The genetic changes underlying the initial steps of animal domestication are still poorly understood. We generated a high-quality reference genome for rabbit and compared it to resequencing data from populations of wild and domestic rabbits. We identified over 100 selective sweeps specific to domestic rabbits, but only a relatively small number of fixed (or nearly fixed) SNPs for derived alleles. SNPs with marked allele frequency differences between wild and domestic rabbits were enriched for conserved non-coding sites. Enrichment analyses suggest that genes affecting brain and neuronal development have often been targeted during domestication. We propose that due to a truly complex genetic background, tame behavior in rabbits and other domestic animals evolved by shifts in allele frequencies at many loci, rather than by critical changes at only a few ‘domestication loci’.
Understanding the genetic structure of domestic species provides a window into the process of domestication and motivates the design of studies aimed at making links between genotype and phenotype. Rabbits exhibit exceptional phenotypic diversity, are of great commercial value, and serve as important animal models in biomedical research. Here, we provide the first comprehensive survey of nucleotide polymorphism and linkage disequilibrium (LD) within and among rabbit breeds. We resequenced 16 genomic regions in population samples of both wild and domestic rabbits and additional 35 fragments in 150 rabbits representing six commonly used breeds. Patterns of genetic variation suggest a single origin of domestication in wild populations from France, supporting historical records that place rabbit domestication in French monasteries. Levels of nucleotide diversity both within and among breeds were ~0.2%, but only 60% of the diversity present in wild populations from France was captured by domestic rabbits. Despite the recent origin of most breeds, levels of population differentiation were high (F(ST) = 17.9%), but the majority of polymorphisms were shared and thus transferable among breeds. Coalescent simulations suggest that domestication began with a small founding population of less than 1,200 individuals. Taking into account the complex demographic history of domestication with two successive bottlenecks, two loci showed deviations that were consistent with artificial selection, including GPC4, which is known to be associated with growth rates in humans. Levels of diversity were not significantly different between autosomal and X-linked loci, providing no evidence for differential contributions of males and females to the domesticated gene pool. The structure of LD differed substantially within and among breeds. Within breeds, LD extends over large genomic distances. Markers separated by 400 kb typically showed r(2) higher than 0.2, and some LD extended up to 3,200 kb. Much less LD was found among breeds. This advantageous LD structure holds great promise for reducing the interval of association in future mapping studies.
Over thousands of years humans changed the genetic and phenotypic composition of several organisms and in the process transformed wild species into domesticated forms. From this close association, domestic animals emerged as important models in biomedical and fundamental research, in addition to their intrinsic economical and cultural value. The domestic rabbit is no exception but few studies have investigated the impact of domestication on its genetic variability. In order to study patterns of genetic structure in domestic rabbits and to quantify the genetic diversity lost with the domestication process, we genotyped 45 microsatellites for 471 individuals belonging to 16 breeds and 13 wild localities. We found that both the initial domestication and the subsequent process of breed formation, when averaged across breeds, culminated in losses of ~20% of genetic diversity present in the ancestral wild population and domestic rabbits as a whole, respectively. Despite the short time elapsed since breed diversification we uncovered a well-defined structure in domestic rabbits where the FST between breeds was 22%. However, we failed to detect deeper levels of structure, probably consequence of a recent and single geographic origin of domestication together with a non-bifurcating process of breed formation, which were often derived from crosses between two or more breeds. Finally, we found evidence for intrabreed stratification that is associated with demographic and selective causes such as formation of strains, colour morphs within the same breed, or country/breeder of origin. These additional layers of population structure within breeds should be taken into account in future mapping studies.
A divergent selection experiment on within-litter homogeneity of birth weight in rabbits was carried out at the INRA experimental farm at Auzeville. The two lines were created by selecting breeding does and bucks from the female strain AGP22 bred at the Grimaud Frères Sélection Company. This involved a new model incorporating a genotypic value for the mean of individual birth weight and a genotypic value for the environmental variance. This new "trait" was modelled in the usual infinitesimal framework, giving estimated breeding values for environmental variability. There was a favourable selection response with a significant difference in within-litter standard deviation of birth weight between the lines selected for increasing (HOM) or decreasing (HET) homogeneity. At the end of the third generation, 31 females from the HOM line and 33 from the HET line were sacrificed to collect the uterine horns and measure their initial length (L1) and their length after elongation with a weight of 50 g (L2) and then 70 g (L3). The length in the homogeneous line was significantly greater, whatever the weight (L1: + 1.3 cm, P = 0.02; L2: + 2.8 cm P b 0.001; L3: + 4.2 cm, P b 0.001). The absolute and the relative elongations were significantly higher in the HOM line. There was no significant effect of the line on the number of ova shed, the weight of the ovary, or the weight of the uterine horns. It is concluded that the divergence between lines for the within-litter homogeneity of birth weight is at least partly due to the characteristics of the genital tract, i.e. the length and capacity for elongation of the uterine horn.
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