Interspecies insertion polymorphism analysis reveals recent activity of transposable elements in extant coelacanths.

Magali Naville,Domitille Chalopin,Jean-Nicolas Volff,Hector Escriva

doi:10.1371/journal.pone.0114382

Magali Naville, Domitille Chalopin + Show 2 more

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https://doi.org/10.1371/journal.pone.0114382

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Abstract

Coelacanths are lobe-finned fish represented by two extant species, Latimeria chalumnae in South Africa and Comoros and L. menadoensis in Indonesia. Due to their intermediate phylogenetic position between ray-finned fish and tetrapods in the vertebrate lineage, they are of great interest from an evolutionary point of view. In addition, extant specimens look similar to 300 million-year-old fossils; because of their apparent slowly evolving morphology, coelacanths have been often described as « living fossils ». As an underlying cause of such a morphological stasis, several authors have proposed a slow evolution of the coelacanth genome. Accordingly, sequencing of the L. chalumnae genome has revealed a globally low substitution rate for protein-coding regions compared to other vertebrates. However, genome and gene evolution can also be influenced by transposable elements, which form a major and dynamic part of vertebrate genomes through their ability to move, duplicate and recombine. In this work, we have searched for evidence of transposition activity in coelacanth genomes through the comparative analysis of orthologous genomic regions from both Latimeria species. Comparison of 5.7 Mb (0.2%) of the L. chalumnae genome with orthologous Bacterial Artificial Chromosome clones from L. menadoensis allowed the identification of 27 species-specific transposable element insertions, with a strong relative contribution of CR1 non-LTR retrotransposons. Species-specific homologous recombination between the long terminal repeats of a new coelacanth endogenous retrovirus was also detected. Our analysis suggests that transposon activity is responsible for at least 0.6% of genome divergence between both Latimeria species. Taken together, this study demonstrates that coelacanth genomes are not evolutionary inert: they contain recently active transposable elements, which have significantly contributed to post-speciation genome divergence in Latimeria.

Highlights

Coelacanths are lobe-finned fish that have been considered extinct since the Late Cretaceous period about 70 million years ago, until a first living specimen, Latimeria chalumnae, was discovered in 1938 in South Africa by Marjorie Courtenay-Latimer [1]
We searched for the presence of species-specific Transposable elements (TEs) insertions in Latimeria by comparing 36 Bacterial Artificial Chromosomes (BACs) clone sequences from the Indonesian coelacanth L. menadoensis with orthologous regions from the recently published genome of its African congener L. chalumnae [6]
Comparative analysis of orthologous regions covering 5.7 Mb of the genome of the two extant coelacanth species strongly sustains the recent activity of TEs in this lineage, with the identification of 13 and 14 species-specific insertions in L. chalumnae and L. menadoensis, respectively

Summary

Introduction

Coelacanths are lobe-finned fish that have been considered extinct since the Late Cretaceous period about 70 million years (my) ago, until a first living specimen, Latimeria chalumnae, was discovered in 1938 in South Africa by Marjorie Courtenay-Latimer [1]. From an evolutionary point of view, coelacanths occupy like lungfishes a key phylogenetic position between ray-finned fish and tetrapods at the basis of the sarcopterygian lineage. While coelacanths formed a highly spread taxonomic group during the Devonian [3, 4], both extant species are nowadays endangered, with only few inventoried individuals (about 300 for L. chalumnae [5]). Despite their geographical remoteness, L. chalumnae and L. menadoensis present a high degree of nucleotide identity at the genomic level [98.7%, based on the comparison of 20 Bacterial Artificial Chromosomes (BACs) from L. menadoensis with their orthologous sequences in the L. chalumnae genome], as well as for exons (.99.7%, based on the comparison of liver and testis transcriptomes from both species) [6, 7]. Considering the faster evolution in the primate lineage, the divergence time between the two coelacanth species was approximated at slightly more than 6–8 million years [6]

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