Young inversion with multiple linked QTLs under selection in a hybrid zone

. 2017 Apr 03 ; 1 (5) : 119. [epub] 20170403

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28812690

Grantová podpora
R01 GM086496 NIGMS NIH HHS - United States

Fixed chromosomal inversions can reduce gene flow and promote speciation in two ways: by suppressing recombination and by carrying locally favoured alleles at multiple loci. However, it is unknown whether favoured mutations slowly accumulate on older inversions or if young inversions spread because they capture pre-existing adaptive quantitative trait loci (QTLs). By genetic mapping, chromosome painting and genome sequencing, we have identified a major inversion controlling ecologically important traits in Boechera stricta. The inversion arose since the last glaciation and subsequently reached local high frequency in a hybrid speciation zone. Furthermore, the inversion shows signs of positive directional selection. To test whether the inversion could have captured existing, linked QTLs, we crossed standard, collinear haplotypes from the hybrid zone and found multiple linked phenology QTLs within the inversion region. These findings provide the first direct evidence that linked, locally adapted QTLs may be captured by young inversions during incipient speciation.

Erratum v

PubMed

Zobrazit více v PubMed

Kirkpatrick M. How and why chromosome inversions evolve. PLoS Biol. 2010;8:e1000501. doi: 10.1371/journal.pbio.1000501. PubMed DOI PMC

Huber B, et al. Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity. 2015;114:515–524. doi: 10.1038/hdy.2015.22. PubMed DOI PMC

Lowry DB, Willis JHA. Widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology. 2010;8:e1000500. doi:1000510.1001371/journal.pbio.1000500. PubMed PMC

Corbett-Detig RB, Hartl DL. Population genomics of inversion polymorphisms in Drosophila melanogaster. PLoS Genet. 2012;8:e1003056. doi: 10.1371/journal.pgen.1003056. PubMed DOI PMC

Kirkpatrick M, Kern A. Where’s the money? Inversions, genes, and the hunt for genomic targets of selection. Genetics. 2012;190:1153–1155. doi: 10.1534/genetics.112.139899. PubMed DOI PMC

Guillen Y, Ruiz A. Gene alterations at Drosophila inversion breakpoints provide prima facie evidence for natural selection as an explanation for rapid chromosomal evolution. BMC Genomics. 2012;13 doi: 10.1186/1471-2164-13-53. PubMed DOI PMC

Smith AC, et al. Maternal gametic transmission of translocations or inversions of human chromosome 11p15.5 results in regional DNA hypermethylation and downregulation of CDKN1C expression. Genomics. 2012;99:25–35. doi: 10.1016/j.ygeno.2011.10.007. PubMed DOI PMC

Kennington WJ, Partridge L, Hoffmann AA. Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation. Genetics. 2006;172:1655–1663. PubMed PMC

Kirkpatrick M, Barton N. Chromosome inversions, local adaptation and speciation. Genetics. 2006;173:419–434. PubMed PMC

Rieseberg LH. Chromosomal rearrangements and speciation. Trends in Ecology & Evolution. 2001;16:351–358. PubMed

Noor MAF, Grams KL, Bertucci LA, Reiland J. Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:12084–12088. PubMed PMC

Navarro A, Barton NH. Accumulating postzygotic isolation genes in parapatry: A new twist on chromosomal speciation. Evolution. 2003;57:447–459. PubMed

Lohse K, Clarke M, Ritchie M, Etges W. Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation. Evolution. 2015 PubMed PMC

Huang CH, et al. Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol Biol Evol. 2016;33:394–412. doi: 10.1093/molbev/msv226. PubMed DOI PMC

Lee CR, Mitchell-Olds T. Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Molec Ecol. 2011;20:4631–4642. doi: 10.1111/j.1365-294X.2011.05310.x. PubMed DOI PMC

Lee CR, Mitchell-Olds T. Complex trait divergence contributes to environmental niche differentiation in ecological speciation of Boechera stricta. Molec Ecol. 2013;22:2204–2217. PubMed PMC

Anderson J, Lee CR, Mitchell-Olds T. Life history QTLs and natural selection on flowering time in Boechera stricta, a perennial relative of Arabidopsis. Evolution. 2010;65:771–787. PubMed PMC

Prasad K, et al. A gain-of-function polymorphism controlling complex traits and fitness in nature. Science. 2012;337:1081–1084. doi: 10.1126/science.1221636. PubMed DOI PMC

Heo JY, et al. Identification of quantitative trait loci and a candidate locus for freezing tolerance in controlled and outdoor environments in the overwintering crucifer Boechera stricta. Plant, Cell & Environment. 2014;37:2459–2469. doi: 10.1111/pce.12365. PubMed DOI PMC

Anderson JT, Lee CR, Mitchell-Olds T. Strong selection genome-wide enhances fitness tradeoffs across environments and episodes of selection. Evolution. 2014;68:16–31. doi: 10.1111/evo.12259. PubMed DOI PMC

Schranz ME, Windsor AJ, Song B-H, Lawton-Rauh A, Mitchell-Olds T. Comparative genetic mapping in Boechera stricta, a close relative of Arabidopsis. Plant Physiol. 2007;144:286–298. doi: 10.1104/pp.107.096685. PubMed DOI PMC

Mehringer PJ, Arno SF, Petersen KL. Postglacial history of Lost Trail Pass Bog, Bitterroot Mountains, Montana. Arctic and Alpine Research. 1977;9:345–368.

Mumma SA, Whitlock C, Pierce K. A 28,000 year history of vegetation and climate from Lower Red Rock Lake, Centennial Valley, Southwestern Montana, USA. Palaeogeography Palaeoclimatology Palaeoecology. 2012;326:30–41. doi: 10.1016/j.palaeo.2012.01.036. DOI

Ossowski S, et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science. 2010;327:92–94. doi: 10.1126/science.1180677. PubMed DOI PMC

Anderson J, Lee CR, Rushworth C, Colautti R, Mitchell-Olds T. Genetic tradeoffs and conditional neutrality contribute to local adaptation. Molec Ecol. 2013;22:699–708. PubMed PMC

Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings Biological Sciences/The Royal Society. 2012;279:3843–3852. doi: 10.1098/rspb.2012.1051. PubMed DOI PMC

Smadja CM, Butlin RK. A framework for comparing processes of speciation in the presence of gene flow. Molecular Ecology. 2011;20:5123–5140. doi: 10.1111/j.1365-294X.2011.05350.x. PubMed DOI

Guerrero RF, Rousset F, Kirkpatrick M. Coalescent patterns for chromosomal inversions in divergent populations. Philosophical Transactions of the Royal Society B-Biological Sciences. 2012;367:430–438. doi: 10.1098/rstb.2011.0246. PubMed DOI PMC

Fay JC, Wu CI. Hitchhiking under positive Darwinian selection. Genetics. 2000;155:1405–1413. PubMed PMC

Naseeb S, et al. Widespread impact of chromosomal inversions on gene expression uncovers robustness via phenotypic buffering. Molecular Biology and Evolution. 2016;33:1679–1696. doi: 10.1093/molbev/msw045. PubMed DOI PMC

Chapman JA, et al. Meraculous: De Novo genome assembly with short paired-end reads. PLoS ONE. 2011;6:e23501. doi: 10.1371/journal.pone.0023501. PubMed DOI PMC

van Oeveren J, et al. Sequence-based physical mapping of complex genomes by whole genome profiling. Genome Research. 2011;21:618–625. doi: 10.1101/gr.112094.110. PubMed DOI PMC

Soderlund C, Humphray S, Dunham A, French L. Contigs Built with Fingerprints, Markers, and FPC V4.7. Genome Research. 2000;10:1772–1787. doi: 10.1101/gr.GR-1375R. PubMed DOI PMC

Nelson W, Soderlund C. Integrating sequence with FPC fingerprint maps. Nucleic Acids Research. 2009;37:e36. doi: 10.1093/nar/gkp034. PubMed DOI PMC

Soderlund C, Bomhoff M, Nelson WM. SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Research. 2011;39:e68. doi: 10.1093/nar/gkr123. PubMed DOI PMC

Slotte T, et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat Genet. 2013;45:831–835. doi: 10.1038/ng.2669. PubMed DOI

Kurtz S, et al. Versatile and open software for comparing large genomes. Genome Biology. 2004;5 doi: 10.1186/gb-2004-5-2-r12. PubMed DOI PMC

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–1760. PubMed PMC

DePristo MA, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics. 2011;43:491–498. doi: 10.1038/ng.806. PubMed DOI PMC

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. 2013:1303.3997.

Li H, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

Wu Y, Bhat PR, Close TJ, Lonardi S. Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. PLoS Genet. 2008;4:e1000212. doi: 10.1371/journal.pgen.1000212. PubMed DOI PMC

Mandáková T, Schranz ME, Sharbel TF, de Jong H, Lysak MA. Karyotype evolution in apomictic Boechera and the origin of the aberrant chromosomes. The Plant Journal. 2015;82:785–793. doi: 10.1111/tpj.12849. PubMed DOI

Mandáková T, Lysak MA. Chromosomal phylogeny and karyotype evolution in x=7 crucifer species (Brassicaceae) Plant Cell. 2008;20:2559–2570. doi: 10.1105/tpc.108.062166. PubMed DOI PMC

Lysak MA, Mandáková T. Analysis of plant meiotic chromosomes by chromosome painting. Humana Press; 2013. PubMed

Zerbino DR, Birney E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research. 2008;18:821–829. doi: 10.1101/gr.074492.107. PubMed DOI PMC

Koressaar T, Remm M. Enhancements and modifications of primer design program Primer3. Bioinformatics. 2007;23:1289–1291. doi: 10.1093/bioinformatics/btm091. PubMed DOI

Rushworth CA, Song BH, Lee CR, Mitchell-Olds T. Boechera, a model system for ecological genomics. Molecular Ecology. 2011;20:4843–4857. doi: 10.1111/j.1365-294X.2011.05340.x. PubMed DOI PMC

Tuinstra RM, Ejeta G, Goldsbrough BP. Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theoretical and Applied Genetics. 1997;95:1005–1011. doi: 10.1007/s001220050654. DOI

Scheiner SM. In: Design and analysis of ecological experiments. Scheiner SM, Gurevitch J, editors. Chapman and Hall; 2001. pp. 99–115.

Schurch N, et al. How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA (New York) 2016;22:839–851. PubMed PMC

Cande J, Andolfatto P, Prud’homme B, Stern DL, Gompel N. Evolution of multiple additive loci caused divergence between Drosophila yakuba and D. santomea in wing rowing during male courtship. PLoS ONE. 2012;7:e43888. doi: 10.1371/journal.pone.0043888. PubMed DOI PMC

R_Core_Team. R Foundation for Statistical Computing. Vienna, Austria: 2013.

Benjamini Y, Yekutieli D. Quantitative trait loci analysis using the false discovery rate. Genetics. 2005;171:783–790. PubMed PMC

Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w(1118); iso-2; iso-3. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC

Bouche F, Lobet G, Tocquin P, Perilleux C. FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Research. 2016;44:D1167–D1171. doi: 10.1093/nar/gkv1054. PubMed DOI PMC

Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet. 2006;2:e190. doi: 10.1371/journal.pgen.0020190. PubMed DOI PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Korneliussen TS, Albrechtsen A, Nielsen R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics. 2014;15:1–13. doi: 10.1186/s12859-014-0356-4. PubMed DOI PMC

Fumagalli M, Vieira FG, Linderoth T, Nielsen R. ngsTools: methods for population genetics analyses from next-generation sequencing data. Bioinformatics. 2014;30:1486–1487. doi: 10.1093/bioinformatics/btu041. PubMed DOI PMC

McKenna A, et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–595. PubMed PMC

Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993;133:693–709. PubMed PMC

Lee C, et al. Selection in a hybrid zone: evidence for linked QTLs in a young inversion. Nature Ecology and Evolution. 2016 in review. PubMed PMC

Clark RM, et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science. 2007;317:338–342. PubMed

Weir B, Cockerham C. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38:1358–1370. PubMed

Danecek P, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–2158. doi: 10.1093/bioinformatics/btr330. PubMed DOI PMC

Nei M, Li WH. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences. 1979;76:5269–5273. PubMed PMC

Nei M. Molecular Evolutionary Genetics. Columbia University Press; 1987.

Purcell S, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–575. PubMed PMC

Browning BL, Browning SR. Improving the accuracy and efficiency of identity-by-descent detection in population data. Genetics. 2013;194:459–471. doi: 10.1534/genetics.113.150029. PubMed DOI PMC

Long Q, et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nature Genetics. 2013;45:884–U218. doi: 10.1038/ng.2678. PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

How Important Are Structural Variants for Speciation?

. 2021 Jul 17 ; 12 (7) : . [epub] 20210717

Chromosomal Evolution and Apomixis in the Cruciferous Tribe Boechereae

. 2020 ; 11 () : 514. [epub] 20200528

Young inversion with multiple linked QTLs under selection in a hybrid zone

. 2017 Apr 03 ; 1 (5) : 119. [epub] 20170403

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...