CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2011 6, No. 060
Review
Visible genetic polymorphisms in domesticated animal species J.J. Lauvergne1, P. Millar1, F. Meutchie`ye2 and D. Bouchel3 Address: 1 COGNOSAG (Committee on Genetic Nomenclature of Sheep and Goats), COGOVICA, 147 C/3 avenue J.B. Cle´ment, 92 140, Clamart, France. 2 Department of Animal Production, Faculty of Agronomy and Agricultural Sciences, University of Dschang, PO Box 222, Cameroon. 3 10, rue Germain Dardan, 92 120, Montrouge, France *Correspondence: jean.lauvergne@sfr.fr 5 September 2011 5 December 2011
Received: Accepted:
doi: 10.1079/PAVSNNR20116060 The electronic version of this article is the deďŹ nitive one. It is located here: http://www.cabi.org/cabreviews g
CAB International 2011 (Online ISSN 1749-8848)
Abstract Visible genetic polymorphisms are very frequent in domesticated animal species. Historically, they were used very early on by breeders to create standardized breeds. If flocks or herds breed at random, polymorphic populations occur (usually variegated, because most of the viable visible alleles that were kept after domestication act on coat colour) in agreement with the laws of population genetics, using the relative value of genotypic fitness coefficients. Such populations became known as primary populations or primary breeds. Numerous descriptions of polymorphic, variegated populations are available, especially for goats and sheep in Africa. Of these, many are probably primary breeds, but records of random mating (panmixia) are scarce. It appears that, after domestication, primary breeds arose, and it was within those that hot spots of standardization appeared later, resulting in standardized breeds. Keywords: polymorphism, visible traits, colour, livestock, domestic animals, primary breeds, panmixia, domestication, selection
Introduction
First Modelling of Genetic Diversity in Domesticated Species: The Standardized Breeds
While sometimes occurring in wild species [1], visible genetic polymorphisms are more frequent in domesticated animal species, as already described in detail [2, 3]. Following the acceptance of Mendelian laws around 1900 [4], it became apparent that such polymorphisms were the result of mutants which remain within the herds, instead of being eliminated by natural selection. In the past, visible polymorphisms were used by breeders to model the genetic landscape of farm animal species, with the first written evidence of this targeted breeding for colour already appearing in some detail in the Bible (Genesis 30 [1,5–19] and 31 [3, 20–30]). This usage has led to divisions within the domesticated species into various types of entities, the classification of which has already been proposed by German authors [26, 31] and later by Mason [7]. The present review demonstrates that ancient breeders instinctively used the principles of population genetics and visible polymorphisms to create two genetic entities: primary populations and standardized breeds.
In the past, although ignorant of Mendel’s laws, breeders created pure lines (=standardized breeds or simply breeds), by mating animals of the same appearance. Dogs and pigeons – two species in which a short generation interval and high fecundity make it easy to create defined types – were the first species in which this widely applied practice was described in some detail: In dogs, pure lines were described and illuminated in Gaston Phoebus’ manuscript of 1389 [11], while a listing of breeds was presented more recently [23, 28]. In pigeons, a list of several breed types was given by Aldrovandi in 1599 [21], and was completed by Darwin who himself was a pigeon fancier and breeder [3]. Most of the breeds are characterized by the colour of their coat or plumage, because most of the visible mutants used in such standardizations control coat or plumage colour, as they have a high degree of viability [32].
