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Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois (genus Rupicapra).

Rodríguez F, Pérez T, Hammer SE, Albornoz J, Domínguez A - BMC Evol. Biol. (2010)

Bottom Line: We found discordant microsatellite (musat) and mitochondrial (mt) DNA phylogenies.Recent drastic reductions in population size can be noted for the subspecies ornata as an extremely low diversity.Our study points to the importance of reticulate evolution, with periods of isolation and reduction of population size followed by expansions and hybridizations, in the diversification at the level of close species or subspecies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biología Funcional, Universidad de Oviedo, Genética, Julián Clavería 6, 33071 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. However, a previous study of cytochrome b revealed that the two proposed species were non-monophyletic. The reconstruction of phylogenetic relationships between animal species often depends on the markers studied. To further elucidate the evolutionary history of chamois, we extended earlier studies by analysing DNA sequences of four mitochondrial regions (ND1, 12S, tRNApro and Control Region) and microsatellites (20 loci) to include all subspecies and cover its entire distribution range.

Results: We found discordant microsatellite (musat) and mitochondrial (mt) DNA phylogenies. Mitochondrial phylogenies form three clades, West, Central and East (mtW, mtC and mtE), at variance with taxonomic classification. Our divergence age estimates indicate an initial separation into branches mtW-mtC and mtE 1.7 million years ago (mya), in the late Pliocene-early Pleistocene, quickly followed by the split of clades mtW and mtC. Clade mtW contains haplotypes from the Iberian peninsula and the western Alps, Clade mtC includes haplotypes from the Apennines and the Massif of Chartreuse and Clade mtE comprises populations to the east of the Alps. Divergence among populations within these three major clades is recent (< 0.5 mya). New microsatellite multilocus genotypes added to previously published data revealed differences between every pair of subspecies, forming three well defined groups (musatW, musatC and musatE) also with a strong geographic signature. Grouping does not correspond with the mitochondrial lineages but is closer to morphology and taxonomic classification. Recent drastic reductions in population size can be noted for the subspecies ornata as an extremely low diversity.

Conclusions: The phylogeographic patterns for mtDNA and microsatellites suggest an evolutionary history with limited range contractions and expansions during the Quaternary period and reflect a major effect of the Alpine barrier on west-east differentiation. The contrasting phylogenies for mtDNA and microsatellites indicate events of hybridization among highly divergent lineages in the central area of distribution. Our study points to the importance of reticulate evolution, with periods of isolation and reduction of population size followed by expansions and hybridizations, in the diversification at the level of close species or subspecies.

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Geographic distribution of the subspecies of the genus Rupicapra. Sampling sites are indicated by circles and labelled with a letter code. The map was modified from the distribution map on the IUCN Red List [54].
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Figure 1: Geographic distribution of the subspecies of the genus Rupicapra. Sampling sites are indicated by circles and labelled with a letter code. The map was modified from the distribution map on the IUCN Red List [54].

Mentions: The chamois (Rupicapra spp.) provides an excellent model for 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 1). 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 [8-11]. There are diverse opinions concerning the phylogenetic relationships between fossil and living forms of Rupicaprini. The Rupicaprini seem to have originated in Asia during the Miocene period [11]; the fossil genus Procamptoceras appeared in Europe in the Villafranchian period (more than 2 million years ago [mya]) and together with Rupicapra is believed to belong to a phyletic lineage that had already separated from the ancestral Rupicaprini [12]. 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 [11]. At present, chamois populations are classified into two species R. pyrenaica and R. rupicapra [13] on the basis of morphological and behavioural 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 northeastern Europe [14]. Analysis of genetic variation in a limited number of subspecies for allozyme loci [15], minisatellites [16], RFLPs of mitochondrial DNA [17] and the major histocompatibility complex [18,19] showed a considerably higher divergence between populations of the two proposed species than between populations within the same species. Microsatellite analysis of 8 of the 10 proposed subspecies showed a clear differentiation between every pair of populations and clearly separated two groups corresponding to the two proposed species of chamois [20]. The geographic distribution of separated mtDNA clades allows the study of historical demographic and dispersal events and the differentiation between mtDNA sequences can be used to date the separation among phylogenetic groups. The study of a fragment of cytochrome b (cytb) of 349 bp revealed that the two proposed species were non-monophyletic [21]. Three cytb lineages were identified: Clade West in the Iberian peninsula and western Alps, Clade Central in the Apennines and the Massif of Chartreuse and Clade East in populations to the east of the Alps. Clades West and Central are represented in both species, while Clade East is restricted to R. rupicapra. The divergence between the main clades has been estimated around 1.5-3 mya [21-25] but this cannot be directly assumed to be the divergence time between species. The study of microsatellites [20] has shown a correlation between genetic and geographic distance between populations, denoting a genetic flow among contiguous populations.


Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois (genus Rupicapra).

