The Evolution of Suidae - Welcome | PalaeoBarn

AV04CH03-Larson ARI 26 October 2015 11:38

RE V I E W

S

IN

AD V A

NC

E

The Evolution of SuidaeLaurent Frantz,1 Erik Meijaard,2,3 Jaime Gongora,4

James Haile,1 Martien A.M. Groenen,5

and Greger Larson1

1Palaeogenomics & Bio-Archaeology Research Network, Research Laboratory for Archaeologyand History of Art, University of Oxford, Oxford OX1 3QY, United Kingdom;email: [email protected]/SSC Wild Pig Specialist Group, Jakarta 15412, Indonesia3School of Archaeology and Anthropology, The Australian National University, Canberra,ACT 0200, Australia4Faculty of Veterinary Science, The University of Sydney, Sydney, New South Wales 2006,Australia5Animal Breeding and Genomics Centre, Wageningen University, 6708 PB Wageningen,The Netherlands

Annu. Rev. Anim. Biosci. 2016. 4:3.1–3.25

The Annual Review of Animal Biosciences is online atanimal.annualreviews.org

This article’s doi:10.1146/annurev-animal-021815-111155

Copyright c© 2016 by Annual Reviews.All rights reserved

Keywords

pigs, hybridization, domestication, phylogeography

Abstract

The Suidae are a family of Cetartiodactyla composed of 17 species classifiedin a minimum of five extant genera that originated at least 20 million yearsago. Their success is evident in the multitude of habitats in which they arefound as both natural and feral populations in tropical Island Southeast Asia,the high plateau of the Himalayas, Siberia, North Africa, the Pacific Islands,Australia, and the Americas. Morphological and molecular analyses of thesespecies have revealed numerous aspects of their biology, including the easewith which many lineages have and continue to hybridize. This trait has madethem an ideal model for evolutionary biologists. Suid species have also shareda deep history with humans, from their association with early hominids inAfrica to their domestication. Here we review the current knowledge of thisfascinating group and provide a comprehensive evolutionary history fromthe Oligocene to the present day.

3.1

Review in Advance first posted online on November 2, 2015. (Changes may still occur before final publication online and in print.)

Changes may still occur before final publication online and in print

Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


INTRODUCTION

The Suidae are a widespread family of Cetartiodactyla that originated in the Oligocene at least20 million years ago (Ma). They last shared a common ancestor with the Tayassuidae (New WorldSuiodae) during the late Eocene/early Oligocene. The Suidae family has been extremely success-ful, having colonized the African and Eurasian continents. Given the diversity of fossil Suidae inEurasia and Africa, they have been used as a stratigraphic dating tool for decades. This diversity isstill apparent today, and the family is composed of a minimum of five extant genera made up of 17species in Africa and Eurasia. The success of these species is evident in the multitude of habitatsin which they are found, including tropical Island Southeast Asia (ISEA); the high plateau ofthe Himalayas; and the diverse environments of Siberia, central and western Eurasia, and NorthAfrica.

Morphological and molecular analyses of these species have revealed numerous aspects of theirbiology, including both their speciation and the ease with which many lineages have and continueto hybridize. This trait has made them an ideal model for evolutionary biologists, though it has alsocomplicated the identification of taxonomic species. Lastly, suid species have had a long sharedhistory with humans, from their association with early hominids in Africa, to their domestication(that today makes them a prime source of protein for billions of people), to their modern use as abiomedical model. Here we review the current knowledge of this fascinating group of organismsand provide a comprehensive evolutionary history, from the Oligocene to the present day.

THE NATURAL HISTORY OF SUIDAE

Paleontological Perspectives

Suiodae (also known as Suina or Suiformes) is a superfamily of even-toed ungulates (Cetartio-dactyla). Suiodae comprises many extant and extinct taxa of pig-like families, such as Tayassuidaein the Americas (tayassuids, peccaries, or javelinas) and Suidae (also known as suids, hogs, or pigs)in Eurasia (Figure 1). For decades the Suiodae were grouped together with Hippopotamidae(hippos) until molecular analyses (1) demonstrated that the latter are instead more closely relatedto Cetacea (whales). Taxonomic relationships within Suoidae have typically been assessed basedon morphological characters (e.g., Reference 2, 3), though molecular studies focusing on fewnuclear and mitochondrial genes (4, 5) have also been employed. Both of these approaches havelimitations, and our understanding of the early evolution of the superfamily remains limited. TheNew World (Tayassuidae) and Old World suids (i.e., Suidae; Figure 1) diverged during the lateEocene or the early Oligocene (∼34.50–39.69 Ma based on molecular estimates) (5) (Figure 1).In addition, morphological analyses of fossils have inconclusively classified multiple Eocenefossils from Eurasia (Palaeochoeridae fossils such as Doliochoerus and Palaeochoerus; Figure 1) andNorth America (e.g., Perchoerus) as crown Tayassuidae or Suidae or as stem groups of Suoidae(e.g., Reference 2). Thus, the monophyly of New World Suiodae remains uncertain, as does thepossibility that suids colonized the Americas more than once. Future molecular work (allowingfor discrimination between Eocene or Oligocene divergence) and morphological studies willsurely shed light on the early evolutionary history of these species.

Poor fossil preservation and homoplasy have made it difficult to resolve the root of Suiodae(2, 6–8), and the classification of the earliest suids dating to the Oligocene remains problematic.Given the presence of fossils found in Pakistan, however, Suidae likely had already radiated intomultiple subfamilies during the Oligocene (9). The first unequivocal and widespread appearanceof the Suidae family is found in early-Miocene deposits of Africa, Europe, and Asia (∼20 Ma; 6,10–12). By the middle Miocene (∼15 Ma), this family had colonized continental Eurasia and Africa

3.2 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


Sus strozzi†

Sus philippensis

Sus xiaozhu†

Hyotheriinae† Hyotheriinae†

Sus verrucosus

Potamochoerus larvatus

Sus barbatus

Sus celebensis

Babyrousinae

Sus peii†

Sus minor†

Perchoerus†

Phacochoerus aethiopicus

Sus scrofa

Palaeochoeridae†

Listriodontinae†

Hylochoerus meinertzhageni

Potamochoerus porcus

Sus cebifrons

Phacochoerus africanus

Tayassuidae

OligoceneEocene Miocene Pleistoscene

5.3 2.511.615.9 0 Ma2333.9

Suidae

Suinae?Suinae?Suinae?

Suoidae

Porcula salvania

Tetraconodontinae† Tetraconodontinae† Tetraconodontinae†

Cainochoerinae† Cainochoerinae†

Microstonyx†Microstonyx†

Propotamochoerus†Propotamochoerus†

Pliocene

Figure 1Phylogeny of extinct and extant Suiodae. A phylogeny of extinct and extant suid species built from molecular (5, 29) and morphological(2) studies. The † symbol represents extinct families or species. The age of each node is approximate and compiled from multiplesources of evidence. The colors of the branches represent the indigenous geographical regions of each extant species: Island SoutheastAsia (dark blue), mainland Asia (light blue), Europe (orange), and Old World ( green). Red dots indicate nodes that are supported usingmolecular analyses.

(6, 13). Recent analyses of fossil material recognized at least four subfamilies of Suidae from theMiocene: Listriodontinae, Cainochoerinae, Hyotheriinae, and Tetraconodontinae (2) (Figure 1).These Miocene subfamilies possessed a great deal of morphological diversity, likely as a result ofthe expansive geographical range they occupied (2, 13, 14). The taxonomy of these species hasbeen studied extensively, especially in Africa, given their usefulness as a bio-chronological markerand their common occurrence with early hominid fossils (i.e., 13, 15–17).

A new subfamily of Suidae, the Suinae, emerged in the fossil record in the late Miocene(>10 Ma) (Figure 1). The Suinae rapidly expanded and diversified into multiple tribes found

www.annualreviews.org • Evolution of Suidae 3.3


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


a b

Figure 2The enigmatic Babyrousa. (a) Picture of a male babirusa. (b) The oldest known cave painting in the world, dated to ∼35 ky ago andfound in Sulawesi, Indonesia, features a depiction of a Babyrousa (155).

in late-Miocene strata across Eurasia and Africa (18, 19). This subfamily’s success was such thatby the end of the Miocene almost all other subfamilies of Suidae had disappeared from the fossilrecord (2, 20). Across Eurasia and Africa, the subfamilies of Suidae, including Listriodontinae (21),Cainochoerinae (22, 23), and Hyotheriinae (24), also went extinct before the Miocene/Plioceneboundary (Figure 1). Their disappearance may have allowed or even induced the diversificationof Suinae in Africa, allowing for the emergence of the ancestors of extant sub-Saharan suids: theforest hogs (Hylochoerus), river hogs and bush pigs (Potamochoerus), and warthogs (Phacochoerus)(5, 13, 25–27). All of the subfamilies of non-Suinae also disappeared in Eurasia shortly after theMiocene/Pliocene boundary. This replacement gave rise to the ancestor of modern pigs (Sus) aswell as a myriad of other, now extinct, tribes.

By the Pliocene/Pleistocene boundary, only two remaining subfamilies of Suidae were foundacross Eurasia: the Suinae (including extant suids) and the Tetraconodontinae [including thegenera Nyanzachoerus in Africa (28) and Conohyus in Europe and South Asia (12)]. Although it isgenerally accepted that only Suinae survived to the present, the species of Babyrousa are a probableexception (Figure 2). These species have been classified as both Suinae and Babyrousinae, andrecent molecular clock analyses reported that they diverged from the extant Suinae during themiddle Miocene, around 13 Ma (18–9 Ma; 5), approximately 3 My before African and EurasianSuinae diverged from a common ancestor (14–7 Ma) (5, 29). Thus, although the inclusion ofBabyrousa within Suinae or in its own subfamily is primarily a nomenclatural issue, this debatehighlights the enigmatic nature of this genus (see sidebar, The Enigmatic Babyrousa).

Many other tribes of Suinae thrived during the Pliocene. For instance, Asian taxa included thePorcula, Sus, and endemic Sulawesi genus Celebochoerus (30). The genus Porcula is currently foundonly in a small pocket of sub-Himalayan grasslands in Northeast India, though it occurred muchmore widely [on the island of Java and in eastern China and Burma (31)] in the Pleistocene.