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In mammals, the study of these mutants is based on homology between colour loci: Agouti, Brown, Extension, Piebald, Dominant White, etc. [14], and currently, according to the method proposed in Mendelian Inheritance in Man [8], these loci have been listed among loci with visible effects in sheep [33], cattle [9] and poultry [27]. During the nineteenth century, in Western Europe, the science of animal breeding had a tendency to take into consideration only standardized breeds [31]. This was a result of a proliferation of breeders’ organizations, which, for commercial and practical reasons, favoured the ‘purity of breeds’, as illustrated by the development of pedigree registration in cattle breeding in western Europe since 1800 [34]. Therefore, from the end of the nineteenth century onwards, it can be said that for the most important farm species in a number of countries including Great Britain, France, Italy, Germany, Switzerland, Austro-Hungarian Empire, USA, etc., livestock species practically comprised solely standardized breeds. Basic Interpretation of Polymorphism in Terms of Population Genetics Visible genetic polymorphisms already existed before the creation of standardized breeds in which a gene with a visible effect is kept at the frequency of 1. In terms of population genetics, a domesticated population may be considered which carries only the wild allele a+ at the locus A. When a mutant named a1 arises, genotypes a1a1, a+a1 and a+a+ have coefficients of fitness s1, s2 and s3, respectively, and, provided that panmixia (random mating) is allowed, gene frequency p of a1 (with p=17q) will be expressed, according to L’he´ritier [5], by an equation obtained by integrating the differential of dp to dt (dp=dt=pq(s1 7s2 )p+(s37 7s2 )q=s1 p2 +2s2 pq+s3 q2 ): The value of p reaches an equilibrium between 0 and 1 when t leads to infinite provided that s1, s2 and s3 have appropriate values. In that case, all three genotypes are present in the population. Moreover, because, as seen above, many mutants belong to loci controlling coat colour, the population will be polymorphic for colour, i.e. variegated. Given that among the domestic species such variegated populations exist, the above explanation is applicable. A survey of the literature shows that even if the tendency was to breed standardized breeds in Western Europe, variegated breeds had already been genetically described, for example in Highland cattle [17], Norwegian cattle [22], Icelandic sheep [19] and in London’s cats [14]. They were also described elsewhere, for example in cattle and sheep of the former French West Africa [30]. Therefore, it follows that visible polymorphisms could be identified within already-established breeds of livestock or other domestic species. However, this kind of
polymorphism is often the result of the presence of recessive alleles at low frequencies. As an example, black sheep may segregate into full white. Birth and Development of the Notion of Primary Populations This type of genetic entity or category of multisegregating breeds was not exactly that considered by German authors [26, 31], but Mason [7] in his classification of ‘Types of breeds and varieties of farm animals’ belonging to seven farm species (ass, buffalo, cattle, goat, horse, pig and sheep) proposed the term ‘varieties’ to name this type of polymorphic breed. Mason’s proposed classification was as follows: (1) (2) (3) (4)
Breeds important numerically or historically. Minor, new or disappearing breeds. Extinct breeds. Varieties – whether geographical or genetic nonuniform populations or geographical terms, e.g. ‘cattle of such-and-such a place or even breeds of suchand-such a place’. (5) Cross-breds or types that are not true-breeding. (6) Wild species. The proposed term ‘traditional populations’ [35] instead of ‘varieties’ was later changed into ‘primary populations’ [36]. We also say here ‘primary breeds’. Other Studies on Polymorphic Breeds Further descriptions of polymorphic (mainly variegated) breeds were published for Icelandic sheep [20], other sheep from the North Atlantic islands [13] and Corsica [37], goats in Provence [38] and pigs in Papua New Guinea [39]. An extensive study devoted to polymorphic sheep and goat populations (then called traditional populations) was then carried out during an INRA Colloquium, at Manosque in 1986, where nine papers were presented on goats and seven articles on sheep [40]. Surveys of goat and sheep in Africa showed that many so-called breeds of sheep and goats were variegated [18]. Studies Involving Random Mating As seen above, laws of population genetics apply to the definition of primary breeds only in the context of random mating. Although the outcome of random mating was studied within the population of London’s cats [14], many studies of polymorphic breeds may not always have considered the existence of random mating. Other situations presented some evidence where both sexes were run together, in which controlled mating was not possible, as
