Evolutionary History of LINE-1 in the Major Clades of Placental Mammals

Paul D Waters,Terence J Robinson,Peter J Waddell,Gauthier Dobigny,James Fraser

doi:10.1371/journal.pone.0000158

Abstract

BackgroundLINE-1 constitutes an important component of mammalian genomes. It has a dynamic evolutionary history characterized by the rise, fall and replacement of subfamilies. Most data concerning LINE-1 biology and evolution are derived from the human and mouse genomes and are often assumed to hold for all placentals.MethodologyTo examine LINE-1 relationships, sequences from the 3′ region of the reverse transcriptase from 21 species (representing 13 orders across Afrotheria, Xenarthra, Supraprimates and Laurasiatheria) were obtained from whole genome sequence assemblies, or by PCR with degenerate primers. These sequences were aligned and analysed.Principal FindingsOur analysis reflects accepted placental relationships suggesting mostly lineage-specific LINE-1 families. The data provide clear support for several clades including Glires, Supraprimates, Laurasiatheria, Boreoeutheria, Xenarthra and Afrotheria. Within the afrotherian LINE-1 (AfroLINE) clade, our tree supports Paenungulata, Afroinsectivora and Afroinsectiphillia. Xenarthran LINE-1 (XenaLINE) falls sister to AfroLINE, providing some support for the Atlantogenata (Xenarthra+Afrotheria) hypothesis.SignificanceLINEs and SINEs make up approximately half of all placental genomes, so understanding their dynamics is an essential aspect of comparative genomics. Importantly, a tree of LINE-1 offers a different view of the root, as long edges (branches) such as that to marsupials are shortened and/or broken up. Additionally, a robust phylogeny of diverse LINE-1 is essential in testing that site-specific LINE-1 insertions, often regarded as homoplasy-free phylogenetic markers, are indeed unique and not convergent.

Highlights

The non-LTR retrotransposons Long Interspersed Nuclear Elements-1 (LINE-1, or L1) are a major component of mammalian genomes (,20% of that of human) that transpose through an RNA intermediate
Previous studies have investigated the paleohistory of LINE-1 families based on the ‘‘genomic fossil record of pseudogenes retroposed at different times from active source genes’’ [10]
To estimate recent activity in the absence of these data, pairwise distances of closely related LINE-1 were checked, and any pair of sequences that were .98% similar to each other are coloured yellow in the tree (Figure 1)

Summary

Background

LINE-1 constitutes an important component of mammalian genomes. It has a dynamic evolutionary history characterized by the rise, fall and replacement of subfamilies. To examine LINE-1 relationships, sequences from the 39 region of the reverse transcriptase from 21 species (representing 13 orders across Afrotheria, Xenarthra, Supraprimates and Laurasiatheria) were obtained from whole genome sequence assemblies, or by PCR with degenerate primers. Xenarthran LINE-1 (XenaLINE) falls sister to AfroLINE, providing some support for the Atlantogenata (Xenarthra+Afrotheria) hypothesis.

INTRODUCTION

RESULTS AND DISCUSSION

MATERIAL AND METHODS