3.4 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


THE ENIGMATIC BABYROUSA

The enigmatic Sulawesi babirusa (Babyrousa) (meaning “pig deer” in Indonesian) is a charismatic and wrinkle-skinnedspecies. Male Babyrousa have characteristic long, thick, and often rotating upper canines (Figure 2). Little is knownabout the evolutionary history of this peculiar species, mainly because of a complete lack of extinct or extant closelyrelated species. Babyrousa is anatomically distinct from other Suidae (156–159) and is restricted to remote areasof Island Southeast Asia (i.e., Sulawesi, Buru and the the Togean Islands, Masbate, Taliabu, and Samana). Thus,this enigmatic species could be considered a relic of the once diverse but now extinct Miocene Suidae. In 2006,despite significant karyotypic differences, an unexpectedly successful hybridization between a male Babyrousa andSus scrofa took place at Copenhagen Zoo (154). The mating produced five offspring, three of which lived for monthsbefore being culled. Lastly, although never domesticated, Babyrousa have interacted with humans for millennia, ashighlighted by one of the earliest cave paintings clearly picturing a Babyrousa female (Figure 2). Babirusas are listedas vulnerable or endangered (depending on the species) by the International Union for Conservation of Nature RedList as a result of deforestation and hunting pressure for meat or Balinese ceremonial masks (160; A McDonald,personal communication).

There is a great deal of debate surrounding the chronology and geographic origins of theearliest Sus fossils (i.e., 31, 32). For instance, though claims for the earliest Sus fossils are dated tothe late Miocene or early Pliocene in Europe, paleontologists and geneticists alike have argued foran East Asian origin of the genus (20, 29). In addition, the genus may well have originated muchlater during the Pliocene (Figure 1). What is not controversial is that by the late Pliocene, thisgenus had colonized most of continental Eurasia and ISEA, effectively replacing all other Suinaegenera besides the sub-Saharan Suinae and Babyrousa.

The genus Sus then diversified into multiple species. Though many remain extant, all but one(Sus scrofa) are restricted to ISEA, including Sus barbatus (Borneo, Sumatra, and Malay Peninsula),Sus verrucosus ( Java and Bawean), Sus cebifrons, Sus oliveri, Sus ahoenobarbus, Sus philippensis (thePhilippines), and Sus celebensis (Sulawesi). Several Sus species once existed on continental Eurasia,including Sus minor from Europe and China (33), Sus strozzi from Europe (34–36), and Sus peii/Susxiaozhu from China (37), but they disappeared following the spread S. scrofa (the ancestor ofdomestic pigs) from Southeast Asia (34, 35).

Genomics Perspectives

Of the three major episodes of species replacement that took place during the evolutionary his-tory of Suidae, including (a) the disappearance of most non-Suinae (except Babyrousa) during theMiocene/Pliocene boundary, (b) the replacement of all non-Sus species in Eurasia during thePliocene, and (c) the replacement of most Sus species by S. scrofa during the Pleistocene, the latteris the best documented. Over the course of 1–2 My, S. scrofa colonized the entirety of Eurasia andNorth Africa and replaced many local species. This large-scale expansion left traces in the genomesof contemporary S. scrofa populations, including evidence of a large increase in its effective pop-ulation size (Ne) before a demographic reduction that occurred during the last glacial maximum(38, 39). S. scrofa adapted to a myriad of new environments over a relatively short evolutionarytimescale. Although they originated in the tropical forests of mainland Southeast Asia (29), thesesuids adapted to life in the high-altitude Himalayas (40), the northern latitudes of Eurasia (41),warm climates in the Near East and North Africa, and temperate climates in mainland Europe(38).



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


Selective sweeps resulting from adaptations to novel habitats during this large-scale expansionare also evident in the genomes of S. scrofa (38, 40, 41). Regulatory mechanisms (microRNAs)and olfactory receptors (ORs) were most affected by natural selection (38, 42). ORs are encodedby small open reading frames (lacking introns) that are expressed in the brain and airways. Theproducts of these genes provide the basics of the smell machinery by binding to specific odormolecules and producing a nerve impulse transmitted to the brain. The swine genome-sequencingconsortium reported that pigs carry over 1,301 OR genes (38) and over 1,113 functional ORs (non-pseudo genes; 43). This number of functional OR is approximately equivalent to the number foundin rats (1,201 ORs) and is more than that of any other mammal sequenced to date [mouse = 908,dogs = 872, humans = 457 (43)]. Moreover, the rate of pseudogenization (loss of function) atOR is lower in pigs than in any other mammalian species (∼13%; 43). The prominence of OR inthe genome of suids highlights their strong reliance on smell for foraging or mate recognition.

Interestingly, ORs are often highly variable in copy number (number of copies of genic ornongenic region) not only in pigs but in many vertebrate species (44–48). Gains and losses of ORare exacerbated in the pig genome, resulting in major copy number variations (CNV) betweenpopulations, often ranging from 1 to 40 or more copies in various populations across Eurasia(Figure 3) (42, 49). Although OR are clearly the most CNV-prone genes in the pig genome,other genes are also affected by these duplications/deletions that accumulate at a much higher ratethan single-nucleotide polymorphisms (SNPs) (1.4 times higher) (44, 49). The great evolutionarypotential of CNV at OR could have provided S. scrofa with the necessary plasticity to evolve newforaging strategies, allowing them to rapidly adapt to novel environments. Interestingly, CNV atORs also may have played a prominent role in the maintenance of reproductive isolation duringthe speciation of Sus species in ISEA, further supporting the importance of olfactory genes duringthe evolutionary history of suids (49).

Resolving Taxonomic Conflicts in the Era of Genomics

Genomic sequences are a powerful tool not only to investigate the effects of natural selection butalso to resolve conflicting taxonomic and phylogeographic perspectives of evolutionary history.In addition, genomes can also provide insights into the mechanisms underlying these conflicts.The evolutionary history of Suidae has been particularly complex (and thus controversial), thoughgenomic sequences from multiple species are now resolving these conundrums.

In 2005, Larson et al. (50) published a worldwide phylogeographic analysis of Sus speciesbased on mitochondrial DNA (mtDNA). This study demonstrated that multiple populations ofS. scrofa across Eurasia were both geographically and genetically differentiated. Despite beingmorphologically well defined, however, species in ISEA lacked any mitochondrial distinctiveness(Figure 1) (50, 51). This paradox was deepened by the lack of agreement between multiple phy-logenetic studies based on mtDNA (4, 52), and the lack of mitochondrial differentiation betweenmorphologically divergent species remained puzzling.

The advent of genome sequencing provided the necessary power to resolve this paradox (29,53). These studies demonstrated that mitochondrial genomes among ISEA Sus species had been ac-quired during hybridization episodes and therefore no longer reflected species divergence patterns(Figure 4). Although the nuclear genomes of these species had also been affected by hybridization,they possessed sufficient resolving power to generate a robust phylogenetic reconstruction and toobtain reliable divergence time estimates of the species (29).

Controversy has surrounded the taxonomy of the sub-Saharan suids as well. Although recentanalyses of nuclear and mitochondrial markers have apparently resolved the debate (5), multiple

3.6 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


AsWB01

AsWB02

AsWB03

EuWB01

EuWB02

EuWB03

AsD01

AsD02

AsD03

AsD04

AsD05

EuD01

EuD02

EuD03

EuD04

EuD05

Olfactory receptors

10

20

30

40CN

Figure 3Heat map picturing the high copy number variability for 100 olfactory receptor genes in multiple piggenomes. Rows represent different pig populations. Each column represents a single olfactory receptor.Colors correspond to the number of copies of each gene in different populations. The raw data wereobtained from Reference 42. Abbreviations: AsD, Asian domestic; AsWB, Asian wild boars; EuD, Europeandomestic; EuWB, European wild boars.

studies of fossil remains yielded contradictory results (13, 15, 54–56). The emerging consiliencenow suggests that Suidae colonized Africa from Eurasia approximately six times (57), the mostrecent of which took place in the Miocene, based upon Suinae fossils found in the Chad depositsfrom the Miocene/Pliocene boundary (∼5.5 Ma; 25). What remained unclear was whether themajor lineages of African Suinae evolved in Eurasia or Africa.

Gongora et al. (58) suggested that the direct ancestors of the major lineages of African Suinaemight have diverged outside of Africa because their divergence times (7–14 Ma) significantly



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


**

*

*

**

9.9

4.2

2.8

2.0

1.5

2.1

0.6

1.21.21.2

1 My1 My1 My 0.02 sub./site0.02 sub./site0.02 sub./site

Sus scrofaSus scrofa

Sus scrofaSus scrofaSus scrofa



Sus scrofa

Sus scrofa







Sus scrofaSus scrofa Sus scrofaSus scrofa



Phacochoerusafricanus



Sus verrucosus

Borneo

Sumatra

Sulawesi

The Philippines

Sus verrucosus

Sus verrucosus

Sus verrucosus

Sus verrucosus

Sus verrucosus

Sus cebifrons

Sus cebifrons

Sus cebifrons

Sus cebifronsSus cebifrons

Sus barbatus

Sus barbatus

Sus barbatus

Sus barbatus

Sus barbatus

Sus barbatus

Sus barbatus

Sus celebensis

Sus celebensis

Sus celebensis

Sus celebensis

Sus celebensis

Sus celebensis




Sus scrofaSus scrofa Sus scrofaSus scrofa



**

**

0.05 sub/site

d e

a

b c

Sus†

Sus verrucosus

Java

Figure 4Conflicting taxonomy across the genome of Sus species—evidence for reticulation in Asian pigs. (a) Map depicting the range of multipleSus species in mainland and Island Southeast Asia. Light gray area represents the contour of Sundaland, a large continental shelf withshallow seas that would have been exposed during glacial periods. (b) Genome-wide phylogeny of Sus species from Reference 78.(c) Mitochondrial phylogeny of Sus from Reference 29 showing all Sundaland species grouping together owing to admixture duringglacial periods. (d ) A phylogeny inferred from a small proportion of chromosome X, adapted from Reference 41, showing how NorthEurasian and South Eurasian populations cluster, most likely as a result of admixture with a now-extinct species in northern China.(e) A diagram depicting known occurrences of hybridization between Suidae species as inferred from genome sequence (29, 41, 154).

3.8 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


predated those of the earliest Suinae fossil in Africa (5.5 Ma). However, the current fossil evidenceof Potamachoerus-like fossils found in Eurasia is from the Early Pliocene strata (59, 60). Thepresence of these fossils may have resulted from the migration back out of Africa by Potamachoerusduring the Pliocene. In addition, and in direct opposition to the data from molecular phylogenies(5), paleontologists have argued that African Suinae may in fact be paraphyletic, and that theAfrican lineages are the result of at least two waves of colonization (13, 57).

These conflicting views stem from peculiar and seemingly homologous morphological char-acteristics among warty pigs found in Eurasia and Africa. The idea of a single warty pigs genus,Dasychoerus, goes back to Gray (61) and was recently resurrected by multiple authors (i.e., 13, 31,32, 57). Dasychoerus includes multiple species, such as the Java warty pig S. verrucosus, the Sulawesiwarty pig S. celebensis, and the giant forest hog Hylochoerus meinertzhageni (13). This perspectivecontradicts recent molecular phylogenies (5, 29). If the molecular sequences are correct, then thelack of monophyly among species in the Dasychoerus genus and the shared morphological features[i.e., facial warts and dental similarities (13)] must be a result of convergent evolution.

Hybridization and Taxonomic Conflicts

The recent sequencing of multiple Sus genomes (29, 38) has provided novel insights into theseparadoxes. The wealth of information afforded by genomes has allowed not only for a resolution ofmultiple, long-standing taxonomic issues (such as the Sus species in ISEA) but also for an in-depthinvestigation of the underlying mechanisms behind these paradoxes (29, 38, 41). It is now evidentthat a bifurcating classification (such as a classic phylogenetic tree, as in Figure 1) for Suidae doesnot provide a comprehensive approximation of their true evolutionary history. Instead, genomesequences have demonstrated that the evolutionary history of Sus is best explained by a reticulatehistory resulting from many episodes of interspecific admixture (Figure 4).

One clear example of the power of genomes to resolve paradoxes in Suidae is the discoveryof recent interspecific admixture events between Sus species that resulted in the apparent lack oftaxonomic information in their mtDNA (29). These interspecific admixture episodes were mostlikely induced by land bridges that appeared between the islands of Borneo, Java, and Sumatra dur-ing the glacial periods of the Plio-Pleistocene (62) (Figure 4a). Interestingly, these introgressionswere markedly asymmetrical (53), as demonstrated by the fact that whereas ∼23% of the genomeof S. scrofa populations from ISEA was acquired from the endemic Javan warty pig (S. verrucosus),only ∼5% of the genome of S. verrucosus was the result of admixture with S. scrofa (53). It is alsopossible that this asymmetry from an endemic species (S. verrucosus) into an “invasive” species(S. scrofa) (29) could have been adaptive.

The same admixture scenario likely also took place as S. scrofa expanded within China, as re-vealed by the discovery of peculiar divergence patterns and unexpected genealogies on the X chro-mosome of S. scrofa populations from southern and northern China (41). The genomic region inquestion spans multiple megabase pairs and displays extreme nucleotide divergence between north-ern and southern Chinese populations of S. scrofa compared with the rest of the genome (29, 38).The divergence in this region is such that southern Chinese S. scrofa cluster with the Sus speciesfrom ISEA, whereas northern Chinese S. scrofa cluster with European populations (Figure 4d ).This region on the X chromosome may also be linked to adaptation to high latitude (41). Oneexplanation for this phylogenic pattern is that it resulted from interbreeding between S. scrofaand an extinct species as the former reached northern China (41). The newly acquired haplotypesswept to fixation owing to the advantage they provided in northern latitudes and were transmittedto European populations during migrations across Eurasia (41).



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


Conclusions

Fossils provide a fundamental source of information that allows for the establishment of newhypotheses regarding the complex evolutionary history of Sus. These can now be tested usingwhole-genome sequencing. Combining information from molecules and fossils, researchers havedemonstrated that although morphological homoplasy may play a role in resolving conflictingphylogenies (2), the lesson from genomic signatures is that interspecific admixture was commonduring the evolution of suids and has led to mixed evolutionary legacies. For example, genomesequences have demonstrated that S. scrofa did not simply replace other species, but often admixedwith them prior to their extinction. This scenario has been demonstrated recently in other species,including humans, who hybridized with other hominins prior to their extinction (63, 64).

Admixture may therefore explain unresolved taxonomic questions (e.g., warty pigs). Hybridiza-tion may also have provided pigs with the means to rapidly adapt to new environments by borrow-ing genetic material, such as OR repertoires, from local, yet closely related species. This mechanismalso appears to be true of humans who were able to survive in high altitudes in Tibet thanks toadmixture with Denisovans (65). This phenomenon provides a testable hypothesis to explain howsuids extended their range and adapted to novel environments on numerous occasions during theirexpansion. The advent of genomic studies, informed by paleontological evidence, will shed lighton the potential of hybridization as an adaptive mechanism in suids. Lastly, it is now clear thatthe complicated evolutionary history of Suidae, involving numerous adaptations, turnovers, andreticulations, makes this family a great model for the study of speciation and adaptation.

THE ARTIFICIAL HISTORY OF SUIDAE

A detailed evolutionary history of Suidae would be incomplete without a discussion of the sharedhistory between humans and pigs. From early translocation by modern hunter-gatherers to in-tensive breeding by modern farmers, suids and humans have interacted for millennia, and theircommon artificial history mirrors the complexity of the natural history of Suidae.

Worldwide Translocation of Wild and Domestic Pig

Over thousands of years, humans have not only domesticated pigs but also translocated suid speciesacross the world as domestic and wild stock (Figure 4). In Africa, humans most likely transportedbush pigs (Potamochoerus larvatus) from the continent to Mayotte, Comoros, and Madagascar(Figure 2), though the chronology of this movement remains uncertain (66, 67). In ISEA, threepresumed translocations of suids stand out for their conservation importance: (a) the suspectedbut as yet unproven introduction of Babyrousa to the Sula and Buru Islands; (b) the introductionof S. celebensis to Simeulue Island, northwest of Sumatra, and to the Moluccas and Lesser Sundas(68, 69); and (c) the introduction of S. scrofa as a domestic animal to the Andaman and NicobarIslands, eastern Indonesia, and New Guinea (51).

The translocation of S. celebensis from Sulawesi throughout ISEA, including the Lesser SundaIslands, such as Flores and Timor, and possibly as far west as Bali, has been established on mor-phological and genetic evidence (Figure 2) (51, 69, 70). The genetic ancestry of pigs found eastof Java (Sus heureni ), however, remains unresolved, and they may be hybrids between introducedS. celebensis and S. scrofa brought by dispersing modern humans. S. celebensis was also possibly in-troduced to Simueleu (71). Although genomic analyses may support this claim (29), how these pigswere transported across the 3,500-km sea voyage from Sulawesi to the west of Sumatra remainsunsolved, because there is no archaeological evidence to track the route or date the arrival of these

3.10 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


?To Polynesia including

Hawaii and New Zealand

Figure 5A map of Eurasia depicting the human-mediated translocation of wild and domestic suids across the worldprior to the fifteenth century AD, when European explorers introduced pigs to the Americas. Green squaresindicate indigenous populations of wild suid species that were transported by people along the routesindicated by the green arrows. The question mark in Africa alludes to the fact that the source population ofPotamochoerus larvatus transported to Madagascar is unknown. The inset shows the transport of wild boar(from either Anatolia or the Levant) to Cyprus prior to the advent of domestication (72). Yellow circlesdepict the locations where East Asian and Anatolian populations of wild boar were independentlydomesticated and then transported away from the domestication centers along the black arrows. Red circlesindicate the regions where genetically and geographically distinct populations of wild boar hybridized withdomestic pigs, often leading to the acquisition of mitochondrial and nuclear DNA from local wild boar intodomestic stocks.

pigs on Simueleu. Before they were domesticated, wild boars from the Near East were transportedto Cyprus ∼11.4 ky ago, and throughout history sailors have been known to seed Mediterraneanislands with wild boars (72).

Not surprisingly, domestic pigs were subjected to human-mediated transport throughoutEurasia and Oceania during prehistory (Figure 5). Pigs also accompanied explorers beginningin the ninth century, when they were introduced to Iceland (73) and Greenland (74), and fromthe fifteenth century onward to the American continents (75), New Zealand, and Australia. Manyof these introduced individuals from various genetics origins (76) were deliberately released orescaped, thus giving rise to feral and invasive populations, and they now pose threats to localbiodiversity worldwide (77). The impact of European domestic pigs can also be seen in Indonesiaand the Philippines, where they have hybridized with local species (78).

Pig Domestication

Though numerous species have been domesticated, the vast majority have entered this relationshipin the past 500 years (79). Pigs were among the first animals, along with goats, sheep, and cows,to be domesticated at the beginning of the Holocene as part of a move toward sedentary societies.



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


Our understanding of the process, timing, and number of independent domestication episodeshas advanced considerably as new evidence and perspectives have recently been published ontheoretical, archaeological, and genetic fronts.

From a more general perspective, there are several morphological and behavioral similaritiesbetween domesticated versions of animals whose ancestors are not closely related. A commonhistorical interpretation of this pattern has posited not only that the process of domesticationwas the same for all species but that human intentionality played a significant role. Both Vigne(80) and Zeder (81) have recently challenged this convention and proposed instead multistageprocesses that do not (at least initially) require deliberate human forethought. In Vigne’s view,early animal domestication proceeded from anthropophily, to commensalism, to control in thewild, to control of captive animals, to extensive breeding, to intensive breeding, and finally to pets.Although this was certainly true for some animals, Zeder further recognized and described threeseparate pathways—commensal, prey, and directed—that animals followed into a domesticatedrelationship with humans.

Crucially, the commensal pathway does not begin with intentional action on the part of peopleto domesticate animals. Instead, populations of some wild animals would have been attracted toelements of the human niche, including human food waste and other smaller animals. Within thecontext of Zeder’s and Vigne’s models, the initial attraction of animals following the commensalroute could have progressed through various stages of intensifying relationships and human controluntil people were responsible for breeding in captivity. In a recent study of global patterns of animaldomestication, Larson & Fuller (79) demonstrated that animals following the commensal pathway(such as dogs) always preceded those that entered into domestication along other trajectories.

Prey pathway taxa are generally associated with settled human communities. Zooarchaeolog-ical assemblages document changes in the management strategies of hunted sheep, goats, pigs,and cows in the Fertile Crescent starting approximately 11,700 years ago. A recent study of an-imal remains at Sha’ar Hagolan, Israel, demonstrated that cows and pigs were overhunted priorto domestication (82), suggesting that intensive exploitation forced humans to adapt their man-agement strategies, after which the animals gradually became domesticated following the preypathway. This pattern of overhunting prior to domestication suggests that the prey pathway wasas unintentional as the commensal pathway (83).

Of the three, only the directed pathway begins with a deliberate human objective to domesticatea species (81). Before these species were domesticated, humans were already reliant upon a widerange of domestic plants and animals. Even in the cases of horses, donkeys, and Old Worldcamels, however, domestication was a multigenerational adaptation to human selection pressures,including tameness, herding behavior, and the ability to breed in captivity. The reason the existenceof different pathways took so long to be recognized is likely because the majority of moderndomestic animals have arisen only in the past few hundred years, including many small animalpets and an increasing number of aquatic species (84), and they have virtually all followed thedirected pathway.

The specific descriptions of the different trajectories animals followed are useful but not mutu-ally exclusive. Pigs, for example, may have been domesticated as populations became accustomedto the human niche, which would suggest a commensal mode, or they may have been hunted andfollowed a prey pathway, or perhaps both. What is clear is that pigs were definitively domesticatedin at least two locations: East Asia and the Near East.

Zooarchaeological records demonstrate clearly that pig domestication took place indepen-dently in the Near East, as revealed by demographic changes in Sus remains excavated fromarchaeological sites in Eastern Anatolia, including Cayonu Tepesi, Hallan Cemi Tepesi, HayazTepe, Tell Hallula, and Gurcutepe. For instance, the site of Cayonu Tepesi possesses a unique

3.12 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


stratigraphic sequence spanning 12,000 to 8,300 years ago (85, 86), demonstrating that pigs werekilled at progressively younger ages, suggesting an intensification of human-mediated selectionconsistent with the onset of domestication. Additional changes associated with intensifying do-mestication, including snout shortening and hypoplastic defects in the dental enamel [as a resultof physiological stress (85, 87)], are also visible. This intensification occurred gradually over theduration of the sequence, and the pigs did not appear domesticated according to modern mor-phological criteria until 8,300 years ago (85).

Excavations at the early Neolithic Turkish site of Hallan Cemi Tepesi (also in the easternTaurus Mountains) have suggested that a shift away from wild behavior may have taken placeeven earlier than at Cayonu. In a review of Sus data from several sites, Peters et al. (88) observed adecrease in the length of the third molar over time, which they said provided “unequivocal morpho-metrical evidence for the occurrence of domestic pigs” in the Late Pre-Pottery Neolithic B phase(89). In addition, Peters et al. (88) highlighted data from other sites, including Hayaz Tepe and TellHallula, to substantiate their claim for the early appearance of domestic pigs. Regardless of the exacttiming, it is apparent from the zooarchaeological evidence that wild boar adapted to human settle-ments in Eastern Turkey, and that this process resulted in the domestic pigs we recognize today.

Outside of the Near East, China is the only other location where clear archaeological evidencehas been presented in support of independent pig domestication. Large-scale excavations haverevealed that agricultural activities were practiced by seasonally mobile cultivators along the YellowRiver ∼8,000 BP (90–92), and plant cultivation may have begun 2,000 years earlier in the YellowRiver Valley (93). In southern China, sedentary hunter-gatherers (94) began cultivating rice alongthe Yangtze River approximately 9,000–8,000 BP, a practice that eventually culminated in thedependence upon rice agriculture by ∼6,000 BP (91). Archaeological evidence suggests that thoughdomestic pigs made up only a small percentage of the earliest mammal bone assemblages, theywere prevalent in both northern and southern China by at least 8,000 BP (95, 96).

Claims for the much earlier appearance of domestic pigs (∼12,500 years BP) at the site ofZengpiyan near Guilin were refuted by a reanalysis of the zooarchaeological record that alsodemonstrated a clear long-term shift toward domestication at the site of Jiahu (97). A revisedanalysis of previously excavated Chinese assemblages, along with the discovery of new sites, hasled to a refined model of pig domestication in China along a long stretch of the Yellow River andon the Lower Yangtze River ∼8,000 years ago (98). The geographic scale of China, where at leasttwo subspecies of wild boar exist, also possesses a substantial diversity of Neolithic cultural entitiesscattered across a mosaic environment (56, 99, 100). Rather than a single geographical setting,these data suggest that, like in Eastern Turkey, pig domestication may have taken place across adiffuse, regional scale.

The first results of a genetic analysis of domestication focused on patterns of mitochondrialvariation in domestic pig and wild boar samples from across the Old World. The initial resultsdemonstrated that domestic pigs from East Asia and Western Europe shared closer affinity to wildboar from those regions than to each other, thus confirming the hypothesis that pigs had beendomesticated at least twice from geographically and genetically differentiated populations of wildboar (101). Numerous subsequent studies using mitochondrial (50, 102, 103) and nuclear markers,including microsatellites (104, 105), SNPs (106), and whole genomes (29, 38, 41), have confirmedthe unique genetic identities of East Asian and European wild boar, as well as the significantgenetic differences between domestic pigs on either side of the Old World.

Most of these studies have not sampled wild boar from across its natural range. An earlymitochondrial study (50) that did so, however, revealed not only that wild boar retained a strongphylogeographic signal but also that many domestic pigs possessed mitochondrial signatures thatclustered in clades consisting of wild boar from Europe and Asia (as expected), as well as Italy,



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


India, and peninsular Southeast Asia. This result led the authors to speculate that wild boar fromnumerous regions may have been domesticated independently.

If this is true, and if pigs followed the same pathway to domestication in many different ge-ographical settings, then the long-term demographic and morphological changes found in pigsrecovered from archaeological sites in Eastern Turkey and China should also be visible in thezooarchaeological records of Western Europe, India, and peninsular Southeast Asia. In fact, theyare not. Domestic pigs appear suddenly alongside wild boar in Europe and in peninsular EastAsia, where they are associated with incoming farmers. This archaeological observation has beensubstantiated by ancient DNA studies of pigs in Anatolia and Europe, demonstrating that theearliest domestic pigs in Europe possessed mitochondrial haplotypes found only in Anatolia andthe Near East (107, 108).

In East Asia there is a similar lack of consistency between the genetic and archeological records.Though ancient DNA signatures from several sites in China match those of modern Chinesedomestic pigs (109), domestic pigs associated with the Austronesian expansion into the Pacificpossessed signatures found in wild boar indigenous to peninsular Southeast Asia (51). As they do inWestern Europe, domestic pigs appear suddenly alongside wild boar (109), and no archaeologicalevidence supports a long-term domestication process in Southeast Asia.

The genetic evidence suggesting widespread and even common domestication of distinct wildboar populations seems to contradict the archaeological evidence that points toward only twocenters of domestication in East Asia and the Near East. A survey of the domestication litera-ture, however, demonstrated that far from being unusual, introgression between indigenous wildpopulations and translocated domestic populations domesticated elsewhere is common in bothplants and animals (110). This admixture often results in an imported domestic population tak-ing on the genetic [and morphological (111)] appearance of the local wild population, leadingresearchers to the false conclusion that the local wild population gave rise to the domestic onethrough an independent domestication process. In fact, this process is so pervasive that Larson &Fuller (79) have suggested the word domestication be reserved only for the independent process(regardless of pathway), and they introduce the term “introgressive capture” to refer to subsequentadmixture between introduced domestic populations and local wild populations that were neverdomesticated.

Combining the evidence from archaeological and genetic perspectives yields two importantinsights. Firstly, despite the presence of geographically and genetically distinct wild boar popula-tions across the Old World, the independent, long-term process of pig domestication took place inonly two regions: Eastern Anatolia and China. Secondly, following these independent processes,domestic pigs accompanied farmers as they dispersed beyond the domestication regions. Oncethere, domestic pigs acquired mitochondrial and nuclear affinities through hybridization with thelocal wild boar. The result of this repeated admixture is that domestic pigs in Europe no longerpossess an obvious genetic legacy of their Near Eastern heritage (107, 108, 112), and pigs nativeto Polynesia carry a mitochondrial signature that is not evident in any modern wild boar in centralor northern China (109).

Hybridization between distinct domestication populations has continued, as exemplified by thedevelopment of improved breeds (hybrids between Chinese and European pigs) in the nineteenthcentury (113), and evidenced by the fact that 30% of the genomes of European commercial pigsare derived from East Asian breeds (114, 115). More generally, hybridization is emerging as acommon feature in the natural and artificial history of suids. Unraveling the spatial and temporalhistories of the appearance and spread of specific traits, as well as the overall pattern of admixturethat may have allowed for the proliferation of pigs in new environments or selection regimes, willrequire both substantial ancient genomic DNA and sophisticated bioinformatic approaches. This

3.14 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


approach is tractable, however, and we may soon arrive at a satisfying history of pig domesticationand dispersal, as well as shed light on the similarities between domestication and speciation.

THREATS TO NATURAL POPULATIONS

Asian Suidae

Apart from the near ubiquitous S. scrofa, all other wild pig species in Asia are listed on the Interna-tional Union for Conservation of Nature (IUCN) Red List of Threatened Species (116) as NearThreatened, Vulnerable (VU), Endangered (EN), or Critically Endangered (CR). All African pigspecies are of lower conservation concern, though taxonomic revisions within the morphologi-cally and genetically highly variable forest hog (H. meinertzhageni ) could result in much smallerranges and higher extinction threat to, for example, the northern forest hog H. meinertzhagenimeinertzhageni in Ethiopia and southern Sudan.

One of the reasons for the different extinction threat levels in Africa and Asia could be the rolethat S. scrofa likely played in the extinction or near extinction of other pig species. S. scrofa occursthroughout mainland Eurasia and many parts of ISEA but only marginally in North Africa. All ofSoutheast Asia’s most threatened pig species, the Visayan warty pig S. celebensis (CR), Javan wartypig S. verrucosus (EN), Mindoro warty pig S. oliveri (EN), the three Babyrousa species (EN or VU),and S. barbatus, S. ahoenobarbus, and S. philippensis (all VU) are endemic to one or a few islands onthe southeastern periphery of the Asian landmass. This raises the question of whether in most ofmainland Asia the ecologically versatile S. scrofa displaced other pig taxa [such as S. (D.) strozzi,see above] during the Pleistocene, leaving only the surviving island species.

During the Middle Pleistocene, pig diversity in mainland Asia remained high, as evidencedby the presence of seven or eight (chrono)species at the Liucheng site in China (31, 117). Thedistribution of the genus Porcula, which now occurs only in pockets of grassland habitat in India, wasalso much greater during the Pleistocene and may have been reduced by the expansion of S. scrofa.All pig species are threatened by anthropogenic factors, such as overhunting and degradation ofnatural habitats. In conservation terms, however, it is important to know whether species werealready on a long decline because of the influence of a nonhuman species such as S. scrofa, and ifmodern humans are only providing a final push toward extinction.

An example of this is the Indonesian island of Java, where the endemic S. verrucosus has co-occurred with S. scrofa since the Late Pleistocene or early Holocene (118). Until historic times, thetwo species lived side by side with limited ecological separation (119). More recently, S. verrucosushas declined rapidly and now survives only in small parts of its former range (120). The two species(S. scrofa and S. verrucosus) are known to hybridize in the wild, and it appears that the more rapidlyreproducing S. scrofa is both outcompeting S. verrucosus and absorbing the species into its genepool. A population of a related taxon, Sus verrucosus blouchi, on the small island of Bawean inthe Java Sea has survived as a small population of approximately 350 animals for many centuries,possibly because S. scrofa is not present on the island (121).

This competition and hybridization model is hypothetical, but similar dynamics may haveplayed a role in the apparent demise of another species. Despite a great deal survey work, Susbucculentus, an endemic species of the Annamite Range in Laos, has not been found in recent times.The three known skulls of this species morphologically resembled S. verrucosus (122), althoughphylogenetic analysis of 12S and cytochrome regions of mtDNA of an alleged S. bucculentusspecimen grouped it with a clade of S. scrofa (123). Full genome sequencing is needed to revealwhether S. bucculentus retains any S. verrucosus–like characteristics. If so, it may have been displacedby S. scrofa (or hunted out) and should be considered either extinct or an invalid species.



