the evolution of the suborder Ruminantia were changes in the digestive physiology and morphology of the digestive organs. This made them able to ferment cellulose with increased efficiency. The estimated time of divergence between the Ruminantia and Suiformes was about 55-60 MYA (Graur and Higgins, 1994). ISystematics and Evolution

Taxonomy and Phylogeny of the Suborder Suiformes

The Suiformes are the third and probably the more primitive lineage among Artiodactyla. Their differences relate to the structure and function of the stomach and the morphology of their teeth. The three living families within the Suiformes include Hippopotamidae (hippos), Tayassuidae () and Suidae ().

Family Hippopotamidae

There are only two genera, each containing one species, which are known as hippos. The first one is amphibius, which was very common in most of at the beginning of the 19th century. Presently these giant animals, whose mature weight may reach 3000 kg, live in very limited areas of Africa and mostly in the national parks. Hippos can be distinguished by their lack of the snout disc and by the fact that the collateral digits on each foot reach the ground (Groves, 1981). The digestive tract is very long (about 60 metres) and the stomach has three compartments. These features increase its capacity to assimi­ late cellulose quite effectively. Hippos were a good source of (one animal can produce more than 500 kg of pure meat), which was one of the primary reasons for the dramatic reduction of this species. Their diploid number is 36 (Gernike, 1965). The other genus is represented by liheriensis, the Pigmy Hippopotamus, which is only 250-260 kg, and has several differences in body composition and morphology of the teeth. The typical habitats of this species are restricted to swamp forests of West Equatorial Africa. The species is now quite rare in its natural habitat. The two genera can be traced back to the latest part of the era, while the family itself possibly originated about 11 MYA (Coryndon, 1977 as cited by Groves, 1981). The latest reconstruction, based on the investigation of the molecular evolution of the ribonuclease superfamily, predicts a later date of about 35 MYA for the separation of Hippopatamidae and Suidae (Jermann et al., 1995)

Family Tayassuidae

The family Tayassuidae (peccaries) was separated from pigs not later than in the era. Their have been found in and even in Africa. However, their modern species live only in the Americas. The peccaries, like pigs, have a snout disc, but the differences between the two families are very significant. The stomach in peccaries is subdivided into three compartments. In several features of the digestive system peccaries resemble ruminants, though whether the features developed independently or in parallel is not known. A. Ruvinsky and M.F. Rothschild I

Peccaries have three hoofs on their back legs. In addition their upper canine teeth point downwards and they have a total of 38 teeth. They have a scent­ producing gland located on their backs. Peccaries are significantly smaller than pigs with an average body size of approximately 30 kg. The Tayassuidae family, according to most recent classification (Grubb, 1993a) includes three genera and three species. The Collared (Pecari tajacu) spread across South and Central America and the southern part of . Their diploid chromosome number is 30. It is a very common species, reproducing well and used widely for , because of its good meat and leather quality. The other species is the White-Lipped Peccary (Tayassu pecan) which is bigger than the . Their diploid chromosome number is 26. Its range is from southern to the south in Central America. Hybridiza­ tion between both species is probably possible, but no hybrids with pigs have been described (Bannikov, 1980). The third species, the (Cat­ agonus wagneri), was known only through records until recently when it was discovered on the Paraguay-Bolivia- border (Wetzel, 1977). This species, as shown by Benirschke et al. (1985), differs significantly from the other two peccaries in chromosome number (2n = 20). This may indicate a consider­ able evolutionary distance between C. wagneri and other Tayassuidae.

Phylogenetic relationships

Tentative phylogenetic relationships between previously described genera and Suidae, which are discussed in the following sections, are represented in Fig. 1.1 . A lack of data prevents, at the moment, construction of a completely justified phylogenetic tree. However, the latest information on the molecular evolution of 12S rRNA (Douzery and Catzeflis, 1995) and numerous classical data have demonstrated the of the suborder of Suiformes and provide an opportunity for rough phylogenetic reconstruction. This phylogenetic recon­ struction shows three groups of species corresponding to three families within Suiformes. A recent comparative cytogenetic study confirms zoological data that Tayassuidae significantly lost homology with the representatives of Suidae and the separation might have occurred quite long ago (Bosma et al., 1995). Addi­ tional data using SINE (short interspersed repetitive elements) sequence analysis have suggested that separation of Tayassuidae and Suidae occurred less than 43.2 MYA (Yasue and Wada, 1996).

