Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete
The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.
Vyšlo v časopise:
Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002820
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002820
Souhrn
The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.
Zdroje
1. BaackEJRiesebergLH 2007 A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17 513 518
2. RiesebergLHEllstrandNC 1993 Introgression and its consequences in plants. In Hybrid Zones and the Evolutionary Process New York Oxford University Press
3. MalletJ 2005 Hybridization as an invasion of the genome. Trends Ecol Evol 20 229 237
4. HaydenBPulciniDKelly-QuinnMO'GradyMCaffreyJ 2010 Hybridisation between two cyprinid fishes in a novel habitat: genetics, morphology and life-history traits. BMC Evol Biol 10 169
5. FeldmanCRBrodieEDJrBrodieEDPfrenderME 2009 The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc Natl Acad Sci U S A 106 13415 13420
6. KulathinalRJStevisonLSNoorMA 2009 The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet 5 e1000550 doi:10.1371/journal.pgen.1000550
7. GrantPRGrantBRPetrenK 2005 Hybridization in the recent past. Am Nat 166 56 67
8. GreenREKrauseJBriggsAWMaricicTStenzelU 2010 A draft sequence of the Neandertal genome. Science 328 710 722
9. EvansPDMekel-BobrovNVallenderEJHudsonRRLahnBT 2006 Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc Natl Acad Sci U S A 103 18178 18183
10. TaoYZengZBLiJHartlDLLaurieCC 2003 Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome. Genetics 164 1399 1418
11. TurelliMBegunDJ 1997 Haldane's rule and X-chromosome size in Drosophila. Genetics 147 1799 1815
12. MachadoCAHaselkornTSNoorMA 2007 Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D. persimilis. Genetics 175 1289 1306
13. YatabeYKaneNCScotti-SaintagneCRiesebergLH 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175 1883 1893
14. CurratMExcoffierL 2004 SPLATCHE: a program to simulate genetic diversity taking into account environmental heterogeneity. Molecular Ecology Notes 4 139 142
15. CurratMRuediMPetitRJExcoffierL 2008 The hidden side of invasions: massive introgression by local genes. Evolution 62 1908 1920
16. ExcoffierLPetitRJ 2009 Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics 40 481 501
17. BakerHG 1948 Stages in invasion and replacement demonstrated by species of Melandrium. The Journal of Ecology 36 96 119
18. SolignacMMonnerotM 1986 Race formation, speciation, and introgression within Drosophila simulans, Drosophila mauritiana, and Drosophila sechellia inferred from mitochondrial DNA analysis. Evolution 40 531 539
19. GoodmanSJBartonNHSwansonGAbernethyKPembertonJM 1999 Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152 355 371
20. DuvernellDDAspinwallN 1995 Introgression of Luxilus cornutus mtDNA into allopatric populations of Luxilus chrysocephalus (Teleostei: Cyprinidae) in Missouri and Arkansas. Mol Ecol 4 173 181
21. KauserudHSvegardenIBDecockCHallenbergN 2007 Hybridization among cryptic species of the cellar fungus Coniophora puteana (Basidiomycota). Mol Ecol 16 389 399
22. O'DonnellKKistlerHCTackeBKCasperHH 2000 Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci U S A 97 7905 7910
23. Le GacMHoodMEFournierEGiraudT 2007 Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61 15 26
24. GladieuxPVerckenEFontaineMCHoodMEJonotO 2011 Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28 459 471
25. GonthierPGarbelottoM 2011 Amplified fragment length polymorphism and sequence analyses reveal massive gene introgression from the European fungal pathogen Heterobasidion annosum into its introduced congener H. irregulare. Mol Ecol 20 2756 2770
26. FriesenTLStukenbrockEHLiuZMeinhardtSLingH 2006 Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38 953 956
27. SlotJCRokasA 2011 Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21 134 139
28. StrandbergRNygrenKMenkisAJamesTYWikL 2010 Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora. Fungal Genet Biol 47 869 878
29. PaolettiMBuckKWBrasierCM 2006 Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol Ecol 15 249 262
30. InderbitzinPHarknessJTurgeonBGBerbeeML 2005 Lateral transfer of mating system in Stemphylium. Proc Natl Acad Sci U S A 102 11390 11395
