Evolutionary history of the mariner element galluhop in avian genomes

Abstract

Background: Transposable elements (TEs) are highly abundant genomic parasites in eukaryote genomes. Although several genomes have been screened for TEs, so far very limited information is available regarding avian TEs and their evolutionary histories. Taking advantage of the rich genomic data available for birds, we characterized the evolutionary history of the galluhop element, originally described in Gallus gallus, through the use of several bioinformatic analyses.

Results: galluhop homologous sequences were found in 6 of 72 genomes analyzed: 5 species of Galliformes (Gallus gallus, Meleagris gallopavo, Coturnix japonica, Colinus virginianus, Lyrurus tetrix) and one Buceritiformes (Buceros rhinoceros). The copy number ranged from 5 to 10,158, in the genomes of C. japonica and G. gallus respectively. All 6 species possessed short elements, suggesting the presence of Miniature Inverted repeats Transposable Elements (MITEs), which underwent an ancient massive amplification in the G. gallus and M. gallopavo genomes. Only 4 species showed potential MITE full-length partners, although no potential coding copies were detected. Phylogenetic analysis of reconstructed coding sequences showed that galluhop homolog sequences form a new mariner subfamily, which we termed Gallus. Inter-species and intragenomic galluhop distance analyses indicated a high identity between the consensus of B. rhinoceros and the other 5 related species, and different emergence ages of the element between the Galliformes species and B. rhinocerus, suggesting that horizontal transfer took place from Galliformes to a Buceritiformes ancestor, probably through an intermediate species.

Conclusions: Overall, our results showed that mariner elements have amplified to high copy numbers in some avian species, and that this transposition burst probably occurred in the common ancestor of G. gallus and M. gallopavo. In addition, although no coding sequences could be found currently, they probably existed, allowing an ancient massive MITE amplification in these 2 species. The other 4 species also have MITEs, suggesting that this new mariner family is prone to give rise to such non-autonomous derivatives. Last, our results suggest that a horizontal transfer event of a galluhop element occurred between Galliformes and Buceritiformes.

Keywords: Avian genome; Galluhop; Genomic parasites; Horizontal transfer; MITEs; Mariner.

Fig. 1

Schematic representation of the reconstructed galluhop copies compared to the galluhop consensus. Regions of terminal inverted repeats shown in red, transposase coding region in light gray, and insertion region in dark gray. Order Galliformes: four genomes (G. gallus, M. gallopavo, C. virginianus and L. tetrix) showed potential complete partners although there are no potential coding copies, and C. japonica showed short elements. Order Bucerotiformes: B. rhinoceros showed only short elements

Fig. 2

Phylogeny of mariner-like transposases. Phylogeny of mariner-like transposases, by maximum likelihood using PHYML (Guindon and Gascuel 2003). Clade colors denote the different subfamilies of the mariner family, indicated to the left of the tree. In gray: the new subfamily, Gallus

Fig. 3

Amplification dynamics of elements within each genome in million of years. a Intragenomic dating of copies found in G. gallus and M. gallopavo. b Intragenomic dating of copies found in B. rhinocerus, C. virginianus and L. tetrix

Fig. 4

Density plot of Kimura 2 parameter distance between B. rhinocerus and L. tetrix. K2P distance of 50 single-copy orthologous genes (gray shading) and consensus TEs (red arrow)

Fig. 5

Horizontal Transfer hypothesis of galluhop elements. Chronogram TENT avian tree from Jarvis et al. [42] with the addition of probable L. tetrix positioning and split data following TimeTree data [44] Red branches denote the evolutionary hypothesis of the Gallus subfamily vertical evolution in the Galliformes, and horizontal transfer from L. tetrix to B. rhinoceros ancestors. X bar below the tree denotes the time in millions of years. Number close to nodes are the mean estimate of ancestors and blue bars are 95% credible interval as estimated by Jarvis et al [42]