Intrapopulation Genome Size Variation in D. melanogaster Reflects Life History Variation and Plasticity

Ellis, Lisa L.; Huang, Wen; Quinn, Andrew; Ahuja, Astha; Alfrejd, Ben; Gomez, Francisco E.; Hjelmen, Carl E.; Moore, Kristi L.; Mackay, Trudy F. C.; Johnston, J. Spencer; Tarone, Aaron M.

doi:10.1371/journal.pgen.1004522

Cited by 62 publications

(64 citation statements)

References 55 publications

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“…Therefore, the deleterious effect of an increase in one satellite DNA group can be alleviated by a decrease in a different group. This load may be determined by the fitness benefits of maintaining an optimal genome size (24), but we find this unlikely given the variability of genome sizes among as well as within species (54) and that total kmer quantities differ greatly between lines. Alternatively, the load may be chromosome-specific, as satellite DNAs often have chromosome-specific distributions.…”

Section: Discussionmentioning

confidence: 83%

Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster

Wei

Grenier

Barbash

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

145

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Tandemly repeating satellite DNA elements in heterochromatin occupy a substantial portion of many eukaryotic genomes. Although often characterized as genomic parasites deleterious to the host, they also can be crucial for essential processes such as chromosome segregation. Adding to their interest, satellite DNA elements evolve at high rates; among Drosophila, closely related species often differ drastically in both the types and abundances of satellite repeats. However, due to technical challenges, the evolutionary mechanisms driving this rapid turnover remain unclear. Here we characterize natural variation in simple-sequence repeats of 2-10 bp from inbred Drosophila melanogaster lines derived from multiple populations, using a method we developed called k-Seek that analyzes unassembled Illumina sequence reads. In addition to quantifying all previously described satellite repeats, we identified many novel repeats of low to medium abundance. Many of the repeats show population differentiation, including two that are present in only some populations. Interestingly, the population structure inferred from overall satellite quantities does not recapitulate the expected population relationships based on the demographic history of D. melanogaster. We also find that some satellites of similar sequence composition are correlated across lines, revealing concerted evolution. Moreover, correlated satellites tend to be interspersed with each other, further suggesting that concerted change is partially driven by higher order structure. Surprisingly, we identified negative correlations among some satellites, suggesting antagonistic interactions. Our study demonstrates that current genome assemblies vastly underestimate the complexity, abundance, and variation of highly repetitive satellite DNA and presents approaches to understand their rapid evolutionary divergence.satellite DNA | population differentiation | rapid evolution H eterochromatin occupies a substantial portion of most eukaryotic genomes and contains vast quantities of tandemly repeating, noncoding DNA elements known as satellite DNA. These sequences, along with transposable elements, are often described as selfish elements or genomic parasites, as they can increase their copy numbers irrespective of host fitness (1, 2). Indeed, they can be highly deleterious for the host genome; for example, ectopic recombination between homologous satellite repeats can lead to devastating chromosomal rearrangements (3, 4). Consequently, these elements are mostly sequestered in repressive chromatin environments around the centromeres and telomeres where there is minimal recombination and transcriptional activity. However, paradoxically, repetitive sequences are also crucial components of euchromatic genomes, as they recruit the centromeric histone H3 variant to form centromeres in many species (5, 6), thereby affecting the fidelity of chromosome segregation (7,8).Adding to the perplexity, satellite DNA turns over at remarkably high rates between species (9, 10). In Drosophila mel...

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Section: Discussionmentioning

confidence: 83%

Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster

Wei

Grenier

Barbash

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

145

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“…S4; Supplemental Data File S8). Genome size differences were verified by the presence of double peaks in copreparations from lines with different average genome size (Ellis et al 2014). The mean genome size of all lines (175.6 Mb) is close to that of the reference strain (175 Mb).…”