Taxonomy and Phylogeny of the Suidae Family

Systematics

The Suidae family includes the most widely spread species of non- even-toed ungulates. All of them have an elongated muzzle with a snout disc and four-toe extremities with well developed side toes. The canine teeth are ISystematics and Evolution sl

~------Pecari tajacu

~------Tayassu pecari

Phacochoerus aethiopicus Phacochoerus africanus

Potamochoerus porcus

Potamochoerus larvatus

Sus salvanius

Sus scrota Sus celebensis

Sus barbatus Sus philippensis

Sus cebifrons

Fig. 1.1. Possible phylogenetic relationships in the suborder Suiformes. The length of branches is not necessarily proportional to real time and genetic distances between taxons. The position of internal nodes as they relate to Sus in particular are not finally resolved.

large and the upper ones are curved. The stomach is simple with an additional sack. The Suidae are . This family traces back to the Oligocene era in . More than a dozen species, which belong to five genera and three subfamilies are living now and have been grouped into subfamilies and tribes (Thenius, 1970; Grubb, 1993a,b): Subfamily Babyrousinae Genus Babyrousa Species Babyrousa babyrussa (the ) A. Ruvinsky and M. F. Rothschild I

Subfamily Phacochoerinae Genus Phacochoerus Species Phacochoerus africanus (the Common ) Species Phacochoerus aethiopicus (the Cape and Somali Warthog) Subfamily Suinae Potamochoerini Genus Potamochoerus Species Potamochoerus porcus (the ) Species Potamochoerus larvatus (the ) Genus Hylochoerus Species Hylochoerus meinertzhageni (the ) Tribe Suini Genus Sus Species Sus scrofa (the Eurasian ) Species Sus salvanius (the ) Species Sus verrucosus (the ) Species Sus barbatus (the Bearded Pig) Species Sus celebensis (the Warty Pig) Species Sus philippensis (the ) Species Sus cebifrons (the ) The general taxonomy of the family seems reasonably justified. However, the taxonomy of some genera, Sus in particular, may be the subject of future reconsiderations. There are indications concerning the existence of at least two more species: Sus bucculentis and Sus heureni, which may inhabit South Viet­ nam and Flores Islands (), respectively. However, the data are not sufficient at the moment to draw any further conclusions.

Subfamily Babyrsousinae

The genus Babyrousa The Babirusa ('babi-' Indonesian, habi =pig, rusa =deer), Babyrousa baby­ russa, differs significantly from other Suinae in that it has Jong legs, a relatively small head and a body free of most . The stomach is more complex. Grass comprises the main source of food and the typical digging or rooting behaviour of pigs is not known. The canine teeth in males are considerably more developed and are very large and curved, sometimes creating a spiral. The most unusual feature is that the mandibular canine and the maxillary canine teeth are both pointed upward, which is uncommon for . The Babirusa spread across Sulawesi and nearby islands. The animals swim well and can cross rivers and even sea harbours. Females usually deliver two offspring. The adults are large in size. Local people in the past used to tame the Babirusa and transport them from place to place. The diploid chromosome number in the Babirusa is 38. Eleven of the autosome pairs and the X chromosome look almost identical to of ISystematics and Evolution the (Bosma et al., 1991a). Future molecular phylogenetic investiga­ tions may give a clearer answer concerning the origin of the Babimsa. According to Groves 0981) it is possible that the Babirusa could have phylogenetic con­ nections with the , the source group of the hippos. If this were the case, the proper systematic position for the Babirusa might be closer to the Hippotamidae family. However, a recent morphological study of the placenta and heart anatomy indicates that the Babirussa has more characters in common with pigs than with hippos (MacDonald, 1994).

