Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps
- PMID: 25706129
- PMCID: PMC4338236
- DOI: 10.1371/journal.pgen.1005004
Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps
Abstract
Adaptation from standing genetic variation or recurrent de novo mutation in large populations should commonly generate soft rather than hard selective sweeps. In contrast to a hard selective sweep, in which a single adaptive haplotype rises to high population frequency, in a soft selective sweep multiple adaptive haplotypes sweep through the population simultaneously, producing distinct patterns of genetic variation in the vicinity of the adaptive site. Current statistical methods were expressly designed to detect hard sweeps and most lack power to detect soft sweeps. This is particularly unfortunate for the study of adaptation in species such as Drosophila melanogaster, where all three confirmed cases of recent adaptation resulted in soft selective sweeps and where there is evidence that the effective population size relevant for recent and strong adaptation is large enough to generate soft sweeps even when adaptation requires mutation at a specific single site at a locus. Here, we develop a statistical test based on a measure of haplotype homozygosity (H12) that is capable of detecting both hard and soft sweeps with similar power. We use H12 to identify multiple genomic regions that have undergone recent and strong adaptation in a large population sample of fully sequenced Drosophila melanogaster strains from the Drosophila Genetic Reference Panel (DGRP). Visual inspection of the top 50 candidates reveals that in all cases multiple haplotypes are present at high frequencies, consistent with signatures of soft sweeps. We further develop a second haplotype homozygosity statistic (H2/H1) that, in combination with H12, is capable of differentiating hard from soft sweeps. Surprisingly, we find that the H12 and H2/H1 values for all top 50 peaks are much more easily generated by soft rather than hard sweeps. We discuss the implications of these results for the study of adaptation in Drosophila and in species with large census population sizes.
Conflict of interest statement
The authors have declared that no competing interests exist.
Figures
![Fig 1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g001.gif)
![Fig 2](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g002.gif)
![Fig 3](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g003.gif)
![Fig 4](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g004.gif)
![Fig 5](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g005.gif)
![Fig 6](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g006.gif)
![Fig 7](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g007.gif)
![Fig 8](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g008.gif)
![Fig 9](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g009.gif)
![Fig 10](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g010.gif)
![Fig 11](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4338236/bin/pgen.1005004.g011.gif)
Similar articles
-
Detection and Classification of Hard and Soft Sweeps from Unphased Genotypes by Multilocus Genotype Identity.Genetics. 2018 Dec;210(4):1429-1452. doi: 10.1534/genetics.118.301502. Epub 2018 Oct 12. Genetics. 2018. PMID: 30315068 Free PMC article.
-
Enhancing the mathematical properties of new haplotype homozygosity statistics for the detection of selective sweeps.Theor Popul Biol. 2015 Jun;102:94-101. doi: 10.1016/j.tpb.2015.04.001. Epub 2015 Apr 16. Theor Popul Biol. 2015. PMID: 25891325 Free PMC article.
-
Detection of hard and soft selective sweeps from Drosophila melanogaster population genomic data.PLoS Genet. 2021 Feb 26;17(2):e1009373. doi: 10.1371/journal.pgen.1009373. eCollection 2021 Feb. PLoS Genet. 2021. PMID: 33635910 Free PMC article.
-
Population genomics of rapid adaptation by soft selective sweeps.Trends Ecol Evol. 2013 Nov;28(11):659-69. doi: 10.1016/j.tree.2013.08.003. Epub 2013 Sep 25. Trends Ecol Evol. 2013. PMID: 24075201 Free PMC article. Review.
-
The recent demographic and adaptive history of Drosophila melanogaster.Heredity (Edinb). 2007 Feb;98(2):65-8. doi: 10.1038/sj.hdy.6800901. Epub 2006 Sep 27. Heredity (Edinb). 2007. PMID: 17006533 Review.
Cited by
-
Signatures of selective sweeps in continuous-space populations.bioRxiv [Preprint]. 2024 Jul 26:2024.07.26.605365. doi: 10.1101/2024.07.26.605365. bioRxiv. 2024. PMID: 39091822 Free PMC article. Preprint.
-
Fast and Accurate Estimation of Selection Coefficients and Allele Histories from Ancient and Modern DNA.Mol Biol Evol. 2024 Aug 2;41(8):msae156. doi: 10.1093/molbev/msae156. Mol Biol Evol. 2024. PMID: 39078618 Free PMC article.
-
Parallel Evolution in Mosquito Vectors-A Duplicated Esterase Locus is Associated With Resistance to Pirimiphos-methyl in Anopheles gambiae.Mol Biol Evol. 2024 Jul 3;41(7):msae140. doi: 10.1093/molbev/msae140. Mol Biol Evol. 2024. PMID: 38985692 Free PMC article.
-
From sub-Saharan Africa to China: Evolutionary history and adaptation of Drosophila melanogaster revealed by population genomics.Sci Adv. 2024 Apr 19;10(16):eadh3425. doi: 10.1126/sciadv.adh3425. Epub 2024 Apr 17. Sci Adv. 2024. PMID: 38630810 Free PMC article.
-
Signatures of adaptation at key insecticide resistance loci in Anopheles gambiae in Southern Ghana revealed by reduced-coverage WGS.Sci Rep. 2024 Apr 15;14(1):8650. doi: 10.1038/s41598-024-58906-x. Sci Rep. 2024. PMID: 38622230 Free PMC article.
References
-
- Fay JC, Wyckoff GJ, Wu CI (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415: 1024–1026. - PubMed
-
- Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415: 1022–1024. - PubMed
-
- Bierne N, Eyre-Walker A (2004) The genomic rate of adaptive amino acid substitution in Drosophila. Molecular Biology and Evolution 21: 1350–1360. - PubMed
-
- Andolfatto P (2005) Adaptive evolution of non-coding DNA in Drosophila. Nature 437: 1149–1152. - PubMed
Publication types
MeSH terms
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases