Strain evolution in Caenorhabditis elegans: Transposable elements as markers of interstrain evolutionary history

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Evolutionary relationships across taxa can be deduced from sequence divergence of proteins, RNA, or DNA; sequences which diverge rapidly, such as those of mitochondrial genes, have been especially useful for comparisons of closely related species, and--within limits--of strains within a species. We have utilized the transposable element Tc1 as a polymorphic marker to evaluate the evolutionary relationships among nine Caenorhabditis elegans strains. For five low-Tc1-copy strains, we compared patterns of restriction fragments hybridizing to a cloned Tc1 probe. Twenty of the 40 Tc1 insertion sites thus characterized were common to all five strains, and so presumably preceded strain divergence; the 20 differential bands were used to construct a maximum-parsimony tree relating these strains. In four high-copy-number stocks (three wild-type strains and a subline), we determined occupancy of 35 individual Tc1 insertion sites by a polymerase chain reaction assay. Surprisingly, the high-copy strains share a common subset of these Tc1 insertions, and the chromosomal distribution of conserved Tc1 sites is "clustered" with respect to the other elements tested. These data imply a close evolutionary relationship among the high-copy strains, such that two of these strains appear to have been derived from the highest-copy-number lineage (represented by two stocks) through crossing with a low-Tc1 strain. Abundances of Tc1 elements were also estimated for the four high-copy-number stocks, at approximately 200-500 copies per haploid genome, by quantitative dot-blot hybridization relative to two low-copy strains. Annealing with 32P-labeled probes corresponding to full-length Tc1, an oligonucleotide within the Tc1 terminal inverted repeats, and an internal Tc1 oligonucleotide, gave essentially identical results--indicating that Tc1 termini exist in the genome primarily as components of full-length Tc1 elements. A composite evolutionary tree is proposed, based on the locations and numbers of Tc1 elements in these strains, which is consistent with a four-branch intraspecific tree deduced previously by maximum-parsimony analyses of mitochondrial sequence changes; it also serves to elucidate the evolutionary history of transposon mobility.