Why is the domestication of plants and animals seen as a form of artificial selection as opposed to natural selection?

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Introduction

Most contemporary evolutionary biologists study evolution experimentally using laboratory organisms such as Drosophila or natural systems in the wild. However, 18th and 19th century evolutionary biologists, including Darwin, emphasised the similarities between natural evolution and artificial ‘ improvement’ of livestock under domestication. They believed that studying domesticated animals and plants could illuminate the mechanisms of natural evolution. Indeed, Chapter 1 of On the Origin of Species… is entitled ‘Variation under domestication’. Recent discoveries reveal the relationship between natural evolutionary mechanisms and the practical technologies used to breed plants, animals, yeasts and, these days, microbes, to produce food, clothing, transport, companionship, decoration, entertainment and most recently medicines. This course is mostly about mammals, particularly dogs and other domesticated livestock, but the basic principles are probably universal. Dogs and other livestock are so familiar that we hope that you will take the opportunity to observe the characters, habits and processes described in this course in animals that you see around you.

This OpenLearn course is an adapted extract from the Open University course : S366 Evolution.

Learning outcomes

After studying this course, you should be able to:

define the terms ‘artificial selection’ and ‘domestication’ and explain the relationship between artificial and natural selection
describe some forms of dwarfism in modern breeds of dogs and explain their relationship to dwarfism in humans and in modern and extinct wild mammals
describe some features of the skin, fur, feathers and the shape of the head frequently observed in domesticated livestock
outline some major conclusions emerging from the sequencing of the dog genome and outline some current theories about when and where dogs were domesticated
explain the functional basis of some of the anatomical changes induced by selective breeding of some modern dog breeds.

1 Phenotypes and genotypes

1.1 Introduction

Since the invention of DNA sequencers in the late 20th century, measuring very small differences between the genes of different organisms has become much easier and more precise than quantifying phenotypic variation. Synonymous mutations and changes to introns are examples of genetic changes that have no consequences for the phenotype. Natural selection acts only on phenotypes, so the relationship between genotypic changes and phenotype is clearly very important to understanding evolution. Discoveries about how and when genes act during the growth and development of animals, the consequences of developmental processes for adult structure, and observations on the relationship between behaviour, physiology and anatomy, have led to new insight into the origin and the evolution of phenotypic traits.

1.2 Artificial selection

Selection acts on phenotypic characters whatever their origin, and can retain or eliminate the characters' genetic basis. Artificial selection is any selective breeding intentionally practiced by humans leading to the evolution of domesticated organisms. Artificial selection may oppose or amplify or be neutral in relation to natural selection. Most livestock, including dogs, cats, goats, pigs, cattle, sheep, guinea pigs, horses, geese and poultry and scores of crop plants were domesticated more than 5000 years ago. (Estimates of dates of domestication based upon the archaeological record differ enormously from those based on genetic analysis for almost all crops and livestock. However, experts agree that dogs were among the first mammalian species to become domesticated, followed by sheep.) During the last few hundred years, people have domesticated a wide range of other animals such as guppies, hamsters, mice and budgerigars, mostly for use as pets, together with thousands of culinary, medicinal and ornamental plants.

Pets and livestock are protected from predators and provided with food and shelter.

SAQ 1

How would these living conditions alter the action of natural selection in domesticated populations?

Answer

Natural selection would be much weakened, particularly for the characters such as ability to recognise and escape predators, finding, eating and digesting food, and tolerance of severe weather conditions.

SAQ 2

Name a wild species in which relaxation of selection for the ability to escape predators has happened naturally. How did the animals' behaviour differ from that of related populations that are exposed to predators?

Answer

Svalbard reindeer have had no natural predators for many thousands of years. Like domesticated cattle, these reindeer have lost the ability and the inclination to run away when approached.

However, unlike many domesticated animals, Svalbard reindeer retain the capacity to forage and breed in a difficult climate. This example emphasises the similarities between evolution in artificial or natural environments, driven by artificial or natural selection.

SAQ 3

On what kind of characters would natural selection continue to act in populations of domesticated livestock?

Answer

Characters that affect fecundity such as age at maturity, litter size and parental behaviour.

SAQ 4

Would domesticated livestock generally produce more or fewer offspring than their wild relations?

Answer

More, because human protection would prevent natural selection against traits such as heavily gravid mothers becoming unable to escape predators or find enough food.

One of the principal differences between domesticated dogs and wolves is that most dogs come into oestrus and breed twice a year. Only the most primitive breeds, including the Australian dingo and the Basenji (an African breed), resemble their wild ancestors in breeding only once a year. In a biological context, primitive just means coming first (as in ‘primary’). The word does not imply inferiority or simplicity.

SAQ 5

Which special form of natural selection relating to reproduction could be eliminated entirely under domestication?

Humans determine which adults breed. Sexually receptive females may be confined with only one male, effectively eliminating sexual selection.

SAQ 6

Which other natural evolutionary processes that determine genotypes as well as phenotypes would continue to operate under domestication?

Answer

Genetic drift and other forms of non-adaptive evolution.

Domesticated animals are usually held in small, isolated populations with limited opportunities for interbreeding. For centuries, drovers herded large numbers of non-breeding pigs, cattle, sheep, geese and poultry to market for slaughter, often over hundreds of kilometres. However, the breeding stocks were usually kept within a small area because moving sexually active bulls and large boars over long distances was much less practical.

Domestication is different from taming of wild animals. Certain individuals of many species, especially juveniles and females, can be tamed and live in captivity where they are protected from predators and provided with food and shelter. Domesticated livestock are also fed and protected, but many generations breed and spend their entire lives in close association with humans.