31. NeafseyDEBarkerBMSharptonTJStajichJEParkDJ 2010 Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res 20 938 946
32. MalletLVBecqJDeschavanneP 2010 Whole genome evaluation of horizontal transfers in the pathogenic fungus Aspergillus fumigatus. BMC Genomics 11 171
33. EllisonCEHallCKowbelDWelchJBremRB 2011 Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci U S A 108 2831 2836
34. DujonB 2010 Yeast evolutionary genomics. Nat Rev Genet 11 512 524
35. MenkisAJacobsonDJGustafssonTJohannessonH 2008 The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet 4 e1000030 doi:10.1371/journal.pgen.1000030
36. NygrenKStrandbergRWallbergANabholzBGustafssonT 2011 A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol Phylogenet Evol 59 649 663
37. MerinoSTNelsonMAJacobsonDJNatvigDO 1996 Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics 143 789 799
38. MenkisABastiaansEJacobsonDJJohannessonH 2009 Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. J Evol Biol 22 1923 1936
39. TurnerBCPerkinsDDFairfieldA 2001 Neurospora from natural populations: a global study. Fungal Genet Biol 32 67 92
40. DettmanJRJacobsonDJTaylorJW 2003 A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57 2703 2720
41. PerkinsDDTurnerBC 1976 Strains of Neurospora collected from nature. Evolution 30 281 313
42. SkupskiMPNatvigDO 1997 Phylogenetic analysis of heterothallic Neurospora species. Fungal Genetics and Biology 21 153 162
43. GallegosAJacobsonDJRajuNBSkupskiMPNatvigDO 2000 Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics 154 623 633
44. JacobsonDJ 2005 Blocked recombination along the mating-type chromosomes of Neurospora tetrasperma involves both structural heterozygosity and autosomal genes. Genetics 171 839 843
45. NicolasMMaraisGHykelovaVJanousekBLaporteV 2005 A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3 e4 doi:10.1371/journal.pbio.0030004
46. LiuZMoorePHMaHAckermanCMRagibaM 2004 A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427 348 352
47. PeichelCLRossJAMatsonCKDicksonMGrimwoodJ 2004 The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14 1416 1424
48. KondoMHornungUNandaIImaiSSasakiT 2006 Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16 815 826
49. EllisonCEStajichJEJacobsonDJNatvigDOLapidusA 2011 Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189 55 69
50. WhittleCAJohannessonH 2011 Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma. Heredity 107 305 314
51. WhittleCASunYJohannessonH 2011 Degeneration in codon usage within the young segment of suppressed recombination in the mating type chromosomes of Neurospora tetrasperma. Eukaryot Cell 10 594 603
52. CarvalhoABClarkAG 2005 Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307 108 110
53. BachtrogD 2005 Sex chromosome evolution: molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res 15 1393 1401
54. CharlesworthB 1991 The evolution of sex chromosomes. Science 251 1030 1033
55. JacobsonDJ 1995 Sexual dysfunction associated with outcrossing in Neurospora tetrasperma, a pseudohomothallic ascomycete. Mycologia 87 604 617
56. ShearCLDodgeBO 1927 Life histories and heterothallism of the red bread-mold fungi of the Monilia sitophila group. J Agric Res 34 1019 1042
57. NatvigDOJacksonDATaylorJT 1987 Random-fragment hybridization analysis of evolution in the genus Neurospora: the status of four-spored strains. Evolution 41 1003 1021
58. TaylorJTNatvigDO 1989 Mitochondrial DNA and evolution of heterothallic and pseudohomothallic Neurospora species. Mycological research 3 257 272
59. RajuNB 1994 Diverse programs of ascus development in pseudohomothallic species of Neurospora, Gelasinospora, and Podospora. Developmental Genetics 15 104 118
60. GalaganJECalvoSEBorkovichKASelkerEUReadND 2003 The genome sequence of the filamentous fungus Neurospora crassa. Nature 422 859 868
61. RosaALHaedoSDTemporiniEDBorioliGAMautinoMR 1997 Mapping chromosome landmarks in the centromere I region of Neurospora crassa. Fungal Genet Biol 21 315 322
62. CambareriEBAisnerRCarbonJ 1998 Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol Cell Biol 18 5465 5477
63. MenkisAWhittleCAJohannessonH 2010 Gene genealogies indicates abundant gene conversions and independent evolutionary histories of the mating-type chromosomes in the evolutionary history of Neurospora tetrasperma. BMC Evol Biol 10 234
