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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. Phylogenetic relationships within and between animal species often depend on the markers studied, as different genes might have different modes of transmission and different histories [ – ]. In addition, hybridization can result in discordant phylogenies between markers. Increasing evidence points to a contribution of reticulate evolution to the speciation process [ – ]. In this context, information on the phylogenies of different markers for closely related species and subspecies is important to the study of processes underlying speciation [ ]. The study of chamois ( Rupicapra spp.) allows exploring the effect of historical and evolutionary events on diversification. It is distributed over most of the medium to high altitude mountain ranges of southern Eurasia (Figure ).
At present, chamois populations are classified into two species, R. Pyrenaica and R. Rupicapra [ ], on the basis of morphological and behavioral characters: Rupicapra pyrenaica (with the subspecies parva, pyrenaica and ornata) from southwestern Europe, and R. Rupicapra (with the subspecies cartusiana, rupicapra, tatrica, carpatica, balcanica, asiatica and caucasica) from central and southeastern Europe and western Asia [ ].
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Analysis of genetic variation in a limited number of subspecies for allozyme loci [ ], minisatellites [ ], RFLPs of mitochondrial DNA [ ] and the major histocompatibility complex [, ] provided some support for this classification. However, the nominal species are paraphyletic for mtDNA [, ].
Descargar Ya No Sufro Por Amor Lucia Etxebarria Pdf To Jpg. Figure 1 Geographic distribution of the subspecies of the genus Rupicapra. Sampling sites are indicated by circles. The map was modified from the distribution map on the IUCN Red List [ ]. The Quaternary glacial ages probably had a major effect on the phylogeography and evolution of the genus Rupicapra, as it did on other animals in Eurasia [ – ].
The Rupicaprini are thought to have originated in Asia during the Miocene period and the sudden appearance of Rupicapra fossils in Europe during the middle Pleistocene age has been interpreted as resulting from immigration from the east during a cold climatic phase [ ]. In contrast with the fossil record, the divergence between the main mtDNA clades has been estimated around 1.5-3 mya [,, – ] but this cannot be directly assumed to be the divergence time between species.
The mitochondrial phylogeny showed three main lineages, originating during the Early Pleistocene [, ]. Nuclear microsatellite genotypes formed three clearly defined groups as well; however those groups did not exactly match the mitochondrial lineages but are closer to morphology and taxonomic classification. The phylogeographic patterns suggest an evolutionary history with range contractions and expansions related to climatic oscillations during the Quaternary period and reflect a major effect of the Alpine barrier on west-east differentiation. The contrasting phylogenies of mtDNA and nuclear microsatellites for populations of Chartreuse and the western Alps indicated events of range overlap and hybridization among highly divergent lineages in the central area of the distribution. Both markers showed differentiation between all pairs of populations [,, ] and a geographic signature in the distribution of variability, suggesting that differentiation occurred without major migrations. To further elucidate the processes leading to the origin and diversification of Rupicapra, we studied the Y-chromosome. The Y-chromosome is paternally inherited and does not undergo recombination at meiosis, providing a marker to study male dispersal [ – ].
The study has the dual purpose of studying the patrilineal phylogenetic position of chamois, compared with Capra, Ovis and Ammotragus, and the male dispersal within the genus Rupicapra. We present the analysis of a sequence of a fragment of the SRY gene promoter together with two male-specific microsatellites UMN2303 and SRYM18, in a sample set of 87 males, 40 of R. Pyrenaica and 47 from R. Rupricapra, which covers the entire distribution range of chamois.
Comparison of the geographic distribution of male-specific markers with mtDNA lineages (defining matrilines) and autosomal markers (biparentally inherited) allows us to follow the evolutionary history of Rupicapra in the context of the climatic oscillations of the Pleistocene age. SRY promoter sequences We have amplified and sequenced 569 nucleotides corresponding to a fragment of the SRY gene promoter from 52 male chamois, 24 of the subspecies R. Pyrenaica (14 parva, 6 pyrenaica and 4 ornata) and 28 of R. Rupicapra (5 cartusiana, 6 rupicapraW, 6 rupicapra CE, 3 tatrica, 3 carpatica, 2 balcanica, 1 asiatica and 2 caucasica).
