The Journal of Heredity 2002:93(3)
© 2002 The American Genetic Association 93:205-209
Brief Communication |
Different Levels of Human Intervention in Domestic Rabbits: Effects on Genetic Diversity
From the Centre de Génétique Moléculaire, CNRS, 91198 Gif sur Yvette Cédex, France (Queney, Vachot, Dennebouy, and Monnerot), Station d'Amélioration Génétique des Animaux, INRA, BP27, 31326 Castanet-Tolosan, France (Brun), and Laboratoire de Génétique Cellulaire, INRA, BP27, 31326 Castanet-Tolosan, France (Mulsant).
Address correspondence to Monique Monnerot at the address above or e-mail: monnerot{at}cgm.cnrs-gif.fr.
 |
Abstract |
|---|
 Top Abstract IntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
The effects of human interaction on domestic rabbits were evaluated through the analysis of animals (up to 267) belonging to fancy breeds (22), a commercial breed (1), and selected strains (2). Microsatellite loci and mtDNA polymorphism revealed that the genetic pool of domestic rabbits studied only originated from that available in France. The good conservation of the original diversity was probably ensured through the multiplicity of samplings from wild populations. Selected strains, because of the breeding strategy, keep a fairly high level of diversity compared to other breeds.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
Domestic rabbits as well as wild rabbits belong to the species Oryctolagus cuniculus (European rabbit), which is the only domesticated mammal of western European origin. Domestic rabbit populations comprise local populations, breeds, and strains (de Rochambeau 1989, 1998; Lauvergne 1982). Local populations, used in traditional backyard farming, are not surveyed and are currently disappearing. According to Arnold (1994), the present establishment of rabbit breeds is extremely recent: unlike other domestic animals, it only began at the end of the 18th century in western Europe (Helmer 1992). Breeds established from the previously mentioned local populations are presently defined by a standard based on external appearance (body shape and size, pattern of fur coloration, etc.).
Breeding associations were set up at the end of the 19th century. They organized agricultural meetings and competitions and the number of rabbit pure breeds increased significantly. For example, French breeders' associations now manage more than 60 pure breeds (as described in the "Standard officiel des lapins de race," 2000), but fancy breeders usually rear a small number of animals. However, one of these breeds (Normand) is commercialized by a private owner for its meat quality. Rabbit strains developed for commercial purposes started in the middle of the 20th century. A strain corresponds to a fairly homogeneous collection of individuals subjected to artificial selection for a performance trait (size at birth, fur, etc.). Most of the strains descend (eventually with mixture) from a few breeds (e.g., New-Zealand White, Californian, Fauve de Bourgogne). Fancy rabbits, commercial breeds, and strains thus represent different states of the domestication process.
The wild rabbit population's history is well documented through genetic and archeological studies (Biju-Duval et al. 1991; Branco et al. 2000; Callou 1995; Ennafaa et al. 1987; Ferrand 1995; Hardy et al. 1994, 1995; Loreille et al. 1997; Monnerot et al. 1994, 1996; Mougel 1997; Queney et al. 2001; van der Loo et al. 1991; Vigne 1988). The European rabbit originates from the southern Iberian Peninsula (Andalusia) and dates back to the middle Pleistocene (Lopez-Martinez 1989). From the upper Pleistocene to the Neolithic, the geographic distribution of the species increased to the south of France. Since late Roman times, the dispersal of the species has been closely related to human activities. The species was first dispersed in northern Europe in the Middle Ages and then to the other parts of the world, especially during the 18th and 19th century (North and South America, Australia, New Zealand, and a great number of Pacific islands). Today, the domestic rabbit coexists with its wild form in western Europe (see review in Callou [1995]).
To better understand the relationship between domestic and wild rabbits, we initiated the genetic characterization of fancy breeds several years ago. We further intended to evaluate, on both the breed and strain levels, the effects of the domestication process on genetic diversity. Two complementary markers were chosen: mitochondrial DNA (mtDNA), able to characterize female lineages, and highly variable nuclear markers (microsatellites), which allowed access to the genetic structure of the populations. These analyses should provide information on the effects of human interaction at the different levels of the domestication process.
