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Ecological Genomics of Adaptation and Speciation in Fungi

  • Jean-Baptiste LeducqEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 781)

Abstract

Fungi play a central role in both ecosystems and human societies. This is in part because they have adopted a large diversity of life history traits to conquer a wide variety of ecological niches. Here, I review recent fungal genomics studies that explored the molecular origins and the adaptive significance of this diversity. First, macro-ecological genomics studies revealed that fungal genomes were highly remodelled during their evolution. This remodelling, in terms of genome organization and size, occurred through the proliferation of non-coding elements, gene compaction, gene loss and the expansion of large families of adaptive genes. These features vary greatly among fungal clades, and are correlated with different life history traits such as multicellularity, pathogenicity, symbiosis, and sexual reproduction. Second, micro-ecological genomics studies, based on population genomics, experimental evolution and quantitative trait loci approaches, have allowed a deeper exploration of early evolutionary steps of the above adaptations. Fungi, and especially budding yeasts, were used intensively to characterize early mutations and chromosomal rearrangements that underlie the acquisition of new adaptive traits allowing them to conquer new ecological niches and potentially leading to speciation. By uncovering the ecological factors and genomic modifications that underline adaptation, these studies showed that Fungi are powerful models for ecological genomics (eco-genomics), and that this approach, so far mainly developed in a few model species, should be expanded to the whole kingdom.

Keywords

Fungi Genomics Life history traits Adaptation Reproduction Population genomics Speciation Hybridization 

Notes

Acknowledgments

I address special thanks to Mary Thaler, Isabelle Gagnon-Arsenault, Guillaume Charron, Emilie Bernatchez, Marie Filteau, Luca Freschi, Philippe Reignault, Sylvain Billiard, Louis Bernier, Christian R. Landry and two anonymous reviewers for helpful comments. This work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant and a Human Frontier Science Program (HFSP) RGY0073/2010 grant allocated to Christian R. Landry. I was supported by a fellowship from the Fonds de Recherche en Santé du Québec (FRSQ).

Glossary

Endophyte

Organism spending its entire life cycle within a plant.

Heterokaryotic

When a cell contains two or more nuclei.

Heterothallism

When sexual reproduction can only occur between two phenotypically indistinct individuals from the same species, but expressing different sexual idiomorphs (allogamy). Mostly present in algae and Fungi.

Homothallism

When sexual reproduction can occur between any individuals from the same species (autogamy), in contrast to heterothallism – Pseudo-homothallism derives from heterothallism but the co-transmission of two sexual idiomorphs during meiosis allows autogamy.

Idiomorph – or Mating-type

Sexual determinants in eukaryotes. Designates compatible sexual partners during reproduction: for instance male and female in plants and animals or MAT-a and MAT-α in yeasts.

Mycorrhiza

Symbiosis between a fungus and roots of a vascular plant. Ectomycorrhiza perform the interaction within the host tissues whereas endomycorrhiza perform the symbiosis within the host cells.

Quantitative Trait Loci (QTL)

Portions of the genome physically co-segregating with an inherited trait, and thus physically linked to at least one gene involved in this trait.

Saprotroph

Fungi able to absorb nutrients from dead or decayed organic matter.

Spore

In Fungi, a unicellular, resistant reproductive structure formed by meiosis or mitosis, able to produce a new individual after possible dispersal and germination. Ascospores are spores produced by Ascomycota.

Symbiosis

Close and reciprocally beneficial interaction between two organisms of different species, providing each other with protection, suitable habitat or nutrients.