Subfamily Pbacocboerinae

The genus Phacochoerus The (Phacochoerus africanus) is widespread in a majority of African countries. The name is derived from the large warts that are located on the muzzle and whose function is not known. The shape of the skull of the Warthog differs essentially from other pigs and the number of teeth is greatly reduced. The canines are large, sharp and represented in both sexes. Adults are approximately 145-190 cm in length, 65-85 cm in height and weigh 50-150 kg. Average litter size is three or four piglets. The offspring are susceptible to the cold immediately after birth and therefore do not leave a burrow, where the temperature is around 30°C constantly. Their main food is grass and the animal grazes on its knees which causes it to have callouses. Adults, in contrast to their offspring, enter the burrow backwards. The species is spread widely in Sub­ Saharan Africa, and not in the rain forests of Western Africa. In southern Africa this species has been reintroduced again for hunting. The diploid chromosome number of the Warthog is 34 (Melander and Hansen-Melander, 1980). The Cape and Somali Warthog, Phacochoerus aethiopicus, was recognized by zoologists as a separate species quite recently (Grubb, 1993b). However, palaeontologists have recognized these two as different species for a long time, mainly because of the lack of functional incisors in P. aethiopicus. The Common Warthog has two incisors in the upper jaw and usually six in the low jaw. Further comparative investigations of both species are desirable.

Subfamily Suinae

The genus Potamochoerus Potamochoerus porcus (Red River Hog) is one of the smallest African pigs. This species is widely spread in the central and southern parts of the continent. It is variable in colour and size and may be made up of several or may be even two to three separate species. The animals that live in West Equatorial Africa, for instance, are usually very bright and are red in colour with a white bar on the back, white on the muzzle and brushes of long hairs on the ears. Males from a majority of habitats are characterized by the canine apophyses (located between the ears and the nose), which in older males looks like two Is A. Ruvinsky and M. F. Rothschild I

small horns directed backwards. Length of the body varies from 100 to 150 cm. The height varies from 55 to 80 cm and the weight may reach 80 kg (Bannikov and Flint, 1989). The number of offspring ranges from three to four. The skull of P. porcus is very much like that of Sus. Groves (1981) considered that the skull structure was an indication that these genera may be more closely related or both have changed little from their more distant common ancestor. The diploid chromosome set of the Red River Hog is 34 (Melander and Hansen-Melander, 1980). However, an absence of comparative cytogenetic data (Bosma et al., 1991a) and molecular data makes it difficult to estimate the phylogenetic dis­ tance from other genera. The range of the Bush pig (Potomochoerus larvatus) is mainly to the east and south of that of P. porcus and occurs not only in East and , but even in . It is also bristly, but bristly pelage extends from the head over the whole body and gives the live animal a shaggy, crested appearance, different from the river hog. Both species are, for the most part, separated territorially but in some places their areas may overlap (Grubb, 1993b). An introgression be­ tween the species is assumed (Kingdon, 1979). The limited amount of informa­ tion about the biology and evolution of both of these species needs to be rectified.

The genus Hylochoerus The Giant Forest Hog, Hylochoerus meinertzhageni, is one of the largest wild pigs (length 155-190 cm, height up to 110 cm, weight up to 250 kg). However, it overlaps in size with the Potamochoerus species. The Giant Forest Hog of East Africa is particularly large (Grubb, 1993b). The head and muzzle are very broad and the snout is big, and well developed for extensive digging. This species and genus is a relatively recent discovery. It was found in earlier in the 20th century and is now known to be found throughout the tropical forest region of Africa. The external appearance of this animal is that it is covered with long black hair. The biology of this species is still under investigation. The diploid chromosome number of the Giant Forest Hog is 32 (Melander and Hansen­ Melander, 1980).

Concluding remarks

Palaeontology data trace the Suidae to the Oligocene (Thenius, 1970). Molecular phylogenetic data are very limited and therefore a comprehensive molecular phylogeny is still absent. It is known, however, that evolutionary rates differ significantly in different Suidae lineages. According to Groves (1981) Potamo­ choerus and Sus had already developed into their modern forms in the , while at the beginning of the the ancestors of the Warthog and Giant Hog were not different enough to be placed in different genera. Bosma et al. (1991a) assume that further cytogenetic analysis is appropriate to point out differences and similarities between chromosomes of the African pigs. It appears that current data support the close phylogenetic links between I Systematics and Evolution sl the African species (i.e. Phacochoerusaethiopicus) and the domestic pig. Figure 1.1 contains a tentative description of the phylogeny of Suidae. The three branches of the family represent modern pigs of African and Eurasian origin.