Question 1

List the similarities and differences between evolution under domestication and natural evolution.

Answer

Similarities

Selection operates, determining that not all individuals born reach maturity and breed successfully.
Selection is for certain characters or combinations of characters but it only causes evolutionary change if the phenotypic characters have a genetic basis.
Mutation and genetic drift can occur leading to adaptive and non-adaptive evolution.

Differences

Artificial selection as well as natural selection operate, but not necessarily in the same direction.
Artificial selection may favour characters that would have been eliminated under natural selection.
Sexual selection is partially or entirely eliminated.
Artificial selection can be severe, with only a small fraction of each generation becoming parents of the next.
Population size of domesticated livestock can be even smaller than natural populations, which promotes inbreeding.

2 Phenotypic change under domestication

2.1 Introduction

For centuries, livestock breeders have nurtured strains of animals that thrive on various diets or in particular climates, or that excel in certain roles or simply please their fancy. The variety of such animals seems bewildering but certain changes consistently emerge in a surprisingly wide range of domesticated species and among humans, suggesting that similar mechanisms are operating. Here we describe just two such clusters of changes, in the skeleton and in the skin.

2.2 Size and shape

The shape of the head is determined mainly by the relative sizes of the jaws and the nose and the back of the skull containing the brain, eyes, ears and, in artiodactyls, the horns or antlers. All these structures may differ greatly between otherwise similar species.

SAQ 7

How are the size and shape of antlers of Svalbard reindeer different from those of the mainland subspecies?

Answer

The antlers of Svalbard reindeer are much smaller and simpler than those of the mainland subspecies.

Figure 1 Domesticated sheep and cattle with variable, reduced or absent horns. (a) Longhorn cattle; (b) Jacob's sheep with three horns; (c) White Park cattle; (d) a modern hornless breed of sheep

This natural and probably relatively recent evolutionary change is believed to arise from the simpler and less combative social structure of Svalbard reindeer, which live in small groups where there is less fighting. The horns and antlers of wild artiodactyls are of consistent shape for each species and nearly symmetrical, at least in mature adults. Many domesticated sheep and cattle are hornless or have horns of variable, often asymmetrical, size and shape. Anomalies such as having three (or four) horns are also common even in modern breeds (Figure 1b). Almost all adult mammals have erect ears (Figure 1b, c and d) but floppy ears appear in many domesticated livestock including sheep, cattle, pigs and rabbits (Figure 2).

Figure 2 Drooping ears in domesticated mammals. (a) Zebu cow; (b) pig; (c) sheep from Jordan; (d) lop-eared rabbit (with prick-eared companion); (e) guinea pig. Although some of these varieties are not commonly seen in Britain, all except rabbits are ancient breeds, long established for the production of meat, milk and/or wool

Dwarfism and gigantism are also common among almost all domesticated mammals and have recently been found among laboratory mice that are bred for research purposes. Some small dogs, such as Figure 3a and b, are miniatures with proportions of the head, body and feet typical of normal puppies, while the head, feet and body of the Shetland pony (Figure 3c) and the basset hound (Figure 3d) are clearly too big relative to the legs. Miniaturisation to infantile size and body proportions similar to Figure 3 a and b is known in certain wild mammals, for example Pleistocene miniature elephants on Crete.

Figure 3 Two forms of dwarfism in domesticated mammals: (a) and (b) miniature dogs; (c) achondroplastic dwarf Shetland pony, and (d) basset hound. Note the different proportions of the head, limbs and trunk

The most common form of dwarfism among humans is achondroplasia (Figure 4a), caused by defects in an autosomal dominant gene that encodes a receptor protein for a key growth factor. (Achondroplasia is derived from Greek words: a- ‘lack of’; chondros, ’cartilage’; plasia, 'molding’. The term is not strictly accurate because such people have cartilage, but its ability to turn into bone is impaired, greatly slowing the growth of all the long bones and the nose.) This gene seems to be unusually susceptible to mutation: more than 80 per cent of human achondroplastic dwarfs are born into families with no history of dwarfism so they must carry a new mutation. Growth of the limbs, hands, feet and nose is more severely curtailed than that of the head or trunk, distorting the body proportions (Figure 4a). Most achondroplastic dwarfs cannot run far or fast. They are very susceptible to joint disorders and many suffer from chronic backache from an early age, but they are mentally normal and some marry and have children.

Figure 4a: AKG-Images; Figure 4b: Prado Museum, Madrid; Figure 4c: AKG-images/Joseph Martin

Figure 4 Dwarfism in humans. These portraits were produced in Spain in the early 17th century by Diego Velázquez (1599–1660) and Rodrigo de Villandrando (1590–1630), court painters to the Spanish royal family. (a) An adult achondroplastic dwarf with the typical disproportionately large head (detail from Las Meninas, 1656–7). Note the similarities to Figure 3c and d. (b) Philip III's son Philip with the dwarf Solplillo. This midget's head, limbs and body are more or less in proportion. (c) The infant Prince Baltasar Carlos with a dwarf servant, 1631

Midgets (Figure 4b and c) are a rarer form of human dwarfism; they are very short but, in contrast to achondroplastic dwarfs, have more or less normal proportions. In the 17th century, midgets such as the Spaniard, Solplillo, were the focus of much curiosity from aristocrats and scientists. The proportions of the face and of the head relative to the body enable you to distinguish the 16 month-old prince (Figure 4c) from his older midget companion. The body proportions of miniature dogs such as those shown in Figure 3a and b and almost all dwarf wild mammals, such as the pygmy hippopotamus (maximum height 1.75 m, body mass 275 kg, compared to the common hippo which weighs up to 4000 kg), resemble those of human midgets. Dwarfism similar to achondroplasia in humans is known in dogs (e.g. basset hounds, Figure 3d), horses (Figure 3c) and among cattle, pigs and goats.

