Genetic Architecture of a Reinforced, Postmating, Reproductive Isolation Barrier between Species Indicates Evolution via Natural Selection
A role for natural selection in reinforcing premating barriers is recognized, but selection for reinforcement of postmating barriers remains controversial. Organisms lacking evolvable premating barriers can theoretically reinforce postmating isolation, but only under restrictive conditions: parental investment in hybrid progeny must inhibit subsequent reproduction, and selected postmating barriers must restore parents' capacity to reproduce successfully. We show that reinforced postmating isolation markedly increases maternal fitness in the fungus Neurospora crassa, and we detect the evolutionary genetic signature of natural selection by quantitative trait locus (QTL) analysis of the reinforced barrier. Hybrid progeny of N. crassa and N. intermedia are highly inviable. Fertilization by local N. intermedia results in early abortion of hybrid fruitbodies, and we show that abortion is adaptive because only aborted maternal colonies remain fully receptive to future reproduction. In the first QTL analysis of postmating reinforcement in microbial eukaryotes, we identify 11 loci for abortive hybrid fruitbody development, including three major QTLs that together explain 30% of trait variance. One of the major QTLs and six QTLs of lesser effect are found on the mating-type determining chromosome of Neurospora. Several reinforcement QTLs are flanked by genetic markers showing either segregation distortion or non-random associations with alleles at other loci in a cross between N. crassa of different clades, suggesting that the loci also are associated with local effects on same-species reproduction. Statistical analysis of the allelic effects distribution for abortive hybrid fruitbody development indicates its evolution occurred under positive selection. Our results strongly support a role for natural selection in the evolution of reinforced postmating isolation in N. crassa.
Vyšlo v časopise:
Genetic Architecture of a Reinforced, Postmating, Reproductive Isolation Barrier between Species Indicates Evolution via Natural Selection. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002204
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002204
Souhrn
A role for natural selection in reinforcing premating barriers is recognized, but selection for reinforcement of postmating barriers remains controversial. Organisms lacking evolvable premating barriers can theoretically reinforce postmating isolation, but only under restrictive conditions: parental investment in hybrid progeny must inhibit subsequent reproduction, and selected postmating barriers must restore parents' capacity to reproduce successfully. We show that reinforced postmating isolation markedly increases maternal fitness in the fungus Neurospora crassa, and we detect the evolutionary genetic signature of natural selection by quantitative trait locus (QTL) analysis of the reinforced barrier. Hybrid progeny of N. crassa and N. intermedia are highly inviable. Fertilization by local N. intermedia results in early abortion of hybrid fruitbodies, and we show that abortion is adaptive because only aborted maternal colonies remain fully receptive to future reproduction. In the first QTL analysis of postmating reinforcement in microbial eukaryotes, we identify 11 loci for abortive hybrid fruitbody development, including three major QTLs that together explain 30% of trait variance. One of the major QTLs and six QTLs of lesser effect are found on the mating-type determining chromosome of Neurospora. Several reinforcement QTLs are flanked by genetic markers showing either segregation distortion or non-random associations with alleles at other loci in a cross between N. crassa of different clades, suggesting that the loci also are associated with local effects on same-species reproduction. Statistical analysis of the allelic effects distribution for abortive hybrid fruitbody development indicates its evolution occurred under positive selection. Our results strongly support a role for natural selection in the evolution of reinforced postmating isolation in N. crassa.
Zdroje
1. DarwinC 1876 On the Origin of Species by Means of Natural Selection London John Murray
2. WallaceAR 1889 Darwinism: an Exposition of the Theory of Natural Selection, with Some of its Applications London MacMillan & Co
3. MarchantJ 1916 Alfred Russel Wallace: Letters and Reminiscences London Cassell and Co
4. FisherRA 1930 The genetical theory of natural selection Oxford Clarendon Press
5. DobzhanskyT 1937 Genetics and the origin of species New York Columbia University Press
6. CoyneJAOrrHA 2004 Speciation Sunderland, MA Sinauer Associates, Inc
7. CoyneJA 1974 The evolutionary origin of hybrid inviability. Evolution 28 505 506
8. JohnsonNAWadeMJ 1995 Conditions for soft selection favoring the evolution of hybrid inviability. Journal of Theoretical Biology 176 493 499
9. WallaceB 1988 Selection for the inviability of sterile hybrids. J Hered 79 204 210
10. Le GacMGiraudT 2008 Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota. Journal of Evolutionary Biology 21 761 772
11. MacleanCJGreigD 2008 Prezygotic reproductive isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus. Bmc Evolutionary Biology 8
