The columbine genus Aquilegia is a classic example of an adaptive radiation, involving a wide variety of pollinators and habitats. Here we present the genome assembly of A. coerulea 'Goldsmith', complemented by high-coverage sequencing data from 10 wild species covering the world-wide distribution. Our analyses reveal extensive allele sharing among species and demonstrate that introgression and selection played a role in the Aquilegia radiation. We also present the remarkable discovery that the evolutionary history of an entire chromosome differs from that of the rest of the genome - a phenomenon that we do not fully understand, but which highlights the need to consider chromosomes in an evolutionary context.

Central European Institute of Technology Masaryk University Brno Czech Republic

Department of Ecology Evolution and Marine Biology University of California Santa Barbara United States

Department of Energy Joint Genome Institute Walnut Creek United States

Department of Organismic and Evolutionary Biology Harvard University Cambridge United States

Gregor Mendel Institute Austrian Academy of Sciences Vienna BioCenter Vienna Austria

HudsonAlpha Institute of Biotechnology Alabama United States

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Olomouc Czech Republic

Vienna Graduate School of Population Genetics Vienna Austria

Zobrazit více v PubMed

Aköz G, Nordborg M. Genome duplication and reorganization in Aquilegia. bioRxiv. 2018 doi: 10.1101/407973~. DOI

Avise JC, Robinson TJ. Hemiplasy: a new term in the lexicon of phylogenetics. Systematic Biology. 2008;57:503–507. doi: 10.1080/10635150802164587. PubMed DOI

Bastida JM, Alcántara JM, Rey PJ, Vargas P, Herrera CM. Extended phylogeny of Aquilegia: the biogeographical and ecological patterns of two simultaneous but contrasting radiations. Plant Systematics and Evolution. 2010;284:171–185. doi: 10.1007/s00606-009-0243-z. DOI

Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM, Kishony R. Inexpensive multiplexed library preparation for megabase-sized genomes. Plos One. 2015;10:e0128036. doi: 10.1371/journal.pone.0128036. PubMed DOI PMC

Bennett MD, Smith JB, Heslop-Harrison JS. Nuclear DNA amounts in angiosperms. Proceedings of the Royal Society B: Biological Sciences. 1982;216:179–199. doi: 10.1098/rspb.1982.0069. PubMed DOI

Bennett MD, Leitch IJ. Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Annals of Botany. 2011;107:467–590. doi: 10.1093/aob/mcq258. PubMed DOI PMC

Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 2003;19:889–890. doi: 10.1093/bioinformatics/btg112. PubMed DOI

Cazaux B, Catalan J, Veyrunes F, Douzery EJP, Britton-Davidian J. Are ribosomal DNA clusters rearrangement hotspots?: A case study in the genus Mus (Rodentia, Muridae) BMC Evolutionary Biology. 2011;11:124. doi: 10.1186/1471-2148-11-124. PubMed DOI PMC

Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC

Cooper EA, Whittall JB, Hodges SA, Nordborg M. Genetic variation at nuclear loci fails to distinguish two morphologically distinct species of Aquilegia. PLoS ONE. 2010;5:e8655. doi: 10.1371/journal.pone.0008655. PubMed DOI PMC

Corbett-Detig RB, Hartl DL, Sackton TB. Natural Selection Constrains Neutral Diversity across A Wide Range of Species. PLOS Biology. 2015;13:e1002112. doi: 10.1371/journal.pbio.1002112. PubMed DOI PMC

Cossard G, Sannier J, Sauquet H, Damerval C, de Craene LR, Jabbour F, Nadot S. Subfamilial and tribal relationships of Ranunculaceae: evidence from eight molecular markers. Plant Systematics and Evolution. 2016;302:419–431. doi: 10.1007/s00606-015-1270-6. DOI

Coyne JA, Orr AH, Orr HA. Speciation. Sunderland, Massachusetts: Sinauer; 2004.

Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW. Widespread genome duplications throughout the history of flowering plants. Genome Research. 2006;16:738–749. doi: 10.1101/gr.4825606. PubMed DOI PMC

DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ. 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

Durand EY, Patterson N, Reich D, Slatkin M. Testing for ancient admixture between closely related populations. Molecular Biology and Evolution. 2011;28:2239–2252. doi: 10.1093/molbev/msr048. PubMed DOI PMC

Fior S, Li M, Oxelman B, Viola R, Hodges SA, Ometto L, Varotto C. Spatiotemporal reconstruction of the Aquilegia rapid radiation through next-generation sequencing of rapidly evolving cpDNA regions. New Phytologist. 2013;198:579–592. doi: 10.1111/nph.12163. PubMed DOI

Grant V. Isolation and hybridization between Aquilegia formosa and A. pubescens. Aliso. 1952;2:341–360.