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J.J. Lauvergne, P. Millar, F. Meutchie`ye and D. Bouchel
described in a large portion of the world’s goat population [16]. In such cases, random mating occurred as the norm. Other studies of random mating in traditional goat and sheep breeding originated in Africa [6,10,25,41]. Nevertheless, measured observations were usually absent. Genetic Dynamics after Domestication Earlier authors working on dogs declared the existence of a kind of ancestral ‘superbreed’, which gave birth to the modern, well-standardized breeds [28]. However, the description of ‘superbreeds’ varies from author to author. Similar descriptions of pigs, sheep and rabbits also took into consideration some ancient mythical populations [31]. Other authors [24, 29, 42] assumed that, after domestication, stocks comprised primary breeds, with hot spots of standardization occurring only later on. Consequences for the Inventory of Genetic Resources As already pointed out by Mason [7] – who, however, omitted to list them separately – polymorphic populations, which probably are primary, are still very numerous in countries in which the use of standardized breeds has not yet been generalized. Although it is already possible to use the visible colour polymorphism in distinguishing primary breeds, in order to verify that these breeds are truly run under random mating, further investigations are necessary. On the other hand, even if primary breeds are, in principle, infinite populations, as a result of local conditions, such as geographical isolation, armed conflicts, famines, tribal migrations, diseases, etc., they can be split into sub-breeds, such as the varieties described by Mason [7]. Characterization of Genetic Polymorphisms at the Molecular Level Studies of genetic polymorphisms at molecular level deal with traits that are outwith the visible sphere, such as biochemical polymorphisms, mapped genes and loci, nucleotide and protein sequences, linkage or meiotic maps, and other means such as statistical analysis of segregation patterns, have been published in hundreds if not thousands and were comprehensively reviewed by COGNOSAG [9,33]. This review aims at defining those genotypes that carry visible mutants mostly controlling coat colour, as identified by Searle [15], which can be easily identified by breeders and used in breeding strategies other than random mating.
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occurred before and separately from the standardized breeds in domesticated livestock and domestic species. These primary breeds can be often identified at first sight by variegation of the coat or plumage colour, but further studies are necessary in order to confirm if random mating (panmixia) is operating within these breeds, and if any split into sub-breeds has occurred for any reason.
References 1. Lode´ T. Cours de ge´ne´tique des populations [A Course on Population Genetics]. Ellipses, Paris; 1998. 126 p. 2. Geoffroy Saint Hilaire I. Acclimatation et domestication des animaux utiles [Taming and Domestication of Useful Animals]. 4e`me e´dition. La Maison Rustique, Paris, France; 1861. 534 p. 3. Darwin C. The Variation of Animals and Plants under Domestication. 2 vols. John Murray, London, UK; 1868. VIII+411 and VIII+486 p. 4. Dunn LC. A Short History of Genetics. McGraw Hill Book Company, St. Louis, MO, USA; 1965. 261 p. 5. L’He´ritier P. Traite´ de Ge´ne´tique. Tome II. La ge´ne´tique des populations. [Treatise of Genetics. II. Population Genetics]. PUF, Paris; 1954. 415 p. 6. Manjeli Y, Teguia A, Njwe RM, Tchoumboue J, Ayong EE. Enqueˆte sur l’e´levage caprin dans les hauts plateaux de l’Ouest Cameroun. In Proceedings of the Third SRNET Biennal Conference in Kampala, Uganda, 5–9 December; 1994. p. 99–103. 7. Mason IL. A World Dictionary of Breeds, Types and Varieties of Livestock. Technical Communication No. 8 of the Commonwealth Bureau of Animal Breeding and Genetics, Edinburgh, Commonwealth Agricultural Bureaux, Farnham House, Farnham Royal, Slough, Bucks., UK; 1951. 270 p. 8. McKusick V. Foreword. In V. McKusick. Mendelian Inheritance in Man. The John Hopkins Press, Baltimore, MD; 1966. vii–xi. 9. Millar P, Lauvergne JJ, Dolling CHS. Mendelian inheritance in Cattle 2000. Wageningen Press, Wageningen, The Netherlands; 2000. 570 p. 10. Moulin CH, Faugere O, Faugere B. L’e´levage traditionnel des petits ruminants au Se´ne´gal. III. Pratiques de conduite et d’exploitation des animaux chez les e´leveurs de la communaute´ rurale de Kaymor (Sine-Saloum, Se´ne´gal). [Traditional small ruminants breeding in Senegal. III. Management practices in the rural community of Kaymor (Sine-Saloum, Senegal)]. Revue d’e´levage et de Me´decine Ve´te´rinaire des Pays Tropicaux 1994;47:223–234. 11. Phoebus G. Le Livre de la Chasse [The Book of Hunting]. Manuscript, Ortez; 1389. 36 p. 12. Pinon L. Livres de zoologie de la Renaissance: une anthologie (1450–1700). [Renaissance Books of Zoology, An Anthology]. Klincksieck, Paris, France; 1995. 152 p.