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


In general, there is limited knowledge of the in situ conservation status of most threatenedpig species. The babirusa species of the Togean, Buru, and Sula Islands (Babyrousa togeanensis andBabyrousa babirussa) remain unstudied, and almost nothing is known regarding S. oliveri (124),which has never been photographed. In addition, population estimates and levels of hybridizationwith S. scrofa remain to be determined for the CR-listed S. cebifrons in the Philippines. Retainingviable populations of these ecologically important species is a high conservation priority (125,126), despite the fact that they do not receive a great deal of international attention.

Pygmy Hog (Porcula salvania)

The pygmy hog (Porcula salvania) is the smallest and the most endangered of the world’s wildsuids. Historically it occurred in early successional tall grasslands along the southern Himalayanfoothills (127), but it now appears to be extinct in Bhutan and Nepal and most of its Indianrange, and it survives only in a few isolated grasslands areas in Assam (128). It is listed on theIUCN Red List of Threatened Species as CR, with loss and degradation of grassland habitatowing to human settlements, agricultural encroachments, dry-season burning, livestock grazing,commercial forestry, and flood control schemes being listed as the primary threats (129).

The recent discovery that the genus Porcula was actually widespread in South and SoutheastAsia (31) during the Late Pleistocene and not restricted to a small sub-Himalayan habitat zonesheds a new light on what could be driving population declines in Porcula. Pygmy hogs are superblyadapted to life in tall grasslands. Their small size and bullet shape allow them to move throughdense grasses, on which they also feed and which they use for building their sleeping and restingnests.

Presumably, Porcula used such grasslands throughout its range. Did all the Southeast andEast Asian tall grasslands disappear at the end of the Pleistocene, leaving only the sub-Himalayanhabitats, or did other factors play a role in the demise of Porcula? Is it possible that habitat alterationor predation by modern humans that arrived in the region some 60,000–100,000 years ago (130,131) played a role? Or did S. scrofa, which dispersed into the region in the Middle Pleistocene,negatively impact Porcula? We currently do not have answers to these questions, but it is clear thatplacing the conservation of P. salvania within an evolutionary perspective more broadly informsour views on extinction threats. The ongoing pygmy hog genome-sequencing project will shedmore light on the evolutionary history of this peculiar species and provide valuable insights forconservation (L. Frantz & M. Groenen, personal communication).

Modern Wild Boar (Sus scrofa)

Groves (56) placed all members of the S. scrofa group in a single species, but the differences betweensome of the taxa in the group are sharper and more consistent than previously recognized. Larsonet al. (108), using the control region of mtDNA, found that this species group has a basal comb(which also included samples of S. celebensis), of which one branch contained all of the Eurasiansamples. It appears that the ancestor of the S. scrofa group originated in Southeast Asia in the earlyPleistocene, then spread to India in the mid-Pleistocene, and from there split into two Europeanlineages and two eastern Asian lineages that separated approximately 600,000 years ago into anorthern and southern group (29, 78, 132). Subsequent division occurred between Indian andEurasian pigs, leading to a final distinctive clade of European and Middle Eastern samples (51, 78).

The genetic differentiation within S. scrofa is mirrored by significant morphological variation(56, 133, 134). Approximately 80 taxa have been described within what we now consider S. scrofa(135), from which 15 are recognized as subspecies (56). Groves & Grubb (136) proposed elevating

3.16 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


three of these to species level on the basis of consistent morphological differences: (a) Sus moupinen-sis (Milne-Edwards 1871) in Burma and China, (2) Sus chirodontus (Heude 1888) in south-centralChina, and (3) Sus ussuricus (Heude 1888) in Heilongjiang/the Far East; however, this proposalremains just that. Further molecular studies are required to assess whether the morphologicaldifferences between the three proposed species are reflected by similar genetic patterns.

Phylogenetic patterns within S. scrofa must be explored further. Clear morphological differencesexist, for example, in the long-maned, thick-haired pigs of mainland India and further west, andthose of northeastern India, Myanmar, and mainland Southeast Asia. The Japanese Ryukyu pig(S. scrofa riukiuanus) also possesses morphologically and genetically distinct characteristics (137–139), and the Indonesian, white-snouted, rough-haired pigs also stand out (56). The so-calledLanyu pigs, which are supposedly derived from the islet of Lanyu off the coast of Taiwan, possessa unique mitochondrial signature, suggesting a possible distinctive evolutionary history as well(140). Differentiation between all these taxa has likely been suppressed through introgressionwith other subspecies and domestic pigs. Indigenous wild boar pig populations are increasinglyisolated from each other in Asia, and as long as they remain extant and avoid assimilation bydomestic pigs, the differences between them may become more pronounced.

MODERN BREEDING AND THREATS TO DOMESTIC POPULATIONS

Threats to naturally occurring suids are not the sole conservation issue for Suidae. Thousandsof years of introgression between wild boar and domestic pigs, as well as crossbreeding betweendomestic stocks, have resulted in a myriad of phenotypic differences between domestic pig popu-lations. The establishment of pig breed societies and herdbooks did not occur until the IndustrialRevolution in the eighteenth and nineteenth centuries, when British breeders started to importand crossbreed Asian and European pigs to meet the increasing demand for pork meat (115). Chinatoo had a long history of breeding, with countless distinct populations. Instead of herdbooks andtypes, Chinese pigs are often named after their geographic location of origin, most likely owingto the large cultural, climatic, and topographic variations found across the country.

Europe is not immune to complications resulting from attempting to define breeds, becausemany countries and breeding companies maintain different populations of the same breed withwidely different genetic ancestry. This is illustrated by the Domestic Animal Diversity Infor-mation System hosted by the Food and Agriculture Organization of the United Nations (FAO)(http://dad.fao.org), which for pigs contains 1,286 different entries for breeds/lines across theworld and 778 specific breeds. Pork is one of the most consumed protein sources worldwide,and approximately 115 million tons are produced globally every year (141), but only a handful ofcommercial breeds are responsible for this production. As a result, many rare and local domesticbreeds are on the verge of extinction. A survey published by the FAO in 2007 (http://ftp.fao.org)lists 742 pig breeds, of which 137 are extinct and another 130 are endangered, all of which arelocal or rare breeds (Table 1).

Over the past two decades, several studies have attempted to characterize the genetic diversity ofdomestic pig populations to establish whether their loss poses a threat to future breeding programsowing to irretrievable loss of unique genetic variants. These studies make use of different genetictechniques, such as microsatellite (104, 105, 142–145), mtDNA (102, 103, 146), and AFLP markers(147, 148).

Unlike European pigs, Chinese breeds harbor a clear geographical structure (105). Clusteringwithin Europe generally shows a clear difference between pigs from the United Kingdom andMediterranean countries, most likely as a result of the importation of Chinese domestic stockinto the United Kingdom during the Industrial Revolution. These results are confirmed by more



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.

http://dad.fao.org

http://ftp.fao.org


Table 1 Conservation status of local breeds in the worlda

CriticalCritical-

maintained EndangeredEndangered-maintained Extinct Not at risk Unknown Total

Africa NA NA 4 NA NA 22 29 55Asia 7 4 11 6 15 116 72 231Europe 27 8 53 18 90 55 28 279LatinAmerica

3 4 2 1 NA 7 43 60

Near andMiddleEast

NA NA NA NA NA NA 1 1

NorthAmerica

2 NA 1 NA NA 1 7 11

SouthwestPacific

NA NA NA NA NA 1 15 17

Total 39 16 71 25 106 202 195 654

aThese numbers are only for local breeds that are unique to each region (row). Critical-maintained and endangered-maintained mean those conservationefforts are ongoing. The raw data were obtained from the Food and Agriculture Organization of the United Nations (http://dad.fao.org/).

recent studies using a panel of 60K SNPs (38, 106). Although these studies provide a good generaloverview of diversity and relatedness, they do not provide an answer to the extent of the numberof specific unique variants within these different breeds.

With the increasing number of pigs whose complete genome has been sequenced (38, 39, 41,149), however, this kind of information is now becoming readily available, and it is now possibleto investigate the genetic diversity of European pig domestic stock. Such large-scale genome-sequencing projects have revealed that the genetic diversity of European local and rare breedsvaries considerably (i.e., Iberian pigs, Mangalitsa from Hungary, or Casertana from Italy).

These variations most likely are due to different degrees of introgression from Chinese pigs(149). Nevertheless, the genetic diversity of European domestic pigs is much greater than thatfound in European wild boar, most likely as a result of the introgression from Chinese pigs intoEuropean stock (38, 113, 150). Rare breeds in Europe have their own, unique genetic ancestry,as revealed by a large-scale assessment of nonsynonymous mutations (149). Moreover, genomesequencing of a few rare breeds, such as Mangalitsa, Casertana, Calabrese, and Iberian, revealedthat these populations harbor over 10,000 unique genetic variants not found in current commercialbreeds (M.A.M. Groenen, unpublished results). This suggests that conservation of rare breeds iscritical because they are a key reservoir of genetic variation that may be important for futurebreeding programs.

Wild boar populations are also a reservoir of genetic variation. However, in Western Europe,many regions where the local populations have gone extinct (e.g., from overhunting) have beenrecently restocked with wild boar populations derived from elsewhere (151, 152). This processresulted in a dramatic loss of genetic diversity compared with that of domestic breeds and wildboars in Asia (38, 39, 153). Until the late Middle Ages, pig breeding in Europe was characterizedby ongoing admixture with wild boar (115), suggesting that much of the wild boar variationis present in modern domestic breeds. However, a comparison of the genome sequence of 38European wild boars and 169 European and Asian pigs revealed 142,249 SNPs found only inEuropean wild boar (M.A.M. Groenen, unpublished results). This suggests that wild boar, and

3.18 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.

http://dad.fao.org/


especially Asian populations, likely harbor a significant amount of genetic variation not found indomestic populations. Conserving wild boar in Europe is therefore important not only for theirsurvival but also to provide future generations with the necessary power to breed better, moreresilient domestic pigs.

CONCLUSION

Since the Oligocene, Suidae lineages have undergone many rounds of adaptation, reticulation,expansion, and species replacement. Their history has been made more complicated by thousandsof years of interactions with humans as prey, by being translocated, and as a domestic animal.Anthropogenic influences on suids, including deforestation, hunting, and translocation, have alsoresulted in loss of biodiversity due to population decline and, often, hybridization. In addition,recent changes in industrial pork production systems have resulted in a loss of genetic diversity innumerous regional domestic populations, threatening future breeding efforts.

