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Comparative Study
.2006 Jun;173(2):919-33.
doi: 10.1534/genetics.105.054106. Epub 2006 Apr 2.

Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus)

Affiliations
Comparative Study

Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus)

Armando Geraldes et al. Genetics.2006 Jun.

Abstract

Hybrid zones provide an excellent opportunity for studying the consequences of genetic changes between closely related taxa. Here we investigate patterns of genetic variability and gene flow at four X-linked loci within and between the two subspecies of European rabbit (Oryctolagus cuniculus cuniculus and O. c. algirus). Two of these genes are located near the centromere and two are located near the telomeres. We observed a deep split in the genealogy of each gene with the root located along the deepest branch in each case, consistent with the evolution of these subspecies in allopatry. The two centromeric loci showed low levels of variability, high levels of linkage disequilibrium, and little introgression between subspecies. In contrast, the two telomeric loci showed high levels of variability, low levels of linkage disequilibrium, and considerable introgression between subspecies. These data are consistent with suppression of recombination near the centromere of the rabbit X chromosome. These observations support a view of speciation where genomic incompatibilities at different loci in the genome create localized differences in levels of gene flow between nascent species.

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Figures

Figure 1.
Figure 1.
Populations of European rabbit sampled and their geographic locations. Dark shading indicates SW populations, light shading indicates CZ populations, and no shading indicates NE populations. The name and number of samples from each population and population names are specified in Table 1.
Figure 2.
Figure 2.
Chromosomal location of the four X-linked loci used in this study. Modified from Chantry-Darmonet al. (2003) and Hayeset al. (2002).
Figure 3.
Figure 3.
Polymorphisms for the four X-linked loci. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The nucleotide found in theL. granatensis sample was used to infer the ancestral state for each position. Numbers in the columns indicate the position of the polymorphism in the alignment. Each row represents one individual. A dot represents the ancestral state, and letters (A, C, G, and T) represent the derived nucleotide. The name of the haplotype defined by each sequence is shown in parentheses. Positions polymorphic for bases other than the one found inL. granatensis are indicated with an asterisk (*) and positions segregating for three different bases inO. cuniculus are indicated by “#” in d. Whenever a polymorphic site inO. cuniculus corresponded to a deletion inL. granatensis, we treated the most frequent base in our sample ofO. cuniculus as the ancestral state.
Figure 3.
Figure 3.
Polymorphisms for the four X-linked loci. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The nucleotide found in theL. granatensis sample was used to infer the ancestral state for each position. Numbers in the columns indicate the position of the polymorphism in the alignment. Each row represents one individual. A dot represents the ancestral state, and letters (A, C, G, and T) represent the derived nucleotide. The name of the haplotype defined by each sequence is shown in parentheses. Positions polymorphic for bases other than the one found inL. granatensis are indicated with an asterisk (*) and positions segregating for three different bases inO. cuniculus are indicated by “#” in d. Whenever a polymorphic site inO. cuniculus corresponded to a deletion inL. granatensis, we treated the most frequent base in our sample ofO. cuniculus as the ancestral state.
Figure 3.
Figure 3.
Polymorphisms for the four X-linked loci. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The nucleotide found in theL. granatensis sample was used to infer the ancestral state for each position. Numbers in the columns indicate the position of the polymorphism in the alignment. Each row represents one individual. A dot represents the ancestral state, and letters (A, C, G, and T) represent the derived nucleotide. The name of the haplotype defined by each sequence is shown in parentheses. Positions polymorphic for bases other than the one found inL. granatensis are indicated with an asterisk (*) and positions segregating for three different bases inO. cuniculus are indicated by “#” in d. Whenever a polymorphic site inO. cuniculus corresponded to a deletion inL. granatensis, we treated the most frequent base in our sample ofO. cuniculus as the ancestral state.
Figure 3.
Figure 3.
Polymorphisms for the four X-linked loci. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The nucleotide found in theL. granatensis sample was used to infer the ancestral state for each position. Numbers in the columns indicate the position of the polymorphism in the alignment. Each row represents one individual. A dot represents the ancestral state, and letters (A, C, G, and T) represent the derived nucleotide. The name of the haplotype defined by each sequence is shown in parentheses. Positions polymorphic for bases other than the one found inL. granatensis are indicated with an asterisk (*) and positions segregating for three different bases inO. cuniculus are indicated by “#” in d. Whenever a polymorphic site inO. cuniculus corresponded to a deletion inL. granatensis, we treated the most frequent base in our sample ofO. cuniculus as the ancestral state.
Figure 4.
Figure 4.
Median-joining haplotype networks representing the phylogenetic relationships among all the alleles found in the European rabbit. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The size of the circles is proportional to the frequency of each haplotype. The population group of the individuals represented in each haplotype is denoted by solid (SW), shaded (CZ), and open (NE) treatment. The point in the network from which the outgroup sequence ofL. granatensis stems is indicated by an arrow. Haplotype IDs correspond to Figure 3.
Figure 4.
Figure 4.
Median-joining haplotype networks representing the phylogenetic relationships among all the alleles found in the European rabbit. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The size of the circles is proportional to the frequency of each haplotype. The population group of the individuals represented in each haplotype is denoted by solid (SW), shaded (CZ), and open (NE) treatment. The point in the network from which the outgroup sequence ofL. granatensis stems is indicated by an arrow. Haplotype IDs correspond to Figure 3.
Figure 4.
Figure 4.
Median-joining haplotype networks representing the phylogenetic relationships among all the alleles found in the European rabbit. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The size of the circles is proportional to the frequency of each haplotype. The population group of the individuals represented in each haplotype is denoted by solid (SW), shaded (CZ), and open (NE) treatment. The point in the network from which the outgroup sequence ofL. granatensis stems is indicated by an arrow. Haplotype IDs correspond to Figure 3.
Figure 4.
Figure 4.
Median-joining haplotype networks representing the phylogenetic relationships among all the alleles found in the European rabbit. (a)Phka2, (b)Smcx, (c)Msn, and (d)Hprt1. The size of the circles is proportional to the frequency of each haplotype. The population group of the individuals represented in each haplotype is denoted by solid (SW), shaded (CZ), and open (NE) treatment. The point in the network from which the outgroup sequence ofL. granatensis stems is indicated by an arrow. Haplotype IDs correspond to Figure 3.
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