Section: Variation In Genome Sizementioning

confidence: 83%

Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines

et al. 2014

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The Drosophila melanogaster Genetic Reference Panel (DGRP) is a community resource of 205 sequenced inbred lines, derived to improve our understanding of the effects of naturally occurring genetic variation on molecular and organismal phenotypes. We used an integrated genotyping strategy to identify 4,853,802 single nucleotide polymorphisms (SNPs) and 1,296,080 non-SNP variants. Our molecular population genomic analyses show higher deletion than insertion mutation rates and stronger purifying selection on deletions. Weaker selection on insertions than deletions is consistent with our observed distribution of genome size determined by flow cytometry, which is skewed toward larger genomes. Insertion/ deletion and single nucleotide polymorphisms are positively correlated with each other and with local recombination, suggesting that their nonrandom distributions are due to hitchhiking and background selection. Our cytogenetic analysis identified 16 polymorphic inversions in the DGRP. Common inverted and standard karyotypes are genetically divergent and account for most of the variation in relatedness among the DGRP lines. Intriguingly, variation in genome size and many quantitative traits are significantly associated with inversions. Approximately 50% of the DGRP lines are infected with Wolbachia, and four lines have germline insertions of Wolbachia sequences, but effects of Wolbachia infection on quantitative traits are rarely significant. The DGRP complements ongoing efforts to functionally annotate the Drosophila genome. Indeed, 15% of all D. melanogaster genes segregate for potentially damaged proteins in the DGRP, and genome-wide analyses of quantitative traits identify novel candidate genes. The DGRP lines, sequence data, genotypes, quality scores, phenotypes, and analysis and visualization tools are publicly available.[Supplemental material is available for this article.]Studies in Drosophila melanogaster have revealed basic principles and mechanisms underlying fundamental genetic concepts of linkage and recombination and were instrumental in identifying canonical and evolutionarily conserved cell signaling pathways.Most D. melanogaster genes are evolutionarily conserved, leading to fly models for understanding common human diseases and behavioral disorders, dipteran disease vectors, and insects impacting agriculture, medicine, and forensics. Despite nearly a century of research on D. melanogaster, however, a large fraction of its coding and noncoding sequence has no known function (McQuilton et al. 2012). Recent efforts to induce mutations in every protein coding gene utilize transposable elements (Bellen et al. 2004(Bellen et al. , 2011, which have a different spectrum of allelic effects than SNPs and small insertions and deletions (indels). Comprehensive efforts to identify regulatory DNA elements in Drosophila (The Ó 2014 Huang et al.

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“…The DGRP strains are characterized by high genetic (Mackay et al., 2012; Massouras et al., 2012) and phenotypic variation (Ayroles et al., 2009; Durham, Magwire, Stone, & Leips, 2014; Ellis et al., 2014; Harbison, McCoy, & Mackay, 2013; Mackay et al., 2012; Unckless, Rottschaefer, & Lazzaro, 2015). Fly stocks were ordered from the Bloomington Stock Center and are kept in standard molasses/soy‐corn flour/agar media‐containing vials.…”

Section: Methodsmentioning

confidence: 99%

Effects of larval crowding on quantitative variation for development time and viability in Drosophila melanogaster

Hórvath

Kalinka

2016

Ecology and Evolution

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Competition between individuals belonging to the same species is a universal feature of natural populations and is the process underpinning organismal adaptation. Despite its importance, still comparatively little is known about the genetic variation responsible for competitive traits. Here, we measured the phenotypic variation and quantitative genetics parameters for two fitness‐related traits—egg‐to‐adult viability and development time—across a panel of Drosophila strains under varying larval densities. Both traits exhibited substantial genetic variation at all larval densities, as well as significant genotype‐by‐environment interactions (GEIs). GEI was attributable to changes in the rank order of reaction norms for both traits, and additionally to differences in the between‐line variance for development time. The coefficient of genetic variation increased under stress conditions for development time, while it was higher at both high and low densities for viability. While development time also correlated negatively with fitness at high larval densities—meaning that fast developers have high fitness—there was no correlation with fitness at low density. This result suggests that GEI may be a common feature of fitness‐related genetic variation and, further, that trait values under noncompetitive conditions could be poor indicators of individual fitness. The latter point could have significant implications for animal and plant breeding programs, as well as for conservation genetics.

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Intrapopulation Genome Size Variation in D. melanogaster Reflects Life History Variation and Plasticity

Cited by 62 publications

References 55 publications

Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster

Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster

Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines

Effects of larval crowding on quantitative variation for development time and viability in Drosophila melanogaster

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