The Suidae are also an excellent model to study speciation and domestication. Genomics ofsuids have shown that both of these processes involved a substantial amount of hybridization. Whatremains unknown, however, is the degree to which these reticulations were adaptive and providedsuids with the phenotypic plasticity to rapidly adapt to novel natural and artificial environments.

Domestication and speciation are often considered distinct processes. The study of Suidaepaleontology, archaeology, and genomics is allowing for an in-depth comparison of these twoevolutionary phenomena and is leading to a greater appreciation for the role that hybridizationand admixture play in both processes. The future of suid research therefore holds many promisesfor our understanding of the basic processes that generate the biodiversity on earth.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

LITERATURE CITED

1. Montgelard C, Catzeflis FM, Douzery E. 1997. Phylogenetic relationships of artiodactyls and cetaceansas deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Mol. Biol.Evol. 14:550–59

2. Orliac M, Pierre-Olivier A, Ducrocq S. 2010. Phylogenetic relationships of the Suidae (Mammalia,Cetartiodactyla): new insights on the relationships within Suoidea. Zool. Scr. 39:315–30

3. Orliac M. 2013. The petrosal bone of extinct Suoidea (Mammalia, Artiodactyla). J. Syst. Palaeontol.11:925–45

4. Randi E, Lucchini V, Diong CH. 1996. Evolutionary genetics of the Suiformes as reconstructed usingmtDNA sequencing. J. Mamm. Evol. 3:163–94

5. Gongora J, Cuddahee RE, Nascimento FF, Palgrave CJ, Lowden S, et al. 2011. Rethinking the evolutionof extant sub-Saharan African suids (Suidae, Artiodactyla). Zool. Scr. 40:327–35

6. Pickford M, Senut B, Hadoto DPM. 1993. Geology and Palaeobiology of the Albertine Rift Valley, Uganda-Zaire: Geology. Orleans, France: CIFEG

7. Ducrocq S. 1994. An Eocene Peccary from Thailand and the Biogeographical Origins of the Artiodactyl FamilyTayassuidae. Dyfed, UK: Palaeontol. Assoc.

8. Harris JM, Li-Ping L. 2007. Superfamily Suoidea. In The Evolution of Artiodactyla, ed. D Prothero,S Foss, pp. 130–50. Baltimore, MD: Johns Hopkins Univ. Press

9. Orliac MJ, Antoine P-O, Roohi G, Welcomme J-L. 2010. Suoidea (Mammalia, Cetartiodactyla) fromthe Early Oligocene of the Bugti Hills, Balochistan, Pakistan. J. Vertebr. Paleontol. 30:1300–5



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


10. Pickford M. 1986. Cainozoic paleontological sites of Western Kenya. Am. J. Phys. Anthr. 76(1):14211. Pickford M. 1988. Revision of the Miocene Suidae of the Indian subcontinent. Munchen, Ger.: F. Pfiel12. Van der Made J. 1998. Biometrical trends in the Tetraconodontinae, a subfamily of pigs. Trans. R. Soc.

Edinb. Earth Sci. 89:199–22513. Pickford M. 2012. Ancestors of Broom’s pigs. Trans. R. Soc. S. Afr. 67:17–3514. Pickford M. 1986. A Revision of the Miocene Suidae and Tayassuidae, (Artiodactyla, Mammalia) of Africa.

Leiden, Neth.: Brill Acad.15. White TD, Harris JM. 1977. Suid evolution and correlation of African hominid localities. Science 198:13–

2116. Leakey LSB. 1958. Some East African Pleistocene Suidae. London: Br. Mus.17. Harris JM, Leakey MG, Brown FH. 1988. Stratigraphy and Paleontology of Pliocene and Pleistocene Localities

West of Lake Turkana, Kenya. Los Angeles, CA: Nat. Hist. Mus. L.A. Cty.18. Roth J, Wagner JA. 1854. Die fossilen Knochen-uberreste von Pikermi in Griechenland: Gemeinschaftlich

bestimmt und beschrieben von den Akademikern. Munchen, Ger.: Verlag Akad.19. Geraads D, Spassov N, Garevski R. 2008. New specimens of Propotamochoerus (Suidae, Mammalia)

from the late Miocene of the Balkans. Neues Jahrb. Geol. Palaontol. Abh. 248:103–1320. Van der Made J, Morales J, Montoya P. 2006. Late Miocene turnover in the Spanish mammal record

in relation to palaeoclimate and the Messinian Salinity Crisis. Palaeogeogr. Palaeoclimatol. Palaeoecol.238:228–46

21. Orliac MJ. 2009. The differentiation of bunodont Listriodontinae (Mammalia, Suidae) of Africa: newdata from Kalodirr and Moruorot, Kenya. Zool. J. Linn. Soc. 157:653–78

22. Pickford M. 1988. Une etrange suidenain du Neogene Superier de Langebaanweg (Afrique du Sud).Ann. Paleontol. 74:229–50

23. Van der Made J. 1996. Listriodontinae (Suidae, Mammalia): their evolution, systematics and distributionin time and space. Contrib. Tert. Quat. Geol. 33:3–254

24. Van der Made J. 1996. Albanohyus, a small Miocene pig. Acta Zool. Crac. 39:293–30325. Brunet M, White T. 2001. Two new suin species (Mammalia, Suidae) from Africa (Chad, Ethiopia).

C. R. Acad. Sci. Ser. II Fasc. A Sci. Terre Planetes 332:51–5726. Cooke H. 1997. The status of the African fossil suids Kolpochoerus limnetes (Hopwood, 1926), K.

Phacochoeroides (Thomas 1884) and “K.” afarensis (Cooke, 1978). Geobios 30:121–2627. Haile-Selassie Y, Simpson SW. 2013. A new species of Kolpochoerus (Mammalia: Suidae) from the

Pliocene of Central Afar, Ethiopia: its taxonomy and phylogenetic relationships. J. Mamm. Evol. 20:115–27

28. White TD, Suwa G. 2004. A new species of Notochoerus (Artiodactyla, Suidae) from the Pliocene ofEthiopia. J. Vertebr. Paleontol. 24:474–80

29. Frantz L, Schraiber JG, Madsen O, Megens H-J, Bosse M, et al. 2013. Genome sequencing reveals finescale diversification and reticulation history during speciation in Sus. Genome Biol. 14:R107

30. Hooijer DA. 1974. Quaternary mammals west and east of Wallace’s Line. Neth. J. Zool. 25:46–5631. Pickford M. 2013. Suids from the Pleistocene of Naungkwe Taung, Kayin State, Myanmar. Paleontol.

Res. 16:307–1732. Azzaroli A. 1992. Suids of the early Villafranchian of Villafranca d’Asti and China. Rend. Lincei 3:109–2433. Montoya P, Ginsburg L, Alberdi MT, Van der Made J, Morales J, Soria MD. 2006. Fossil large mammals

from the early Pliocene locality of Alcoy (Spain) and their importance in biostratigraphy. Geodiversitas28:137–73

34. Fistani AB. 1996. Sus scrofa priscus (Goldfuss, De Serres) (Mammalia, Artiodactyla, Suidae) from theMiddle Pleistocene layers of Gajtan 1 site, southeast of Shkoder (north Albania). Ann. Paleontol. 82:177–229

35. Guerin C, Faure M. 1997. The wild boar (Sus scrofa priscus) from the post-Villafranchian Lower Pleis-tocene of Untermassfeld. In Das Pleistozan von Untermassfeld bei Meiningen (Thuringen), ed. RD Kahlke,1:375–84. Mainz, Ger.: Rom. Ger. Zentralmus.

36. Faure M, Guerin C. 1984. Sus strozzii et Sus scrofa, deux mammiferes artiodactyles, marqueurs despaleoenvironnements. Palaeogeogr. Palaeoclimatol. Palaeoecol. 48:215–28

3.20 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


37. Wang W, Potts R, Baoyin Y, Huang W, Cheng H, et al. 2007. Sequence of mammalian fossils, includinghominoid teeth, from the Bubing Basin caves, South China. J. Hum. Evol. 52:370–79

38. Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, et al. 2012. Analyses of pig genomesprovide insight into porcine demography and evolution. Nature 491:393–98

39. Bosse M, Megens H-J, Madsen O, Paudel Y, Frantz LA, et al. 2012. Regions of homozygosity in theporcine genome: consequence of demography and the recombination landscape. PLOS Genet. 8:e1003100

40. Li M, Tian S, Jin L, Zhou G, Li Y, et al. 2013. Genomic analyses identify distinct patterns of selectionin domesticated pigs and Tibetan wild boars. Nat. Genet. 45:1431–38

41. Ai H, Fang X, Yang B, Huang Z, Chen H, et al. 2015. Adaptation and possible ancient interspeciesintrogression in pigs identified by whole-genome sequencing. Nat. Genet. 47:217–25

42. Paudel Y, Madsen O, Megens H-J, Frantz LA, Bosse M, et al. 2013. Evolutionary dynamics of copynumber variation in pig genomes in the context of adaptation and domestication. BMC Genom. 14:449

43. Nguyen DT, Lee K, Choi H, Choi M-k, Le MT, et al. 2012. The complete swine olfactory subgenome:expansion of the olfactory gene repertoire in the pig genome. BMC Genom. 13:584

44. Sudmant PH, Huddleston J, Catacchio CR, Malig M, Hillier LW, et al. 2013. Evolution and diversityof copy number variation in the great ape lineage. Genome Res. 23:1373–82

45. Ache BW, Young JM. 2005. Olfaction: diverse species, conserved principles. Neuron 48:417–3046. Nozawa M, Kawahara Y, Nei M. 2007. Genomic drift and copy number variation of sensory receptor

genes in humans. PNAS 104:20421–2647. Go Y, Niimura Y. 2008. Similar numbers but different repertoires of olfactory receptor genes in humans

and chimpanzees. Mol. Biol. Evol. 25:1897–90748. Niimura Y, Nei M. 2007. Extensive gains and losses of olfactory receptor genes in mammalian evolution.

PLOS ONE 2:e70849. Paudel Y, Madsen O, Megens H-J, Frantz LA, Bosse M, et al. 2015. Copy number variation in the

speciation of pigs: a possible prominent role for olfactory receptors. BMC Genom. 16:33050. Larson G, Dobney K, Albarella U, Fang M, Matisoo-Smith E, et al. 2005. Worldwide phylogeography

of wild boar reveals multiple centers of pig domestication. Science 307:1618–2151. Larson G, Cucchi T, Fujita M, Matisoo-Smith E, Robins J, et al. 2007. Phylogeny and ancient DNA of

Sus provides insights into neolithic expansion in Island Southeast Asia and Oceania. PNAS 104:4834–3952. Lucchini V, Meijaard E, Diong CH, Groves CP, Randi E. 2005. New phylogenetic perspectives among

species of South-east Asian wild pig (Sus sp.) based on mtDNA sequences and morphometric data.J. Zool. 266:25–35

53. Frantz LA, Madsen O, Megens HJ, Groenen MA, Lohse K. 2014. Testing models of speciation fromgenome sequences: divergence and asymmetric admixture in Island South-East Asian Sus species duringthe Plio-Pleistocene climatic fluctuations. Mol. Ecol. 23:5566–74

54. Bender PA. 1992. A reconsideration of the fossil suid Potamochoeroides shawi, from the Makapansgat Lime-works, Potgietersrus, Northern Transvaal. Bloemfontein: Navors. Nas. Mus.

