Lizards and LINEs: selection and demography affect the fate of L1 retrotransposons in the genome of the green anole (Anolis carolinensis)

Abstract

Autonomous retrotransposons lacking long terminal repeats (LTR) account for much of the variation in genome size and structure among vertebrates. Mammalian genomes contain hundreds of thousands of non-LTR retrotransposon copies, mostly resulting from the amplification of a single clade known as L1. The genomes of teleost fish and squamate reptiles contain a much more diverse array of non-LTR retrotransposon families, whereas copy number is relatively low. The majority of non-LTR retrotransposon insertions in nonmammalian vertebrates also appear to be very recent, suggesting strong purifying selection limits the accumulation of non-LTR retrotransposon copies. It is however unclear whether this turnover model, originally proposed in Drosophila, applies to nonmammalian vertebrates. Here, we studied the population dynamics of L1 in the green anole lizard (Anolis carolinensis). We found that although most L1 elements are recent in this genome, truncated insertions accumulate readily, and many are fixed at both the population and species level. In contrast, full-length L1 insertions are found at lower population frequencies, suggesting that the turnover model only applies to longer L1 elements in Anolis. We also found that full-length L1 inserts are more likely to be fixed in populations of small effective size, suggesting that the strength of purifying selection against deleterious alleles is highly dependent on host demographic history. Similar mechanisms seem to be controlling the fate of non-LTR retrotransposons in both Anolis and teleostean fish, which suggests that mammals have considerably diverged from the ancestral vertebrate in terms of how they interact with their intragenomic parasites.

Keywords: Anolis carolinensis; green anole; non-LTR retrotransposon; population genomics.

Fig. 1.—

Neighbor-joining phylogenetic tree depicting the evolutionary relationships between the ORF2 consensus sequences of the 20 L1 families found in the Anolis genome. Node support was assessed with 1,000 bootstrap replicates (greater than 95% is shown). Tips are labeled with the L1 family name and within each parenthesis are the copy number and percent pair wise divergence from consensus sequence as reported in Novick et al. (2009).

Fig. 2.—

The geographic distribution of localities from which the green anole samples used in this study were collected is indicated by solid black circles. The geographic distribution of the five major evolutionary lineages of green anoles, summarized from Tollis et al. (2012) and Campbell-Staton et al. (2012) is indicated by colored polygons: Everglades (magenta), Suwannee (blue), Central Florida (brown), Gulf–Atlantic (green), and North Carolina (yellow).

Fig. 3.—

Number of fixed and polymorphic L1 elements extrapolated from population data according to their divergence from consensus.

Fig. 4.—

Fraction of polymorphic and fixed L1 elements according to their length in green anole populations. The distribution is based on 52 L1-containing loci retrieved from the Anolis genome database.

Fig. 5.—

The frequency distributions of FL and TR L1 elements in five green anole populations.