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Tracing the History of LINE and SINE Extinction in Sigmodontine Rodents

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Tracing the History of LINE and SINE Extinction in Sigmodontine Rodents

Lei Yang et al. Mob DNA.

Abstract

Background: L1 retrotransposons have co-evolved with their mammalian hosts for the entire history of mammals and currently compose ~ 20% of a mammalian genome. B1 retrotransposons are dependent on L1 for retrotransposition and span the evolutionary history of rodents since their radiation. L1s were found to have lost their activity in a group of South American rodents, the Sigmodontinae, and B1 inactivation preceded the extinction of L1 in the same group. Consequently, a basal group of sigmodontines have active L1s but inactive B1s and a derived clade have both inactive L1s and B1s. It has been suggested that B1s became extinct during a long period of L1 quiescence and that L1s subsequently reemerged in the basal group.

Results: Here we investigate the evolutionary histories of L1 and B1 in the sigmodontine rodents and show that L1 activity continued until after the L1-extinct clade and the basal group diverged. After the split, L1 had a small burst of activity in the former group, followed by extinction. In the basal group, activity was initially low but was followed by a dramatic increase in L1 activity. We found the last wave of B1 retrotransposition was large and probably preceded the split between the two rodent clades.

Conclusions: Given that L1s had been steadily retrotransposing during the time corresponding to B1 extinction and that the burst of B1 activity preceding B1 extinction was large, we conclude that B1 extinction was not a result of L1 quiescence. Rather, the burst of B1 activity may have contributed to L1 extinction both by competition with L1 and by putting strong selective pressure on the host to control retrotransposition.

Conflict of interest statement

Competing interestsThe authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Phylogeny of the sigmodontine rodents. L1 and B1 activity displayed on the phylogeny shows that L1 extinction preceded that of B1. The phylogeny is based on Schenk et al. [57]. Taxa are the genera sampled; tribes are indicated on the right side of the taxa. Eight of the nine tribes and 12 of the 14 genera sampled by Rinehart et al. [52] are shown. L1 and B1 activity of each taxon is demonstrated by color: black, active L1 and B1; deep blue, active L1 and inactive B1; deep red, inactive L1 and inactive B1; light blue, L1 activity cannot be inferred; and, light red, L1 and B1 can be inferred to be inactive. “+” corresponds to active L1 and B1 and “o” corresponds to inactive L1 and B1
Fig. 2
Fig. 2
Phylogenies of L1 and B1 families. The phylogenies show species specificity of L1 and B1 families, and that S. hispidus-specific L1 families exist, but not B1 families. Panel a shows the L1 tree and b shows the B1 tree. To reflect divergence of the families, the trees were based on the distances between them. The distance between any two families was calculated by taking the average pairwise distance of the consensus sequences of subfamilies that belong to each family. Numbering of the L1 and B1 families is in chronological order of each element - similarly numbered L1 and B1 families do not necessarily correspond to the same time period
Fig. 3
Fig. 3
Divergence distribution of L1 families. L1 families were shared and had similar copy numbers in O. palustris and S. hispidus until just prior to the extinction of L1. L1 experienced a slow-down (middle left panel) in S. hispidus until it recovers (bottom panels - note that the copy number axis is 10x that of the top and middle panels). L1 families in each row are arranged in chronological order with the youngest families on the left. The species analyzed in each row is indicated at the right. Names of families are noted on the top of each panel. L1 copy number is plotted by percent divergence from the corresponding subfamily consensus in 1% bins. The divergence of each family is approximated by the peak of the distribution. L1 copy numbers are normalized as copies per three Gbp of MiSeq sequence which approximates the copy number per haploid genome. Panel a shows the shared families and panel b shows the Sigmodon-specific families. L1 and B1 families (in all figures) that correspond to similar divergence are given the same color and this color coding is consistent in all figures showing L1 and B1 divergence: L1-OS2, red; L1-OSP1, green; and, L1-OSP2, blue
Fig. 4
Fig. 4
Divergence distribution of B1 families. B1 families in each row are arranged in chronological order with the youngest families on the left. The species analyzed in each row is indicated at the right. Names of families are noted on the top of each panel. B1 copy number is plotted by percent divergence from the corresponding subfamily consensus in 1% windows. The divergence of each family is approximated by the peak of the distribution. B1 copy numbers are normalized as copies per three Gbp of MiSeq sequence which approximates the copy number per haploid genome. L1 and B1 families (in all figures) that correspond to similar divergence are given the same color and this color coding is consistent in all figures showing L1 and B1 divergence: B1-OS1, red; B1-OSP1, green; and, B1-OSP3, blue
Fig. 5
Fig. 5
Comparison of the divergence and copy numbers of L1 and B1 families. Curves represent the divergence distribution of L1 and B1 families based on kernel smoothing of the 1% divergence bin size histogram of the family. Vertical dashed lines represent the peaks of the distributions. L1 and B1 families (in all figures) that correspond to similar divergence are given the same color and this color coding is consistent in all figures showing L1 and B1 divergence: L1-OS2 and B1-OS1, red; L1-OSP1 and B1-OSP1, green; and, L1-OSP2 and B1-OSP3, blue. The oldest two S. hispidus-specific L1 families are also shown: L1-S5, black; L1-S4, brown. The top portion of the L1-S5 curve (above the horizontal black dashed line) is truncated for visualization purposes, but its peak coordinate is shown by the vertical black dashed line

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