Functional organization of the genome may shape the species boundary in the house mouse
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
25631927
PubMed Central
PMC4408407
DOI
10.1093/molbev/msv011
PII: msv011
Knihovny.cz E-zdroje
- Klíčová slova
- hybrid zone, mouse genome, speciation,
- MeSH
- druhová specificita MeSH
- genom * MeSH
- jednonukleotidový polymorfismus MeSH
- myši MeSH
- reprodukční izolace * MeSH
- selekce (genetika) * MeSH
- vznik druhů (genetika) * MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Genomic features such as rate of recombination and differentiation have been suggested to play a role in species divergence. However, the relationship of these phenomena to functional organization of the genome in the context of reproductive isolation remains unexplored. Here, we examine genomic characteristics of the species boundaries between two house mouse subspecies (Mus musculus musculus/M. m. domesticus). These taxa form a narrow semipermeable zone of secondary contact across Central Europe. Due to the incomplete nature of reproductive isolation, gene flow in the zone varies across the genome. We present an analysis of genomic differentiation, rate of recombination, and functional composition of genes relative to varying amounts of introgression. We assessed introgression using 1,316 autosomal single nucleotide polymorphism markers, previously genotyped in hybrid populations from three transects. We found a significant relationship between amounts of introgression and both genomic differentiation and rate of recombination with genomic regions of reduced introgression associated with higher genomic differentiation and lower rates of recombination, and the opposite for genomic regions of extensive introgression. We also found a striking functional polarization of genes based on where they are expressed in the cell. Regions of elevated introgression exhibit a disproportionate number of genes involved in signal transduction functioning at the cell periphery, among which olfactory receptor genes were found to be the most prominent group. Conversely, genes expressed intracellularly and involved in DNA binding were the most prevalent in regions of reduced introgression. We hypothesize that functional organization of the genome is an important driver of species divergence.
Department of Biology Northern Michigan University
Department of Ecology and Evolutionary Biology and Museum of Zoology University of Michigan
Department of Zoology Faculty of Science Charles University Prague Prague Czech Republic
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Albrechtová J, Albrecht T, Baird SJ, Macholán M, Rudolfsen G, Munclinger P, Tucker PK, Piálek J. Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse. Proc Biol Sci. 2012;279:4803–4810. PubMed PMC
Anderson E, Hubricht L. Hybridization in Tradescantia. III. The evidence for introgressive hybridization. Am J Bot. 1938;25:396–402.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000;25:25–29. PubMed PMC
Barbash DA, Siino DF, Tarone AM, Roote J. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A. 2003;1009:5302–5307. PubMed PMC
Barton N, Bengtsson BO. The barrier to genetic exchange between hybridising populations. Heredity. 1986;57:357–376. PubMed
Barton NH. Multilocus clines. Evolution. 1983;37:454–471. PubMed
Barton NH, Hewitt GM. Analysis of hybrid zones. Annu Rev Ecol Syst. 1985;16:113–148.
Bayes JJ, Malik HS. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science. 2009;326:1538–1541. PubMed PMC
Bierne N, Welch J, Loire E, Bonhomme F, David P. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol. 2011;20:2044–2072. PubMed
Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science. 2006;314:1292–1295. PubMed
Britton-Davidian J, Fel-Clair F, Lopez J, Alibert P, Boursot P. Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biol J Linn Soc. 2005;84:379–393.
Butlin RK. Recombination and speciation. Mol Ecol. 2005;14:2621–2635. PubMed
Cox A, Ackert-Bicknell CL, Dumont BL, Ding Y, Bell JT, Brockmann GA, Wergedal JE, Bult C, Paigen B, Flint J, et al. A new standard genetic map for the laboratory mouse. Genetics. 2009;182:1335–1344. PubMed PMC
Coyne JA, Orr HA. Speciation. Sunderland (MA): Sinauer Associates; 2004.
Cruickshank TE, Hahn MW. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol. 2014;23:3133–3157. PubMed
Davisson MT, Roderick TH, Doolittle DP. Recombination percentages and chromosomal assignments. In: Lyon MF, Searle AG, editors. Genetic variants and strains of the laboratory mouse. Oxford: Oxford University Press; 1989. pp. 432–505.
Dobzhansky T. Studies on hybrid sterility. 11. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics. 1936;21:113–135. PubMed PMC
Duvaux L, Belkhir K, Boulesteix M, Boursot P. Isolation and gene flow: inferring the speciation history of European house mice. Mol Ecol. 2011;20:5248–5264. PubMed
Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, Künstner A, Mäkinen H, Nadachowska-Brzyska K, Qvarnström A, et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature. 2012;491:756–760. PubMed
Feder JL, Gejji R, Yeaman S, Nosil P. Establishment of new mutations under divergence and genome hitchhiking. Philos Trans R Soc Lond B Biol Sci. 2012;367:461–474. PubMed PMC
Ferree PM, Barbash DA. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 2009;7:e1000234. PubMed PMC
Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. Ensembl 2014. Nucleic Acids Res. 2014;42:D749–D755. PubMed PMC
Forejt J, Iványi P. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.) Genet Res. 1974;24:189–206. PubMed
Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, Belmont JW, Boudreau A, Hardenbol P, Leal SM. A second generation human haplotype map of over 3.1 million SNPs. Nature. 2007;449:851–861. PubMed PMC
Geraldes A, Basset P, Gibson B, Smith KL, Harr B, Yu HT, Bulatova N, Ziv Y, Nachman MW. Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol. 2008;17:5349–5363. PubMed PMC
Geraldes A, Basset P, Smith KL, Nachman MW. Higher differentiation among subspecies of the house mouse (Mus musculus) in genomic regions with low recombination. Mol Ecol. 2011;20:4722–4736. PubMed PMC
Godfrey PA, Malnic B, Buck LB. The mouse olfactory receptor gene family. Proc Natl Acad Sci U S A. 2004;101:2156–2161. PubMed PMC
Gompert Z, Buerkle CA. Bayesian estimation of genomic clines. Mol Ecol. 2011;20:2111–2127. PubMed
Gompert Z, Buerkle CA. bgc: software for Bayesian estimation of genomic clines. Mol Ecol Resour. 2012;12:1168–1176. PubMed
Good JM, Dean MD, Nachman MW. A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics. 2008;179:2213–2228. PubMed PMC
Good JM, Handel MA, Nachman MW. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution. 2008;62:50–65. PubMed PMC
Harr B. Genomic islands of differentiation between house mouse subspecies. Genome Res. 2006;16:730–737. PubMed PMC
Hedrick PW. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol. 2013;22:4606–4618. PubMed
Janoušek V, Wang L, Luzynski K, Dufková P, Vyskočilová MM, Nachman MW, Munclinger P, Macholán M, Piálek J, Tucker PK. Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol Ecol. 2012;21:3032–3047. PubMed PMC
Kim PM, Korbel JO, Gerstein MB. Positive selection at the protein network periphery: evaluation in terms of structural constraints and cellular context. Proc Natl Acad Sci U S A. 2007;104:20274–20279. PubMed PMC
Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25:1–18.
Macholán M, Baird SJ, Munclinger P, Dufková P, Bímová B, Piálek J. Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? BMC Evol Biol. 8. 2008:271. PubMed PMC
Mihola O, Trachtulec Z, Vlček C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009;323:373–375. PubMed
Muller HJ. Bearing of the Drosophila work on systematics. In: Huxley JS, editor. The new systematics. Oxford: Clarendon Press; 1940. pp. 185–268.
Muller HJ. Isolating mechanisms, evolution, and temperature. Biol Symp. 1942;6:71–125.
Nachman MW, Payseur BA. Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philos Trans R Soc Lond B Biol Sci. 2012;367:409–421. PubMed PMC
Noor MA, Bennett SM. Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity. 2009;103:439–444. PubMed PMC
Nosil P, Feder JL. Genomic divergence during speciation: causes and consequences. Philos Trans R Soc Lond B Biol Sci. 2012;367:332–342. PubMed PMC
Nosil P, Funk DJ, Ortiz-Barrientos D. Divergent selection and heterogeneous genomic divergence. Mol Ecol. 2009;18:375–402. PubMed
Orr HA, Masly JP, Presgraves DC. Speciation genes. Curr Opin Genet Dev. 2004;14:675–679. PubMed
Payseur BA. Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol Ecol Resour. 2010;10:806–820. PubMed
Phadnis N, Orr HA. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science. 2009;323:376–379. PubMed PMC
Phifer-Rixey M, Bomhoff M, Nachman MW. Genome-wide patterns of differentiation among house mouse subspecies. Genetics. 2014;198:283–297. PubMed PMC
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team. 2014. nlme: linear and nonlinear mixed effects models. R package version 3.1-117. Available from: http://CRAN.R-project.org/package=nlme.