SAQ 8

Would achondroplasia be more readily favoured by artificial selection in domesticated livestock than by natural selection in wild animals?

Answer

Yes. As long as the animals could breed successfully, impaired mobility would not reduce fecundity.

SAQ 9

Would a dominant gene be more easily selected than a recessive gene in domestic livestock?

Answer

Yes. Artificial selection would be much more efficient for dominant genes because all animals that have the gene display the dwarf phenotype.

Question 2

Why would achondroplastic dwarfism be much rarer in dwarf races of wild mammals than the midget form, even though mutations of the genes that produce achondroplasia probably occur much more frequently?

Answer

The experience of human achondroplastic dwarfs suggests that wild animals with this form of dwarfism would be unable to run far or fast. They would therefore be very vulnerable to predation and have difficulty catching food. Such dwarfs would be eliminated by natural selection in the wild. Movement is much less impaired in proportionate, midget dwarfs, so they are more likely to survive and therefore to become the ancestors of reduced-size races of large mammals.

2.3 Skin pigmentation and pattern

Most domesticated livestock differ from their wild ancestors in the colour and pattern of the skin, hair or feathers.

SAQ 10

What gene-associated factors determine the colour of feathers in modern birds?

Answer

Melanin and other pigments are synthesised and become incorporated into the feather early in its development. Different-coloured feathers can emerge from the same follicle in successive moults, showing that this process is modulated by hormones especially, but not exclusively, sex hormones.

Figure 5 Wild animals that closely resemble the ancestors of some domesticated mammals. (a) Pigs. (b) Timber or grey wolf. (c) ‘Aurochs’; this zoo animal is an artificially bred reconstruction of the now-extinct wild ancestor of European domesticated cattle. (d) Przewalski's wild horse, which was widespread throughout Europe and Asia in the Pleistocene but is now confined to a small area of Mongolia in central Asia

Most mammals, including extant descendants of the wild ancestors of domesticated species, are brown or black (Figure 5), or have markings that conform to consistent patterns (Figure 6). Many domesticated mammals and birds are white or piebald or skewbald (see Figures 2 and 3): pigs, sheep, horses, cattle (Figures 1 and 7) and dogs and cats (Figure 8) often have irregular and asymmetrical spots and blotches but very rarely the regular, symmetrical patterns seen in wild mammals (Figure 6). (Piebald (= black-and-white) and skewbald (= any other colour and white) are mostly frequently applied to horses, but as this section explains, very similar patterns are found in a wide variety of other domesticated species. These terms are still correct only for livestock; the equivalent term for wild animals is pied, e.g. pied wagtail.)

Figure 6 Patterned wild mammals: (a) zebra (Equus burchelli); (b) giraffe (Giraffa camelopardalis); (c) tiger (Panthera tigris); (d) fallow deer (Dama dama)

Such irregularly patterned hair and plumage has appeared spontaneously among many lineages of livestock. Farmers and pet fanciers selectively bred preferred animals, producing ‘pure’ strains of livestock. For example, sheep have been bred so that the fleece is usually a uniform creamy white (Figures 1d and Figure 9a), but the occasional exceptions (Figure 9b) are still common and viable, and the faces and legs of those with white fleeces are often black (Figure 9c) or mottled (Figures 1d and Figure 9d). Note the similarity in the speckled patterns of these sheep and that of some dogs (Figure 8d). The patterns of ‘belted’ pigs and cattle (Figure 7 a and b) are also remarkably similar.

Figure 7 Piebald and skewbald domesticated mammals: (a) belted pigs; (b) belted bullock; (c) Friesian cows; (d) spotted piglets; (e) skewbald mare and foal

Figure 8 Piebald and skewbald dogs and cat: (a) Dalmatian; (b) collie sheepdog; (c) Shih-tzu, an ancient oriental breed related to Pekinese dogs; (d) pointer; (e) piebald cat

Mottled and white feathers are also common in birds that have been bred under domestication (Figure 10). Domestic fowl are order Galliformes, related to peafowl and pheasants; the breeding plumage of male galliforms is almost always colourful and elaborate, but that of females is speckled brown because they and they alone incubate the eggs and protect the chicks. For similar reasons, the plumage of mallards and many other ducks (order Anseriformes) is sexually dimorphic, at least during the breeding season.

Figure 9 Various domesticated sheep

Figure 10 White or pied domesticated birds compared to their wild relatives. (a) Domestic poultry: (i) brown hens; (ii) adult male inbreeding plumage similar to that of the wild ancestors; (iii) adult male (left) and female (right) that are white with some pied neck feathers; (iv) adults of a pure white breed. Note that none of these birds is true albino: all have red combs and pigmented beaks and legs. (b) (i) Greylag geese (Anser anser) that are the ancestors of (ii) European domestic geese. (c) Indian peacocks (Pavo cristatus), with plumage of natural breeding colours (i), and white domesticated forms (ii)

Question 3

Why would white plumage in poultry (Figure 10a) and peacocks (Figure 10c) during the breeding season be eliminated by natural selection in (a) males and (b) females?

Discussion

(a) Males without the species-specific breeding plumage would attract very few females and would be unlikely to succeed in male-male rivalry.
(b) Conspecific males may be unable to recognise white females as members of their own species. Predators would more easily notice white females brooding eggs on a nest than well camouflaged hens.