55. Cooke H. 1978. Suid evolution and correlation of African hominid localities: an alternative taxonomy.Science 201:460–63

56. Groves CP. 1981. Ancestors for the pigs: taxonomy and phylogeny of the genus Sus. Tech. Bull., Dep. Prehist.,Res. School Pac. Stud., Aust. Natl. Univ.

57. Pickford M. 2006. Synopsis of the biochronology of African Neogene and Quaternary Suiformes. Trans.R. Soc. S. Afr. 61:51–62

58. Gongora J, Cuddahee RE, Ferreira do Nascimento F, Palgrave CJ, Lowden S, et al. 2011. Rethinkingthe evolution of extant sub-Saharan African suids (Suidae, Artiodactyla). Zool. Scr. 40:327–35

59. Kumar S, Gaur R. 2013. First record of maxillary dentition of Potamochoerus theobaldi (Suidae, Mammalia)from the Upper Siwaliks of India. Riv. Ital. Paleontol. Stratigr. 119:57–63

60. Arribas A, Garrido G. 2008. A new wild boar belonging to the genus Potamochoerus (Suidae, Artiodactyla,Mammalia) from the Eurasian Late Upper Pliocene (Fonelas P-1, Cuenca de Guadix, Granada). Cuad.Mus. Geomin. 10:337–64

61. Gray J. 1873. L.—Observations on pigs (Sus, Linnæus; Setifera, Illiger) and their skulls, with the de-scription of a new species. J. Nat. Hist. 11:431–39



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


62. de Bruyn M, Stelbrink B, Morley RJ, Hall R, Carvalho GR, et al. 2014. Borneo and Indochina are majorevolutionary hotspots for Southeast Asian biodiversity. Syst. Biol. 63:879–901

63. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, et al. 2010. A draft sequence of the Neandertalgenome. Science 328:710–22

64. Lohse K, Frantz LA. 2014. Neandertal admixture in Eurasia confirmed by maximum-likelihood analysisof three genomes. Genetics 196:1241–51

65. Huerta-Sanchez E, Jin X, Bianba Z, Peter BM, Vinckenbosch N, et al. 2014. Altitude adaptation inTibetans caused by introgression of Denisovan-like DNA. Nature 512:194–97

66. Vercammen P, Seydack AHW, Oliver WLR. 1993. The bush pigs (Potamochoerus porcus and P. larvatus).In Pigs, Peccaries and Hippos, ed. WLR Oliver, pp. 93–100. Gland, Switz.: IUCN

67. Blouch RA. 1993. The Javan warty pig (Sus verrucosus). In Pigs, Peccaries and Hippos, ed. WLR Oliver,pp. 129–35. Gland, Switz.: IUCN

68. Blouch RA. 1995. Conservation and research priorities for threatened suids of South and Southeast Asia.Ibex 3:21–25

69. Schwarz E. 1914. Saugetiere von Timor: Mit 8 Tafeln (Tafel 2–9). Stuttgart, Ger.: Im Kommissionverlagder E. Schweizerbartschen Verlagsbuchhandlung

70. Groves CP. 1984. Of mice and men and pigs in the Indo-Australian Archipelago. Canberra Anthropol.7:1–19

71. Groves CP. 1983. Pigs east of the Wallace Line. J. Soc. Ocean. 39:105–1972. Vigne J-D, Zazzo A, Saliege J-F, Poplin F, Guilaine J, Simmons A. 2009. Pre-Neolithic wild boar

management and introduction to Cyprus more than 11,400 years ago. PNAS 106:16135–3873. Hambrecht G. 2012. Zooarchaeology and modernity in Iceland. Int. J. Hist. Archaeol. 16:472–8774. Nelson DE, Heinemeier J, Møhl J, Arneborg J. 2012. Isotopic analysis of the domestic animals of Norse

Greenland. J. N. Atl. 3(Spec. Vol.):77–9275. Burgos-Paz W, Souza CA, Megens HJ, Ramayo-Caldas Y, Melo M, et al. 2013. Porcine colonization of

the Americas: a 60k SNP story. Heredity 110:321–3076. Gongora J, Fleming P, Spencer PB, Mason R, Garkavenko O, et al. 2004. Phylogenetic relationships of

Australian and New Zealand feral pigs assessed by mitochondrial control region sequence and nuclearGPIP genotype. Mol. Phylogenet. Evol. 33(2):339–48

77. Barrios-Garcia MN, Ballari SA. 2012. Impact of wild boar (Sus scrofa) in its introduced and native range:a review. Biol. Invasions 14:2283–300

78. Frantz LAF, Schraiber J, Madsen O, Megens HJ, Semiadi G, et al. 2013. Genome sequencing reveals finescale diversification and reticulation history during speciation in Sus (Suidae: Cetartiodactyla). GenomeBiol. 14:R107

79. Larson G, Fuller DQ. 2014. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 45:115–3680. Vigne J-D. 2011. The origins of animal domestication and husbandry: a major change in the history of

humanity and the biosphere. C. R. Biol. 334:171–8181. Zeder MA. 2012. The domestication of animals. J. Anthropol. Res. 68:161–9082. Marom N, Bar-Oz G. 2013. The prey pathway: a regional history of cattle (Bos taurus) and pig (Sus scrofa)

domestication in the northern Jordan Valley, Israel. PLOS ONE 8:e5595883. Zohary D, Tchernov E, Horwitz L. 1998. The role of unconscious selection in the domestication of

sheep and goats. J. Zool. 245:129–3584. Duarte CM, Marba N, Holmer M. 2007. Rapid domestication of marine species. Science 316:382–8385. Ervynck A, Dobney K, Hongo H, Meadow R. 2001. Born free? New evidence for the status of Sus scrofa

at Neolithic Cayonu Tepesi (Southeastern Anatolia, Turkey). Paleorient 27(2):47–7386. Hongo H, Meadow RH. 1998. Pig exploitation at neolithic Cayonu Tepesi (Southeastern Anatolia). In

Ancestors for the Pigs: Pigs in Prehistory, ed. SM Nelson, pp. 77–98. Philadelphia: Univ. Pa. Mus. Archaeol.Anthropol.

87. Dobney K, Ervynck A, Albarella U, Rowley-Conwy P. 2004. The chronology and frequency of a stressmarker (linear enamel hypoplasia) in recent and archaeological populations of Sus scrofa in north-westEurope, and the effects of early domestication. J. Zool. 264:197–208

88. Peters J, Helmer D, von den Driesch A, Sana Segui M. 1999. Early animal husbandry in the NorthernLevant. Paleorient 25(2):27–48

3.22 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


89. Albarella U, Dobney K, Rowley-Conwy P. 2006. The domestication of the pig (Sus scrofa): new challengesand approaches. In Documenting Domestication: New Genetic and Archaeological Paradigms, ed. MA Zeder,pp. 209–27. Berkeley: Univ. Calif. Press

90. Barton L, Newsome SD, Chen F-H, Wang H, Guilderson TP, Bettinger RL. 2009. Agricultural originsand the isotopic identity of domestication in northern China. PNAS 106:5523–28

91. Fuller DQ, Qin L, Zheng Y, Zhao Z, Chen X, et al. 2009. The domestication process and domesticationrate in rice: spikelet bases from the Lower Yangtze. Science 323:1607–10

92. Liu X, Hunt HV, Jones MK. 2009. River valleys and foothills: changing archaeological perceptions ofNorth China’s earliest farms. Antiquity 83:82–95

93. Lu H, Zhang J, Liu K-b, Wu N, Li Y, et al. 2009. Earliest domestication of common millet (Panicummiliaceum) in East Asia extended to 10,000 years ago. PNAS 106:7367–72

94. Fuller DQ, Qin L. 2009. Water management and labour in the origins and dispersal of Asian rice. WorldArchaeol. 41:88–111

95. Flad RK, Jing Y, Shuicheng L. 2007. Zooarchaeological evidence for animal domestication in northwestChina. In Late Quaternary Climate Change and Human Adaptation in Arid China, ed. DB Madsen, X Gao,FH Chen, pp. 167–204. Amsterdam: Elsevier. 1st ed.

96. Yuan J, Flad R. 2002. Pig domestication in ancient China. Antiquity 76:724–3297. Cucchi T, Hulme-Beaman A, Yuan J, Dobney K. 2011. Early Neolithic pig domestication at Jiahu,

Henan Province, China: clues from molar shape analyses using geometric morphometric approaches.J. Archaeol. Sci. 38:11–22

98. Jiang L. 2004. Kuahuqiao. Beijing: Wenwu99. Groves CP. 2007. Current views on taxonomy and zoogeography of the genus Sus. In Pigs and Humans:

10,000 Years of Interaction, ed. U Albarella, K Dobney, A Ervynck, P Rowley-Conwy, pp. 15–29. Oxford:Oxford Univ. Press

100. Groves CP, Grubb P. 1993. The Eurasian Suids (Sus and Babyrousa). Taxonomy and description. In Pigs,Peccaries and Hippos, ed. WLR Oliver, pp. 107–12. Gland, Switz.: IUCN

101. Giuffra E, Kijas J, Amarger V, Carlborg O, Jeon J-T, Andersson L. 2000. The origin of the domesticpig: independent domestication and subsequent introgression. Genetics 154:1785–91

102. Fang M, Andersson L. 2006. Mitochondrial diversity in European and Chinese pigs is consistent withpopulation expansions that occurred prior to domestication. Proc. R. Soc. B Biol. Sci. 273:1803–10

103. Kim KI, Lee JH, Li K, Zhang YP, Lee SS, et al. 2002. Phylogenetic relationships of Asian and Europeanpig breeds determined by mitochondrial DNA D-loop sequence polymorphism. Anim. Genet. 33:19–25

104. Fang M, Hu X, Jiang T, Braunschweig M, Hu L, et al. 2005. The phylogeny of Chinese indigenous pigbreeds inferred from microsatellite markers. Anim. Genet. 36:7–13

105. Megens H-J, Crooijmans R, San Cristobal M, Hui X, Li N, Groenen M. 2008. Biodiversity of pig breedsfrom China and Europe estimated from pooled DNA samples: differences in microsatellite variationbetween two areas of domestication. Genet. Sel. Evol. 40:103–28