References

  1. Aa E, Townsend JP, Adams RI, Nielsen KM, Taylor JW (2006) Population structure and gene evolution in Saccharomyces cerevisiae. FEMS Yeast Res 6(5):702–715PubMedCrossRefGoogle Scholar
  2. Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M et al (2006) An overview of the higher level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98(6):896–905PubMedCrossRefGoogle Scholar
  3. Anderson JB, Funt J, Thompson DA, Prabhu S, Socha A, Sirjusingh C et al (2010) Determinants of divergent adaptation and Dobzhansky-Muller interaction in experimental yeast populations. Curr Biol 20(15):1383–1388PubMedCrossRefGoogle Scholar
  4. Araya CL, Payen C, Dunham MJ, Fields S (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11:88PubMedCrossRefGoogle Scholar
  5. Billiard S, Lopez-Villavicencio M, Devier B, Hood ME, Fairhead C, Giraud T (2011) Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev Camb Philos Soc 86(2):421–442PubMedCrossRefGoogle Scholar
  6. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS et al (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7(2):e1001287PubMedCrossRefGoogle Scholar
  7. Burmester A, Shelest E, Glockner G, Heddergott C, Schindler S, Staib P et al (2011) Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biol 12(1):R7PubMedCrossRefGoogle Scholar
  8. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA et al (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459(7247):657–662PubMedCrossRefGoogle Scholar
  9. Cai L, Giraud T, Zhang N, Begerow D, Cai GH, Shivas RG (2011) The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Divers 50(1):121–133CrossRefGoogle Scholar
  10. Chang SL, Lai HY, Tung SY, Leu JY (2013) Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLoS Genet 9(1):e1003232PubMedCrossRefGoogle Scholar
  11. Cowen LE, Nantel A, Whiteway MS, Thomas DY, Tessier DC, Kohn LM et al (2002) Population genomics of drug resistance in Candida albicans. Proc Natl Acad Sci USA 99(14):9284–9289PubMedCrossRefGoogle Scholar
  12. Cubillos FA, Billi E, Zorgo E, Parts L, Fargier P, Omholt S et al (2011) Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol Ecol 20(7):1401–1413PubMedCrossRefGoogle Scholar
  13. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK et al (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109(13):5110–5115PubMedCrossRefGoogle Scholar
  14. Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ, Oliver SG (2003) Engineering evolution to study speciation in yeasts. Nature 422(6927):68–72PubMedCrossRefGoogle Scholar
  15. Demogines A, Wong A, Aquadro C, Alani E (2008) Incompatibilities involving yeast mismatch repair genes: a role for genetic modifiers and implications for disease penetrance and variation in genomic mutation rates. PLoS Genet 4(6):e1000103PubMedCrossRefGoogle Scholar
  16. Demuth JP, De Bie T, Stajich JE, Cristianini N, Hahn MW (2006) The evolution of mammalian gene families. PLoS One 1(1):e85PubMedCrossRefGoogle Scholar
  17. Dettman JR, Jacobson DJ, Taylor JW (2003a) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57(12):2703–2720PubMedGoogle Scholar
  18. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003b) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution 57(12):2721–2741PubMedGoogle Scholar
  19. Dujon B (2005) Hemiascomycetous yeasts at the forefront of comparative genomics. Curr Opin Genet Dev 15(6):614–620PubMedCrossRefGoogle Scholar
  20. Dujon B (2006) Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet 22(7):375–387PubMedCrossRefGoogle Scholar
  21. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I et al (2004) Genome evolution in yeasts. Nature 430(6995):35–44PubMedCrossRefGoogle Scholar
  22. Dunn B, Sherlock G (2008) Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Res 18(10):1610–1623PubMedCrossRefGoogle Scholar
  23. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, Kroll E et al (2013) Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet 9(3):e1003366PubMedCrossRefGoogle Scholar
  24. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL et al (2011a) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci USA 108(7):2831–2836PubMedCrossRefGoogle Scholar
  25. Ellison CE, Stajich JE, Jacobson DJ, Natvig DO, Lapidus A, Foster B et al (2011b) Massive changes in genome architecture accompany the transition to self-fertility in the Filamentous Fungus Neurospora tetrasperma. Genetics 189(1):55–69, U652PubMedCrossRefGoogle Scholar
