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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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Comparison of mitochondrial DNA and SRY-promoter phylogenies on chamois. Neighbor-Joining trees under Jukes-Cantor showing the relationships among chamois and the outgroups Ovis aries, Capra hircus and Bos taurus. a) Tree constructed with a combined sequence of 1708 nucleotides of mtDNA [17]. Sequences in clades mtW, Clade mtC and Clade mtE, in black, grey and white respectively, were collapsed. b) Tree constructed with a sequence of 531 nucleotides of the SRY promoter. For both trees the number of individuals in the external branches is indicated in parentheses.
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Figure 4: Comparison of mitochondrial DNA and SRY-promoter phylogenies on chamois. Neighbor-Joining trees under Jukes-Cantor showing the relationships among chamois and the outgroups Ovis aries, Capra hircus and Bos taurus. a) Tree constructed with a combined sequence of 1708 nucleotides of mtDNA [17]. Sequences in clades mtW, Clade mtC and Clade mtE, in black, grey and white respectively, were collapsed. b) Tree constructed with a sequence of 531 nucleotides of the SRY promoter. For both trees the number of individuals in the external branches is indicated in parentheses.

Mentions: When comparing the phylogenetic trees based on mtDNA or the sequences of the SRY promoter (Figure 4), a clear difference emerges. All the Rupicapra belong to one unique clade for the SRY promoter while three, well differentiated, clades formed for mtDNA. The observed number of substitutions per nucleotide between the pairs of species Ovis-Rupicapra, Capra-Rupicapra and Ovis-Capra for the sequences of mtDNA in our former study [17] were 0.1125, 0.1264 and 0.1186 respectively to be compared with 0.0520, 0.0346 and 0.0489 substitutions per nucleotide respectively for the SRY promoter sequence. The distance between pairs of species for mtDNA is about two or three times that of the SRY promoter, consistent with observations in other mammals including humans [39-42]. The level of differentiation among Y-chromosomes in chamois is remarkably low. The haplogroups Y-Rpyr and Y-Rrup within the Rupicapra genus differ by one single nucleotide, leading to an estimated average number of substitutions per nucleotide of 0.0019 that is 24.6 times lower than the average distance between the three clades of mtDNA (0.0468). The time of divergence between the SRY haplotypes estimated from the phylogenetic tree places the split 655 kya, in the middle of the Pleistocene. Thus, all modern chamois seem to descend of one very young male lineage. The low diversity in the number of microsatellite repeats, both between species and within species, compared with the Y-specific evolutionary mutation rate of 2.6 × 10-4 mutations per generation [43], gives further support to this interpretation. Thereafter, our data suggest that the divergence of Y-chromosomal variants took place well after the divergence of mtDNA lineages [17,22,44], in a period compatible with the sudden appearance of Rupicapra fossils in Europe [21].


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

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

Comparison of mitochondrial DNA and SRY-promoter phylogenies on chamois. Neighbor-Joining trees under Jukes-Cantor showing the relationships among chamois and the outgroups Ovis aries, Capra hircus and Bos taurus. a) Tree constructed with a combined sequence of 1708 nucleotides of mtDNA [17]. Sequences in clades mtW, Clade mtC and Clade mtE, in black, grey and white respectively, were collapsed. b) Tree constructed with a sequence of 531 nucleotides of the SRY promoter. For both trees the number of individuals in the external branches is indicated in parentheses.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Comparison of mitochondrial DNA and SRY-promoter phylogenies on chamois. Neighbor-Joining trees under Jukes-Cantor showing the relationships among chamois and the outgroups Ovis aries, Capra hircus and Bos taurus. a) Tree constructed with a combined sequence of 1708 nucleotides of mtDNA [17]. Sequences in clades mtW, Clade mtC and Clade mtE, in black, grey and white respectively, were collapsed. b) Tree constructed with a sequence of 531 nucleotides of the SRY promoter. For both trees the number of individuals in the external branches is indicated in parentheses.
Mentions: When comparing the phylogenetic trees based on mtDNA or the sequences of the SRY promoter (Figure 4), a clear difference emerges. All the Rupicapra belong to one unique clade for the SRY promoter while three, well differentiated, clades formed for mtDNA. The observed number of substitutions per nucleotide between the pairs of species Ovis-Rupicapra, Capra-Rupicapra and Ovis-Capra for the sequences of mtDNA in our former study [17] were 0.1125, 0.1264 and 0.1186 respectively to be compared with 0.0520, 0.0346 and 0.0489 substitutions per nucleotide respectively for the SRY promoter sequence. The distance between pairs of species for mtDNA is about two or three times that of the SRY promoter, consistent with observations in other mammals including humans [39-42]. The level of differentiation among Y-chromosomes in chamois is remarkably low. The haplogroups Y-Rpyr and Y-Rrup within the Rupicapra genus differ by one single nucleotide, leading to an estimated average number of substitutions per nucleotide of 0.0019 that is 24.6 times lower than the average distance between the three clades of mtDNA (0.0468). The time of divergence between the SRY haplotypes estimated from the phylogenetic tree places the split 655 kya, in the middle of the Pleistocene. Thus, all modern chamois seem to descend of one very young male lineage. The low diversity in the number of microsatellite repeats, both between species and within species, compared with the Y-specific evolutionary mutation rate of 2.6 × 10-4 mutations per generation [43], gives further support to this interpretation. Thereafter, our data suggest that the divergence of Y-chromosomal variants took place well after the divergence of mtDNA lineages [17,22,44], in a period compatible with the sudden appearance of Rupicapra fossils in Europe [21].

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