Green DM. Muller's Ratchet and the evolution of supernumerary chromosomes. Genome. 1990;33:818–824. doi: 10.1139/g90-123. DOI

Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Ž, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, de la Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S. A draft sequence of the Neandertal genome. Science. 2010;328:710–722. doi: 10.1126/science.1188021. PubMed DOI PMC

Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research. 2003;31:5654–5666. doi: 10.1093/nar/gkg770. PubMed DOI PMC

Haas BJ, Delcher AL, Wortman JR, Salzberg SL. DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics. 2004;20:3643–3646. doi: 10.1093/bioinformatics/bth397. PubMed DOI

Han Y, Zhang T, Thammapichai P, Weng Y, Jiang J. Chromosome-Specific painting in Cucumis species using bulked oligonucleotides. Genetics. 2015;200:771–779. doi: 10.1534/genetics.115.177642. PubMed DOI PMC

Herlihy CR, Eckert CG. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature. 2002;416:320–323. doi: 10.1038/416320a. PubMed DOI

Hizume M, Shiraishi H, Matsusaki Y, Shibata F. Localization of 45S and 5S rDNA on chromosomes of Nigella damascena, Ranunculaceae. Cytologia. 2013;78:379–381. doi: 10.1508/cytologia.78.379. DOI

Hodges SA, Arnold ML. Columbines: a geographically widespread species flock. PNAS. 1994a;91:5129–5132. doi: 10.1073/pnas.91.11.5129. PubMed DOI PMC

Hodges SA, Arnold ML. Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. PNAS. 1994b;91:2493–2496. doi: 10.1073/pnas.91.7.2493. PubMed DOI PMC

Hodges SA, Whittall JB, Fulton M, Yang JY. Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and Aquilegia pubescens. The American Naturalist. 2002;159 Suppl 3:S51–S60. doi: 10.1086/338372. PubMed DOI

Hodges SA, Fulton M, Yang JY, Whittall JB. Verne Grant and evolutionary studies of Aquilegia. New Phytologist. 2004;161:113–120. doi: 10.1046/j.1469-8137.2003.00950.x. DOI

Hodges SA, Derieg NJ. Adaptive radiations: From field to genomic studies. PNAS. 2009;106:9947–9954. doi: 10.1073/pnas.0901594106. PubMed DOI PMC

Huang J, Ma L, Yang F, Fei SZ, Li L. 45S rDNA regions are chromosome fragile sites expressed as gaps in vitro on metaphase chromosomes of root-tip meristematic cells in Lolium spp. PLoS ONE. 2008;3:e2167. doi: 10.1371/journal.pone.0002167. PubMed DOI PMC

Hudson RR, Slatkin M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992;132:583–589. PubMed PMC

Jaffe DB, Butler J, Gnerre S, Mauceli E, Lindblad-Toh K, Mesirov JP, Zody MC, Lander ES. Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Research. 2003;13:91–96. doi: 10.1101/gr.828403. PubMed DOI PMC

Jones RN. B chromosomes in plants. New Phytologist. 1995;131:411–434. doi: 10.1111/j.1469-8137.1995.tb03079.x. PubMed DOI

Karasov TL, Horton MW, Bergelson J. Genomic variability as a driver of plant-pathogen coevolution? Current Opinion in Plant Biology. 2014;18:24–30. doi: 10.1016/j.pbi.2013.12.003. PubMed DOI PMC

Kent WJ. BLAT--the BLAST-like alignment tool. Genome Research. 2002;12:656–664. doi: 10.1101/gr.229202. PubMed DOI PMC

Kimura M. The Neutral Theory of Molecular Evolution. Cambridge: Cambridge University Press; 1983.

Kocsis E, Trus BL, Steer CJ, Bisher ME, Steven AC. Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. Journal of Structural Biology. 1991;107:6–14. doi: 10.1016/1047-8477(91)90025-R. PubMed DOI

Korneliussen TS, Albrechtsen A, Nielsen R. ANGSD: Analysis of next generation sequencing data. BMC Bioinformatics. 2014;15:356. doi: 10.1186/s12859-014-0356-4. PubMed DOI PMC

Kramer EM. Aquilegia: a new model for plant development, ecology, and evolution. Annual Review of Plant Biology. 2009;60:261–277. doi: 10.1146/annurev.arplant.043008.092051. PubMed DOI

Kramer EM, Hodges SA. Aquilegia as a model system for the evolution and ecology of petals. Philosophical Transactions of the Royal Society B: Biological Sciences. 2010;365:477–490. doi: 10.1098/rstb.2009.0230. PubMed DOI PMC

Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, Promerová M, Rubin CJ, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L. Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature. 2015;518:371–375. doi: 10.1038/nature14181. PubMed DOI

Langlet O. Beiträge zur Zytologie der Ranunculazeen. Svenk Botanisk Tidskrift. 1927;21:1–17.

