Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans - PubMed (original) (raw)

doi: 10.1371/journal.pbio.0050310.

Alisha K Holloway, Kristian Stevens, Ladeana W Hillier, Yu-Ping Poh, Matthew W Hahn, Phillip M Nista, Corbin D Jones, Andrew D Kern, Colin N Dewey, Lior Pachter, Eugene Myers, Charles H Langley

Affiliations

Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans

David J Begun et al. PLoS Biol. 2007.

Abstract

The population genetic perspective is that the processes shaping genomic variation can be revealed only through simultaneous investigation of sequence polymorphism and divergence within and between closely related species. Here we present a population genetic analysis of Drosophila simulans based on whole-genome shotgun sequencing of multiple inbred lines and comparison of the resulting data to genome assemblies of the closely related species, D. melanogaster and D. yakuba. We discovered previously unknown, large-scale fluctuations of polymorphism and divergence along chromosome arms, and significantly less polymorphism and faster divergence on the X chromosome. We generated a comprehensive list of functional elements in the D. simulans genome influenced by adaptive evolution. Finally, we characterized genomic patterns of base composition for coding and noncoding sequence. These results suggest several new hypotheses regarding the genetic and biological mechanisms controlling polymorphism and divergence across the Drosophila genome, and provide a rich resource for the investigation of adaptive evolution and functional variation in D. simulans.

PubMed Disclaimer

Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. Patterns of Polymorphism and Divergence of Nucleotides along Chromosome Arms

Nucleotide π (blue) and div on the D. simulans lineage (red) in 150-kbp windows are plotted every 10 kbp. χ[–log(p)] (olive) as a measure of deviation (+ or –) in the proportion of polymorphic sites in 30-kbp windows is plotted every 10 kbp (see Materials and Methods). C and T correspond to locations of centromeres and telomeres, respectively. Chromosome arm 3R coordinates correspond to D. simulans locations after accounting for fixed inversion on the D. melanogaster lineage.

Figure 2

Figure 2. Patterns of Polymorphism for Nucleotides, Small Insertions, and Small Deletions along Chromosome Arms

π for nucleotides (blue), π for small (≤ 10 bp) insertions (orange), and π for small (≤ 10 bp) deletions (orchid) among the D. simulans lines in 150-kbp windows are plotted every 10 kbp (see Materials and Methods). C and T correspond to locations of centromeres and telomeres, respectively. Chromosome arm 3R coordinates correspond to D. simulans locations after accounting for fixed inversion on the D. melanogaster lineage.

Figure 3

Figure 3. Rate of Crossing-Over per Base Pair (Green), Nucleotide Polymorphism (Blue) and Nucleotide Divergence (Red) along the X Chromosome

Nucletotide π (blue) and div on the D. simulans lineage (red) in 150-kbp windows are plotted every 10 kbp. Estimated rate of crossing-over (green) is plotted for specific genomic segments (see Materials and Methods).

Figure 4

Figure 4. Hitchhiking Effects Can Induce a Correlation between Polymorphism and Divergence

Hypothetical gene geneoligies in ancestral populations (A or B) and extant populations (C or D) for genomic regions of high crossing-over and low crossing-over (respectively) experiencing different hitchhiking effects. On average, time to the most recent common ancestor in the ancestral population is greater in regions of higher crossing-over (A) and therefore contributes more to the divergence, TH. Regions of lower crossing-over have smaller gene genealogies (D versus C) and less divergence (TL versus TH).

Figure 5

Figure 5. Snapshot of UCSC Browser Tracks in a Genomic Region Showing Significantly Reduced Heterozygosity Relative to Divergence

Nucletotide π (blue, labeled “PI 10K”) and div on the D. simulans lineage (black), labeled “DIV 10K” in 10-kbp windows are plotted every 10 kbp. χ2[-log(p)] (green, labeled “HKA 10K”) as a measure of deviation (+ or −) in the proportion of polymorphic sites in 10-kbp windows is plotted every 10 kbp (see Materials and Methods). The genes scpr-A, scpr-B, and scpr-C exhibit high levels of expression in the testes and are indicated in red.

Similar articles

Cited by

References

    1. Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993;134:1289–1303. - PMC - PubMed
    1. Hudson RR, Kreitman M, Aguade M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987;116:153–159. - PMC - PubMed
    1. Kaplan NL, Hudson RR, Langley CH. The “hitchhiking effect” revisited. Genetics. 1989;123:887–899. - PMC - PubMed
    1. McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila . Nature. 1991;351:652–654. - PubMed
    1. Kimura M. The neutral theory of molecular evolution. Cambridge (UK): Cambridge University Press; 1983.

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources