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

Abstract

BackgroundThe 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.ResultsDespite 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.ConclusionsIn 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.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4714-x) contains supplementary material, which is available to authorized users.

Movement of transposable elements contributes to cichlid diversity

“…fishes (Volff 2005). TE movement is sometimes ascribed to stress in fishes (Symonova et al 2013, Auvinet et al 2018. Studies in very young hybrids show that TE number can increase as a result of tandem duplication though they did not find evidence of new insertions (Dennenmoser et al 2019).…”

Transposable elements in vertebrates: species evolution and environmental adaptation

“…TEs are considered the major drivers of genomic and biological diversity and thus of speciation and evolution. Indeed, the activity of transposons has been found to be responsible for genome expansion and chromosomal rearrangements (Rebollo et al 2010;Zhang et al 2011;Auvinet et al 2018), but also to generate, through co-optation and exaptation, regulatory sequences, coding exons, or entirely new genes that represented evolutionary advantages for the host (Sundaram et al 2014;Chalopin et al 2015;Warren et al 2015;Sotero-Caio et al 2017). Bursts of TEs have accompanied the genesis of new phylogenetic groups.…”

“…This aspect is extremely interesting since chromosomal rearrangements may drive lineage-specific diversification (Biscotti et al 2015a(Biscotti et al , 2015bWarren et al 2015). Recently Auvinet et al (2018) have reported the location of DIRS1 (DIctyostelium Repetitive Sequence 1) in "hot spots" of insertion along chromosomes. This event likely facilitated nonhomologous recombinations responsible for the high chromosomal diversity observed in the Antarctic teleost genus Trematomus.…”

“…For the Antarctic teleost genus Trematomus (Notothenioidei: Nothotheniidae) TE mobilization has been proposed as possible responsible for chromosomal diversification and consequent rapid speciation in this taxon. As mentioned in the previous paragraph Auvinet et al (2018) performed an extensive phylogenetic and cytogenetic analyses evidencing a preferential accumulation of four families of DIRS1 in pericentromeric and centromeric regions in species of this genus but not in outgroups. This difference was attributed to the multiple glacial-interglacial cycles that occurred in Antarctic continental shelf.…”

Why did theTc1-like elements of mollusks acquired the spliceosomal introns?

“…An exposure to physical, chemical, and biological stressors can induce the TE transpositions. Genome instability due to the TE activity facilitates the origin of new features, which, in turn, can result in adaptations and future evolution (Yurchenko et al 2011;Piacentini et al 2014;Auvinet et al 2018).…”