Question 4

What features of the plumage of the peacocks (Figure 10c) show that the only difference between the wild and domesticated forms is pigmentation, i.e. the mechanism of formation of the feathers is unaltered?

Discussion

The crown of feathers on the head and the long tail feathers are the same sizes and shapes in both the wild-type and white birds. Feather size and shape are determined by elaborately controlled proliferation, maturation and death of keratinocytes. A distinct lineage of cells, the pigment cells, synthesise various coloured molecules, or none, and may or may not be incorporated into the developing feather. If the pigment cells are absent or inactive, the feathers are white.

3 Domesticated dogs

3.1 The origins of domesticated dogs

Archaeologists and biologists agree that dogs (Canis familiaris) were the first species to become domesticated. Francis Galton, Darwin's younger cousin, suggested at the end of the 19th century that domestication began when humans captured and raised wolf puppies. The resulting adults ate scraps of human food, assisted in hunting and acted as guard dogs around camps. Among the evidence in support of this hypothesis is the observation that tribal people all over the world take wild animals as pets. As well as wolf puppies, animals as diverse as goldfish, bear cubs and parrots are fed and tended as companions or objects of curiosity, not as food. Some ‘pets’ acquired a sacred dimension, becoming personal or tribal totems that are often represented as models or images. More recent research suggests that pet-keeping by itself cannot explain domestication of dogs (see below).

At the end of 2005, the first sequencing of the dog genome was published, based on material from a female boxer, chosen because she appeared to have very few heterozygous loci. The second dog genome to be sequenced was that of a standard poodle. Single nucleotide polymorphisms (SNPs pronounced ‘snips’) identified in the boxer were compared with those of 11 other breeds of dogs and samples taken from wolves, jackals and coyotes collected in various parts of the world. The best match was with wolves (Figures 5b and 11a), particularly those native to northern China, suggesting that the Far East was a major site of dog domestication and grey wolves (Canis lupus) were the principal ancestors. However, there was also clear evidence of genes derived from jackals (Figure 11b), coyotes (Canis latrans) and Ethiopian wolves (Canis simensis) in domestic dogs. Recent sequencing of exons and introns of small fractions of the genomes of 31 (of 34) living species of Canidae (Lindblad-Toh et al., 2005) suggests that golden jackals diverged from coyotes, wolves and dogs about 3–4 My ago. Nonetheless, all these species of the genus Canis can interbreed under artificial conditions. Evidently, these interspecific hybrids were fertile because their descendants are our working dogs and pets. Modern genetic studies reveal a small amount of natural interbreeding between several wild canid species.

Figure 11 (a) Members of a pack of timber or grey wolves (Canis lupus). (b) Golden jackal (Canis aureus)

The grey wolf (Figures 5b and 11a) used to be among the most widespread of all mammals; at the end of the Pleistocene (about 10 000 years ago), the species occurred throughout the Northern Hemisphere except in arid deserts, and was common in many places. Small isolated populations survive today only in areas of Scandinavia, Russia, Mongolia, northwestern China, Canada and Alaska that are too barren to support domesticated livestock or agriculture. There are some regional differences in adult size and coat colour, but the patterns were always camouflaged and graded (as in Figures 5b and 11a), never piebald.

Wolves are the most social of all living canids. They live and hunt in packs led by one or a few dominant animals. Usually only the senior pairs breed, but subordinate, non-reproducing pack members catch and bring food to the pups. Pack hierarchy is maintained and the wolves’ activities are coordinated by varied and elaborate communications involving gestures and postures of the ears, eyes, muzzle, fur, tail and body (Figure 11a), and a wide range of sounds and scents.

SAQ 11

Domesticated dogs use most of these behaviours to communicate with each other. Observe some local dogs and list some calls, postures, gestures and facial expressions. Do dogs recognise and respond to human sounds and gestures?

Answer

Dogs communicate with each other and with people by tail-wagging, licking, erecting hair on the back, ears laid back, growling, snarling, whining, submissive crouching and many more such behaviours. Dogs respond to human commands and signals and to many unintentional communications, e.g. they recognise people's fear.

Hunting in packs enables wolves to kill animals much larger than themselves. They mainly prey on bovids, cervids and wild horses, but when food is scarce, they take smaller species and sometimes scavenge.

Jackals and their New World equivalent, coyotes, are smaller than wolves and are scavengers as well as predators of rodents, rabbits, ground-nesting birds and other small species. Several jackal species are monogamous and forage in pairs rather than in packs, and even where larger family groups do form, their social behaviour is not as elaborate or as well coordinated as that of wolves. Coyotes and several species of jackals are still widespread and, in places, fairly common.

Modern studies of ancient dog bones reveal numerous cut marks, indicating that humans' first use for dogs was as food. In parts of the Far East and Polynesia, dogs are still bred and raised for the table, alongside domesticated artiodactyls (Figures 1, 2, 7 and 9) and poultry (Figure 10). However, in most of the rest of the world (including modern China), dogs are used for managing other livestock, for various roles in hunting including following scent trails, pointing and retrieving, as guards and as companions. In these roles, temperament, intelligence, learning ability and other aspects of behaviour are as important as physique.