Presgraves DC. The molecular evolutionary basis of species formation. Nat Rev Genet. 2010;11:175–180. PubMed
Presgraves DC, Balagopalan L, Abmayr SM, Orr HA. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature. 2003;423:715–719. PubMed
Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. PubMed PMC
R Development Core Team. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2014.
Renaut S, Grassa CJ, Yeaman S, Moyers BT, Lai Z, Kane NC, Bowers JE, Burke JM, Rieseberg LH. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nat Commun. 2013;4:1827. PubMed
Ruegg K, Anderson EC, Boone J, Pouls J, Smith TB. A role for migration-linked genes and genomic islands in divergence of a songbird. Mol Ecol. 2014;23:4757–4769. PubMed
Salcedo T, Geraldes A, Nachman MW. Nucleotide variation in wild and inbred mice. Genetics. 2007;177:2277–2291. PubMed PMC
Sánchez-Pla A, Salicrú M, Ocaña J. Statistical methods for the analysis of high-throughput data based on functional profiles derived from the gene ontology. J Stat Plan Inference. 2007;137:3975–3989.
Sarkar D. Lattice: multivariate data visualization with R. New York: Springer; 2008.
Sawamura K, Yamamoto MT. Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity. 1997;79:97–103.
Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, Peichel CL, Saetre GP, Bank C, Brännström A, et al. Genomics and the origin of species. Nat Rev Genet. 2014;15:176–192. PubMed
Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, Mott R, Flint J. A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol. 2006;4:e395. PubMed PMC
Staubach F, Lorenc A, Messer PW, Tang K, Petrov DA, Tautz D. Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus) PLoS Genet. 2012;8:e1002891. PubMed PMC
Storchová R, Gregorová S, Buckiová D, Kyselová V, Divina P, Forejt J. Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm Genome. 2004;15:515–524. PubMed
Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22:1540–1542. PubMed
Tan PN, Steinbach M, Kumar V. Introduction to data mining. Boston: Addison-Wesley Longman Publishing Co., Inc; 2005.
Tang S, Presgraves DC. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science. 2009;323:779–782. PubMed PMC
Teeter KC, Payseur BA, Harris LW, Bakewell MA, Thibodeau LM, O’Brien JE, Krenz JG, Sans-Fuentes MA, Nachman MW, Tucker PK. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 2008;18:67–76. PubMed PMC
Teeter KC, Thibodeau LM, Gompert Z, Buerkle CA, Nachman MW, Tucker PK. The variable genomic architecture of isolation between hybridizing species of house mice. Evolution. 2010;64:472–485. PubMed
Ting CT, Tsaur SC, Wu ML, Wu CI. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998;282:1501–1504. PubMed
Turner LM, Schwahn DJ, Harr B. Reduced male fertility is common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution. 2012;66:443–458. PubMed
Turner TL, Hahn MW, Nuzhdin SV. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 2005;3:e285. PubMed PMC
Vošlajerová-Bímová B, Macholán M, Baird SJ, Munclinger P, Dufková P, Laukaitis CM, Karn RC, Luzynski K, Tucker PK, Piálek J. Reinforcement selection acting on the European house mouse hybrid zone. Mol Ecol. 2011;20:2403–2424. PubMed
Vyskočilová M, Pražanová G, Piálek J. Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17. Mamm Genome. 2009;20:83–91. PubMed
Vyskočilová M, Trachtulec Z, Forejt J, Piálek J. Does geography matter in hybrid sterility in house mice? Biol J Linn Soc. 2005;84:663–674.
Wang L, Luzynski K, Pool JE, Janoušek V, Dufková P, Vyskočilová MM, Teeter KC, Nachman MW, Munclinger P, Macholán M, et al. Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone. Mol Ecol. 2011;20:2985–3000. PubMed
White MA, Steffy B, Wiltshire T, Payseur BA. Genetic dissection of a key reproductive barrier between nascent species of house mice. Genetics. 2011;189:289–304. PubMed PMC
Yang H, Wang JR, Didion JP, Buus RJ, Bell TA, Welsh CE, Bonhomme F, Yu AH, Nachman MW, Piálek J, et al. Subspecific origin and haplotype diversity in the laboratory mouse. Nat Genet. 2011;43:648–655. PubMed PMC