Rodríguez F, Pérez T, Hammer SE, Albornoz J, Domínguez A - BMC Evol. Biol. (2010)

Geographic distribution of the subspecies of the genus Rupicapra. Sampling sites are indicated by circles and labelled with a letter code. The map was modified from the distribution map on the IUCN Red List [54].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2923631&req=5

Figure 1: Geographic distribution of the subspecies of the genus Rupicapra. Sampling sites are indicated by circles and labelled with a letter code. The map was modified from the distribution map on the IUCN Red List [54].
Mentions: The chamois (Rupicapra spp.) provides an excellent model for 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 1). 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 [8-11]. There are diverse opinions concerning the phylogenetic relationships between fossil and living forms of Rupicaprini. The Rupicaprini seem to have originated in Asia during the Miocene period [11]; the fossil genus Procamptoceras appeared in Europe in the Villafranchian period (more than 2 million years ago [mya]) and together with Rupicapra is believed to belong to a phyletic lineage that had already separated from the ancestral Rupicaprini [12]. 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 [11]. At present, chamois populations are classified into two species R. pyrenaica and R. rupicapra [13] on the basis of morphological and behavioural 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 northeastern Europe [14]. Analysis of genetic variation in a limited number of subspecies for allozyme loci [15], minisatellites [16], RFLPs of mitochondrial DNA [17] and the major histocompatibility complex [18,19] showed a considerably higher divergence between populations of the two proposed species than between populations within the same species. Microsatellite analysis of 8 of the 10 proposed subspecies showed a clear differentiation between every pair of populations and clearly separated two groups corresponding to the two proposed species of chamois [20]. The geographic distribution of separated mtDNA clades allows the study of historical demographic and dispersal events and the differentiation between mtDNA sequences can be used to date the separation among phylogenetic groups. The study of a fragment of cytochrome b (cytb) of 349 bp revealed that the two proposed species were non-monophyletic [21]. Three cytb lineages were identified: Clade West in the Iberian peninsula and western Alps, Clade Central in the Apennines and the Massif of Chartreuse and Clade East in populations to the east of the Alps. Clades West and Central are represented in both species, while Clade East is restricted to R. rupicapra. The divergence between the main clades has been estimated around 1.5-3 mya [21-25] but this cannot be directly assumed to be the divergence time between species. The study of microsatellites [20] has shown a correlation between genetic and geographic distance between populations, denoting a genetic flow among contiguous populations.

Bottom Line: We found discordant microsatellite (musat) and mitochondrial (mt) DNA phylogenies.Recent drastic reductions in population size can be noted for the subspecies ornata as an extremely low diversity.Our study points to the importance of reticulate evolution, with periods of isolation and reduction of population size followed by expansions and hybridizations, in the diversification at the level of close species or subspecies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biología Funcional, Universidad de Oviedo, Genética, Julián Clavería 6, 33071 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. However, a previous study of cytochrome b revealed that the two proposed species were non-monophyletic. The reconstruction of phylogenetic relationships between animal species often depends on the markers studied. To further elucidate the evolutionary history of chamois, we extended earlier studies by analysing DNA sequences of four mitochondrial regions (ND1, 12S, tRNApro and Control Region) and microsatellites (20 loci) to include all subspecies and cover its entire distribution range.

Results: We found discordant microsatellite (musat) and mitochondrial (mt) DNA phylogenies. Mitochondrial phylogenies form three clades, West, Central and East (mtW, mtC and mtE), at variance with taxonomic classification. Our divergence age estimates indicate an initial separation into branches mtW-mtC and mtE 1.7 million years ago (mya), in the late Pliocene-early Pleistocene, quickly followed by the split of clades mtW and mtC. Clade mtW contains haplotypes from the Iberian peninsula and the western Alps, Clade mtC includes haplotypes from the Apennines and the Massif of Chartreuse and Clade mtE comprises populations to the east of the Alps. Divergence among populations within these three major clades is recent (< 0.5 mya). New microsatellite multilocus genotypes added to previously published data revealed differences between every pair of subspecies, forming three well defined groups (musatW, musatC and musatE) also with a strong geographic signature. Grouping does not correspond with the mitochondrial lineages but is closer to morphology and taxonomic classification. Recent drastic reductions in population size can be noted for the subspecies ornata as an extremely low diversity.

Conclusions: The phylogeographic patterns for mtDNA and microsatellites suggest an evolutionary history with limited range contractions and expansions during the Quaternary period and reflect a major effect of the Alpine barrier on west-east differentiation. The contrasting phylogenies for mtDNA and microsatellites indicate events of hybridization among highly divergent lineages in the central area of distribution. Our study points to the importance of reticulate evolution, with periods of isolation and reduction of population size followed by expansions and hybridizations, in the diversification at the level of close species or subspecies.

Show MeSH
Related in: MedlinePlus