  26. Fernandez-Fueyo E, Ruiz-Duenas FJ, Ferreira P, Floudas D, Hibbett DS, Canessa P et al (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci USA 109(14):5458–5463PubMedCrossRefGoogle Scholar
  27. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715–1719PubMedCrossRefGoogle Scholar
  28. Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, Dietrich FS et al (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2(12):e384PubMedCrossRefGoogle Scholar
  29. Fraser JA, Stajich JE, Tarcha EJ, Cole GT, Inglis DO, Sil A et al (2007) Evolution of the mating type locus: insights gained from the dimorphic primary fungal pathogens Histoplasma capsulatum, Coccidioides immitis, and Coccidioides posadasii. Eukaryot Cell 6(4):622–629PubMedCrossRefGoogle Scholar
  30. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, Shang Y et al (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7(1):e1001264PubMedCrossRefGoogle Scholar
  31. Giraud T, Refregier G, Le Gac M, de Vienne DM, Hood ME (2008) Speciation in fungi. Fungal Genet Biol 45(6):791–802PubMedCrossRefGoogle Scholar
  32. Gomes AC, Miranda I, Silva RM, Moura GR, Thomas B, Akoulitchev A et al (2007) A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol 8(10):R206PubMedCrossRefGoogle Scholar
  33. Goodwin SB, M’Barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK et al (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7(6):e1002070PubMedCrossRefGoogle Scholar
  34. Gordon JL, Armisen D, Proux-Wera E, OhEigeartaigh SS, Byrne KP, Wolfe KH (2011) Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. Proc Natl Acad Sci USA 108(50):20024–20029PubMedCrossRefGoogle Scholar
  35. Gourbiere S, Mallet J (2010) Are species real? The shape of the species boundary with exponential failure, reinforcement, and the “missing snowball”. Evolution 64(1):1–24PubMedCrossRefGoogle Scholar
  36. Greig D (2007) A screen for recessive speciation genes expressed in the gametes of F1 hybrid yeast. PLoS Genet 3(2):e21PubMedCrossRefGoogle Scholar
  37. Greig D, Borts RH, Louis EJ, Travisano M (2002) Epistasis and hybrid sterility in Saccharomyces. Proc R Soc B 269(1496):1167–1171PubMedCrossRefGoogle Scholar
  38. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D et al (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40(Database issue):D26–D32PubMedCrossRefGoogle Scholar
  39. Hane JK, Rouxel T, Howlett BJ, Kema GHJ, Goodwin SB, Oliver RP (2011) A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 12(5):R45PubMedCrossRefGoogle Scholar
  40. Hibbett DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 98(6):917–925PubMedCrossRefGoogle Scholar
  41. Hibbett DS, Taylor JW (2013) Fungal systematics: is a new age of enlightenment at hand? Nat Rev Microbiol 11(2):129–133PubMedCrossRefGoogle Scholar
  42. Hittinger CT, Goncalves P, Sampaio JP, Dover J, Johnston M, Rokas A (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464(7285):54–58PubMedCrossRefGoogle Scholar
  43. Hyma KE, Fay JC (2013) Mixing of vineyard and oak-tree ecotypes of Saccharomyces cerevisiae in North American vineyards. Mol Ecol 22:2917PubMedCrossRefGoogle Scholar
  44. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ et al (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443(7113):818–822PubMedCrossRefGoogle Scholar
  45. Joneson S, Stajich JE, Shiu SH, Rosenblum EB (2011) Genomic transition to pathogenicity in Chytrid fungi. PLoS Pathog 7(11):e1002338PubMedCrossRefGoogle Scholar
  46. Kao KC, Schwartz K, Sherlock G (2010) A genome-wide analysis reveals no nuclear Dobzhansky-Muller pairs of determinants of speciation between S. Cerevisiae and S. Paradoxus, but suggests more complex incompatibilities. PLoS Genet 6(7):e1001038PubMedCrossRefGoogle Scholar
  47. Kelkar YD, Ochman H (2012) Causes and consequences of genome expansion in fungi. Genome Biol Evol 4(1):13–23PubMedCrossRefGoogle Scholar
  48. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428(6983):617–624PubMedCrossRefGoogle Scholar
  49. Kendrick B (2001) Fungi: ecological importance and impact on humans. In: eLS. Wiley & Sons, Ltd: ChichesterGoogle Scholar
  50. Kohn LM (2005) Mechanisms of fungal speciation. Annu Rev Phytopathol 43:279–308PubMedCrossRefGoogle Scholar
  51. Koonin EV (2011) The logic of chance: the nature and origin of biological evolution. Ft Press, Upper Saddle RiverGoogle Scholar