Conclusion
13. Ryder ML, Land RB. Coat colour inheritance in Soay, Orkney and Shetland sheep. Journal of Zoology, London 1974;173:477–85.
Genetic analysis of visible polymorphisms made it possible to appraise primary breeds as a genetic entity which
14. Searle AG. Gene frequency in London’s cats. Journal of Genetics 1949;49:214–20.
http://www.cabi.org/cabreviews
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Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources
15. Searle AG. Comparative Genetics of Coat Colour in Mammals. Logos Press, London and Academic Press, New York; 1968. 308 p. 16. Shelton M. Reproduction and breeding of goats. Journal of Dairy Science 1978;61:994–1010.
31. Kru¨ger L. 12. Kapitel. Geschichtliche Entwicklung der Rassen in der europa¨ischen Tierzucht [History of the expansion of farm animal breeds in Europe]. In: Hammond J, Johansson I, Haring F, editors. Handbuch der Tierzu¨chtung. Dritte Band, Rassenkunde, Erster Halbband; 1961. p. 25–56.
17. Wilson J. The colours of highland cattle. Science Proceedings of the Royal Dublin Society 1909;12:66–76.
32. Lauvergne JJ. A brief history of mammalian coat colour genetics. CAB Reviews 2010;5(No. 011):5.
18. Wilson RT. Small Ruminant production and the small ruminant genetic resources in Tropical Africa. FAO Animal Production and Health Paper No. 88; 1991. 177 p.
33. Lauvergne JJ, Dolling CHS, Renieri C. Mendelian Inheritance in Sheep. COGOVICA COGNOSAG/University of Camerino, Clamart, France and Camerino, Italy; 1996. 210 p.
19. Zophoniasson P. Nogle Bemaerkninger om enkelte Arvelighedsforhold hos de islandske Faar [Some observations on fleece color of Icelandic sheep]. Nord Jordbruksforsk 1934;16:217–23.
34. Engeler W. Studies on the Development and Situation of Pedigree Registering in the Cattle Breeding. International Institute of Agriculture, Rome; 1931. 92 p.