|
Material and Methods |
|---|
|
TopAbstractIntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
Breeds, Strains, and Populations
Table 1 provides the characteristics of the individuals analyzed and gathered within three categories: (1) fancy breeds: 144 rabbits belonging to 22 breeds were reared for competitions by private breeders [names and geographical locations of breeders can be found in Vachot (1996)]; (2) commercial breeds: 44 rabbits from the Normand breed which was under selection for a label in meat quality (Bergamelli J-M, personal communication); (3) strains: 80 rabbits came from two strains, A1601 and A2066, from INRA (National Agronomical Research Institute, France). Strain A2066 was formed in the 1970s from animals of the Russian giant and Californian breeds and selected for litter size in a closed selection nucleus. Strain A1601 descended by duplication from the "Verde" strain, which was founded in 1981 from two hybrids of four strains and selected for litter size at INIA (Research Institute in Valencia, Spain).
|
Previously analyzed wild populations (Queney et al. 2001) were used to reflect the potential diversity of wild rabbits. Populations from the Iberian Peninsula and France were gathered as two subsets, labeled IP and FR, respectively.
Genetic Characterization
Blood samples were collected from the marginal vein of the ear on visits to fancy breeders or breed exhibitions and by cardiac punctures for synthetic strains. Total DNA was extracted following the method described by Rico et al. (1992) and used directly for amplification. Rapid discrimination between mtDNA types B1 and B3–4 (2% nucleotide divergence in the noncoding domain), the most frequently described in France (Mougel 1997), and other lineages (more divergent) was done using diagnostic sites in two mtDNA fragments (565 bp from the cytochrome b gene, digested with AluI and 586 bp from the noncoding region, digested with RsaI) according to Mougel (1997). The analysis also used six microsatellite loci: sat 2, sat 4, sat 5, sat 7, sat 8, sat 12 (Mougel et al. 1997).
Statistical Analysis
Intrapopulation structure was investigated using the FIS parameter and genetic differentiation between populations within groups (domestic or wild) was estimated from the FST parameter. Estimators of FIS (f) and FST (
) and their 95% confidence intervals (CIs) were calculated using FSTAT (Goudet 1995). A Wilcoxon–Mann–Whitney test was used to test for significant differences in allelic diversity (STATVIEW; Abacus Concepts Inc., Berkeley, CA, 1996). Genetic distances between populations based on allelic frequencies (Nei's standard distance; Nei 1987) were calculated and a neighbor-joining network of populations was constructed with the help of the PHYLIP package (Felsenstein 1993).
|
Results |
|---|
|
TopAbstractIntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
Mitochondrial DNA
The results of mtDNA typing are given in Table 1: only the B1 and B3–4 lineages were detected, the B1 lineage being widespread and the only one in the strains.
Microsatellite Loci
Table 2 summarizes the data on allelic diversity for domestic breeds and strains and the two groups of wild populations considered (FR and IP). The difference in allelic diversity between domestic and wild populations from France (FR) was only significant at P = .05, but not at P = .01, when P < .0001 for the difference between FR and IP. The mean number of alleles per locus for all domestic individuals was 3.6, a probably underestimated value due to the low sampling size of fancy breeds. Domestic animals did not exhibit private alleles; furthermore, all the alleles of domesticated animals but two were present in the wild populations studied from France.
|
Checking for heterozygote proportions could only be performed for the Normand breed and the two strains. Observed heterozygosity was relatively high for each one (Ho = 0.504, 0.477, and 0.486), but lower than that of wild populations (Ho = 0.596 and 0.693 for groups FR and IP, respectively). The two strains showed a deficit for heterozygotes (He = 0.520 and 0.491), but FIS was not significantly different from zero (95% CI not shown), when the Normand breed exhibited a significant excess of heterozygotes (FIS = -0.090). The differentiation between the Normand breed and the two strains was significantly (95% CI not shown) higher (FST = 0.283) than that between the wild populations (FST = 0.144 within FR and 0.062 within IP).