The central role of behaviour in domesticated dogs was recognised by scientists more than two centuries ago. The 18th-century surgeon and anatomist John Hunter, like many of his contemporaries, was very interested in the biology of domestication, which he believed illuminated the mechanisms of natural evolution. He and his collaborators made several attempts to hybridise dogs and wolves and for a while in the 1770s, he owned a wolf-dog hybrid. In 1786, he obtained a puppy born from the mating of a male spaniel with a female jackal (probably Canis aureus, see Figure 11b) originating from India. He sent one of this animal's offspring to his former pupil and lifelong friend Edward Jenner who kept it at his home in Berkeley, Gloucestershire. This astute observer of animal and human behaviour reported in a letter to Hunter: ‘The little jackal bitch you gave me is grown a fine, handsome animal but she certainly does not possess the understanding of common dogs. She is easily lost when I take her out and is quite inattentive to a whistle.’ In other words, this hybrid was anatomically and physiologically sound, but lacked the mental ability to interact with humans as well as domesticated dogs can.

(Dr Edward Jenner FRS (1749–1823) is chiefly remembered as a pioneer of vaccination against smallpox, the basis for the only completely successful extermination of a human pathogen. During his lifetime, he was known for fundamental research on the anatomy and habits of cuckoos and the relationship between angina, heart attacks and fatty deposits in the arteries.)

Many breeds of dogs originated from a very few ancestors. The small ancestral gene pool combined with much inbreeding favour genes becoming common through genetic drift. Such effects have undoubtedly occurred, and many purebred dogs are unusually prone to certain diseases including hereditary deafness and some forms of cancer.

SAQ 12

Would the action of natural selection eliminate (a) deafness and (b) cancer?

Answer

(a) Yes, because deaf animals would be more vulnerable to predators and other hazards, including traffic.
(b) Only if the cancer directly affected fertility or became disabling early enough in life to reduce lifetime fecundity and nurturing the offspring. Natural selection cannot eliminate diseases of old age.

With the recent rise in the keeping of specialised breeds of dogs (e.g. terriers, dachshunds, retrievers, bulldogs) as pets rather than as working dogs, hybrids between breeds have become very common. Some have become feral: although descended from domesticated ancestors, they live and breed as wild animals. All modern breeds of dogs, with their variation in size and shape, habits, coat colour and texture, are mutually fertile and share certain species-specific physiological characteristics; for example, the length of the gestation period is the same for all breeds regardless of body size. In spite of the huge range of phenotypes, dogs have not formed discrete species.

Question 5

List some reasons why the intensive study of many different aspects of dog biology provides insight into the process of evolution under domestication.

Answer

Relevant topics include:

Dogs are among the most ancient domesticated animals.
The dog genome has now been sequenced.
Dogs are highly social mammals that communicate using sounds, facial expressions and postures; these behaviours are readily interpreted by humans and dogs respond to human-generated sounds and to human gestures.
Dog behaviour has been thoroughly studied.
Many breeds that differ in habits and behaviour also differ in structure and appearance.
Many dog breeds are highly inbred but mongrels are also common and viable.

3.2 Structure and behaviour in modern dog breeds

Dogs are one of the most diverse of all living species, differing in size and shape of the skull and the proportions of the body, especially the head and legs, and in the colour and texture of the coat (Figures 3a, b and d, 8a–d and 12). People have ‘improved’ dogs for specific properties and uses by artificial selection for visible anatomical characters and for more subtle aspects of behaviour, habits and intelligence. An example is the two major kinds of hounds selectively bred for hunting wild mammals.

Foxhounds (Figure 12a) hunt almost entirely by smell and chase their quarry over long distances. They perform best in large packs, communicating with each other and their human handlers by sound – ‘giving tongue’ as the huntsmen describe it – and gestures with their prominent tails. Their sturdy, wolf-like body proportions (compare Figures 5b and 11a with Figure 12a) equip them for endurance as well as speed and enable them to gallop with the sensitive nose close to the ground. If given the opportunity, they can kill small animals with their powerful jaws and necks.

Figures 12a, b, f,: Copyright © Caroline Pond; Figure 12c: Copyright © Gerard Lacz/ FLPA; Figure 12d: Copyright © Mandy Dyson; Figure 12e: Neff, M. W. and Rine, J. (2006) ‘A fetching model organism’, Cell, 124(2) ©

Figure 12 Phenotypic diversity of some modern breeds of dogs. (a) Foxhound; note the stout head and jaws, large floppy ears, sturdy, well-proportioned body and legs, multicoloured coat and prominent tail. (b) Greyhound; note the narrow jaws and head with relatively large, forward-directed eyes, small floppy ears, long, flexible back, chest much larger than abdomen, long athletic legs with disproportionately long thighs and shoulders, and tail held between the hindlegs (where it is almost invisible). (c) Mastiff. (d) Boston terrier. (e) Ibizan hound. (f) Cocker spaniel

SAQ 13

Which morphological features of foxhounds are characteristic of domesticated dogs but not of wolves?

Answer

Foxhounds have floppy ears. Their coat colours are very varied, mostly piebald or skewbald (see Figure 12a).

Greyhounds (Figure 12b) are also specialised hunters, first developed in Egypt and the Middle East around 4000 years ago for hunting very fast mammals such as gazelles, antelopes and hares by sight rather than by scent. They always gallop with the head pointing forward not downwards. Pairs or groups of greyhounds have long been raced for display, and are now bred mainly for such organised competitions. Greyhounds have relatively large eyes, bark and howl only rarely and do not communicate with tail gestures as readily as most other dogs. Their slender, athletic bodies and long legs make them the fastest of all dogs for short sprints but they lack foxhounds’ stamina and ability to cope with rough ground. Greyhounds are also surprisingly timid dogs that are reluctant to attack large prey with their weak jaws: actually killing the quarry was left to their human handlers.

SAQ 14

With reference to Figure 11a, what aspect of intraspecific communication would be impossible for foxhounds, greyhounds and other floppy-eared dogs?

