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. 2018 May 9;19(1):339.
doi: 10.1186/s12864-018-4714-x.

Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: the case for the Antarctic teleost genus Trematomus

Affiliations

Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: the case for the Antarctic teleost genus Trematomus

J Auvinet et al. BMC Genomics. .

Abstract

Background: The importance of transposable elements (TEs) in the genomic remodeling and chromosomal rearrangements that accompany lineage diversification in vertebrates remains the subject of debate. The major impediment to understanding the roles of TEs in genome evolution is the lack of comparative and integrative analyses on complete taxonomic groups. To help overcome this problem, we have focused on the Antarctic teleost genus Trematomus (Notothenioidei: Nototheniidae), as they experienced rapid speciation accompanied by dramatic chromosomal diversity. Here we apply a multi-strategy approach to determine the role of large-scale TE mobilization in chromosomal diversification within Trematomus species.

Results: Despite the extensive chromosomal rearrangements observed in Trematomus species, our measurements revealed strong interspecific genome size conservation. After identifying the DIRS1, Gypsy and Copia retrotransposon superfamilies in genomes of 13 nototheniid species, we evaluated their diversity, abundance (copy numbers) and chromosomal distribution. Four families of DIRS1, nine of Gypsy, and two of Copia were highly conserved in these genomes; DIRS1 being the most represented within Trematomus genomes. Fluorescence in situ hybridization mapping showed preferential accumulation of DIRS1 in centromeric and pericentromeric regions, both in Trematomus and other nototheniid species, but not in outgroups: species of the Sub-Antarctic notothenioid families Bovichtidae and Eleginopsidae, and the non-notothenioid family Percidae.

Conclusions: In contrast to the outgroups, High-Antarctic notothenioid species, including the genus Trematomus, were subjected to strong environmental stresses involving repeated bouts of warming above the freezing point of seawater and cooling to sub-zero temperatures on the Antarctic continental shelf during the past 40 millions of years (My). As a consequence of these repetitive environmental changes, including thermal shocks; a breakdown of epigenetic regulation that normally represses TE activity may have led to sequential waves of TE activation within their genomes. The predominance of DIRS1 in Trematomus species, their transposition mechanism, and their strategic location in "hot spots" of insertion on chromosomes are likely to have facilitated nonhomologous recombination, thereby increasing genomic rearrangements. The resulting centric and tandem fusions and fissions would favor the rapid lineage diversification, characteristic of the nototheniid adaptive radiation.

Keywords: Chomosomal rearrangements; DIRS1 insertion hot spots; FISH; Nototheniidae; Retrotransposons; Speciation; Trematomus.

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Conflict of interest statement

Authors’ information

2: LP is in charge of the cytometers from the imaging platform of Sorbonne Université, 75,252 Paris, cedex 05

Ethics approval and consent to participate

Ethical approval for all procedures was granted by the ethics committee of the Ministère de l’Environnement and the French Polar Research Institute (Institut Paul Emile Victor – IPEV), which approved all our fieldwork. The experiments complied with the Code of Ethics of Animal Experimentation in the Antarctic sector.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
NJ bootstrap consensus tree for DIRS1 based on the RT/RH amino acid sequences. Only the branch containing the nototheniid DIRS1 families and the closest related sequences are shown. The four nototheniid DIRS1 families (bold font) group with the other bony fish sequences: Tetraodon nigroviridis, Gasterosteus aculeatus, Danio rerio, Oryzias latipes. Distances were calculated with the JTT model and a gamma distribution correction for amino acid. Support for individual clusters was evaluated using non-parametric bootstrapping with 1000 replicates. Only bootstraps over 60 are presented. Nodes with bootstraps < 60% were collapsed. See full tree in Additional file 3
Fig. 2
Fig. 2
NJ bootstrap consensus tree for Gypsy based on the RT/RH (a), INT (b) regions. Only the branch containing the nototheniid Gypsy and the closest related amino acid sequences are presented. Except for GyNotoI and GyNotoRT, the seven nototheniid Gypsy families shown (bold font) group with bony fish sequences: Takifugu rubripes -sushi-ichi and Danio rerio -Amn-ni in addition to other vertebrate Gypsy sequences: Xenopus/Silurana tropicalis. Distances were calculated with the JTT model and a gamma distribution correction for amino acid. Support for individual clusters was evaluated using non-parametric bootstrapping with 1000 replicates. Only bootstraps over 60 are presented. Nodes with bootstraps < 60% were collapsed. See full tree in Additional file 4
Fig. 3
Fig. 3
NJ bootstrap consensus tree for Copia based on the RT/RH amino acid sequences. Only the branch containing the nototheniid Copia families and the closest related sequences are shown. The two nototheniid Copia families (bold font) identified in nototheniid genomes group with bony fish sequences: Dicentrarchus labrax, Xiphophorus maculatus, Danio rerio, Oreochromis niloticus and Neolamprologus brichardi. Distances were calculated with the JTT model and the gamma distribution correction for amino acid. Support for individual clusters was evaluated using non-parametric bootstrapping with 1000 replicates. Only bootstraps over 60 are presented. Nodes with bootstraps < 60% were collapsed. See full tree in Additional file 5
Fig. 4
Fig. 4
Mapping of TEs on the chromosomes of five nototheniid species by FISH. Each probe was labeled with biotin and bound probe was detected with incubation with Avidin-FITC (fluorescein, greenish spots). (Probe characteristics are indicated in Additional file 6). Chromosomal DNA was counterstained with DAPI. One family of each retrotransposon superfamily is represented in this figure: YNotoJ for DIRS1, GyNotoA for Gypsy and CoNotoB for Copia elements. (see Additional files 7 and 8 for FISH mapping with the second family of DIRS1 (YnotoR) and Gypsy (GyNotoE)). Examples of TE distribution patterns for type 1: d, h; type 2: c, i; type 1 + 2: e, j, p. White arrows point examples of TE accumulations. Scale bars: 10 μm
Fig. 5
Fig. 5
Mapping of TEs on the chromosomes of the three outgroups by FISH. Each probe was labeled with biotin and bound probe was detected with incubation with Avidin-FITC (fluorescein, greenish spots). (Probe characteristics are indicated in Additional file 6). Chromosomal DNA was counterstained with DAPI. One family of each retrotransposon superfamily is represented in this figure: YNotoJ for DIRS1, GyNotoA for Gypsy and CoNotoB for Copia elements. Scale bars: 10 μm

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