Skip to main content

Advertisement

SpringerLink
Log in

Power of Neutrality Tests to Detect Bottlenecks and Hitchhiking

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The power of several neutrality tests to reject a simple bottleneck model is examined in a coalescent framework. Several tests are considered including some relying on the frequency spectrum of mutations and some reflecting the linkage disequilibrium structure of the data. We evaluate the effect of the age and of the strength of the bottleneck, and their interaction. We contrast two qualitatively different bottleneck effects depending on their strength. In genealogical terms, during severe bottlenecks, all lineages coalesce leading to a star-like gene genealogy of the sample. Some time after the bottleneck, once new mutations have arisen, they tend to show an excess of rare variants and a slight excess of haplotypes. On the contrary, more moderate bottlenecks allow several lineages to survive the demographic crash, leading to a balanced genealogy with long internal branches. Soon after the event, data tend to show an excess of intermediate frequency variants and a deficit of haplotypes. We show that for moderate sequencing efforts, severe bottlenecks can be detected only after an intermediate time period has allowed for mutations to occur, preferably by frequency spectrum statistics. Moderate bottlenecks can be more easily detected for more recent events, especially using haplotype statistics. Finally, for a single locus, the bottleneck results closely approximate those of a simple hitchhiking model. The main difference concerns the frequency distribution of mutations and haplotypes after moderate perturbations. Hitchhiking increases the number of rare ancestral mutations and leads to a more predominant major haplotype class. Thus, despite a number of common features between the two processes, hitchhiking cannot be strictly modeled by bottlenecks.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. P Andolfatto JD Wall M Kreitman (1999) ArticleTitleUnusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics 153 1297–1311 Occurrence Handle1:CAS:528:DyaK1MXnslSjsbw%3D Occurrence Handle10545460

    CAS  PubMed  Google Scholar 

  2. NH Barton (1998) ArticleTitleThe effect of hitch-hiking on neutral genealogies. Genet Res 72 123–133 Occurrence Handle10.1017/S0016672398003462 Occurrence Handle1:CAS:528:DyaK1MXmvVantg%3D%3D

    Article  CAS  Google Scholar 

  3. NH Barton (2000) ArticleTitleGenetic hitchhiking. Philos Trans R Soc Lond B Biol Sci 355 1553–1562 Occurrence Handle10.1098/rstb.2000.0716 Occurrence Handle1:CAS:528:DC%2BD3MXkvVymsw%3D%3D Occurrence Handle11127900

    Article  CAS  PubMed  Google Scholar 

  4. JM Braverman RR Hudson NL Kaplan CH Langley W Stephan (1995) ArticleTitleThe hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140 783–796 Occurrence Handle1:CAS:528:DyaK28Xht1CgsLs%3D Occurrence Handle7498754

    CAS  PubMed  Google Scholar 

  5. F Depaulis S Mousset M Veuille (2001) ArticleTitleHaplotype tests using coalescent simulations conditional on the number of segregating sites. Mol Biol Evol 18 1136–1138 Occurrence Handle1:CAS:528:DC%2BD3MXktFemu78%3D Occurrence Handle11371602

    CAS  PubMed  Google Scholar 

  6. F Depaulis S Mousset M Veuille (in press) Detecting selective sweeps with haplotype tests. D Nurminsky (Eds) Selective sweep. Landes Bioscience Georgetown, USA

    Google Scholar 

  7. F Depaulis M Veuille (1998) ArticleTitleNeutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol 15 1788–1790 Occurrence Handle1:CAS:528:DyaK1MXjtV2j Occurrence Handle9917213

    CAS  PubMed  Google Scholar 

  8. WJ Ewens (1972) ArticleTitleThe sampling theory of selectively neutral alleles. Theor Pop Biol 3 87–112 Occurrence Handle1:STN:280:CSyB2MrlslY%3D

    CAS  Google Scholar 

  9. JC Fay CI Wu (1999) ArticleTitleA human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol Biol Evol 16 1003–1005 Occurrence Handle1:CAS:528:DyaK1MXksFOlsL0%3D Occurrence Handle10406117

    CAS  PubMed  Google Scholar 

  10. JC Fay CI Wu (2000) ArticleTitleHitchhiking under positive Darwinian selection. Genetics 155 1405–1413 Occurrence Handle1:STN:280:DC%2BD3cvgsVSntQ%3D%3D Occurrence Handle10880498

    CAS  PubMed  Google Scholar 

  11. J Felsenstein (1992) ArticleTitleEstimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. Genet Res 59 139–147 Occurrence Handle1:STN:280:By2A3s7ptFI%3D Occurrence Handle1628818

    CAS  PubMed  Google Scholar 

  12. YX Fu (1996) ArticleTitleNew statistical tests of neutrality for DNA samples from a population. Genetics 143 557–570 Occurrence Handle1:CAS:528:DyaK28XjtVKjsL0%3D Occurrence Handle8722804

    CAS  PubMed  Google Scholar 

  13. YX Fu (1997) ArticleTitleStatistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147 915–925 Occurrence Handle1:STN:280:ByiH2snjtlM%3D Occurrence Handle9335623

