#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genomic Identification of Founding Haplotypes Reveals the History of the Selfing Species


The shift from outcrossing to self-fertilization is among the most common evolutionary transitions in flowering plants. Until recently, however, a genome-wide view of this transition has been obscured by both a dearth of appropriate data and the lack of appropriate population genomic methods to interpret such data. Here, we present a novel population genomic analysis detailing the origin of the selfing species, Capsella rubella, which recently split from its outcrossing sister, Capsella grandiflora. Due to the recency of the split, much of the variation within C. rubella is also found within C. grandiflora. We can therefore identify genomic regions where two C. rubella individuals have inherited the same or different segments of ancestral diversity (i.e. founding haplotypes) present in C. rubella's founder(s). Based on this analysis, we show that C. rubella was founded by multiple individuals drawn from a diverse ancestral population closely related to extant C. grandiflora, that drift and selection have rapidly homogenized most of this ancestral variation since C. rubella's founding, and that little novel variation has accumulated within this time. Despite the extensive loss of ancestral variation, the approximately 25% of the genome for which two C. rubella individuals have inherited different founding haplotypes makes up roughly 90% of the genetic variation between them. To extend these findings, we develop a coalescent model that utilizes the inferred frequency of founding haplotypes and variation within founding haplotypes to estimate that C. rubella was founded by a potentially large number of individuals between 50 and 100 kya, and has subsequently experienced a twenty-fold reduction in its effective population size. As population genomic data from an increasing number of outcrossing/selfing pairs are generated, analyses like the one developed here will facilitate a fine-scaled view of the evolutionary and demographic impact of the transition to self-fertilization.


Vyšlo v časopise: Genomic Identification of Founding Haplotypes Reveals the History of the Selfing Species. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003754
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003754

Souhrn

The shift from outcrossing to self-fertilization is among the most common evolutionary transitions in flowering plants. Until recently, however, a genome-wide view of this transition has been obscured by both a dearth of appropriate data and the lack of appropriate population genomic methods to interpret such data. Here, we present a novel population genomic analysis detailing the origin of the selfing species, Capsella rubella, which recently split from its outcrossing sister, Capsella grandiflora. Due to the recency of the split, much of the variation within C. rubella is also found within C. grandiflora. We can therefore identify genomic regions where two C. rubella individuals have inherited the same or different segments of ancestral diversity (i.e. founding haplotypes) present in C. rubella's founder(s). Based on this analysis, we show that C. rubella was founded by multiple individuals drawn from a diverse ancestral population closely related to extant C. grandiflora, that drift and selection have rapidly homogenized most of this ancestral variation since C. rubella's founding, and that little novel variation has accumulated within this time. Despite the extensive loss of ancestral variation, the approximately 25% of the genome for which two C. rubella individuals have inherited different founding haplotypes makes up roughly 90% of the genetic variation between them. To extend these findings, we develop a coalescent model that utilizes the inferred frequency of founding haplotypes and variation within founding haplotypes to estimate that C. rubella was founded by a potentially large number of individuals between 50 and 100 kya, and has subsequently experienced a twenty-fold reduction in its effective population size. As population genomic data from an increasing number of outcrossing/selfing pairs are generated, analyses like the one developed here will facilitate a fine-scaled view of the evolutionary and demographic impact of the transition to self-fertilization.


Zdroje

1. Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilised by insects and on the good effects of crossing. London: Murray.

2. Darwin C (1876) The effects of cross- and self-fertilisation in the vegetable kingdom. London: Murray.

3. GoodwilleC, KaliszS, EckertC (2005) The evolutionary enigma of mixed mating systems in plants: Occurrence, theoretical explanations, and empirical evidence. Annual review of ecology, evolution and systematics 36: 47–79.

4. IgicB, KohnJR (2006) The distribution of plant mating systems: study bias against obligately outcrossing species. Evolution 60: 1098–103.