106. Ai H, Huang L, Ren J. 2013. Genetic diversity, linkage disequilibrium and selection signatures in Chineseand Western pigs revealed by genome-wide SNP markers. PLOS ONE 8:e56001

107. Ottoni C, Flink LG, Evin A, Georg C, De Cupere B, et al. 2012. Pig domestication and human-mediateddispersal in western Eurasia revealed through ancient DNA and geometric morphometrics. Mol. Biol.Evol. 30(4):824–32

108. Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, et al. 2007. Ancient DNA, pig domes-tication, and the spread of the Neolithic into Europe. PNAS 104:15276–81

109. Larson G, Liu R, Zhao X, Yuan J, Fuller D, et al. 2010. Patterns of East Asian pig domestication,migration, and turnover revealed by modern and ancient DNA. PNAS 107:7686–91

110. Larson G, Burger J. 2013. A population genetic theory of animal domestication. Trends Genet. 29:197–205111. Evin A, Girdland Flink L, Krause-Kyora B, Makarewicz C, Hartz S, et al. 2014. Exploring the complexity

of domestication: a response to Rowley-Conwy and Zeder. World Archaeol. 46:825–34112. Ramırez O, Burgos-Paz W, Casas E, Ballester M, Bianco E, et al. 2015. Genome data from a sixteenth

century pig illuminate modern breed relationships. Heredity 114:175–84113. Bosse M, Madsen O, Megens H-J, Frantz LA, Paudel Y, et al. 2014. Hybrid origin of European com-

mercial pigs examined by an in-depth haplotype analysis on chromosome 1. Front. Genet. 5:442



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


114. Bosse M, Megens HJ, Madsen O, Frantz LA, Paudel Y, et al. 2014. Untangling the hybrid nature ofmodern pig genomes: a mosaic derived from biogeographically distinct and highly divergent Sus scrofapopulations. Mol. Ecol. 23:4089–102

115. White S. 2011. From globalized pig breeds to capitalist pigs: a study in animal cultures and evolutionaryhistory. Environ. Hist. 16:94–120

116. Int. Union Conserv. Nat. 2014. Red List of Threatened Species. Version 2012.2. Gland, Switz.: IUCN117. Han D. 1987. Artiodactyla fossils from Liucheng Gigantopithecus cave in Guangxi. Mem. Inst. Vert.

Palaeontol. Palaeoanthropol. 18:135–208118. Hardjasamita HS. 1987. Taxonomy and phylogeny of the Suidae (Mammalia) in Indonesia. Scr. Geol.

85:1–68119. Meijaard E. 2014. A literature review of ecological separation between Sus verrucosus and S. Scrofa. Suiform

Sound. 12:18–25120. Semiadi G, Meijaard E. 2006. Distribution and conservation of Javan Warty Pig (Sus verrucosus). Oryx

40:50–56121. Rode-Margono EJ, Rademaker M. 2015. Preliminary results of the first ecological study on Bawean

warty pigs Sus blouchi. Suiform Sound. 13:15–18122. Groves CP, Schaller GB, Amato G, Khounboline K. 1997. Rediscovery of the wild pig Sus bucculentus.

Nature 386:335123. Robins JH, Ross HA, Allen MS, Matisoo-Smith E. 2006. Taxonomy: Sus bucculentus revisited. Nature

440:E7124. Schutz E. 2015. Records of Mindoro warty pig (Sus oliveri ) in the interior of Mindoro Island–Philippines.

Suiform Sound. 13:13–16125. Curran L, Leighton M. 2000. Vertebrate responses to spatiotemporal variation in seed production of

mast-fruiting Dipterocarpaceae. Ecol. Monogr. 70:101–28126. Fujinuma J, Harrison RD. 2012. Wild pigs (Sus scrofa) mediate large-scale edge effects in a lowland

tropical rainforest in peninsular Malaysia. PLOS ONE 7:e37321127. Hodgson B. 1847. On a new form of the hog kind or Suidae. J. Asiat. Soc. Bengal 16:423–28128. Oliver W. 2006. Pygmy hogs in southern Nepal (or news at last on the so-called ‘Hormel Expedition’)?

Suiform Sound. 6:19–22129. Narayan G, Deka P, Oliver W. 2008. Porcula salvania. In The IUCN Red List of Threatened Species. Version

2014.3. Gland, Switz.: IUCN130. Dennell R. 2010. Palaeoanthropology: early Homo sapiens in China. Nature 468:512–13131. Mellars P, Gori KC, Carr M, Soares PA, Richards MB. 2013. Genetic and archaeological perspectives

on the initial modern human colonization of southern Asia. PNAS 110:10699–704132. Cho I-C, Han S-H, Fang M, Lee S-S, Ko M-S, et al. 2009. The robust phylogeny of Korean wild boar

(Sus scrofa coreanus) using partial D-loop sequence of mtDNA. Mol. Cells 28:423–30133. Genov PV. 1999. A review of the cranial characteristics of the wild boar (Sus scrofa Linnaeus 1758), with

systematic conclusions. Mamm. Rev. 29:205–34134. Meijaard E, Groves CP. 2013. New taxonomic proposals for the Sus scrofa group in eastern Asia. Suiform

Sound. 12:26–30135. Wilson DE, Reeder DM. 1993. Mammal Species of the World. A Taxonomic and Geographic Reference.

Washington, DC: Smithson. Inst. Press. 1206 pp.136. Groves C, Grubb P. 2011. Ungulate Taxonomy. Baltimore, MD: Johns Hopkins Univ. Press137. Endo H, Kurohmaru M, Hayashi Y, Ohsako S, Matsumoto M, et al. 1998. Multivariate analysis of

mandible in the Ryukyu wild pig (Sus scrofa riukiuanus). J. Vet. Med. Sci. 60:731–33138. Watanobe T, Okumura N, Ishiguro N, Nakano M, Matsui A, et al. 1999. Genetic relationship and

distribution of the Japanese wild boar (Sus scrofa leucomystax) and Ryukyu wild boar (Sus scrofa riukiuanus)analysed by mitochondrial DNA. Mol. Ecol. 8:1509–12

139. Li C, Chang Q, Chen J, Zhang B, Zhu L, Zhou K. 2005. Population structure and phylogeography ofthe wild boar Sus scrofa in Northeast Asia based on mitochondrial DNA control region variation analysis.Acta Zool. Sin. 51:640–49

140. Wu C, Jiang Y, Chu H, Li S, Wang Y, et al. 2007. The type I Lanyu pig has a maternal genetic lineagedistinct from Asian and European pigs. Anim. Genet. 38:499–505

3.24 Frantz et al.


Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.


141. Food Agric. Organ. 2015. Fifteenth regular session of the Commission on Genetic Resources for Food andAgriculture, Rome, 19–23 Jan. CGRFA-15/15/Rep.

142. Laval G, Iannuccelli N, Legault C, Milan D, Groenen MA, et al. 2000. Genetic diversity of elevenEuropean pig breeds. Genet. Sel. Evol. 32:187–204

143. Martınez AM, Delgado JV, Rodero A, Vega-Pla JL. 2000. Genetic structure of the Iberian pig breedusing microsatellites. Anim. Genet. 31:295–301

144. Zhang G, Wang Z, Sun F, Chen W, Yang G, et al. 2003. Genetic diversity of microsatellite loci infifty-six Chinese native pig breeds. Acta Genet. Sin. 30:225–33

145. SanCristobal M, Chevalet C, Haley C, Joosten R, Rattink A, et al. 2006. Genetic diversity within andbetween European pig breeds using microsatellite markers. Anim. Genet. 37:189–98

146. Herrero-Medrano JM, Megens H-J, Groenen MA, Ramis G, Bosse M, et al. 2013. Conservation genomicanalysis of domestic and wild pig populations from the Iberian Peninsula. BMC Genet. 14:106

147. Foulley J, Van Schriek M, Alderson L, Amigues Y, Bagga M, et al. 2006. Genetic diversity analysis usinglowly polymorphic dominant markers: the example of AFLP in pigs. J. Hered. 97:244–52

148. SanCristobal M, Chevalet C, Peleman J, Heuven H, Brugmans B, et al. 2006. Genetic diversity inEuropean pigs utilizing amplified fragment length polymorphism markers. Anim. Genet. 37:232–38

149. Herrero-Medrano JM, Megens H-J, Groenen MA, Bosse M, Perez-Enciso M, Crooijmans RP. 2014.Whole-genome sequence analysis reveals differences in population management and selection of Euro-pean low-input pig breeds. BMC Genom. 15:601

150. Frantz LAF, Schraiber JG, Madsen O, Megens H-J, Cagan A, et al. 2015. Evidence of long-term geneflow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nat.Genet. 47:1141–48

151. Briedermann L. 1990. Schwarzwild. Berlin: VEB Dtsch. Landwirtsch.152. Yalden D. 2010. The History of British Mammals. Edinburgh: A&C Black153. Amaral AJ, Megens H-J, Crooijmans RP, Heuven HC, Groenen MA. 2008. Linkage disequilibrium

decay and haplotype block structure in the pig. Genetics 179:569–79154. Thomsen PD, Schausera K, Bertelsenc MF, Vejlsted M, Grøndahl C, Christensen K. 2011. Meiotic

studies in infertile domestic pig-babirusa hybrids. Cytogenet. Genome Res. 132:124–28155. Aubert M, Brumm A, Ramli M, Sutikna T, Saptomo EW, et al. 2014. Pleistocene cave art from Sulawesi,

Indonesia. Nature 514:223–27156. Langer P. 1988. The Mammalian Herbivore Stomach: Comparative Anatomy, Function and Evolution. New

York: G. Fischer157. Macdonald AA. 1994. The placenta and cardiac foramen ovale of the babirusa (Babyrousa babyrussa). Anat.

Embryol. 190:489–94158. Ziehmer B, Ogle S, Signorella A, Knorr C, Macdonald A. 2010. Anatomy and histology of the repro-

ductive tract of the female Babirusa (Babyrousa celebensis). Theriogenology 74:184–93159. Ziehmer B, Signorella A, Kneepkens A, Hunt C, Ogle S, et al. 2013. The anatomy and histology of the

reproductive tract of the male Babirusa (Babyrousa celebensis). Theriogenology 79:1054–64160. Nijman V, Nekaris KAI. 2014. Trade in Babirusa skulls on Bali in 2013. Suiform Sound. 12:34–36



Ann

u. R

ev. A

nim

. Bio

sci.

2016

.4. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

Acc

ess

prov

ided

by

Uni

vers

ity o

f O

xfor

d -

Bod

leia

n L

ibra

ry o

n 11

/09/

15. F

or p

erso

nal u

se o

nly.

The Evolution of Suidae - Welcome | PalaeoBarn

Documents

Transcript of The Evolution of Suidae - Welcome | PalaeoBarn