Taxonomy of the Genus Sus

Introductory remarks

Groves (1981) has presented a very comprehensive and complete analysis of the taxonomy and phylogeny of the genus Sus based on morphological, palaeonto­ logical, biogeographical and other data. Recently Groves and Grubb (1993) made a revision of Sus systematics. This analysis is summarized in the following description. At present, seven species comprise the genus Sus. Investigations for the past 150 years of this genus have taken different approaches and the number of discriminated species has varied from very few to a total of 37. It is very likely that future classifications, based on classical and molecular phylogenetic data, may change our current knowledge concerning Sus taxonomy and evolution. Wild pigs spread naturally through vast territories, covering most of Europe, Asia and some areas of northern Africa. They were introduced into North and , Australia and Oceania. Domestic pigs are very common in a majority of countries worldwide, except in those where religious restrictions exist. Several features, including teeth and skull morphology, external propor­ tions, hair and colour patterns, biochemical and molecular polymorphisms, ecology and behaviour, reproductive isolation and natural areas, are used for discrimination of the many species in the genus.

Sus scrofa (the Eurasian Wild Boar)

This is one of the most widespread mammalian species. Sus scrofa is the main ancestor for domesticated pigs and this issue is discussed in Chapter 2. S. scrofa is extremely variable in the majority of traits studied. The number of subspecies is uncertain and depends upon the definition of the subspecies. However, it is possible to discriminate at least 16 more or less distinct subspecies (Groves, 1981; Groves and Grubb, 1993). S. s. scrofa Western, Central and parts of Southern Europe S. s. attila East Europe, northern slope of Caucasus, parts of Western Siberia, Central and Western Asia. S. s. meridionalis South , Corsica and Sardinia. S. s. algira North- S. s. libica Asia Minor, Middle East, southern part of Eastern Europe S. s. nigripes Southern Siberia, Central Asia S. s. sibiricus Eastern Siberia, Mongolia S. s. ussuricus Russian Far East, Korea 110 A. Ruvinsky and M. F. Rothschild I

S. s. moupinensis Eastern , South East Asia S. s. leucomystax Japan S. s. riukiuanus Ryukyu Islands S. s. taivanus Taiwan S. s. davidi Western S. s. cristatus Eastern India, western part of Indochina S. s. affinis Southern India, Sri Lanka S. s. vittatus Malaysia, southern Indonesian Islands Areas of these subspecies are close and the level of discriminating differ­ ences may be quite small, involving size, colour, proportions, skull characters and in several cases chromosome numbers. The variation in chromosome num­ ber is a result of two distinct Robertsonian translocations, which were found in the different geographic areas of the species (Tikhonov and Troshina, 1974). The usual number of chromosomes in S. scrofa is 38 chromosomes (Bosma, 1976). However, translocation I CT I) involving chromosomes 16 and 17 and translocation II (T II) involving chromosomes 15 and 17 were found in Kirgizian and European Boars (Tikhonov and Troshina, 1978), reduces the number to 37 chromosomes in heterozygotes and to 36 chromosomes in homozygotes. A full description of these translocations is presented in Chapter 8. Adaptations of these animals to different food and climatic conditions have been amazing. The flexible behaviour of the wild boar is perhaps one of the important features providing this adaptability. S. scrofa are well adapted to Siberian winters, tropical conditions, mountains and semi-deserts. Pigs can tolerate temperature conditions from -50°C to +50°C due to well developed thermoregulation and nest building behaviour. Despite being under significant and predator pressure, there are populations of wild boar that are quite numerous in many parts of the world. Body size variations are significant among subspecies. The largest are S. s. ussuricus (males up to 300 kg) and S. s. attila (males up to 275 kg). Generally, mature weight is quite variable depending on age, sex, food availability, season and habitat. Body and head length is about 130-175 cm and height ranges up to 100 cm. The smallest forms of wild boar are from Asia. Detailed description of skulls, and osteometrical studies are published elsewhere (Groves, 1981; Endo et al., 1994). Current knowledge concerning the evolution of S. scrofa is still limited and fragmented data do not create a full-scale picture of the origin and phylogeny of the species. It is known that a fully evolved S. scrofa lived in the Biharian fauna in Europe and replaced the previously existing lineages of S. minor and S. strozzi (Hi.inermann, 1969). The facial shortening that occurred in S. celebensis and in S. scrofa has been used as a possible argument in favour of their common origin from perhaps southern or the south-eastern regions of Asia. The spread of the two above mentioned Robertsonian translocations does not contradict this possibility. However, it is obvious that an extensive molecular genetics study of the problem would be necessary before any clear conclusions can be drawn. ISystematics and Evolution

Sus salvanius (the Pygmy Hog)