  52. Kuehne HA, Murphy HA, Francis CA, Sniegowski PD (2007) Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Curr Biol 17(5):407–411PubMedCrossRefGoogle Scholar
  53. Leducq JB, Charron G, Diss G, Gagnon-Arsenault I, Dube AK, Landry CR (2012) Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genet 8(12):e1003161PubMedCrossRefGoogle Scholar
  54. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, Leu JY (2008) Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135(6):1065–1073PubMedCrossRefGoogle Scholar
  55. Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, Heitman J (2010) Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLoS One 5(5):e10539PubMedCrossRefGoogle Scholar
  56. Libkind D, Hittinger CT, Valerio E, Goncalves C, Dover J, Johnston M et al (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci USA 108(35):14539–14544PubMedCrossRefGoogle Scholar
  57. Liti G, Barton DB, Louis EJ (2006) Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174(2):839–850PubMedCrossRefGoogle Scholar
  58. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA et al (2009a) Population genomics of domestic and wild yeasts. Nature 458(7236):337–341PubMedCrossRefGoogle Scholar
  59. Liti G, Haricharan S, Cubillos FA, Tierney AL, Sharp S, Bertuch AA et al (2009b) Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet 5(9):e1000659PubMedCrossRefGoogle Scholar
  60. Louis VL, Despons L, Friedrich A, Martin T, Durrens P, Casaregola S et al (2012) Pichia sorbitophila, an interspecies yeast hybrid, reveals early steps of genome resolution after polyploidization. G3 (Bethesda) 2(2):299–311CrossRefGoogle Scholar
  61. Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M et al (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5(7):e1000549PubMedCrossRefGoogle Scholar
  62. Magwene PM, Kayikci O, Granek JA, Reininga JM, Scholl Z, Murray D (2011) Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 108(5):1987–1992PubMedCrossRefGoogle Scholar
  63. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F et al (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452(7183):88–92PubMedCrossRefGoogle Scholar
  64. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O et al (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464(7291):1033–1038PubMedCrossRefGoogle Scholar
  65. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP et al (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106(6):1954–1959PubMedCrossRefGoogle Scholar
  66. Menkis A, Jacobson DJ, Gustafsson T, Johannesson H (2008) The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet 4(3):e1000030PubMedCrossRefGoogle Scholar
  67. Metin B, Findley K, Heitman J (2010) The mating type locus (MAT) and sexual reproduction of Cryptococcus heveanensis: insights into the evolution of sex and sex-determining chromosomal regions in fungi. PLoS Genet 6(5):e1000961PubMedCrossRefGoogle Scholar
  68. Muller LA, Lucas JE, Georgianna DR, McCusker JH (2011) Genome-wide association analysis of clinical vs. nonclinical origin provides insights into Saccharomyces cerevisiae pathogenesis. Mol Ecol 20(19):4085–4097PubMedCrossRefGoogle Scholar
  69. Nash TH (2008) Lichen biology, 2nd edn. Cambridge University Press, Cambridge/New YorkCrossRefGoogle Scholar
  70. Neafsey DE, Barker BM, Sharpton TJ, Stajich JE, Park DJ, Whiston E et al (2010) Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res 20(7):938–946PubMedCrossRefGoogle Scholar
  71. Nicholson MJ, McSweeney CS, Mackie RI, Brookman JL, Theodorou MK (2010) Diversity of anaerobic gut fungal populations analysed using ribosomal ITS1 sequences in faeces of wild and domesticated herbivores. Anaerobe 16(2):66–73PubMedCrossRefGoogle Scholar
  72. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW et al (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8(12):e1003037PubMedCrossRefGoogle Scholar
  73. Peyretaillade E, El Alaoui H, Diogon M, Polonais V, Parisot N, Biron DG et al (2011) Extreme reduction and compaction of microsporidian genomes. Res Microbiol 162(6):598–606PubMedCrossRefGoogle Scholar
  74. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47(4):376–391CrossRefGoogle Scholar
  75. Rep M, Kistler HC (2010) The genomic organization of plant pathogenicity in Fusarium species. Curr Opin Plant Biol 13(4):420–426PubMedCrossRefGoogle Scholar
  76. Rice DP, Townsend JP (2012) A test for selection employing quantitative trait locus and mutation accumulation data. Genetics 190(4):1533–1545PubMedCrossRefGoogle Scholar