20. Adalsteinsson S. Colour inheritance in Icelandic sheep and relation between colour, fertility and fertilization. Journal of Agricultural Research in Iceland 1970;2:3–135. 21. Aldrovandi U. 1599. Ornithologia. Bologna. Quoted by PINON (1995). 22. Berge S. Inheritance of dun, brown and brindle colour in cattle. Heredity 1949;5:195–204. 23. Buffon GLL, Daubenton LC. Le chien [The dog]. In: Comte de Buffon, editor. Histoire naturelle ge´ne´rale et particulie`re. 2. Histoire des animaux. Imprimerie Royale, Paris; 1750. 24. Can˜on X, Dunner S, Alia MJ. Le sce´nario du peuplement caprin espagnol ancien. In: Lauvergne JJ, editor. Populations traditionnelles et premie`res races standardise´es d’Ovicaprinæ dans le Bassin me´diterrane´en.[Traditional Populations and First Standardized Breeds of Sheep and Goats in the Mediterrranean]. Colloque INRA No. 47, INRA, Paris; 1988. p. 245–52. 25. Clement V, Poivey JP, Faugere O, Tillard E, Lancelot R, Gueye A et al. Etude de la variabilite´ des caracte`res de reproduction chez les petits ruminants en milieu d’e´levage traditionnel au Se´ne´gal. Revue d’e´levage et de Me´decine Ve´te´rinaire des Pays Tropicaux 1997;50:235–49. 26. Comberg G. Die deutsche Tierzucht im 19. Und 20. Jahrhundert. [Animal Breeding in Germany During 19th and 20th Centuries]. Eugen Ulmer, Stuttgart; 1984. 804 p. 27. Coquerelle G. Les poules. Diversite´ ge´ne´tique visible. [Poultry: Visible Genetic Diversity]. INRA, Paris; 2000. 181 p. 28. Courreau JF. Parente´ et filiation des races de chiens d’apre`s les donne´es de la litte´rature, quelques exemples [Parentage and lines of dog breeds from the data in litte´rature, some examples]. Ethnozootechnie 2006;78:71–5. 29. Denis B. A propos de la notion de race: point de vue d’un zootechnicien. [About the notion of breed: point of view of a zootechnician]. Ethnozootechnie 1982;29:61–7. 30. Doutressoulle G. L’e´levage en Afrique Occidentale Franc¸ aise.[Animal Breeding in French Western Africa]. Larose, Paris, France; 1947. 288 p.
35. Lauvergne JJ. Genetics in animal populations after domestication: the consequence for breed conservation. In: Second World Congress of Genetics Applied to Animal Production, Madrid; 1982. vol. 6, p. 77–87. 36. Lauvergne JJ. Breed development and breed differentiation. In: Simon D, Buchenauer D, editors. Data Collection, Conservation and Use of Farm Animal Genetic Resources, Proceedings of the CEC Workshop and Training Course, Hannover, 7–9 December 1992; 1993. p. 53–64. 37. Lauvergne JJ, Adalsteinsson S. Ge`nes pour la couleur de la toison de la brebis Corse. [Genes for fleece colour of Corsican ewe]. Annales de Genetique et de Selection Animale 1976;8:153–72. 38. Lauvergne JJ, Renieri C, Audiot, Annick. Estimating erosion of phenotypic variation in a French traditional Goat population. Journal of Heredity 1987;78:307–314. 39. Lauvergne JJ, Malynicz GL, Quartermain AR. Coat colour variants of village pigs in Papua New Guinea. Annales de Genetique et de Selection Animale 1982;14:49–62. 40. Lauvergne JJ (editeur). Populations traditionnelles et premie`res races standardise´es d’Ovicaprinæ dans le Bassin me´diterrane´en.[Traditional populations and first standardized breeds of Sheep and Goats in the Mediterrranean]. Colloque INRA No. 47, INRA, Paris; 1988. 298 p. 41. Faugere O, Dockes AC, Perrot C, Faugere B. L’e´levage traditionnel des petits ruminants au Se´ne´gal. I. Pratiques de conduite et d’exploitation des animaux chez les e´leveurs de la re´gion de Kolda. [Traditional small ruminants breeding in Senegal. I. Management practices in the Kolda region]. Revue d’e´levage et de Me´decine Ve´te´rinaire des Pays Tropicaux 1990;43:249–59. 42. Lauvergne JJ, Renieri C, Pieramati C. Le sce´nario du peuplement caprin me´diterrane´en ancien. In Lauvergne JJ, editor. Populations traditionnelles et premie`res races standardise´es d’Ovicaprinæ dans le Bassin me´diterrane´en. [Traditional Populations and First Standardized Breeds of Sheep and Goats in the Mediterrranean]. Colloque INRA No. 47, INRA, Paris; 1988. p. 253–66.
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