Relationships Between Domestic and Wild Populations
The network presented in Figure 1, based on Nei's genetic distances, includes the two strains from INRA (A1601 and A2066), the Normand breed, all the animals from the fancy breeds pooled together, and the two groups of wild populations considered (FR and IP). All domestic populations (bold and underlined characters in Figure 1) fell within wild populations from France (FR) and further from the other wild populations (IP). The Normand breed, fancy breeds, and one strain fell along the same line.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
For most domesticated species, the biological and geographical origins are on the way to being understood. Multiple origins are frequently evidenced, for example, for cattle (Mannen et al. 1998 and references therein), dogs [for a review see Vilà et al. (1999)], goats (Luikart et al. 2001), horses (Vilà et al. 2001), pigs (Giuffra et al. 2000), and sheep (Heindleder et al. 1998). The situation for domestic rabbits is theoretically simple, since both wild and domestic animals belong to the same species, Oryctolagus cuniculus, originating from Europe, and domestication is recent compared to that of other species. However, knowledge of the diversity of breeds and strains, a prerequisite for a comparison of domestic animals with wild populations in an attempt to accurately define the effect of domestication processes, is needed. A first set of data (Biju-Duval et al. 1991; Ennafaa et al. 1987; Monnerot et al. 1994) has shown the existence, in wild populations, of two maternal lineages, labeled A and B, separated for about 2 million years and restricted, for the first lineage, to the southwestern part of the Iberian Peninsula, while the second was observed in the north of Spain, in the rest of Europe, and in most populations spread all over the world. The very few domestic animals (about 20) analyzed at this time belonged to the B lineage, and more precisely to mtDNA type B1. Present data confirm that domestic breeds and strains are only related to the B maternal lineage. These data reveal that the mtDNA polymorphism is slightly higher than what was first believed, but that the mtDNA type B1 remains predominant (72% of individuals from breeds, 100% of individuals from strains) more so than in wild populations from France (52%, unpublished results). None of the types solely described in wild populations from the Iberian Peninsula (Mougel 1997) were found.
When nuclear markers were considered, domestic individuals were a pretty good image of the diversity described in wild populations from France, but contrasted with the characteristics of wild populations from the Iberian Peninsula (Queney et al. 2001). This is illustrated by the location of domestic populations on the network presented in Figure 1 (as well as from genetic distances; data not shown).
All results thus converge toward the idea that domestic breeds (at least the ones involved in this study) only originated from the genetic pool available in France. These results are congruent with data on the polymorphism of immunoglobulins (van der Loo et al. 1991) and proteins (Ferrand 1995), but on a less representative sampling.
At this point, the effects of initial human intervention may be summarized as follows: (1) a slight decrease in allelic diversity (the mean number of alleles per locus per population ranging from 3.2 to 4 instead of 3.3 to 6.5), (2) a strong differentiation between domestic populations as attested by the high FST value. The latter could simply be a consequence of the low level of allelic diversity, but both probably reflect the existence of some founder effect at the origin of each domestic population, followed by genetic drift. In other words, breeds (at least at their origin) could represent various independent samplings within the original genetic pool.
The next step in human intervention can be appraised through the characteristics of the Normand breed, which has been commercialized for meat quality. The relatively low nuclear diversity (3.2 alleles/locus) probably reflects the low number of individuals at the origin of the sampled population. However, there is no inbreeding (FIS not significantly different from zero) and the negative value of FIS probably has to be correlated with the habits of the breeder, which introduces, from time to time, males from other breeds to precisely escape from inbreeding.
The last step leads to the establishment of strains. Occurring within one breed, strain breeding is expected to cause the loss of alleles through founder effects and genetic drift. However, when the strain formation involves several breeds (as in the synthetic strain), an initial increase in genetic diversity occurs through initial crossbreeding. Our study did not allow the evaluation of the effects of strain breeding, since initial breeds were not individually known. In both strains studied, the total number of alleles was not much different from that in the pool of fancy breeds. Two facts account for the fairly high genetic diversity of these strains: they are both synthetics and the selection strategy (within sire family selection) is aimed at keeping the number of paternal lineages constant. When comparing the strains A2066 and A1601, however, the higher number of alleles in strain A1601 was consistent with its larger genetic base and its shorter selection history.
The differentiation of microsatellite loci between strains A2066 and A1601 (FST = 0.327) was associated with that of quantitative trait loci as revealed by the high level of heterosis in the cross between the two strains (Brun et al. 1999): about 20% of the parental average on litter size, 14% on fertility rate, and 5% on doe body weight.
The present work was not designed to link a given breed to an original wild population: more individuals per breed, with a broader sampling, are required. The RESGEN project, supported by the European Community (Bolet et al. 1999), which involves 12 breeds (some endangered ones, with as many as 30 individuals per breed) will help solve this problem.