5. Stebbins GL (1950) Variation and evolution in plants. New York, New York, USA: Columbia University Press.

6. Stebbins GL (1974) Flowering plants: Evolution above the species level. Cambridge, MA, USA: Belknap Press.

7. BakerH (1955) Self-compatibility and establishment after ‘long-distance’ dispersal. Evolution 9: 347–349.

8. FisherRA (1941) Average excess and average effect of a gene substitution. Annals of Human Genetics 11: 53–63.

9. SchoenD, LloydD (1984) The selection of cleistogamy and heteromorphic diaspores. Biological Journal of the Linnean Society 23: 303–322.

10. LandeR, SchemskeD (1985) The evolution of self-fertilization and inbreeding depression in plants. i. genetic models. Evolution 39: 24–40.

11. CharlesworthD (2006) Evolution of plant breeding systems. Current Biology 16: R726–R735.

12. StebbinsGL (1957) Self fertilization and population variability in higher plants. American Naturalist 91: 337–354.

13. TakebayashiN, MorrellPL (2001) Is self-fertilization an evolutionary dead end? revisiting an old hypothesis with genetic theories and a macroevolutionary approach. Am J Bot 88: 1143–1150.

14. GoldbergEE, KohnJR, LandeR, RobertsonKA, SmithSA, et al. (2010) Species selection maintains self-incompatibility. Science 330: 493–495.

15. SlotteT, HazzouriKM, AgrenJA, KoenigD, MaumusF, et al. (2013) The capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat Genet 45: 831–5.

16. FoxeJP, SlotteT, StahlEA, NeufferB, HurkaH, et al. (2009) Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci U S A 106: 5241–5.

17. GuoYL, BechsgaardJS, SlotteT, NeufferB, LascouxM, et al. (2009) Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. PNAS 106: 5246–51.

18. St OngeKR, KällmanT, SlotteT, LascouxM, PalméAE (2011) Contrasting demographic history and population structure in Capsella rubella and Capsella grandiflora, two closely related species with different mating systems. Mol Ecol 20: 3306–20.

19. SlotteT, HazzouriKM, SternD, AndolfattoP, WrightSI (2012) Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66: 1360–1374.

20. ReichD, ThangarajK, PattersonN, PriceAL, SinghL (2009) Reconstructing indian population history. Nature 461: 489–494.

21. PattersonN, MoorjaniP, LuoY, MallickS, RohlandN, et al. (2012) Ancient admixture in human history. Genetics 192: 1065–1093.

22. NordborgM (2000) Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154: 923–9.

23. GléminS (2007) Mating systems and the efficacy of selection at the molecular level. Genetics 177: 905–16.

24. PtakSE, PrzeworskiM (2002) Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet 18: 559–63.

25. KochM, HauboldB, Mitchell-OldsT (2001) Molecular systematics of the brassicaceae: evidence from coding plastidic matk and nuclear chs sequences. Am J Bot 88: 534–44.

26. OssowskiS, SchneebergerK, Lucas-LledóJI, WarthmannN, ClarkRM, et al. (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327: 92–4.

27. HudsonRR, KreitmanM, AguadéM (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153–9.

28. AndersonEC, SlatkinM (2007) Estimation of the number of individuals founding colonized populations. Evolution 61: 972–83.

29. LebloisR, SlatkinM (2007) Estimating the number of founder lineages from haplotypes of closely linked snps. Molecular Ecology 16: 2237–2245.

30. SweigartAL, WillisJH (2003) Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evolution 57: 2490–506.

31. WuCA, LowryDB, CooleyAM, WrightKM, LeeYW, et al. (2008) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220–30.

32. MableBK, AdamA (2007) Patterns of genetic diversity in outcrossing and selfing populations of Arabidopsis lyrata. Mol Ecol 16: 3565–80.

33. BuschJW, JolyS, SchoenDJ (2011) Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Mol Biol Evol 28: 1717–29.

34. PettengillJB, MoellerDA (2012) Tempo and mode of mating system evolution between incipient Clarkia species. Evolution 66: 1210–25.

35. CaicedoAL, WilliamsonSH, HernandezRD, BoykoA, Fledel-AlonA, et al. (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3: 1745–56.

