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. 2021 Nov 26;12(1):27.
doi: 10.1186/s13100-021-00254-y.

Population analysis of retrotransposons in giraffe genomes supports RTE decline and widespread LINE1 activity in Giraffidae

Malte Petersen  1 , Sven Winter  2 , Raphael Coimbra  2   3 , Menno J de Jong  2 , Vladimir V Kapitonov  2   4 , Maria A Nilsson  5   6
Affiliations

Population analysis of retrotransposons in giraffe genomes supports RTE decline and widespread LINE1 activity in Giraffidae

Malte Petersen et al. Mob DNA. .

Abstract

Background: The majority of structural variation in genomes is caused by insertions of transposable elements (TEs). In mammalian genomes, the main TE fraction is made up of autonomous and non-autonomous non-LTR retrotransposons commonly known as LINEs and SINEs (Long and Short Interspersed Nuclear Elements). Here we present one of the first population-level analysis of TE insertions in a non-model organism, the giraffe. Giraffes are ruminant artiodactyls, one of the few mammalian groups with genomes that are colonized by putatively active LINEs of two different clades of non-LTR retrotransposons, namely the LINE1 and RTE/BovB LINEs as well as their associated SINEs. We analyzed TE insertions of both types, and their associated SINEs in three giraffe genome assemblies, as well as across a population level sampling of 48 individuals covering all extant giraffe species.

Results: The comparative genome screen identified 139,525 recent LINE1 and RTE insertions in the sampled giraffe population. The analysis revealed a drastically reduced RTE activity in giraffes, whereas LINE1 is still actively propagating in the genomes of extant (sub)-species. In concert with the extremely low activity of the giraffe RTE, we also found that RTE-dependent SINEs, namely Bov-tA and Bov-A2, have been virtually immobile in the last 2 million years. Despite the high current activity of the giraffe LINE1, we did not find evidence for the presence of currently active LINE1-dependent SINEs. TE insertion heterozygosity rates differ among the different (sub)-species, likely due to divergent population histories.

Conclusions: The horizontally transferred RTE/BovB and its derived SINEs appear to be close to inactivation and subsequent extinction in the genomes of extant giraffe species. This is the first time that the decline of a TE family has been meticulously analyzed from a population genetics perspective. Our study shows how detailed information about past and present TE activity can be obtained by analyzing large-scale population-level genomic data sets.

Keywords: BovB; Genome; Giraffe; LINE; LINE1/L1; Non-LTR retrotransposons; RTE; Ruminantia; SINE; Structural variation; TE; Transposable elements.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
LINE1 and RTE have different activity in giraffe genomes. A Repeat Landscape of the Northern Kordofan giraffe genome showing the distribution of LINE1 (dark blue) and RTE (brown) genomic percentage across the Kimura (K2P) distance to the TE consensus sequence. DNA transposons are orange, and LTRs are green. B Heterozygous (0/1, blue) and homozygous (1/1, green) L1-1_Gir insertions per subspecies. C Number of LINE1 and RTE insertions per subspecies next to the giraffe phylogeny. The giraffe species names are indicated on the internal branches of the phylogeny
Fig. 2
Fig. 2
Phylogenetic incongruence of TE insertions across the giraffe species complex. NeighborNet network and UpSet plot showing the supporting TE insertions for different nodes in the giraffe data set. 2270 insertions (blue) support the grouping of the four species. Each species is supported by between 1535 (southern) to 821 (northern) unique insertions. 839 insertions (green) support northern and reticulated giraffe and 414 insertions (orange) support Masai and southern giraffe. 307 insertions (red) support the clustering of northern, Masai, and reticulated giraffe. The branch of the outgroup okapi has been shortened. See Fig. S5 for the NeighborNet tree with individual names
Fig. 3
Fig. 3
TE heterozygosity differs across giraffe lineages. Higher proportions of heterozygous TE-insertions are observed in the lineages leading to northern and reticulated giraffes compared to lineages leading to southern and Masai giraffe. A UPGMA-tree based on a 9.4 K TE-dataset, showing the node numbers referred to in (B). B Barplot showing the number of homozygous (1/1, green) and heterozygous (0/1, yellow) TE-insertions inferred per node. Values above the bars indicate the percentage of heterozygous insertions (Table S6). Giraffe images by Jón Baldur Hlíðberg
Fig. 4
Fig. 4
A comparison between population-genetic inferences from TE and SNP data. TE-based population differentiation and genetic diversity estimates are generally in agreement with SNP-based inferences, except for the northern (Nubian, Kordofan and West African) giraffes. A Principal component analyses using a 48 K SNP dataset. B Idem, using a 9.4 K TE dataset. C Scatterplot showing sample specific heterozygosity estimates inferred from a 9.4 K TE dataset (y-axis) against genome-wide heterozygosity estimates (x-axis) reported by Coimbra et al. (2021). D Scatterplot showing Nei’s genetic distance estimates between subspecies inferred from a 9.4 K TE dataset (y-axis) against estimates inferred from a 48 K SNP dataset (x-axis). Color-coding follows the phylogeny in Fig. 3
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