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Genome Biol Evol
2012 Jan 01;412:1340-8. doi: 10.1093/gbe/evs103.
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Slow DNA loss in the gigantic genomes of salamanders.
Sun C, López Arriaza JR, Mueller RL.
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Evolutionary changes in genome size result from the combined effects of mutation, natural selection, and genetic drift. Insertion and deletion mutations (indels) directly impact genome size by adding or removing sequences. Most species lose more DNA through small indels (i.e., ~1-30 bp) than they gain, which can result in genome reduction over time. Because this rate of DNA loss varies across species, small indel dynamics have been suggested to contribute to genome size evolution. Species with extremely large genomes provide interesting test cases for exploring the link between small indels and genome size; however, most large genomes remain relatively unexplored. Here, we examine rates of DNA loss in the tetrapods with the largest genomes-the salamanders. We used low-coverage genomic shotgun sequence data from four salamander species to examine patterns of insertion, deletion, and substitution in neutrally evolving non-long terminal repeat (LTR) retrotransposon sequences. For comparison, we estimated genome-wide DNA loss rates in non-LTR retrotransposon sequences from five other vertebrate genomes: Anolis carolinensis, Danio rerio, Gallus gallus, Homo sapiens, and Xenopus tropicalis. Our results show that salamanders have significantly lower rates of DNA loss than do other vertebrates. More specifically, salamanders experience lower numbers of deletions relative to insertions, and both deletions and insertions are skewed toward smaller sizes. On the basis of these patterns, we conclude that slow DNA loss contributes to genomic gigantism in salamanders. We also identify candidate molecular mechanisms underlying these differences and suggest that natural variation in indel dynamics provides a unique opportunity to study the basis of genome stability.
Fig.
1.—. Overall DNA loss rates from nine vertebrate genomes.
Salamanders lose DNA more slowly than do other vertebrates.
Fig. 2.—. DNA
loss rate estimates for individual non-LTR element copies. All species show
heterogeneous rates of DNA loss across the genome. Outliers are excluded from plot
to allow visualization of data. Element sequences are different lengths and include
variable numbers of indels. Lower variance in salamanders may reflect smaller data
sets for these taxa.
Fig.
3.—. Proportion of total numbers of deletion events (top)
and insertion events (bottom) that create indels of different size categories.
Salamanders are outlined in red; other vertebrates are solid colors. Salamanders
have higher relative numbers of the smallest (i.e., 1–5 bp) insertions and
deletions.
Fig. 4.—. DNA loss rates
calculated for indels of different size categories. Salamanders are outlined in red;
other vertebrates are solid colors. Salamanders lose less DNA/substitution than
Xenopus tropicalis, Gallus gallus, and
Danio rerio across all indel size categories. Homo
sapiens and Anolis carolinensis each show DNA loss rate
overlap with salamanders in at least one indel size category. Batrachoseps
nigriventris and Desmognathus ochrophaeus gain more DNA
than they lose for indels 1–5 bp in length.
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