    CAS  PubMed  Google Scholar 

  14. YX Fu WH Li (1993) ArticleTitleStatistical tests of neutrality of mutations. Genetics 133 693–709 Occurrence Handle1:STN:280:ByyB3c3kvVU%3D Occurrence Handle8454210

    CAS  PubMed  Google Scholar 

  15. N Galtier F Depaulis NH Barton (2000) ArticleTitleDetecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics 155 981–987 Occurrence Handle1:CAS:528:DC%2BD3cXkslyqurc%3D Occurrence Handle10835415

    CAS  PubMed  Google Scholar 

  16. RR Hudson (1993) The how and why of generating gene genealogies. N Takahata AG Clarck (Eds) Mechanism of molecular evolution. Japan Scientific Societies Press Sinauer Associates, Inc., Sunderland, MA 23–36

    Google Scholar 

  17. RR Hudson K Bailey D Skarecky J Kwiatowski FJ Ayala (1994) ArticleTitleEvidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136 1329–1340 Occurrence Handle1:CAS:528:DyaK2cXmslOjtLc%3D Occurrence Handle8013910

    CAS  PubMed  Google Scholar 

  18. RR Hudson NL Kaplan (1985) ArticleTitleStatistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111 147–164 Occurrence Handle1:STN:280:BiqB1cnjtVw%3D Occurrence Handle4029609

    CAS  PubMed  Google Scholar 

  19. RR Hudson M Kreitman M Aguadé (1987) ArticleTitleA test of neutral molecular evolution based on nucleotide data. Genetics 116 153–159 Occurrence Handle1:CAS:528:DyaL2sXktlCgsLk%3D Occurrence Handle3110004

    CAS  PubMed  Google Scholar 

  20. JK Kelly (1997) ArticleTitleA test of neutrality based on interlocus associations. Genetics 146 1197–1206 Occurrence Handle1:CAS:528:DyaK2sXmsVarurY%3D Occurrence Handle9215920

    CAS  PubMed  Google Scholar 

  21. M Nordborg S Tavaré (2002) ArticleTitleLinkage disequilibrium: What history has to tell us. Trends Genet 18 83–90 Occurrence Handle10.1016/S0168-9525(02)02557-X Occurrence Handle1:CAS:528:DC%2BD38XovFantQ%3D%3D Occurrence Handle11818140

    Article  CAS  PubMed  Google Scholar 

  22. M Przeworski (2002) ArticleTitleThe signature of positive selection at randomly chosen loci. Genetics 160 1179–1189 Occurrence Handle11901132

    PubMed  Google Scholar 

  23. MH Schierup J Hein (2000) ArticleTitleRecombination and the molecular clock. Mol Biol Evol 17 1578–1789 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Cntr8%3D Occurrence Handle11018163

    CAS  PubMed  Google Scholar 

  24. W Stephan THE Wiehe MW Lenz (1992) ArticleTitleThe effect of strongly selected substitutions on neutral polymorphism: Analytical results based on diffusion theory. Theor Popul Biol 41 237–254

    Google Scholar 

  25. C Strobeck (1987) ArticleTitleAverage number of nucleotide differences in a sample from a single subpopulation: A test for population subdivision. Genetics 117 149–154

    Google Scholar 

  26. F Tajima (1989) ArticleTitleStatistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585–595 Occurrence Handle1:CAS:528:DyaK3cXhslentA%3D%3D Occurrence Handle2513255

    CAS  PubMed  Google Scholar 

  27. JD Wall (1999) ArticleTitleRecombination and the power of statistical tests of neutrality. Genet Res 74 65–69 Occurrence Handle10.1017/S0016672399003870

    Article  Google Scholar 

  28. JD Wall (2000) ArticleTitleA comparison of estimators of the population recombination rate. Mol Biol Evol 17 156–163 Occurrence Handle1:CAS:528:DC%2BD3cXot1SjtQ%3D%3D Occurrence Handle10666715

    CAS  PubMed  Google Scholar 

  29. JD Wall RR Hudson (2001) ArticleTitleCoalescent simulations and statistical tests of neutrality. Mol Biol Evol 18 1134–1135 Occurrence Handle1:CAS:528:DC%2BD3MXktFemu74%3D Occurrence Handle11371601

    CAS  PubMed  Google Scholar 

  30. GA Watterson (1975) ArticleTitleOn the number of segregation sites. Theoret Popul Biol 7 256–276 Occurrence Handle1:STN:280:CSqC1MbgvF0%3D

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire d’Ecologie, CNRS UMR 7625-EPHE, Université Pierre-et-Marie Curie, Paris, France

    Frantz Depaulis, Sylvain Mousset & Michel Veuille

Authors
  1. Frantz Depaulis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sylvain Mousset
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Veuille
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frantz Depaulis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Depaulis, F., Mousset, S. & Veuille, M. Power of Neutrality Tests to Detect Bottlenecks and Hitchhiking . J Mol Evol 57 (Suppl 1), S190–S200 (2003). https://doi.org/10.1007/s00239-003-0027-y

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-0027-y

Keywords

Search

Navigation