Transposable elements in sexual and ancient asexual taxa

Abstract

Sexual reproduction allows deleterious transposable elements to proliferate in populations, whereas the loss of sex, by preventing their spread, has been predicted eventually to result in a population free of such elements [Hickey, D. A. (1982) Genetics 101, 519-531]. We tested this expectation by screening representatives of a majority of animal phyla for LINE-like and gypsy-like reverse transcriptases and mariner/Tc1-like transposases. All species tested positive for reverse transcriptases except rotifers of the class Bdelloidea, the largest eukaryotic taxon in which males, hermaphrodites, and meiosis are unknown and for which ancient asexuality is supported by molecular genetic evidence. Mariner-like transposases are distributed sporadically among species and are present in bdelloid rotifers. The remarkable lack of LINE-like and gypsy-like retrotransposons in bdelloids and their ubiquitous presence in other taxa support the view that eukaryotic retrotransposons are sexually transmitted nuclear parasites and that bdelloid rotifers evolved asexually.

Figure 1

Domain structure of RTases (A) and transposases (B) indicating regions targeted for nested PCR. Conserved domains are denoted by filled boxes, interdomain regions by lines. Domains A-E (4) correspond to RTase domains 3–7, respectively (5). For DNA transposases, two primers (I and II) cover conserved residues in the C-terminal domain. Single-feathered and double-feathered arrows indicate first- and second-step amplification primers, respectively. Filled bars represent second-step amplicons. Not to scale.

Figure 2

Nested PCR assays for (A and B) LINE-like or (C) gypsy-like RTases, and (D) mariner-like transposases. Twenty additional cycles of second-step amplification were done for B. Brackets indicate expected size ranges. Lane numbers correspond to species numbers in Table 1. Bdelloid rotifers are underlined. E, Escherichia coli; S, Saccharomyces cerevisiae.

Figure 3

Alignments of deduced (A) LINE-like RTase, (B) gypsy-like RTase, and (C) mariner-like transposase amino acid sequences with similarity to previously identified clades (–8); newly designated LINE-like clades Gia, Aca and Pla; or known mariner subfamilies (3). Except for primer sequences, which are not included, the regions of RTases and transposases depicted correspond to the filled bars in Fig. 1. Rotifer species are underlined, with bdelloids in red and other rotifers in green. All other RTase or transposase sequences we determined are in blue. Three LINE-like sequences and nine gypsy-like sequences contained stop codons and/or frame shifts (*, stop codon; #, frameshift). LINE-like sequences are shown in two separate groups, corresponding to their difference in the B-C distance. Clones within parentheses have identical nucleotide sequences. Dendrograms obtained by neighbor-joining illustrate sequence similarity. For comparison, sequences of two or three known members of each clade are included in black. (Scale bar: 10% amino acid difference.)