The alignment resulted in only two haplotypes, one in R. Pyrenaica and the other in R. These haplotypes differ only in one nucleotide (site 267 in our alignment), which is A in the haplotype pyrenaica and G in rupicapra. 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 ). 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 [ ] 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 ), 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. 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 [ ] and Ammotragus lervia 2 refers to the sequence obtained in this work. The estimated divergence time of the two Rupicapra haplotypes from the SRY promoter sequence was 655 kya (95% CI: 10-1,611).
The mean substitution rate per nucleotide calculated with TRACER from the MCMC samples was 2.09E-3 ± 1.08E-5 per million years. Y-chromosome microsatellites. Out of 14 microsatellite markers tested, only UMN2303 and SRYM18 produced male-specific products. Amplification from 87 males, 40 of R. Pyrenaica and 47 from R. Rupricapra, revealed two different length fragments for UMN2303 and seven for SRYM18 (Table ).
For each microsatellite, fragments within each length variant were further analyzed by cloning and sequencing, and the architecture was compared with their homologous loci in other Bovidae. The UMN2303 repeated motif was found to be [TTTTG] n differing from the repeat [TG] n reported in Bos taurus. Rupicapra pyrenaica presented two alleles, 125 and 130, differing in one repetition, and R. Rupicapra was monomorphic, with only the 125 allele. The microsatellite SRYM18 lacks the pentanucleotide [TTTTG] and the dinucleotide [TG] motifs common in sheep [ ] and instead presents a trinucleotide [TTC] m and a mononucleotide [T] n motifs. Rupicapra pyrenaica haplotypes were [TTC] mA[T] n and R.
Rupicapra haplotypes were [TTC] m[T] n, these two structures were reported in Ammotragus lerviae (Acc. N° DQ272449) and Ovis aries breed Balami (Acc. N° DQ272459.1), respectively. Combinations of variation in number of repeats in both motifs in R. Rupicapra resulted in homoplasy, where PCR products with the same size had different sequence architecture. The trinucleotide motif, [TTC] m, was polymorphic in the species R.
Rupicapra but not in R. Pyrenaica while the mononucleotide motif was polymorphic in both subspecies (Table ). Haplotype description Frequency SRY promoter UMN2303 SRYM18 R.
Rupicapra Haplotype A/G Size Size [TTC]m SNP A/T [T]n par pyr orn cat rupW rupC rupE tat cap bal asi cau Y-Rpyr1 A 130 102 2 A 9 17 (3) 9 (4) Y-Rpyr2 A 125 102 2 A 9 1 (1) 7 (3) Y-Rpyr3 A 125 105 2 A 12 6 (1) Y-RrupA1 G 125 109 3 T 13 1 (1) 6 (1) 1 1 (1) Y-RrupA2 G 125 110 3 T 14 1 (1) 2 (1) 2 (1) 5 (4) 6 (4) 3 (2) Y-RrupA3 G 125 111 3 T 15 5 (1) 4 (1) Y-RrupA4 G 125 112 3 T 16 4 (1) 1 (1) Y-RrupB1 G 125 111 4 T 12 3 (3) Y-RrupB2 G 125 113 4 T 14 1 (1) Y-RrupC G 125 112 5 T 10 1 (1). The abbreviated name of the subspecies are: par, parva; pyr, pyrenaica; orn, ornata; cat, cartusiana; rupW, rupicapraW; rupC, rupicapraC; rupE, rupicapraE; tat, tatrica; cap, carpatica; bal, balcanica; asi, asiatica; and cau, caucasica. Free Download Program Illinois Urban Manual Drawings Of Roses. Number of samples sequenced for SRYM18 are given in parenthesis. Network of Y haplotypes Altogether, ten haplotypes could be differentiated in the Rupicapra genus (Table ). Total Y-chromosome haplotype diversity was 0.82 with on average one distinct haplotype over 8.7 individuals (87/10). Three private haplotypes were found in west chamois R.
