Strong Selective Sweeps on the X Chromosome in the Human-Chimpanzee Ancestor Explain Its Low Divergence


Because the speciation events that led to human, chimpanzee and gorilla were close in time, the genetic relationship of these species varies along the genome. While human and chimpanzee are the closest related species, in 15% of the genome, human and gorilla are more closely related, and in another 15% of the genome the chimpanzee and gorilla are more closely related—a phenomenon called incomplete lineage sorting (ILS). The amount and distribution of ILS can be predicted using population genetics theory and is affected by demography and selection in the ancestral populations. It was previously reported that the X chromosome, in contrast to autosomes, has less than the expected level of ILS. Using a full genome alignment of the X chromosome, we show that this low level of ILS affects only one third of the chromosome. Regions with low level of ILS also show reduced diversity in the extant populations of human and great apes and coincide with regions devoid of Neanderthal introgression. We propose that these regions are targets of selection and that they played a role in the formation of reproductive barriers.


Vyšlo v časopise: Strong Selective Sweeps on the X Chromosome in the Human-Chimpanzee Ancestor Explain Its Low Divergence. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005451
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1005451

Souhrn

Because the speciation events that led to human, chimpanzee and gorilla were close in time, the genetic relationship of these species varies along the genome. While human and chimpanzee are the closest related species, in 15% of the genome, human and gorilla are more closely related, and in another 15% of the genome the chimpanzee and gorilla are more closely related—a phenomenon called incomplete lineage sorting (ILS). The amount and distribution of ILS can be predicted using population genetics theory and is affected by demography and selection in the ancestral populations. It was previously reported that the X chromosome, in contrast to autosomes, has less than the expected level of ILS. Using a full genome alignment of the X chromosome, we show that this low level of ILS affects only one third of the chromosome. Regions with low level of ILS also show reduced diversity in the extant populations of human and great apes and coincide with regions devoid of Neanderthal introgression. We propose that these regions are targets of selection and that they played a role in the formation of reproductive barriers.


Zdroje

1. Meisel RP, Connallon T. The faster-X effect: integrating theory and data. Trends Genet TIG. 2013;29: 537–544.

2. Vicoso B, Charlesworth B. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet. 2006;7: 645–653. 16847464

3. Gottipati S, Arbiza L, Siepel A, Clark AG, Keinan A. Analyses of X-linked and autosomal genetic variation in population-scale whole genome sequencing. Nat Genet. 2011;43: 741–743. doi: 10.1038/ng.877 21775991

4. Arbiza L, Gottipati S, Siepel A, Keinan A. Contrasting X-linked and autosomal diversity across 14 human populations. Am J Hum Genet. 2014;94: 827–844. doi: 10.1016/j.ajhg.2014.04.011 24836452

5. Hammer MF, Woerner AE, Mendez FL, Watkins JC, Cox MP, Wall JD. The ratio of human X chromosome to autosome diversity is positively correlated with genetic distance from genes. Nat Genet. 2010;42: 830–831. doi: 10.1038/ng.651 20802480

6. Maynard Smith J, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974;23: 23–35. 4407212

7. Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993;134: 1289–1303. 8375663

8. Hvilsom C, Qian Y, Bataillon T, Li Y, Mailund T, Sallé B, et al. Extensive X-linked adaptive evolution in central chimpanzees. Proc Natl Acad Sci U S A. 2012;109: 2054–2059. doi: 10.1073/pnas.1106877109 22308321

9. Bataillon T, Duan J, Hvilsom C, Jin X, Li Y, Skov L, et al. Inference of purifying and positive selection in three subspecies of chimpanzees (Pan troglodytes) from exome sequencing. Genome Biol Evol. 2015;7: 1122–1132. doi: 10.1093/gbe/evv058 25829516

10. Veeramah KR, Gutenkunst RN, Woerner AE, Watkins JC, Hammer MF. Evidence for increased levels of positive and negative selection on the X chromosome versus autosomes in humans. Mol Biol Evol. 2014.

11. Kousathanas A, Halligan DL, Keightley PD. Faster-X adaptive protein evolution in house mice. Genetics. 2014;196: 1131–1143. doi: 10.1534/genetics.113.158246 24361937

12. Laurie CC. The weaker sex is heterogametic: 75 years of Haldane’s rule. Genetics. 1997;147: 937–951. 9383043

13. Schilthuizen M, Giesbers MCWG, Beukeboom LW. Haldane’s rule in the 21st century. Heredity. 2011;107: 95–102. doi: 10.1038/hdy.2010.170 21224879

14. Sankararaman S, Mallick S, Dannemann M, Prüfer K, Kelso J, Pääbo S, et al. The genomic landscape of Neanderthal ancestry in present-day humans. Nature. 2014;

15. Hurst LD, Pomiankowski A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane’s rule and related phenomena. Genetics. 1991;128: 841–858. 1916248

16. Haig D, Grafen A. Genetic scrambling as a defence against meiotic drive. J Theor Biol. 1991;153: 531–558. 1806752

17. Meiklejohn CD, Tao Y. Genetic conflict and sex chromosome evolution. Trends Ecol Evol. 2010;25: 215–223. doi: 10.1016/j.tree.2009.10.005 19931208

18. Nam K, Munch K, Hobolth A, Dutheil JY, Veeramah KR, Woerner AE, et al. Extreme selective sweeps independently targeted the X chromosomes of the great apes. Proc Natl Acad Sci U S A. 2015.

19. Frank SA. Divergence of Meiotic Drive-Suppression Systems as an Explanation for Sex- Biased Hybrid Sterility and Inviability. Evolution. 1991;45: 262–267.

20. McDermott SR, Noor MAF. The role of meiotic drive in hybrid male sterility. Philos Trans R Soc Lond B Biol Sci. 2010;365: 1265–1272. doi: 10.1098/rstb.2009.0264 20308102

21. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, et al. Insights into hominid evolution from the gorilla genome sequence. Nature. 2012;483: 169–175. doi: 10.1038/nature10842 22398555

22. Hobolth A, Christensen OF, Mailund T, Schierup MH. Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet. 2007;3: e7. 17319744

23. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. Genetic evidence for complex speciation of humans and chimpanzees. Nature. 2006;441: 1103–1108. 16710306

24. Dutheil JY, Ganapathy G, Hobolth A, Mailund T, Uyenoyama MK, Schierup MH. Ancestral population genomics: the coalescent hidden Markov model approach. Genetics. 2009;183: 259–274. doi: 10.1534/genetics.109.103010 19581452

25. Dutheil JY, Hobolth A. Ancestral population genomics. Methods Mol Biol Clifton NJ. 2012;856: 293–313.

26. Mailund T, Munch K, Schierup MH. Lineage Sorting in Apes. Annu Rev Genet. 2014;

27. Takahata N. Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics. 1989;122: 957–966. 2759432

28. McVicker G, Gordon D, Davis C, Green P. Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet. 2009;5: e1000471. doi: 10.1371/journal.pgen.1000471 19424416

29. Nordborg M, Charlesworth B, Charlesworth D. The effect of recombination on background selection. Genet Res. 1996;67: 159–174. 8801188

30. Charlesworth B. The Role of Background Selection in Shaping Patterns of Molecular Evolution and Variation: Evidence from Variability on the Drosophila X Chromosome. Genetics. 2012;191: 233–246. doi: 10.1534/genetics.111.138073 22377629

31. Genomes Project Consortium, Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, et al. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491: 56–65. doi: 10.1038/nature11632 23128226

32. Keinan A, Reich D. Can a sex-biased human demography account for the reduced effective population size of chromosome X in non-Africans? Mol Biol Evol. 2010;27: 2312–2321. doi: 10.1093/molbev/msq117 20453016

33. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, et al. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508: 488–493. doi: 10.1038/nature13151 24759410

34. Mueller JL, Skaletsky H, Brown LG, Zaghlul S, Rock S, Graves T, et al. Independent specialization of the human and mouse X chromosomes for the male germ line. Nat Genet. 2013;45: 1083–1087. doi: 10.1038/ng.2705 23872635

35. Dutheil JY, Gaillard S, Stukenbrock EH. MafFilter: a highly flexible and extensible multiple genome alignment files processor. BMC Genomics. 2014;15: 53. doi: 10.1186/1471-2164-15-53 24447531

36. Hudson RR. Gene genealogies and the coalescent process. 1991. pp. 1–44.

37. Chen FC, Li WH. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet. 2001;68: 444–456. 11170892

38. Azzalini A. A Class of Distributions Which Includes the Normal Ones. Scand J Stat. 1985;12: 171–178.

39. Durrett R. Probability Models for DNA Sequence Evolution [Internet]. 2nd ed. Springer; 2002. http://www.springer.com/mathematics/probability/book/978-0-387-78168-6

40. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, et al. A high-resolution recombination map of the human genome. Nat Genet. 2002;31: 241–247. 12053178

41. Genomes Project Consortium, Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, et al. A map of human genome variation from population-scale sequencing. Nature. 2010;467: 1061–1073. doi: 10.1038/nature09534 20981092

42. Rands CM, Meader S, Ponting CP, Lunter G. 8.2% of the Human genome is constrained: variation in rates of turnover across functional element classes in the human lineage. PLoS Genet. 2014;10: e1004525. doi: 10.1371/journal.pgen.1004525 25057982

43. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995; 289–300.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa