A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence

We create a new assembly of the Drosophila simulans genome using 142 million paired short-read sequences and previously published data for strain w501. Our assembly represents a higher-quality genomic sequence with greater coverage, fewer misassemblies, and, by several indexes, fewer sequence errors. Evolutionary analysis of this genome reference sequence reveals interesting patterns of lineage-specific divergence that are different from those previously reported. Specifically, we find that Drosophila melanogaster evolves faster than D. simulans at all annotated classes of sites, including putatively neutrally evolving sites found in minimal introns. While this may be partly explained by a higher mutation rate in D. melanogaster, we also find significant heterogeneity in rates of evolution across classes of sites, consistent with historical differences in the effective population size for the two species. Also contrary to previous findings, we find that the X chromosome is evolving significantly faster than autosomes for nonsynonymous and most noncoding DNA sites and significantly slower for synonymous sites. The absence of a X/A difference for putatively neutral sites and the robustness of the pattern to Gene Ontology and sex-biased expression suggest that partly recessive beneficial mutations may comprise a substantial fraction of noncoding DNA divergence observed between species. Our results have more general implications for the interpretation of evolutionary analyses of genomes of different quality.

• Publication year

  2013

• Venue

  Genome Research

• Publication date

  2013-01-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1101/gr.141689.112PMID 22936249PMCID 3530686
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A Comparison of Models to Infer the Distribution of Fitness Effects of New Mutations

  2013cited by this paper
• The Drosophila melanogaster Genetic Reference Panel

  2012cited by this paper
• A Population Genetics-Phylogenetics Approach to Inferring Natural Selection in Coding Sequences

  2011cited by this paper
• Repetitive DNA and next-generation sequencing: computational challenges and solutions

  2011cited by this paper
• Whole-genome sequencing of multiple Arabidopsis thaliana populations

  2011cited by this paper
• Correlated Evolution of Nearby Residues in Drosophilid Proteins

  2011cited by this paper
• Multiplexed shotgun genotyping for rapid and efficient genetic mapping.

  2011influential reference
• On the utility of short intron sequences as a reference for the detection of positive and negative selection in Drosophila.

  2010influential reference
• Quake: quality-aware detection and correction of sequencing errors

  2010cited by this paper
• Molecular population genomics: a short history.

  2010cited by this paper
• A map of human genome variation from population-scale sequencing

  2010cited by this paper
• EFFECTIVE POPULATION SIZE AND THE FASTER‐X EFFECT: EMPIRICAL RESULTS AND THEIR INTERPRETATION

  2010cited by this paper
• Effective Population Size and the Efficacy of Selection on the X Chromosomes of Two Closely Related Drosophila Species

  2010cited by this paper
• Phenotypic connections in surprising places

  2010cited by this paper
• The Sequence Alignment/Map format and SAMtools

  2009influential reference
• Fast Statistical Alignment

  2009cited by this paper
• Effective population size and patterns of molecular evolution and variation

  2009cited by this paper
• Genetic recombination and molecular evolution.

  2009cited by this paper
• Positive and negative selection on noncoding DNA in Drosophila simulans.

  2008influential reference
• Velvet: algorithms for de novo short read assembly using de Bruijn graphs.

  2008influential reference
• The Impact of Natural Selection on the Genome: Emerging Patterns in Drosophila and Arabidopsis

  2008cited by this paper
• The distribution of fitness effects of new mutations

  2007cited by this paper
• Evolution of genes and genomes on the Drosophila phylogeny

  2007influential reference
• Codon usage in twelve species of Drosophila

  2007cited by this paper
• Constraint and turnover in sex-biased gene expression in the genus Drosophila

  2007cited by this paper
• Genome-scale analysis of positionally relocated genes.

  2007cited by this paper
• Demasculinization of X chromosomes in the Drosophila genus

  2007cited by this paper
• PAML 4: phylogenetic analysis by maximum likelihood.

  2007cited by this paper
• Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans

  2007cited by this paper
• Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison.

  2006cited by this paper
• Maximum likelihood estimation of ancestral codon usage bias parameters in Drosophila.

  2006cited by this paper
• Evolution on the X chromosome: unusual patterns and processes

  2006influential reference
• Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression

  2006influential reference
• The Distribution of Fitness Effects of New Deleterious Amino Acid Mutations in Humans

  2006cited by this paper
• Adaptive evolution of non-coding DNA in Drosophila

  2005influential reference
• MUSCLE: a multiple sequence alignment method with reduced time and space complexity

  2004cited by this paper
• Versatile and open software for comparing large genomes

  2004influential reference
• Effective population size.

  2002influential reference
• BLAT--the BLAST-like alignment tool.

  2002cited by this paper
• Adaptive protein evolution in Drosophila

  2002cited by this paper
• Testing the neutral theory of molecular evolution with genomic data from Drosophila

  2002influential reference
• The frequency distribution of nucleotide variation in Drosophila simulans.

