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Y-chromosome phylogeny in the evolutionary net of chamois (genus Rupicapra).

Pérez T, Hammer SE, Albornoz J, Domínguez A - BMC Evol. Biol. (2011)

Bottom Line: The SRY promoter sequences of two samples of Barbary sheep (Ammotragus lervia) were also determined and compared with the sequences of Bovidae available in the GenBank.The diversity of Y-chromosomes in chamois is very low.The differences in patterns of variation among Y-chromosome, mtDNA and biparental microsatellites reflect the evolutionary characteristics of the different markers as well as the effects of sex-biased dispersal and species phylogeography.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biología Funcional, Genética, Universidad de Oviedo, Julián Clavería 6, 33006 Oviedo, Spain.

ABSTRACT

Background: The chamois, distributed over most of the medium to high altitude mountain ranges of southern Eurasia, provides an excellent model for exploring the effects of historical and evolutionary events on diversification. Populations have been grouped into two species, Rupicapra pyrenaica from southwestern Europe and R. rupicapra from eastern Europe. The study of matrilineal mitochondrial DNA (mtDNA) and biparentally inherited microsatellites showed that the two species are paraphyletic and indicated alternate events of population contraction and dispersal-hybridization in the diversification of chamois. Here we investigate the pattern of variation of the Y-chromosome to obtain information on the patrilineal phylogenetic position of the genus Rupicapra and on the male-specific dispersal of chamois across Europe.

Results: We analyzed the Y-chromosome of 87 males covering the distribution range of the Rupicapra genus. We sequenced a fragment of the SRY gene promoter and characterized the male specific microsatellites UMN2303 and SRYM18. The SRY promoter sequences of two samples of Barbary sheep (Ammotragus lervia) were also determined and compared with the sequences of Bovidae available in the GenBank. Phylogenetic analysis of the alignment showed the clustering of Rupicapra with Capra and the Ammotragus sequence obtained in this study, different from the previously reported sequence of Ammotragus which groups with Ovis. Within Rupicapra, the combined data define 10 Y-chromosome haplotypes forming two haplogroups, which concur with taxonomic classification, instead of the three clades formed for mtDNA and nuclear microsatellites. The variation shows a west-to-east geographical cline of ancestral to derived alleles.

Conclusions: The phylogeny of the SRY-promoter shows an association between Rupicapra and Capra. The position of Ammotragus needs a reinvestigation. The study of ancestral and derived characters in the Y-chromosome suggests that, contrary to the presumed Asian origin, the paternal lineage of chamois originated in the Mediterranean, most probably in the Iberian Peninsula, and dispersed eastwards through serial funding events during the glacial-interglacial cycles of the Quaternary. The diversity of Y-chromosomes in chamois is very low. The differences in patterns of variation among Y-chromosome, mtDNA and biparental microsatellites reflect the evolutionary characteristics of the different markers as well as the effects of sex-biased dispersal and species phylogeography.

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Phylogenetic tree constructed with SRY-promoter sequences. Neighbor-Joining tree based on the number of substitutions per nucleotide under the model of Tamura 3-parameter. Numbers at the nodes are bootstrap support using NJ, ML, MP and Bayesian posterior probabilities. Ammotragus lervia 1 refers to the sequence of Meadows and Kijas [35] and Ammotragus lervia 2 refers to the sequence obtained in this work.
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Figure 2: Phylogenetic tree constructed with SRY-promoter sequences. Neighbor-Joining tree based on the number of substitutions per nucleotide under the model of Tamura 3-parameter. Numbers at the nodes are bootstrap support using NJ, ML, MP and Bayesian posterior probabilities. Ammotragus lervia 1 refers to the sequence of Meadows and Kijas [35] and Ammotragus lervia 2 refers to the sequence obtained in this work.

Mentions: To investigate the evolutionary history of the Y-chromosome of Rupicapra, the two haplotypes were aligned with the sequences of other Bovidae available in the GenBank, Ammotragus lervia, Capra hircus, Ovis aries and Bos taurus (see Table 1). In addition, two individual Ammotragus lervia have been sequenced in our laboratory and both had identical sequence with a deletion of 44 nucleotides with respect to the rest of Bovidae. The aligned dataset contains 531 nucleotides (481 nt, indels excluded) with 78 variable sites of which 34 are fixed and 44 are variable among Caprinae. The phylogenetic relationships were studied using Neighbor-Joining, Maximum Likelihood, Maximum Parsimony, or Bayesian approaches under different models of nucleotide substitution, either the simple model of Jukes-Cantor or the substitution model that describes better the substitution pattern of the dataset, a Tamura 3-parameter model [30] with non-uniformity of evolutionary rate among sites (T92+G). The three parameters were nucleotide frequencies 0.3392 for A and T, 0.1608 for C and G, Ts/Tv ratio: 1.6281 and rate heterogeneity: 0.4762. For the construction of the Bayesian tree, the model of nucleotide substitution was HKI+G (also appropriate to describe the observed substitution pattern since it has the second lowest BIC score obtained with MEGA) and the parameters were obtained by the program BEAST itself. There were 36 parsimony-informative sites. Model-free Parsimony Analysis performed with MEGA led to three equally parsimonious trees with a total length of 87 steps. The different methods of tree construction all led to topologies with two main well supported nodes (Figure 2), one grouping Ovis with the published sequences of Ammotragus and the other grouping Rupicapra, Capra and the sequence of Ammotragus obtained in this work. The relationships within this second group varied, depending on the method used for tree construction, and they were poorly supported. All the 10 different Bovidae sequences present, like pyrenaica, A in site 267 in our alignment, suggesting that this is the ancestral haplotype.


Y-chromosome phylogeny in the evolutionary net of chamois (genus Rupicapra).

Pérez T, Hammer SE, Albornoz J, Domínguez A - BMC Evol. Biol. (2011)

Phylogenetic tree constructed with SRY-promoter sequences. Neighbor-Joining tree based on the number of substitutions per nucleotide under the model of Tamura 3-parameter. Numbers at the nodes are bootstrap support using NJ, ML, MP and Bayesian posterior probabilities. Ammotragus lervia 1 refers to the sequence of Meadows and Kijas [35] and Ammotragus lervia 2 refers to the sequence obtained in this work.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198967&req=5

Figure 2: Phylogenetic tree constructed with SRY-promoter sequences. Neighbor-Joining tree based on the number of substitutions per nucleotide under the model of Tamura 3-parameter. Numbers at the nodes are bootstrap support using NJ, ML, MP and Bayesian posterior probabilities. Ammotragus lervia 1 refers to the sequence of Meadows and Kijas [35] and Ammotragus lervia 2 refers to the sequence obtained in this work.
Mentions: To investigate the evolutionary history of the Y-chromosome of Rupicapra, the two haplotypes were aligned with the sequences of other Bovidae available in the GenBank, Ammotragus lervia, Capra hircus, Ovis aries and Bos taurus (see Table 1). In addition, two individual Ammotragus lervia have been sequenced in our laboratory and both had identical sequence with a deletion of 44 nucleotides with respect to the rest of Bovidae. The aligned dataset contains 531 nucleotides (481 nt, indels excluded) with 78 variable sites of which 34 are fixed and 44 are variable among Caprinae. The phylogenetic relationships were studied using Neighbor-Joining, Maximum Likelihood, Maximum Parsimony, or Bayesian approaches under different models of nucleotide substitution, either the simple model of Jukes-Cantor or the substitution model that describes better the substitution pattern of the dataset, a Tamura 3-parameter model [30] with non-uniformity of evolutionary rate among sites (T92+G). The three parameters were nucleotide frequencies 0.3392 for A and T, 0.1608 for C and G, Ts/Tv ratio: 1.6281 and rate heterogeneity: 0.4762. For the construction of the Bayesian tree, the model of nucleotide substitution was HKI+G (also appropriate to describe the observed substitution pattern since it has the second lowest BIC score obtained with MEGA) and the parameters were obtained by the program BEAST itself. There were 36 parsimony-informative sites. Model-free Parsimony Analysis performed with MEGA led to three equally parsimonious trees with a total length of 87 steps. The different methods of tree construction all led to topologies with two main well supported nodes (Figure 2), one grouping Ovis with the published sequences of Ammotragus and the other grouping Rupicapra, Capra and the sequence of Ammotragus obtained in this work. The relationships within this second group varied, depending on the method used for tree construction, and they were poorly supported. All the 10 different Bovidae sequences present, like pyrenaica, A in site 267 in our alignment, suggesting that this is the ancestral haplotype.

Bottom Line: The SRY promoter sequences of two samples of Barbary sheep (Ammotragus lervia) were also determined and compared with the sequences of Bovidae available in the GenBank.The diversity of Y-chromosomes in chamois is very low.The differences in patterns of variation among Y-chromosome, mtDNA and biparental microsatellites reflect the evolutionary characteristics of the different markers as well as the effects of sex-biased dispersal and species phylogeography.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biología Funcional, Genética, Universidad de Oviedo, Julián Clavería 6, 33006 Oviedo, Spain.

ABSTRACT

Background: The chamois, distributed over most of the medium to high altitude mountain ranges of southern Eurasia, provides an excellent model for exploring the effects of historical and evolutionary events on diversification. Populations have been grouped into two species, Rupicapra pyrenaica from southwestern Europe and R. rupicapra from eastern Europe. The study of matrilineal mitochondrial DNA (mtDNA) and biparentally inherited microsatellites showed that the two species are paraphyletic and indicated alternate events of population contraction and dispersal-hybridization in the diversification of chamois. Here we investigate the pattern of variation of the Y-chromosome to obtain information on the patrilineal phylogenetic position of the genus Rupicapra and on the male-specific dispersal of chamois across Europe.

Results: We analyzed the Y-chromosome of 87 males covering the distribution range of the Rupicapra genus. We sequenced a fragment of the SRY gene promoter and characterized the male specific microsatellites UMN2303 and SRYM18. The SRY promoter sequences of two samples of Barbary sheep (Ammotragus lervia) were also determined and compared with the sequences of Bovidae available in the GenBank. Phylogenetic analysis of the alignment showed the clustering of Rupicapra with Capra and the Ammotragus sequence obtained in this study, different from the previously reported sequence of Ammotragus which groups with Ovis. Within Rupicapra, the combined data define 10 Y-chromosome haplotypes forming two haplogroups, which concur with taxonomic classification, instead of the three clades formed for mtDNA and nuclear microsatellites. The variation shows a west-to-east geographical cline of ancestral to derived alleles.

Conclusions: The phylogeny of the SRY-promoter shows an association between Rupicapra and Capra. The position of Ammotragus needs a reinvestigation. The study of ancestral and derived characters in the Y-chromosome suggests that, contrary to the presumed Asian origin, the paternal lineage of chamois originated in the Mediterranean, most probably in the Iberian Peninsula, and dispersed eastwards through serial funding events during the glacial-interglacial cycles of the Quaternary. The diversity of Y-chromosomes in chamois is very low. The differences in patterns of variation among Y-chromosome, mtDNA and biparental microsatellites reflect the evolutionary characteristics of the different markers as well as the effects of sex-biased dispersal and species phylogeography.

Show MeSH
Related in: MedlinePlus