This is the smallest representative of the genus. It is the second non-warty pig of the genus Sus, besides S. scrofa. Body and head length is 66-71 cm in males and 55-62 cm in females. The shoulder height is correspondingly 23-30 cm and 20-22 cm and weight is 9-10 kg and 6-7 kg in males and females, respectively (Mallinson, 1978). The basic colour is dark brown. Structure of the skull differs significantly from that of S. scrofa. The number of pairs of teats is three, instead of six pairs typical for other Sus species, and the number of piglets born is usually three to four. Ears are large and rounded. The tail is very short and the inner toes are short compared with other species in the genus (Groves, 1981). S. salvanius is distributed currently in quite a narrow part of northern Assam (India) in the long-grass belt. The number of animals in the area is very small. This species is therefore considered to be endangered. Diploid chromosome number is 38. Comparative analysis of G-bands shows that the pygmy hog chromosomes are very similar to those of domestic pig and those wild S. scrofa that possess 2n = 38 chromosomes (Bosma et al., 1983). Except for small size of the body there are relatively few characters which may serve as diagnostic for discrimination between this species and S. scrofa.

Sus ven-ucosus (theJavan Warty Pig)

This species lives now mainly in Java. Two subspecies have been described (Groves and Grubb, 1993). The most typical common feature is three warts on a specific location of the muzzle strongly developed in the adult males. Colour varies from overall black to a pale red. Size also varies from relatively large to small. Sexual dimorphism in size is greater than in other species. Diploid chromosome number is 38. In spite of some differences in G-banding and the structure of Y chromosome with S. scrofa vittatus and S. celebensis, similarity is significant (Bosma et al., 1991b). Closeness of S. verrucosus and S. scrofa vittatus is supported by the observation and precise description of interspecies hybrids in (Blauch and Groves, 1990). Several morphological features make S. verrucosus close to the other South East Asian species, S. barbatus.

Sus barbatus (the Bearded Pig)

The common name of this pig is due to the elongated whiskers around the muzzle from the mouth to the ears. A few warts on the muzzle are very typical. Mature size varies significantly between several subspecies and is on average close to that of S. scrofa. The length ranges from 100 to 160 cm and the weight is approximately 100 kg. Some males are much bigger. The Bearded Pig inhabits the Malaysian peninsula, Sumatra, Java, Borneo, Palau, Bangka, and some other islands. S. barbatus sometimes migrates and these migrations A. Ruvinsky and M.F. Rothschild I

involve thousand of animals. Fertile hybrids with S. scrofa obtained in captivity are known (Blouch and Groves, 1990).

Sus celebensis (the Sulawesi Warty Pig)

This wild pig from Sulawesi and several other islands including possibly Timor has been recognized as separate from the S. verrucosus species by Groves (1981). Recent cytogenetic analysis strongly supported this point. The diploid chromosome number is 38, but the structure of the Y chromosome is different from S. verrucosus (Bosma et al. , 1991b). Animals are usually black with a few white or yellowish hairs intermixed and they have crown tufts of hair. Other colour types have been described. The muzzle is short, like the Eurasian wild pig, and is of small size. Legs are also short, and it has small short ears with a relatively large head. It occurs on Sulawesi and other offshore islands. There are indications that S. celebensis was domesticated during the early and spread as far as Roti, a medium sized island south-west of New Guinea, where they are living now (Groves, 1981). In other places they probably have been replaced by domestic S. scrofa vittatus. The several forms of wild pigs in New Guinea could be a result of hybridization between S. scrofa vittatus and S. celebensis (Groves, 1981). It appears that strong reproductive isolation has not been developed by this species.

Sus philippensis (the Philippine Warty Pig)

According to the latest information there are sufficient arguments to discriminate this species from S. celebensisand S. barbatus(Groves, 1981 ; Groves and Grubb, 1993). It occurs on several islands of the eastern . The colour is black, sometimes with a pale snout-band and red-brown patches in the mane. This pig is smaller than S. barbatus. Further investigations of this species are desirable.

Sus cebifrons (the Visayan Warty Pig)

This small pig occurs allopatrically to S. philippensis on the west central islands of the Philippines (Groves and Grubb, 1993). The data about the biology of this species are very limited.

