High intrinsic: Rate of DNA loss in Drosophila

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Nature (Impact Factor: 42.35). 12/1996; 384(6607):346-9. DOI: 10.1038/384346a0
Source: PubMed

ABSTRACT Pseudogenes are common in mammals but virtually absent in Drosophila. All putative Drosophila pseudogenes show patterns of molecular evolution that are inconsistent with the lack of functional constraints. The absence of bona fide pseudogenes is not only puzzling, it also hampers attempts to estimate rates and patterns of neutral DNA change. The estimation problem is especially acute in the case of deletions and insertions, which are likely to have large effects when they occur in functional genes and are therefore subject to strong purifying selection. We propose a solution to this problem by taking advantage of the propensity of retrotransposable elements without long terminal repeats (non-LTR) to create non-functional, 'dead-on-arrival' copies of themselves as a common by-product of their transpositional cycle. Phylogenetic analysis of a non-LTR element, Helena, demonstrates that copies lose DNA at an unusually high rate, suggesting that lack of pseudogenes in Drosophila is the product of rampant deletion of DNA in unconstrained regions. This finding has important implications for the study of genome evolution in general and the 'C-value paradox' in particular.

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    • "In Cryptobranchus, as in plethodontid salamanders, slower rates of DNA loss reflect fewer and smaller deletion events per substitution than are found in other vertebrate taxa (Sun, Arriaza, et al. 2012). Indels 30 bp in length have long been attributed to uncharacterized errors in DNA replication and/or recombination (Petrov et al. 1996; Kvikstad et al. 2007). Recently, comparative genomic analyses have begun to leverage natural variation in indel dynamics, across both genomes and lineages , to reveal the specific mechanisms of indel formation (Kvikstad et al. 2007, 2009; Hu et al. 2011; Nam and Ellegren 2012). "
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    ABSTRACT: Among animals, genome sizes range from 20 Mb to 130 Gb, with 380-fold variation across vertebrates. Most of the largest vertebrate genomes are found in salamanders, an amphibian clade of 660 species. Thus, salamanders are an important system for studying causes and consequences of genomic gigantism. Previously, we showed that plethodontid salamander genomes accumulate higher levels of LTR retrotransposons than do other vertebrates, although the evolutionary origins of such sequences remained unexplored. We also showed that some salamanders in the family Plethodontidae have relatively slow rates of DNA loss through small insertions and deletions. Here, we present new data from Cryptobranchus alleganiensis, the hellbender. Cryptobranchus and Plethodontidae span the basal phylogenetic split within salamanders; thus, analyses incorporating these taxa can shed light on the genome of the ancestral crown salamander lineage, which underwent expansion. We show that high levels of LTR retrotransposons likely characterize all crown salamanders, suggesting that disproportionate expansion of this TE class contributed to genomic expansion. Phylogenetic and age distribution analyses of salamander LTR retrotransposons indicate that salamanders' high TE levels reflect persistence and diversification of ancestral TEs rather than horizontal transfer events. Finally, we show that relatively slow DNA loss rates through small indels likely characterize all crown salamanders, suggesting that a decreased DNA loss rate contributed to genomic expansion at the clade's base. Our identification of shared genomic features across phylogenetically distant salamanders is a first step towards identifying the evolutionary processes underlying accumulation and persistence of high levels of repetitive sequence in salamander genomes.
    Genome Biology and Evolution 06/2014; 6(7). DOI:10.1093/gbe/evu143 · 4.53 Impact Factor
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    • "It is possible that a mutator allele may have become fixed in the inbred ancestor of these lines. We also detected small deletion events only (i.e., no small insertions), consistent with the deletion bias that has been observed among small indel events in Drosophila (Petrov et al. 1996; Haag-Liautard et al. 2007). "
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    ABSTRACT: We employed deep genome sequencing of two parents and 12 of their offspring to estimate the mutation rate per site per generation in a full-sib family of Drosophila melanogaster recently sampled from a natural population. Sites that were homozygous for the same allele in the parents and heterozygous in one or more offspring were categorized as candidate mutations and subjected to detailed analysis. In 1.23 x 10(9) callable sites from 12 individuals, we confirmed six single nucleotide mutations. We estimated the false negative rate in the experiment by generating synthetic mutations using the empirical distributions of numbers of non-reference bases at heterozygous sites in the offspring. The proportion of synthetic mutations at callable sites that we failed to detect was less than 1%, implying that the false negative rate was extremely low. Our estimate of the point mutation rate is 2.8 x 10(-9) (95% confidence interval = 1.0 x 10(-9) - 6.1 x 10(-9)) per site per generation, which is at the low end of the range of previous estimates, and suggests an effective population size for the species of ~1.4 x 10(6). At one site, point mutations were present in two individuals, indicating that there had been a premeiotic mutation cluster, although surprisingly one individual had a G→A transition and the other a G→T transversion, possibly associated with error-prone mismatch repair. We also detected three short deletion mutations and no insertions giving a deletion mutation rate of 1.2 x 10(-9) (95% confidence interval = 0.7 x 10(-9) - 11 x 10(-9)).
    Genetics 11/2013; 196(1). DOI:10.1534/genetics.113.158758 · 4.87 Impact Factor
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    • "Earlier, it was thought that retrogenes are usually processed pseudogenes (Jeffs & Ashburner, 1991; Petrov et al., 1996). But during the late 1980s, abundant retrogenes having intriguing novel functions have been reported (McCarrey & Thomas, 1987). "
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    ABSTRACT: The origination of new genes is an important process for evolutionary innovation. These genes often provide novel and adaptive functions. Every evolutionary lineage harbors new genes. However, the origination of these genes at the functional level is still poorly understood. New genes could arise from duplication or rearrangement processes of existing genes or part of genes as well as from non coding genomic regions. These processes appear to give rise to new genes which result in the generation of genetic novelties during the evolution of an organism.
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