Multilocus Intron Trees Reveal Extensive Male-Biased Homogenization of Ancient Populations of Chamois (Rupicapra spp.) across Europe during Late Pleistocene.

Trinidad Pérez,Sabine E Hammer,Margarita Fernández,Ana Domínguez

doi:10.1371/journal.pone.0170392

Trinidad Pérez, Sabine E Hammer + Show 2 more

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https://doi.org/10.1371/journal.pone.0170392

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Abstract

The inferred phylogenetic relationships between organisms often depend on the molecular marker studied due to the diverse evolutionary mode and unlike evolutionary histories of different parts of the genome. Previous studies have shown conflicting patterns of differentiation of mtDNA and several nuclear markers in chamois (genus Rupicapra) that indicate a complex evolutionary picture. Chamois are mountain caprine that inhabit most of the medium to high altitude mountain ranges of southern Eurasia. The most accepted taxonomical classification considers two species, R. 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. Phylogenies of mtDNA revealed three very old clades (from the early Pleistocene, 1.9 Mya) with a clear geographical signal. Here we analyze a set of 23 autosomal introns, comprising 15,411 nucleotides, in 14 individuals covering the 10 chamois subspecies. Introns offered an evolutionary scenario that contrasts with mtDNA. The nucleotidic diversity was 0.0013± 0.0002, at the low range of what is found in other mammals even if a single species is considered. A coalescent multilocus analysis with *BEAST indicated that introns diversified 88 Kya, in the late Pleistocene, and the effective population size at the root was lower than 10,000 individuals. The dispersal of some few migrant males should have rapidly spread trough the populations of chamois, given the homogeneity of intron sequences. The striking differences between mitochondrial and nuclear markers can be attributed to strong female philopatry and extensive male dispersal. Our results highlight the need of analyzing multiple and varied genome components to capture the complex evolutionary history of organisms.

Highlights

Phylogenetic studies try to reconstruct the evolutionary history of organisms from the comparison of parts of the genome
We study whether different introns present conflicting phylogenies and compare these results with previous studies on mtDNA, other nuclear biparental markers and the chromosome Y to explore the role of different components of the genome in the differentiation and evolutionary history of chamois
We evaluated the phylogenetic signal obtained from introns by comparison with other sets of data previously obtained: two sets of nuclear data, Y-chromosomal data [23] and the melacortin-1 receptor gene (MC1R, 954 nt) [22]} and a mitochondrial data set consisting of sequences of five mtDNA regions (CYTB, ND1, 12S, tRNApro and Control Region, 1646 nt) [18, 19]

Summary

Introduction

Phylogenetic studies try to reconstruct the evolutionary history of organisms from the comparison of parts of the genome. After the great development of molecular analyses in the last few decades it was frequently observed that the trees obtained for different markers were discordant. In some cases, these observations can be interpreted as incomplete lineage sorting, and coalescent methods have been implemented for species assignment from the integration of gene trees [1]. The alternative explanation in terms of reticulate evolution, where populations that diverge in isolation eventually reconnect and interchange parts of genome is likely to be true [2]. The patterns of differentiation for different molecular markers in chamois (Rupicapra spp.) can be best explained as reticulate evolution [2]

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