Answer

Wolves (and prick-eared dogs) express fear and threat by laying back their ears (note particularly the ‘underdog’ and the bystander at the back of the picture), which would be impossible for dogs with disproportionately long floppy ears.

As well as fur colour (Section 2.3), features of the head, including the size and shape of the jaws, skull and ears are among the most variable features of most mammals including dogs and humans. For example, the snout and upper jaw of the miniature dachshund (Figure 3b) are clearly longer than its lower jaw. Figure 12 illustrates the range of sizes and shapes of ears and skulls found in modern breeds of dogs. These superficial features seem to occur in all possible combinations, but there are functional limits to phenotypic modifications that can be perpetuated by artificial selection.

SAQ 15

Greyhounds (Figure 12b) and Boston terriers (Figure 12d) have similar-shaped bodies and legs, but very different heads and necks. Which of these breeds would be best able to reproduce successfully without human assistance?

Answer

Greyhounds. Giving birth through narrow hips to puppies with flat, long, narrow heads would be very much easier than to those with wide, round skulls.

Some modern breeds including bulldogs and Boston terriers have great difficulty giving birth naturally and are usually delivered by Caesarean section. Clearly such procedures were impossible for long-established breeds. The greyhound's narrow skull was probably not specifically selected as a desirable trait but appeared in association with more important qualities such as running speed.

Question 6

Using your own general experience and comparing all the dogs in Figures 3a, b and d, 8 and 12, answer (a) and (b) below.

(a) Are floppy or prick ears associated with any particular sort of snout shape or temperament?
(b) Are dogs with disproportionately long, thick coats (e.g. sheep dog, Figure 8b; Shih-tzu, Figure 8c) as capable of prolonged exercise in hot weather as those with sleek coats (e.g. Figures 3a and b, 8a and d, and 12)?

Answer

(a) No. Foxhounds and mastiffs (Figures 12a and c) that are bred to bite with powerful jaws have floppy ears, as do docile breeds like spaniels (Figure 12f), basset hounds (Figure 3d) and miniature dogs (Figures 3b and 8c). Conversely, some toy dogs (Figure 3a) have prick ears and long snouts.
(b) Dogs with very thick coats become uncomfortably overheated in hot weather even when sedentary. Dogs with naturally short coats or those that have been clipped are much more willing and able to perform prolonged strenuous exercise.

4 Experimental study of evolution and domestication

4.1 Introduction

Domestication of dogs and of most other livestock took place so long ago that reconstructing the course of events is extremely difficult. Written records and illustrations describing the origins of many modern breeds are also sparse until the 19th century. We can only guess at what the domesticators were aiming to produce and how and when domesticated traits appeared in the species subjected to artificial selection. However, a little-known experiment on the domestication of red foxes (Vulpes vulpes) provides unique insight into the relationship between behaviour and structure under artificial selection.

V. vulpes is by far the most successful extant species of the family Canidae. Its natural range is very similar to that of the wolf, comprising Europe, USA and Canada, and northern and central Asia (including almost the whole of Russia, China and Japan), but in contrast to wolves, foxes are still widespread and common in many areas. Its coat colour varies from red (Figure 13a) to very dark brown; the underparts are usually paler, sometimes white, and the ears, legs and feet are darker, often almost black, and a white tip on the tail is common. So far as we know, the species has never been domesticated, though it has long been hunted for its valuable fur and, especially in Russia, kept in captivity for the same purpose.

4.2 Experimental domestication of foxes

In 1959, the Russian geneticist Dmitri K. Belyaev (1917–1985) launched a long-term experiment to tame captive-bred red foxes by selecting for a single behavioural trait: lack of fear and aggression towards humans. Over 40 years, more than 45 000 foxes were bred in captivity at a remote farm near Novosibirsk, Siberia. Various behavioural, physiological and morphological characters were studied in each fox. Selection for tameness was strict: each animal was assessed once a month for seven months for its willingness to approach people, take food from human hands and be stroked (Figure 13b). Only the tamest 5 per cent of males and 20 per cent of females of each generation were allowed to breed. The control population was bred randomly with respect to their behaviour with people.

SAQ 16

Are these levels of artificial selection strong compared with natural selection measured in wild populations?

Answer

Yes, very strong. In natural populations, the chances of survival and successful reproduction of individuals with or without particular traits usually differ by only a few per cent, i.e. selection coefficients are much less than 1.

Selection at this level in small isolated populations is likely to make some inbreeding unavoidable.

SAQ 17

What simple intervention would reduce inbreeding?

Answer

Eliminating breeding between the brothers and sisters.

Figure 13 (a) Wild red fox. (b) In July 1983, Professor Aubrey Manning (hand-feeding a fox) visited Dmitri K Belyaev (third from left) and Ludmilla Trut (far left) who is now in charge of the fox domestication project in Novosibirsk. (c) Some foxes selectively bred for tameness with handlers; note the range of colours and the white blaze on the face of the grey fox on the far left. (d) Some tamed fox cubs; note the blazes on the faces, the white ‘socks’ and the white collar on the cub at the back of the picture

By applying this rule in each generation, inbreeding was maintained at about 3–7 per cent (compared to around 12 per cent in many contemporary pedigree dogs).

SAQ 18

What evidence would show that the change in behaviour had a genetic basis?

Answer

A strong response to selection in the form of greater frequency of tameness behaviour in the offspring of foxes selected for this trait.