In conclusion, one may consider that the relatively recent domestication process in the European rabbit only involved rabbits issued from the genetic pool available in France. In that respect, the loss of genetic diversity through rabbit domestication is real, but not dramatic, when breeds are globally considered. When a breeding strategy is well applied, strains grown for commercial purposes keep a fairly high level of diversity compared to pure breeds.
|
Acknowledgments |
|---|
We thank J. Arnold for his constant interest in our work, J.-C. Mounolou for helpful discussions and W. Brand-Williams for English revision of the manuscript. The authors are also indebted to Messrs. Baty, Beltzung, Bergamelli, Bocquet, Bohrer, Boucher, Cabrespine, Charlemaine, Forny, Ginfray, Hebert, Holzhaus, Koegele, Kurtz, Lehner, Liger, Meioni, A. Meyer, C. Meyer, R. Meyer, Munch, Neyer, Pichard, Roger, Soleilhac, and Thomas for their welcome and allowing (and even for some of them actively participating in) the collection of blood samples from very precious individuals. A.-M. Vachot is currently at the Department of Obstetrics and Gynaecology, Westmead Hospital, Westmead, Sydney, NSW 2145, Australia.
|
Footnotes |
|---|
Corresponding Editor: Robert Wayne
Received October 14, 2000
Accepted March 5, 2002
|
References |
|---|
|
TopAbstractIntroductionMaterial and MethodsResultsDiscussionReferences |
|---|
-
Arnold J, 1994. Historique de l'élevage du lapin. C R Acad Agric Fr 80:3–12.
Biju-Duval C, Ennafaa H, Dennebouy N, Monnerot M, Mignotte F, Soriguer RC, El Gaaïed A, El Hili A, and Mounolou J-C, 1991. Mitochondrial DNA evolution in lagomorphs: origin of systematic heteroplasmy, organisation of diversity in European rabbits. J Mol Evol 33:93–102.
Bolet G, Monnerot M, Arnal C, Arnold J, Bell D, Bergoglio G, Besenfelder U, Bosze S, Boucher S, Brun JM, Chanteloup N, Ducourouble M-C, Durand-Tardif M, Esteves PJ, Ferrand N, Hewitt G, Joly T, Koehl J-F, Laube T, Lechevestrier S, Lopez M, Masoero G, Piccinin R, Queney G, Saleil G, Surridge A, Van der Loo W, Vanhommmerig J, Vicente JS, Virag G, Zimmermann J-M, 1999. A program for the inventory, characterisation, evaluation, conservation and utilisation of European rabbit (Oryctolagus cuniculus) genetic resources. Anim Genet Resourc Inform Bull 25:57–70.
Branco M, Ferrand N, and Monnerot M, 2000. Phylogeography of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula inferred from RFLP analysis of cytochrome b gene. Heredity 85:307–317.[Medline]
Brun J-M, Bolet G, Theau-Clement M, Esparbie et Falieres J, 1999. Constitution d'une souche synthétique de lapins à l'INRA: I. Evolution des caractères de reproduction et du poids des lapines dans les premières générations. 8èmes Journées de la Recherche Cunicole, Paris.
Callou C, 1995. Modifications de l'aire de répartition du Lapin (Oryctolagus cuniculus) en France et en Espagne. Etat de la question. Anthropozoologica 21:95–114.
de Rochambeau H, 1989. La génétique du lapin producteur de viande. INRA Prod Anim 2:287–295.
de Rochambeau H, 1998. La diversité génétique chez les animaux domestiques: description et gestion. C R Acad Agric Fr 84(6):81–95.
Ennafaa H, Monnerot M, El Gaaied A, and Mounolou J-C, 1987. Rabbit mitochondrial DNA: preliminary comparison between some domestic and wild animals. Genet Sel Evol 19:279–288.
Fédération Fran;alcaise de Cuniculture, 2000. Les lapins de race: spécificités zoologiques, standards officiels. Paris: Fédération Fran;alcaise de Cuniculture.
Felsenstein J, 1993. PHYLIP (phylogeny inference package), version 3.5. Distributed by the author. Seattle: University of Washington.
Ferrand N, 1995. Variação genetica de proteinas em populações de coelho (Oryctolagus cuniculus) (PhD dissertation). Porto, Portugal: University of Porto.
Giuffra E, Kijas JM, Amarger V, Carlborg O, Jeon JT, and Andersson L, 2000. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154:1785–1791.
Goudet J, 1995. F-STAT version 1-2: a computer program to calculate F-statistic. J Hered 86:485–486.
Hardy C, Callou C, Vigne J-D, Casane D, Dennebouy N, Mounolou J-C, and Monnerot M, 1995. Rabbit mitochondrial DNA diversity from prehistoric to modern times. J Mol Evol 40:227–237.[CrossRef][ISI][Medline]
Hardy C, Vigne J-D, Casane D, Dennebouy N, Mounolou J-C, and Monnerot M, 1994. Origin of European rabbit (Oryctolagus cuniculus) in a Mediterranean island: zooarchaeology and ancient DNA examination. J Biol Evol 7:217–226.[CrossRef]
Heindleder S, Lewalski H, Wassmuth R, and Janke A, 1998. The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the major ovine haplotype. J Mol Evol 47:441–448.[CrossRef][ISI][Medline]
Helmer D, 1992. La domestication des animaux par les hommes préhistoriques. Paris: Collection Préhistoire.
Lauvergne J-J, 1982. Genetica en poblaciones animales depués de la domesticacion: consequencias para la conservacion de las razas. Proc 2nd World Congr Genet Appl Livestock Prod 6:77–87.
Lopez-Martinez N, 1989. Revision sistematica y biostratigrafica de los lagomorphos (Mammalia) del neogeno y cuaternario de Espana. Memorias del museo paleontologico de la Universidad de Zaragoza. Diputacion general de Aragon (eds).
Loreille O, Mounolu J-C, and Monnerot M, 1997. Histoire des lapins et ADN ancien. Historical expansion of rabbits and ancient DNA. C R Soc Biol 191:537–544.
Luikart G, Gielly L, Excoffier L, Vigne J-D, Bouvet J, and Taberlet P, 2001. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc Natl Acad Sci USA 98:5927–5932.
Mannen H, Tsuji S, Loftus RT, and Bradley DG, 1998. Mitochondrial DNA variation and evolution of Japanese black cattle (Bos taurus). Genetics 150:1169–1175.
Monnerot M, Loreille O, Mougel F, Vachot A-M, Dennebouy N, Callou C, Vigne J-D, and Mounolou J-C, 1996. The European rabbit: wild population evolution and domestication. Proc 6th World Rabbit Congr 2:331–334.
Monnerot M, Vigne J-D, Biju-Duval C, Casane D, Callou C, Hardy C, Mougel F, Soriguer R, Dennebouy N, and Mounolou J-C, 1994. Rabbit and man: genetic and historic approach. Genet Sel Evol 26:S167–S182.
Mougel F, 1997. Variations de trois types de marqueurs génétiques dans l'évolution de l'espèce Oryctolagus cuniculus: aspects moléculaires et relations avec la biologie et la structure des populations (PhD dissertation). Paris: University of Paris-Sud.
Mougel F, Mounolou J-C, and Monnerot M, 1997. Nine polymorphic microsatellite loci in the rabbit Oryctolagus cuniculus. Anim Genet 28:58–71.[CrossRef][ISI][Medline]
Nei M, 1987. Molecular evolutionary genetics. New York: Columbia University Press.
Queney G, Ferrand N, Weiss S, Mougel F, and Monnerot M, 2001. Stationary distributions of microsatellite loci between divergent population groups of the European rabbit (Oryctolagus cuniculus). Mol Biol Evol 18:2169–2178.
Rico C, Kuhnlein U, and Fitzgerald GJ, 1992. Male reproductive tactics in the treespine stickleback: an evaluation by DNA fingerprinting. Mol Ecol 1:79–87.[Medline]
Vachot A-M, 1996. Homologies et singularités interspécifiques (Ranidés) et intraspécifiques (Lapins) (PhD dissertation). Paris: University of Paris-Sud.
van der Loo W, Ferrand N, and Soriguer RC, 1991. Estimation of gene diversity at the b locus of the constant region of the immunoglobulin light chain in natural populations of European rabbit (Oryctolagus cuniculus) in Portugal, Andalusia and on the Azorean islands. Genetics 127:789–799.[Abstract]
Vigne J-D, 1988. Données préliminaires sur l'histoire du peuplement mammalien de l'ilôt de Zembra (Tunisie). Mammalia 52:567–574.
Vilà C, Maldonado JE, and Wayne RK, 1999. Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J Hered 90:71–77.
Vilà C, Leonard AL, Götherström A, Marklunnd S, Sandberg K, Lidén K, Wayne RK, and Ellegren H, 2001. Widespread origins of domestic horse lineages. Science 291:474–477.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||