Interrelationships of the species in the genus Sus

A high level of morphological similarities between all species of the genus is an argument in favour of their relatively recent origin from a common ancestor. The same chromosome number and their high level of homology support this ISystematics and Evolution conclusion. However, these close relationships complicate phylogenetic recon­ struction. A possible phylogeny of the genus Sus is presented at Fig. 1.1. It follows from the previous description that, in several cases, different Sus species coexist in the same area yet have maintained significant differences in morphology, ecology and behaviour. This may be reasonably explained by a reproductive isolation that appears to exist between the species that may have contact. This is applicable to S. scrofa and S. salvanius in northern India and S. scrofa and the 'Indonesian' species: S. barbatus, S. verrucosus and S. celebensis. However, interspecies hybridization with S. scrofa can occur and this probably indicates a limited reproductive isolation (Groves, 1983). Fertile hybrids between a European Wild Boar and Bearded Pig sows (S. barbatus) have been reported (Lotsy, 1922). Hybridization between S. scrofa and S. verricosus has been recorded fairly recently in Java (Blauch and Groves, 1990). According to Groves 0996, personal communication) in some parts of the Philippines the indigenous wild pigs (especially S. cebifrons) are in danger of being hybridized out of existence by crossing with domestic pigs. Groves 0981) assumed that the ancestors of these species were separated at lea5t in Middle Pleistocene, but this may have happened much longer ago. Discriminant analysis based on 16 morphological traits was used to evaluate the level of differences and similarities among the Sus species (Groves, 1981). Results from this analysis are given in Fig. 1.2 and reveal that there are

verrucas us ,. -----, ' / / ' \ I \ I I I I I ,,,,..,,.---- -:...... I / I / \ ' I / ,,. \ '' I ,' \ ', ,, / celebensis

:\ ~ ',___~<' ' I ------' '\ ~,~------, \ \ ,. \ \ \ ' \ / J \ \ I \ ( I ' \ 1 ',, \ I ',, \ I I .... \ ' ..... ' I scrota'...... /l,, ...... , ...... \ I ...... ,,,. ' ..... , I ' , ' I ...... ,.,..,,,,. -- barbatus-----

Fig. 1.2. Representation of morphological similarities based on discriminant analysis between S. scrota, S. verrucosus, S. celebensisand S. barbatus. (From Groves, 1981, with permission.) A. Ruvinsky and M.F. Rothschild I

some overlaps of the four species based on several factors in the discriminant functions. A hypothetical scenario of Sus evolution has been suggested (Groves, 1981). He proposed that the verrucosurbarbatus lineage, which has been present from the beginning of the Pliocene in Europe, entered Indonesia about 2 MYA. It appears that these animals cohabited with the older celebensis lineage. S. scrofa may possibly have evolved out of the celebensis lineages and entered Europe about 700,000 years ago, where it replaced verrucosus-like pigs. The high level of similarity in chromosome structure of S. scrofa and S. celebensis does not contradict this hypothesis. Several independent sets of data support a Far East origin of S. scrqfa and steady spreading in a westerly direction. The previously mentioned Robertsonian translocations, which are typical for some Siberian, Central Asian and European populations, probably appeared and became fixed in the populations after or during their western movement. Numerous investigations have been devoted to comparing geographic distribu­ tion of alleles for blood group antigens, isozymes and other proteins, but have not directly used these data as arguments in resolution of the problem of the species origins (Gorelov, 1994). Further study of this problem may yield more information. It seems very likely that South East Asia and the Indonesian Islands may have played a special role in the Sus speciation and evolution.

Conclusions

The information presented in this chapter gives the general overview of the systematic position and phylogeny of the wild ancestors of the domestic pig. The family Suidae appeared during the evolution of the early Oligocene relatively soon after separation of the suborder Suiformes from other Artiodactyla. From a morphological point of view the Suiformes are more primitive and less specialized. Suidae has spread widely across Africa, Europe and Asia. Sus itself appeared in the Lower Pliocene at least 3-5 MYA in Europe and Indonesia. A distribution of these ancestors' species through the Indonesian Islands was possibly essential for speciation within the genus. One of these species, S. scrqfa, was tremendously successful and spread through Asia and Europe replacing previous species. A number of more or less distinctive subspecies emerged and some of them were independently involved in the process which began over 5000 years ago.

Acknowledgements

We wish to express our gratitude to Dr Colin P. Groves from the Australian National University, whose critical comments were very important and useful and also for permission to reproduce Fig. 1.2. ISystematics and Evolution

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