64. LargetBRKothaSKDeweyCNAneC 2010 BUCKy: gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26 2910 2911
65. AneCLargetBBaumDASmithSDRokasA 2007 Bayesian estimation of concordance among gene trees. Mol Biol Evol 24 412 426
66. YangZ 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591
67. BossuCMNearTJ 2009 Gene trees reveal repeated instances of mitochondrial DNA introgression in orangethroat darters (percidae: etheostoma). Syst Biol 58 114 129
68. ZhangABSotaT 2007 Nuclear gene sequences resolve species phylogeny and mitochondrial introgression in Leptocarabus beetles showing trans-species polymorphisms. Mol Phylogenet Evol 45 534 546
69. AnéC 2010 Reconstructing concordance trees and testing the coalescent model from genomewide data sets. KnowlesLLKL 35 52 Estimating species trees: Practical and theoretical aspects: Wiley-Blackwell
70. BaumDA 2007 Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon 56 417 426
71. PinhoCHeyJ 2010 Divergence with gene flow: models and data. Annual Review of Ecology, Evolution, and Systematics Vol 41 41 215 230
72. BartonN 1979 Gene flow past a cline. Heredity 43 333 339
73. NamKEllegrenH 2008 The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180 1131 1136
74. LahnBTPageDC 1999 Four evolutionary strata on the human X chromosome. Science 286 964 967
75. PresgravesDC 2002 Patterns of postzygotic isolation in Lepidoptera. Evolution 56 1168 1183
76. PriceTDBouvierMM 2002 The evolution of F1 postzygotic incompatibilities in birds. Evolution 56 2083 2089
77. CoyneJA 1992 Genetics and speciation. Nature 355 511 515
78. TurnerEJacobsonDJTaylorJW 2011 Genetic architecture of a reinforced, postmating, reproductive isolation barrier between Neurospora species indicates evolution via natural selection. PLoS Genet 7 e1002204 doi:10.1371/journal.pgen.1002204
79. MaheshwariR 2005 Nuclear behavior in fungal hyphae. FEMS Microbiol Lett 249 7 14
80. RoperMEllisonCTaylorJWGlassNL 2011 Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr Biol 21 R786 793
81. HillWGRobertsonA 1966 The effect of linkage on limits to artificial selection. Genet Res 8 269 294
82. GordoICharlesworthB 2001 Genetic linkage and molecular evolution. Curr Biol 11 R684 686
83. RandallTAMetzenbergRL 1995 Species-specific and mating type-specific DNA regions adjacent to mating type idiomorphs in the genus Neurospora. Genetics 141 119 136
84. RokasAWilliamsBLKingNCarrollSB 2003 Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425 798 804
85. JohannessonHStenlidJ 1999 Molecular identification of wood-inhabiting fungi from a primeval forest in Sweden. Forest Ecol Managm 115 203 211
86. LiHHandsakerBWysokerAFennellTRuanJ 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 2078 2079
87. YangZ 2006 Computational molecular evolution xvi Oxford Oxford University Press 357
88. StamatakisA 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 2688 2690
89. PosadaD 2008 jModelTest: phylogenetic model averaging. Mol Biol Evol 25 1253 1256
90. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797
91. WikLKarlssonMJohannessonH 2008 The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8 109
92. VillaltaCFJacobsonDJTaylorJW 2009 Three new phylogenetic and biological Neurospora species: N. hispaniola, N. metzenbergii and N. perkinsii. Mycologia 101 777 789
93. ZwicklD 2006 Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. [Ph.D. dissertation]. [PhD dissertation] The University of Texas Austin
94. RonquistFHuelsenbeckJP 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574
95. HuelsenbeckJPRonquistF 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755
96. RambautADrummondA TRACER V1.5. Available from http://beastbioedacuk/Tracer
97. NylanderJAWilgenbuschJCWarrenDLSwoffordDL 2008 AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24 581 583
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 7
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Guidelines for Genome-Wide Association Studies
- The Role of Rice HEI10 in the Formation of Meiotic Crossovers
- Identification of Chromatin-Associated Regulators of MSL Complex Targeting in Dosage Compensation
- GWAS Identifies Novel Susceptibility Loci on 6p21.32 and 21q21.3 for Hepatocellular Carcinoma in Chronic Hepatitis B Virus Carriers