Pyrenaica, giving a haplotypic diversity of 51.50% and the other seven haplotypes were private of the east chamois R. Rupicapra with a diversity of 74.69%. Figure 3 Network of Y-chromosome haplotypes. Median-joining network for the Y-chromosome haplotypes constructed using variation at the SRY promoter sequence and at the microsatellites UMN2303 (number of pentanucleotide repeats) and SRYM18 (one SNP, number of trinucleotide repeats and number of mononucleotide repeats). The size of pie areas corresponds to haplotypic frequencies and the proportion accounted for by the different subspecies is represented in different colors as in Figure 1.
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Different types of mutations in each branch are represented by different symbols (white square: SNP; black squares with a number inside: microsatellites with mononucleotide [1], trinucleotide [3] and pentanucleotide [5] motifs). The network is represented over a map according to the approximate geographical origin of the haplotypes. Branch lengths are not scaled.
Analysis of chromosome Y presented a pattern of variation different from the one obtained from either mitochondrial or biparental nuclear DNA, both on diversity as well as on the spread and geographic boundaries of dispersion. However, the east/west phylogeographic signal in the distribution of haplotypes is present again and once more the suture zone places in the Alps. It is remarkable that, contrary to mtDNA and autosomal microsatellites that formed three clades (although not exactly concordant), the variation for the Y-chromosome conforms to the two species currently accepted, Rupicapra pyrenaica and R. This could explain the concurrence of coat patterns, cranial morphometry and several courtship behavioral patterns in Iberian and Apennine chamois [,, ] that remained unexplained from the study of mtDNA and nuclear microsatellites [ ]. Phylogenetic relationships between chamois and other caprini The phylogeny of SRY promoter shows an association between Rupicapra, Capra and the Ammotragus sequence obtained in this work ( Ammotragus 2). This association concurs with the relationships revealed from the study of the complete mitochondrial genome [ ]. Previously, Meadows and Kijas [ ] reported a very close relation between the SRY promoter of Ammotragus ( Ammotragus lervia 1 in Table and Figure ) and Ovis, but we found 15 differences (3.33%) between this previously reported sequence and the new sequences produced in our laboratory ( Ammotragus lervia 2 in Table and Figure ).
This large difference is not expected between two individuals of the same species. In contrast, the reported sequence of Ammotragus presents only 4 differences (0.83%) with Ovis canadensis. Our sequence has been obtained from good quality samples (muscle) from two specimens (both repeated twice) with identical results. So, we think that the sequence reported by Meadows and Kijas could be contaminated with DNA of Ovis canadensis. An alternative interpretation to take into account is the polyphyly of Ammotragus. The affinities of Ammotragus with either Capra or Ovis have been widely discussed in the literature as it exhibits a particular combination of goat-like and sheep-like characters [ ].
The structure of the microsatellite SRYM18 of west chamois is identical to Ammotragus and different to most Ovis, but the African breed Balami of O. Aries shares the repeat structure with Ammotragus and Rupicapra. This observation had lead Meadows and Kijas [ ] to hypothesize the possible gene flow from Barbary to domestic sheep. The observed similarities between Ammotragus lerviae and the genus Rupicapra and the apparent spread of male chamois south to north reopen the question of the possible position of Ammotragus as an ancestor of the Caprinae [ ]. It can also be noted that Rupicapra and Ammotragus have similar karyotype with 58 chromosomes [ ]. Additional studies of Y-chromosome phylogenies of Caprinae could offer very important information to clarify this issue. Patrilineal phylogeography of chamois.
When comparing the phylogenetic trees based on mtDNA or the sequences of the SRY promoter (Figure ), 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 [ ] 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 [ – ]. 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 [ ], gives further support to this interpretation. Thereafter, our data suggest that the divergence of Y-chr.
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