  2001cited by this paper
• SSAHA: a fast search method for large DNA databases.

  2001influential reference
• Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans.

  2001cited by this paper
• Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila.

  2001cited by this paper
• Comparative Genomics of Mitochondrial DNA in Members of the Drosophila melanogaster Subgroup

  2000cited by this paper
• Patterns of nucleotide substitution in Drosophila and mammalian genomes.

  1999cited by this paper
• Natural selection and the frequency distributions of "silent" DNA polymorphism in Drosophila.

  1997cited by this paper
• Intraspecific nuclear DNA variation in Drosophila.

  1996cited by this paper
• Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster.

  1996cited by this paper
• Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA.

  1995influential reference
• Amino acid substitution at the Adh locus of Drosophila is facilitated by small population size.

  1993cited by this paper
• The effect of deleterious mutations on neutral molecular variation.

  1993cited by this paper
• The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence.

  1988cited by this paper
• The Relative Rates of Evolution of Sex Chromosomes and Autosomes

  1987cited by this paper
• Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora)

  1984cited by this paper
• The positive and the negative

  1983influential reference
• The neutral theory of molecular evolution.

  1983cited by this paper
• Evolution of Protein Molecules

  1979cited by this paper
• Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) - II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences

  1976cited by this paper
• Slightly Deleterious Mutant Substitutions in Evolution

  1973cited by this paper
• CHAPTER 24 – Evolution of Protein Molecules

  1969cited by this paper
• Mammalian protein metabolism

  1964cited by this paper

• An RNAi-based platform for spatiotemporal control of histone gene expression during animal development

  2026cites this paper
• Gene model for the ortholog of Glys in Drosophila simulans

  2025cites this paper
• Dichotomous transcriptome divergence at the cell-type level between the Drosophila male and female germlines

  2025cites this paper
• Adaptive gene expression parallelism in the male reproductive tract of two Drosophila species.

  2025cites this paper
• Nested likelihood-ratio testing of the nonsynonymous:synonymous ratio suggests greater adaptation in the piRNA machinery of Drosophila melanogaster compared with Drosophila ananassae and Drosophila willistoni, two species with higher repeat content

  2025cites this paper
• An RNAi-based platform for spatiotemporal control of histone gene expression during animal development

  2025cites this paper
• Comparative analysis of Wolbachia maternal transmission and localization in host ovaries

  2024cites this paper
• Two major-effect loci influence interspecific mating in females of the sibling species, Drosophila simulans and D. sechellia

  2024cites this paper
• Two major-effect loci influence assortative mating in females of the sibling species, Drosophila simulans and D. sechellia

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• Comparative analysis of Wolbachia maternal transmission and localization in host ovaries

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  2024cites this paper
• Chromosome-scale genome of the polyphagous pest Anastrepha ludens (Diptera: Tephritidae) provides insights on sex chromosome evolution in Anastrepha.

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• IntroUNET: Identifying introgressed alleles via semantic segmentation

  2024cites this paper
• Selection efficacy differs between lifestages in the haploid-diploid Marchantia polymorpha subsp. ruderalis

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• The influence of GC-biased gene conversion on nonadaptive sequence evolution in short introns of Drosophila melanogaster

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• Evolutionary conservation and diversification of auditory neural circuits that process courtship songs in Drosophila

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  2022cites this paper
• Testing the Drosophila maternal haploid gene for functional divergence and a role in hybrid incompatibility

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• Responses of different Drosophila species to temperature changes.

  2022cites this paper
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• Greater strength of selection and higher proportion of beneficial amino acid changing mutations in humans compared with mice and Drosophila melanogaster

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• Drosophila Evolution over Space and Time (DEST): A New Population Genomics Resource

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  2021cites this paper
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  2020cites this paper
• Genes underlying species differences in CHC production between Drosophila melanogaster and D. simulans.

  2020cites this paper
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• Two decades of suspect evidence for adaptive DNA-sequence evolution – Less negative selection misconstrued as positive selection

  2020cites this paper
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  2020cites this paper
• The complex genetic architecture of male mate choice evolution between Drosophila species

  2020cites this paper
• Evolution of genome structure in the Drosophila simulans species complex

  2020influential citation
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  2020cites this paper
• Pervasive Strong Selection at the Level of Codon Usage Bias in Drosophila melanogaster

  2019cites this paper
• Rapid and Predictable Evolution of Admixed Populations Between Two Drosophila Species Pairs

  2019cites this paper
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  2019cites this paper
• Rapid evolution of gained essential developmental functions of a young gene via interactions with other essential genes.

  2019cites this paper
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  2018cites this paper
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• Drosophila simulans: A Species with Improved Resolution in Evolve and Resequence Studies

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  2017cites this paper
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  2017cites this paper
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  2017influential citation
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  2017cites this paper
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  2017influential citation
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
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  2017cites this paper
• Supplemental Text S 1

  2016cites this paper
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  2016cites this paper
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  2016cites this paper
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  2016influential citation
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  2016cites this paper