  77. Rocha R, Pereira PJ, Santos MA, Macedo-Ribeiro S (2011) Unveiling the structural basis for translational ambiguity tolerance in a human fungal pathogen. Proc Natl Acad Sci USA 108(34):14091–14096PubMedCrossRefGoogle Scholar
  78. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L (2006) Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38(9):1077–1081PubMedCrossRefGoogle Scholar
  79. San-Blas G, Calderone RA (2008) Pathogenic fungi: insights in molecular biology. Caister Academic Press, NorfolkGoogle Scholar
  80. Santana MF, Silva JC, Batista AD, Ribeiro LE, da Silva GF, de Araujo EF et al (2012) Abundance, distribution and potential impact of transposable elements in the genome of Mycosphaerella fijiensis. BMC Genomics 13(1):720PubMedCrossRefGoogle Scholar
  81. Schacherer J, Shapiro JA, Ruderfer DM, Kruglyak L (2009) Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458(7236):342–345PubMedCrossRefGoogle Scholar
  82. Sniegowski PD, Dombrowski PG, Fingerman E (2002) Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res 1(4):299–306PubMedGoogle Scholar
  83. Souciet JL, Dujon B, Gaillardin C, Johnston M, Baret PV, Cliften P et al (2009) Comparative genomics of protoploid Saccharomycetaceae. Genome Res 19(10):1696–1709PubMedCrossRefGoogle Scholar
  84. Stajich JE, Berbee ML, Blackwell M, Hibbett DS, James TY, Spatafora JW et al (2009) The fungi. Curr Biol 19(18):R840–R845PubMedCrossRefGoogle Scholar
  85. Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R, Zala M et al (2011) The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res 21(12):2157–2166PubMedCrossRefGoogle Scholar
  86. Sun S, Heitman J (2011) Is sex necessary? BMC Biol 9(56)Google Scholar
  87. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS et al (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31(1):21–32PubMedCrossRefGoogle Scholar
  88. Taylor JW, Turner E, Townsend JP, Dettman JR, Jacobson D (2006) Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom fungi. Philos Trans R Soc B 361(1475):1947–1963CrossRefGoogle Scholar
  89. Tsai IJ, Bensasson D, Burt A, Koufopanou V (2008) Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc Natl Acad Sci USA 105(12):4957–4962PubMedCrossRefGoogle Scholar
  90. Tsui CKM, DiGuistini S, Wang Y, Feau N, Dhillon B, Bohlmann J et al (2013) Unequal recombination and evolution of the Mating-Type (MAT) Loci in the pathogenic fungus Grosmannia clavigera and relatives. G3-Genes Genom Genet 3(3):465–480Google Scholar
  91. Votintseva AA, Filatov DA (2009) Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182(4):1391–1396PubMedCrossRefGoogle Scholar
  92. Wang H, Xu Z, Gao L, Hao B (2009) A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol Biol 9:195PubMedCrossRefGoogle Scholar
  93. Wang QM, Liu WQ, Liti G, Wang SA, Bai FY (2012a) Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol Ecol 21(22):5404–5417PubMedCrossRefGoogle Scholar
  94. Wang Z, Kin K, Lopez-Giraldez F, Johannesson H, Townsend JP (2012b) Sex-specific gene expression during asexual development of Neurospora crassa. Fungal Genet Biol 49(7):533–543PubMedCrossRefGoogle Scholar
  95. Warringer J, Zorgo E, Cubillos FA, Zia A, Gjuvsland A, Simpson JT et al (2011) Trait variation in yeast is defined by population history. PLoS Genet 7(6):e1002111PubMedCrossRefGoogle Scholar
  96. Whittle CA, Johannesson H (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 (Edinb) 107(4):305–314CrossRefGoogle Scholar
  97. Whittle CA, Sun Y, Johannesson H (2011) Degeneration in codon usage within the region of suppressed recombination in the mating-type chromosomes of Neurospora tetrasperma. Eukaryot Cell 10(4):594–603PubMedCrossRefGoogle Scholar
  98. Wik L, Karlsson M, Johannesson H (2008) The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8:109PubMedCrossRefGoogle Scholar
  99. Will JL, Kim HS, Clarke J, Painter JC, Fay JC, Gasch AP (2010) Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLoS Genet 6(4):e1000893PubMedCrossRefGoogle Scholar
  100. Xu M, He X (2011) Genetic incompatibility dampens hybrid fertility more than hybrid viability: yeast as a case study. PLoS One 6(4):e18341PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Institut de Biologie Intégrative et des Systèmes, Département de Biologie, PROTEO, Pavillon Charles-Eugène-MarchandUniversité LavalQuébecCanada

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