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

Abstract

We create a new assembly of the Drosophila simulans genome using 142 million paired short-read sequences and previously published data for strain w 501 . 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.[Supplemental material is available for this article.]The completion of genomes for an increasing number of eukaryotic species promises unprecedented power to distinguish among models of genome evolution. Population genetic theory predicts that the amount of divergence along a species lineage should depend on the mutation rate, the strength and mode of natural selection, and the species effective population size (N e ), as well as the genomic context such as sex linkage, recombination rate, and other factors (Kimura 1983;Charlesworth et al. 1987Charlesworth et al. , 2009. How these factors ultimately contribute to observed patterns of genome evolution is an empirical question that has been the subject of intense investigation in population genetics for the past several decades (Charlesworth 2010).Studies of Drosophila, particularly Drosophila melanogaster and its close relatives, have historically been at the forefront of such investigations. Ohta (1993) first raised the point that the protein alcohol dehydrogenase evolves more quickly in Hawaiian Drosophila than other Drosophilids, consistent with a reduction in the efficacy of purifying selection on weakly deleterious amino acid substitutions associated with smaller N e in this species. Ohta also noted elevated rates of protein evolution in primates and rodents, again, consistent with smaller N e in these species than in many Drosophilids. Using a larger collection of genes, Akashi (1995Akashi ( , 1996 showed that rates of synonymous and nonsynonymous substit...

The recent invasion of natural Drosophila simulans populations by the P-element

“…These differences suggest that we sampled the Florida (2010) population in the early phase of P-element invasion and the South African population (2012) at a more advanced phase. Consistent with a recent invasion of D. simulans populations, we did not find any P-element insertions in a pool of African (Sub-Saharan) D. simulans flies sampled between 2001 and 2009 (25) nor in diverse strains collected before 1998 from multiple locations including California, North America, Madagascar, New Caledonia, and Kenya (26,27). Using sequence data from individual flies, we confirmed that the presence of the P-element in D. simulans is not due to a low level of contamination of the pooled flies with D. melanogaster or to a technical artifact.…”

Genome comparisons indicate recent transfer ofwRi‐likeWolbachiabetween sister speciesDrosophila suzukiiandD. subpulchrella

“…We used BLAST to identify orthologs in the D. suzukii assembly of Ometto et al. (2013), the unpublished draft D. subpulchrella assembly described above, a D. biarmipes assembly (Chen et al., 2014), and a second‐generation D. simulans assembly (Hu, Eisen, Thornton, & Andolfatto, 2013). Data for H2A and amylase were eliminated because H2A had multiple nonidentical paralogs in each species and homologs of D. melanogaster amylase could not be found in the assemblies.…”

Estimating the parameters of background selection and selective sweeps in Drosophila in the presence of gene conversion

“…For this analysis, we used the D. melanogaster-D. simulans-D. yakuba gene alignments of ref. 60, from which we selected the coding and UTR regions corresponding to our chosen transcripts. We applied a custom Perl script to infer ancestral versus derived substitutions along the D. melanogaster lineage, counting nonsynonymous and substitutions as in ref.…”