Flying Around in the Genome: Characterization of LINE-1 in Chiroptera

Abstract

L1s are transposable elements that move by a copy-and-paste mechanism that continuously increases their copy number in the genome, such that each genome has a record of the L1 history in that host lineage. They make up about 20% of the genomes of eutherian mammals and have played a major role in shaping genome evolution. Chiroptera has the lowest average genome size among mammalian orders and the only documented case of L1 extinction affecting an entire mammalian family. Herein, L1 activity and extinction are characterized in all families of the order Chiroptera using a method that enriches for the youngest lineages of L1s in the genome. In addition to the previously reported L1 extinction in Pteropodidae, L1 extinction was documented to occur in Mormoops blainvilli, but this event did not affect all species of Mormoopidae. Further, there was no evidence of concordance between the evolution of L1s and their chiropteran host. There were two L1 lineages present before the divergence of all extant bats. Both lineages are extinct in the Pteropodidae. One or the other L1 lineage is extinct in almost all bat families, but Taphozous melanopogon maintains active members of both. Most intriguingly, some families within the Rhinolophoidea retain one active L1 lineage whereas other families retain the other, creating a deep discontinuity between L1 phylogeny and chiropteran phylogeny. These results indicate that there have been numerous losses of active L1 lineages over the history of chiropteran evolution, but that all chiropteran families except Pteropodidae have retained L1 activity.

Keywords: Chiroptera; L1; LINE-1; bat; evolution; phylogeny; retrotransposons; transposable elements.

Figure 1.

Structure of a typical mammalian L1. Full-length elements are ~7 kb in length and have four major segments: 5′ and 3′ untranslated regions (UTRs) and two open reading frames (ORFs). ORF1 has a 5′ hypervariable region (V) and ORF2 contains four conserved domains: endonuclease (E), an octapeptide-containing sequence (Z), reverse transcriptase (RT) and a RNase-H-like zinc finger (C). A G-rich polypurine tract (G) resides in the 3′ UTR and elements terminate with a poly-A tail. The region cloned for this study straddles the RT domain in ORF2 and was isolated by PCR with degenerate primers.

Figure 2.

Example L1 phylogenies of 20 elements from eight bat species. Taxa names have been removed; a black dot represents an L1 with an open reading frame across the region of analysis, indicating recent L1 activity. Terminal branch lengths reflect relative time since insertion. The trees demonstrate the variation in bat L1 evolutionary dynamics: single and multiple lineages as well as cessation of activity.

Figure 3.

Comparison of phylogénies of bat families and bat L1 lineages. Taxa from all 18 bat families are included. Colors indicate families and genera within superfamilial groups: Rhinolophoidea, red; Emballonuroidea, purple; Noctillonoidea, blue; and, Verpertillonoidea, green. A. Family tree of Chiroptera derived from Teeling et al. Figure 2 (2005), from a maximum-likelihood analysis of a 13.7 kb concatenated data set. B. Maximum likelihood free of L1s from the same genera as in tree A. Five L1s with open reading frames from each species plus reconstructed ancestral L1s from extinct lineages in Pteropus (Pteropus 1, Pteropus 2) and Mormoops (Mormoops 1 and Mormoops 2) are included in the analysis. Numbers at the nodes indicate majority rule bootstrap support values.

Figure 4.

An example of activity and extinction of two ancient L1 lineages mapped onto the phylogeny of Chiroptera. Colors of taxa names indicate families and genera within superfamilial groups: Rhinolophoidea, red; Emballonuroidea, purple; Noctillonoidea, blue; and, Verpertillonoidea, green. Vertical bars represent activity of L1 lineages in common ancestors and Xs indicate extinction events: lineage 1, red; lineage 2, blue. Numbers to the right of the taxa are the lineage(s) active in the corresponding genus.