36. LamHM, XuX, LiuX, ChenW, YangG, et al. (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42: 1053–9.

37. BrancaA, PaapeTD, ZhouP, BriskineR, FarmerAD, et al. (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci U S A 108: E864–70.

38. NessRW, WrightSI, BarrettSCH (2010) Mating-system variation, demographic history and patterns of nucleotide diversity in the tristylous plant Eichhornia paniculata. Genetics 184: 381–92.

39. NessRW, SiolM, BarrettSCH (2011) De novo sequence assembly and characterization of the floral transcriptome in cross- and self-fertilizing plants. BMC Genomics 12: 298.

40. LiH, DurbinR (2011) Inference of human population history from individual whole-genome sequences. Nature 475: 493–496.

41. Wakeley (2006) An Introduction to Coalescent Theory. Roberts & Co.

42. AdamsAM, HudsonRR (2004) Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked single-nucleotide polymorphisms. Genetics 168: 1699–712.

43. KeinanA, ClarkAG (2012) Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336: 740–743.

44. PollakE (1987) On the theory of partially inbreeding finite populations. i. partial selfing. Genetics 117: 353–60.

45. NordborgM, DonnellyP (1997) The coalescent process with selfing. Genetics 146: 1185–95.

46. CharlesworthB, MorganMT, CharlesworthD (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289–1303.

47. CutterAD, PayseurBA (2003) Selection at linked sites in the partial selfer caenorhabditis elegans. Molecular Biology and Evolution 20: 665–673.

48. HedrickPW (1980) Hitchhiking: a comparison of linkage and partial selfing. Genetics 94: 791–808.

49. CharlesworthD, WrightS (2001) Breeding systems and genome evolution. Current Opinion In Genetics & Development 11: 685–690.

50. BaudryE, KerdelhueC, InnanH, StephanW (2001) Species and recombination effects on dna variability in the tomato genus. Genetics 158: 1725–1735.

51. SchoenD, MorganM, BataillonT (1996) How does self-pollination evolve? inferences from floral ecology and molecular genetic variation. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 351: 1281–1290.

52. IngvarssonPK (2002) A metapopulation perspective on genetic diversity and differentiation in partially self-fertilizing plants. Evolution 56: 2368–73.

53. WrightSI, LaugaB, CharlesworthD (2003) Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol 12: 1247–63.

54. WrightS, NessR, FoxeJ, BarrettS (2008) Genomic consequences of selfing and outcrossing in plants. International Journal of Plant Sciences 169: 105–118.

55. GléminS, RonfortJ (2013) Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution 67: 225–40.

56. GléminS, BazinE, CharlesworthD (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc Biol Sci 273: 3011–9.

57. TrapnellC, PachterL, SalzbergSL (2009) Tophat: discovering splice junctions with rna-seq. Bioinformatics 25: 1105–1111.

58. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The genome analysis toolkit: a mapreduce framework for analyzing next-generation dna sequencing data. Genome Res 20: 1297–303.

59. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation dna sequencing data. Nat Genet 5 43: 491–8.

60. R Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. ISBN 3-900051-07-0.

61. ParadisE, ClaudeJ, StrimmerK (2004) Ape: analyses of phylogenetics and evolution in r language. Bioinformatics 20: 289–290.

62. BallouxF, LehmannL, de MeeûsT (2003) The population genetics of clonal and partially clonal diploids. Genetics 164: 1635–44.

63. GutenkunstRN, HernandezRD, WilliamsonSH, BustamanteCD (2009) Inferring the joint demographic history of multiple populations from multidimensional snp frequency data. PLoS Genet 5: e1000695.

64. HudsonRR (2001) Two-locus sampling distributions and their application. Genetics 159: 1805–17.

65. LarribeF, FearnheadP (2011) On composite likelihoods in statisticall genetics. Statistica Sinica 21: 43–69.

66. WiufC (2006) Consistency of estimators of population scaled parameters using composite likelihood. Journal of Mathematical Biology 53: 821–841.

67. GriffithsR, TavareS (1999) The ages of mutations in gene trees. Annals of Applied Probability 9: 567–590.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
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

#ADS_BOTTOM_SCRIPTS#