The experimenters found that after 10 generations, 18 per cent of the foxes in the selected population showed clear signs of tameness. They approached and licked people, wagged their tails, whined and begged for food offered by hand. After 20 generations, the proportion of foxes showing this kind of behaviour had risen to 35 per cent, clear evidence of response to selection for inherited traits.

Question 7

Using the theory and terms developed for the study of natural selection, was artificial selection for tameness in the fox experiment:

(a) stronger in male or female foxes?
(b) directional, stabilising or diversifying?
(c) promoting or reducing genetic diversity in the population?
(d) operating in the same direction as or opposing natural selection?

Discussion

(a) Males, as a smaller proportion of each generation were allowed to breed.
(b) Selection for tameness was strongly directional because the same character was favoured in each generation.
(c) Such a small proportion of the population was allowed to breed that genetic diversity must have been reduced.
(d) Natural selection favours adaptations that enable animals to thrive in the wild; the artificial selection opposes such natural selection by making the foxes less afraid of large potential predators such as people, and by favouring coat colours and temperaments that reduce their ability to find and catch their own food.

4.3 Phenotypic changes that appeared without being selected

As well as these behavioural changes, many of the selected foxes had unusual white markings (Figures 13c and d). The first colour change that the Russian investigators noted in their foxes was a white ‘star’ on the forehead similar to that of other domesticated mammals (Figure 14a), which enlarged in later generations to form a blaze (Figure 13c and d). Both these patterns are very common in domesticated horses (Figures 14a and b) and cattle (Figure 14d), but absent from their wild ancestors (Figure 5c and d). Many of the tamest foxes were piebald or skewbald (as in other species, Figures 3a, c and d, 7, 14c and d), had floppy ears (similar to those of the animals in Figures 2, 3b and d, 8a, c and d, 12a, c and f) and longer, silkier fur (as in certain dogs, Figures 8c and 12f). After more than 40 years of selective breeding, the coat patterns of some of the foxes (Figure 13d) were remarkably like those of collie dogs (Figure 8b). None of these features of the coat or ears were deliberately selected for; they were the accidental consequences of selection for tameness and tameness alone.

Figure 14 Some coat patterns common in domesticated horses and cattle that also appeared in experimentally domesticated foxes. (a) White ‘star’ on centre of forehead; (b) blaze around the midline of the head from forehead to snout; irregular skewbald colouring in (c) a Shetland pony and (d) a bullock

More detailed study of some of the early fox fetuses revealed that the pigment-forming cells migrate to the skin two days later in the tame foxes than in unselected wild-types, and a much higher proportion of the cells die.

SAQ 19

Would this mechanism produce a piebald coat?

Answer

Yes. Patches of fetal skin that were successfully invaded by pigment-forming cells would produce dark hair, while those with few or no pigment-forming cells would produce lighter hair, or white hair.

Dermal cells that form pigments are derived in the developing embryo from an important and diverse group of embryonic cells called the neural crest. If these cells fail to migrate to an area of skin, do not mature properly or die in the fetus, that area of skin and all the dermal structures derived from it, such as hair and feathers, lack the correct pigment in the adult.

In an attempt to identify the molecular and cellular bases for these changes under domestication, the breeders also measured some anatomical features of the brains and assayed corticosteroid hormones from blood samples. (Techniques for measuring these hormones and knowledge of their structural and functional diversity have improved greatly since this research began in the 1960s. The family of signal molecules includes glucocorticoids (e.g. cortisol), corticotropins and several more.) Levels of these hormones rise within seconds of acute episodes of pain or fear and the background levels are also higher in animals (and people) that are subject to chronic stress or anxiety. After 12 generations of artificial selection, the average levels of these hormones were down at half those of the control population, and to only a quarter by the 30th generation.

SAQ 20

What are the problems for interpreting these observations on a population of wild animals kept under confined conditions in captivity?

Answer

Hormone levels could be unnaturally high in unselected foxes because of the husbandry conditions. The selection regime could be just favouring those foxes that maintain normal levels of hormones in spite of the conditions. However, all wild animals, particularly predators, experience stress as an integral part of finding food, competing for mates and avoiding danger.

The average total mass of the brain was about 25 per cent less in tamer foxes than in controls. Sex differences in the size and shape of the skull were also reduced, with males becoming feminised. In spite of the smaller size of their brains, rigorous psychological tests showed that ‘domesticated’ fox cubs were better than wild foxes, and as good as dog puppies, at responding appropriately to social cues from people, such as investigating an object that the handler points at. A byproduct of reduction of fearfulness and stress by selective breeding for tameness seems to be improvement in such ‘social intelligence’, though the mechanisms remain to be explored.

The time course of postnatal development also changed. Tamer cubs opened their eyes and showed clear responses to loud sounds an average of two days earlier than the controls. The appearance of obvious fear was delayed: posture and facial expression indicating fear were first detected at an average age of nine weeks in selected foxes, compared to six weeks in the controls.

Other behavioural traits, including barking like domestic dogs, were also noted in far greater frequency in the selected population of foxes. The similarities in behaviour and appearance between dogs and domesticated red foxes are even more impressive in view of the conclusion from the phylogenetic analysis (Lindblad-Toh et al., 2005, see Section 3.1) that these species’ last common ancestor lived at least 10 My ago.

Intense selection for tameness has altered brain chemistry and anatomy and the time course of development, though gene expression seems to be almost unchanged. Researchers at Uppsala University in Sweden compared mRNA expression in three regions of the brains of farmed and wild foxes: of nearly 30 000 genes studied, the expression of only about 40 (0.1 per cent) was altered by selection for tameness (Lindberg et al., 2005).

SAQ 21

Can major phenotypic difference accompanied by only minimal genetic change appear naturally?

Answer

Yes. An example is plumage colour in bananaquits that arose from a point mutation that alters a single base pair. There are probably many more.

Factors that mediate fear control the action of certain other genes that determine the maturation of other behavioural and anatomical characters. One interpretation is that behaviours such as whining, barking and tail wagging are ‘released’ when fear is reduced. This explanation is indeed inadequate, and not all the changes observed in the selected populations of foxes could be easily explained on this hypothesis. In the first few pages of On the Origin of Species… Darwin noted that ‘colour and constitutional peculiarities go together’, citing the example that ‘Cats with blue eyes are invariably deaf.’ 19th-century knowledge of development, physiology and genetics could not explain these associations, leaving Darwin to describe them as ‘quite whimsical’; understanding these relationships, now termed epigenetics, is one of the triumphs of 21st-century biology.

Other anatomical changes recorded in the tamer foxes also seen in other domesticated mammals were drooping ears (Figures 3b and d and 12a, b, c and f), shorter, upturned tails, shorter snouts (Figure 12d), and differences in the proportions of the head, especially the relative length of the upper and lower jaws (Figure 3b). The range of dog breeds shows that these anatomical characters can occur in many different combinations. The fox experiment suggests how this variation, which humans have developed and exaggerated under artificial selection, may have originated.

5 Conclusion

Domesticated organisms evolve in artificial environments under artificial selection, and opportunistic or enforced hybridisation often occurs between species that would not normally interbreed. Natural selection cannot be eliminated and continues to operate. At least two different forms of dwarfism are common in domesticated livestock and humans, but only the rarer midget type of dwarfism occurs in wild lineages. Domesticated mammals and birds have distinctive patterns of skin pigmentation that resemble each other and differ from those found in wild animals. Genetic analysis reveals that the principal ancestors of dogs are grey wolves, but hybridisation with jackals and coyotes has also occurred. Modern dogs are genetically very similar in spite of their large phenotypic differences that include behavioural as well as structural and physiological traits. Intense artificial selection and inbreeding have produced extensive anatomical change, especially in the structure of the skull and jaws and in the shape and relative size of the ears and tail and in coat characteristics. Many features and habits of domesticated dogs appeared in red foxes that were selectively bred over many generations for tameness. This Russian experiment suggests that epigenetic processes linked to the reduction of fear alter the structure and properties in the brain and several other features, particularly skin pigmentation.

Question 8

Outline the mechanisms by which the pigment-forming cells in the skin that determine the colour of epidermal structures including feathers and hair are modulated during normal development, by hormones and by minor genetic changes.

Discussion

In wild birds, the same feather follicle can produce feathers of different colours as the bird matures, and under the influence of sex hormones. The plumage difference in bananaquits concerned a point mutation in the gene for the black pigment melanin in the pigment cells that were incorporated into the feathers. Several species of birds have lost all or part of their feather pigmentation under domestication (Figure 10), although this character was not the focus of artificial selection. Similarly, fur pigmentation of most domestic mammals (Figures 1, 7, 8 and 9) is very different from that of their wild ancestors (Figure 6).

Question 9

From your own observations and Figures 3a and b, 8 and 12, which of the characters that appeared in the experimentally tamed foxes are also present in certain modern breeds of dogs?

Discussion

All these features are present in at least one modern breed of dog. The coats of border collie sheepdogs, Dalmatians, some setters and spaniels and many other breeds are piebald. Spaniels, foxhounds, basset hounds, Shih-tzu and many toy dogs have floppy ears. In bulldogs, boxers and pugs, the snout is short with the lower jaw longer than the upper jaw.

References

Lindberg, J., Bjornerfeldt, S., Saetre, P. et al. (2005) Selection for tameness has changed brain gene expression in silver foxes, Current Biology, 15, R915–R916.

Lindblad-Toh, K., Wade, C. M., Mikkelsen, T. S. et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog, Nature, 438, 803–819.

Acknowledgements

The content acknowledged below is Proprietary (see terms and conditions). This content is made available under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 Licence

Grateful acknowledgement is made to the following sources for permission to reproduce material in this course:

Course image: Ralf Κλενγελ in Flickr made available under Creative Commons Attribution-NonCommercial 2.0 Licence.

The content acknowledged below is Proprietary and is used under licence.

Figure 4a AKG-Images;

Figure 4b Prado Museum, Madrid;

Figure 4c AKG-images/Joseph Martin;

Figure 12e Neff, M. W. and Rine, J. (2006) ‘A fetching model organism’, Cell, 124(2);

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Why is the domestication of animals considered artificial selection?

A domestic animal is one whose mate choice is influenced by humans and whose tameness and tolerance of humans is genetically determined. Controlled breeding amounts to prezygotic selection, a critical element to domestication (because captive breeding allows for the strongest, most direct artificial selection).

Is domestication natural or artificial selection?

Introduction: Darwin and Domestication There is little doubt that Darwin considered the process by which animals and plants are domesticated (artificial selection) as a useful analogy for the mechanism by which adaptive evolution occurs in the wild (natural selection).

How does domestication relate to artificial selection?

All of our domesticated species, including crop plants, livestock, and pets, are the products of artificial selection for desirable traits, such as seeds and fruits that do not disperse readily, increased meat and milk production, and docile behavior.

Why is animal and plant breeding by farmers artificial selection?

Artificial selection appeals to humans since it is faster than natural selection and allows humans to mold organisms to their needs. scientist who studies living organisms. practice of selectively pairing breeding pairs of animals together to achieve desired traits in animal offspring.