12. GrantV 1966 The selective origin of incompatibility barriers in the plant genus Gilia. American Naturalist 100 99 118
13. StephensSG 1946 The Genetics of Corky .1. The New World Alleles and Their Possible Role as an Interspecific Isolating Mechanism. Journal of Genetics 47 150
14. MatuteDR 2010 Reinforcement of gametic isolation in drosophila. PLoS Biol 8 e1000341 doi:10.1371/journal.pbio.1000341
15. DettmanJRJacobsonDJTurnerEPringleATaylorJW 2003 Reproductive isolation and phylogenetic divergence in Neurospora: Comparing methods of species recognition in a model eukaryote. Evolution 57 2721 2741
16. TurnerEJacobsonDJTaylorJW 2010 Biogeography of postmating reproductive isolation barriers is consistent with reinforcement selection in Neurospora, a model microbial eukaryote. Journal of Evolutionary Biology 23 1642 1656
17. PerkinsDDTurnerBCBarryEG 1976 Strains of Neurospora collected from nature. Evolution 30 281 313
18. TurnerBCPerkinsDDFairfieldA 2001 Neurospora from natural populations: A global study. Fungal Genetics and Biology 32 67 92
19. SpiethPT 1975 Population genetics of allozyme variation in Neurospora intermedia. Genetics 80 785 805
20. PerkinsDDTurnerBC 1988 Neurospora from natural populations: toward the population biology of a haploid eukaryote. Experimental Mycology 12 91 131
21. DettmanJRJacobsonDJTaylorJW 2003 A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57 2703 2720
22. DettmanJRTaylorJW 2004 Mutation and evolution of microsatellite loci in neurospora. Genetics 168 1231 1248
23. StrandbergRNygrenKMenkisAJamesTYWikL 2010 Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora. Fungal Genetics and Biology 46 869 878
24. 2010 Fungal genomics program. Joint Genome Institute
25. PoggelerS 2000 Two pheromone precursor genes are transcriptionally expressed in the homothallic ascomycete Sordaria macrospora. Current Genetics V37 403 411
26. KarlssonMNygrenKJohannessonH 2008 The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Molecular Biology and Evolution 25 168 178
27. HoweHBPrakashV 1969 A regulatory system controlling inhibition in the sexual cycle of Neurospora. Can J Genet Cytol 11 689 705
28. CoxDR 1972 Regression models and life-tables. Journal of the Royal Statistical Society Series B (Methodological) 34 187 220
29. Ortiz-BarrientosDCountermanBANoorMAF 2004 The genetics of speciation by reinforcement. PLoS Biol 2 e416 doi:10.1371/journal.pbio.0020416
30. Ortiz-BarrientosDNoorMA 2005 Evidence for a one-allele assortative mating locus. Science 310 1467
31. SaetherSASaetreGPBorgeTWileyCSvedinN 2007 Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318 95 97
32. OrrHA 1998 Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149 2099 2104
33. AndersonECSlatkinM 2003 Orr's quantitative trait loci sign test under conditions of trait ascertainment. Genetics 165 445 446
34. BatesonW 1909 Heredity and variation in modern lights. SewardAC Darwin and Modern Science Cambridge Cambridge University Press 85 101
35. EllisonCEHallCKowbelDWelchJBremRB 2011 Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci U S A In press
36. 2010 Neurospora crassa database. Broad Institute
37. NosilPCrespiBJSandovalCP 2003 Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proceedings of the Royal Society Biological Sciences Series B 270 1911 1918
38. HoskinCJHiggieM 2010 Speciation via species interactions: the divergence of mating traits within species. Ecology Letters 13 409 420
39. TaoYChenSHartlDLLaurieCC 2003 Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164 1383 1397
40. TrueJRWeirBSLaurieCC 1996 A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142 819 837
41. 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
42. DettmanJRAndersonJBKohnLM 2008 Divergent adaptatioin promotes reproductive isolation among experimental populations of the filamentous fungus Neurospora. BMC Evol Biol 8 35
43. DettmanJRAndersonJBKohnLM 2010 Genome-wide investigation of reproductive isolation in experimental lineages and natural species of Neurospora: Identifying candidate regions by microarray-based genotyping and mapping. Evolution 64 694 709
44. LeuJ-YMurrayAW 2006 Experimental evolution of mating discrimination in budding yeast. Current Biology 16 280 286
45. KorbeckaGKlinkhamerPGLKV 2002 Selective embryo abortion hypothesis revisited—a molecular approach. Plant Biology (Stuttgart) 4 298 310
46. PoggelerSKuckU 2000 Comparative analysis of the mating-type loci from Neurospora crassa and Sordaria macrospora: identification of novel transcribed ORFs. Molecular and General Genetics V263 292 301
47. KaraogluHLeeCMYMeyerW 2005 Survey of simple sequence repeats in completed fungal genomes. Molecular Biology and Evolution 22 639 649
48. RozenSSkaletskyH 2000 Primer3 on the WWW for general users and biologist programmers. Methods in Molecular Biology 132 365 386
49. LanderESGreenPAbrahamsonJBarlowADalyMJ 1987 Mapmaker an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1 174 181
50. BromanKWWuHSenSChurchillGA 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19 889 890
51. RaymondMRoussetF 1995 Genepop (Version-1.2) - Population-genetics software for exact tests and ecumenicism. Journal of Heredity 86 248 249
52. WangSBastenCJZengZ-B 2010 Windows QTL Cartographer 2.5. Department of Statistics. North Carolina State University, Raleigh, NC
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 8
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