Langlet O. Über Chromosomenverhaltnisse und Systematik der Ranunculaceae. Svenk Botanisk Tidskrift. 1932;26:381–400.

Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, Venkat A, Andolfatto P, Przeworski M. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biology. 2012;10:e1001388. doi: 10.1371/journal.pbio.1001388. PubMed DOI PMC

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–1760. doi: 10.1093/bioinformatics/btp324. PubMed DOI PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

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

Li LF, Wang HY, Pang D, Liu Y, Liu B, Xiao HX. Phenotypic and genetic evidence for ecological speciation of Aquilegia japonica and A. oxysepala. The New Phytologist. 2014;204:1028–1040. doi: 10.1111/nph.12967. PubMed DOI

Liao L, Xu L, Zhang D, Fang L, Deng H, Shi J, Li T. Multiple hybridization origin of Ranunculus cantoniensis (4x): evidence from trnL-F and ITS sequences and fluorescent in situ hybridization (FISH) Plant Systematics and Evolution. 2008;276:31–37. doi: 10.1007/s00606-008-0083-2. DOI

Linnert G. Cytologische Untersuchungen an Arten und Artenbastarden von Aquilegia - I. Struktur und Polymorphismus der Nukleolen-chromosomen, Quadrivalente und B-chromosomen. Chromosoma. 1961;12:449–459. PubMed

Loh YH, Bezault E, Muenzel FM, Roberts RB, Swofford R, Barluenga M, Kidd CE, Howe AE, Di Palma F, Lindblad-Toh K, Hey J, Seehausen O, Salzburger W, Kocher TD, Streelman JT. Origins of shared genetic variation in African cichlids. Molecular Biology and Evolution. 2013;30:906–917. doi: 10.1093/molbev/mss326. PubMed DOI PMC

Lyons E, Freeling M. How to usefully compare homologous plant genes and chromosomes as DNA sequences. The Plant Journal. 2008;53:661–673. doi: 10.1111/j.1365-313X.2007.03326.x. PubMed DOI

Malinsky M, Svardal H, Tyers AM, Miska EA, Genner MJ, Turner GF, Durbin R. Whole genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. bioRxiv. 2017 doi: 10.1101/143859. PubMed DOI PMC

Mallet J, Besansky N, Hahn MW. How reticulated are species? BioEssays. 2016;38:140–149. doi: 10.1002/bies.201500149. PubMed DOI PMC

Mandáková T, Lysak MA. Current Protocols in Plant Biology. Hoboken, NJ, USA: John Wiley & Sons, Inc; 2016. Painting of Arabidopsis chromosomes with chromosome-specific BAC clones; pp. 359–371. PubMed

Marçais G, Kingsford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011;27:764–770. doi: 10.1093/bioinformatics/btr011. PubMed DOI PMC

McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research. 2012;40:4288–4297. doi: 10.1093/nar/gks042. PubMed DOI PMC

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. 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

McVean GA, Altshuler DM, Durbin RM, Abecasis GR, Bentley DR, Chakravarti A, Clark AG, Donnelly P, Eichler EE, Flicek P, Gabriel SB, Gibbs RA, Green ED, Hurles ME, Knoppers BM, Korbel JO, Lander ES, Lee C, Lehrach H, Mardis ER, Marth GT, McVean GA, Nickerson DA, Schmidt JP, Sherry ST, Wang J, Wilson RK. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491:56–65. doi: 10.1038/nature11632. PubMed DOI PMC

Melters DP, Bradnam KR, Young HA, Telis N, May MR, Ruby JG, Sebra R, Peluso P, Eid J, Rank D, Garcia JF, DeRisi JL, Smith T, Tobias C, Ross-Ibarra J, Korf I, Chan SW. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biology. 2013;14:R10. doi: 10.1186/gb-2013-14-1-r10. PubMed DOI PMC

Miller CA, Hampton O, Coarfa C, Milosavljevic A. ReadDepth: a parallel R package for detecting copy number alterations from short sequencing reads. PLoS ONE. 2011;6:e16327. doi: 10.1371/journal.pone.0016327. PubMed DOI PMC

Ming R, Bendahmane A, Renner SS. Sex chromosomes in land plants. Annual Review of Plant Biology. 2011;62:485–514. doi: 10.1146/annurev-arplant-042110-103914. PubMed DOI

Mlinarec J, Papeš DA, Besendorfer V. Ribosomal, telomeric and heterochromatin sequences localization in the karyotype of Anemone hortensis. Botanical Journal of the Linnean Society. 2006;150:177–186. doi: 10.1111/j.1095-8339.2006.00467.x. DOI

Montalvo AM. Inbreeding depression and maternal effects in Aquilegia caerulea, a partially selfing plant. Ecology. 1994;75:2395. doi: 10.2307/1940893. DOI

Munz PA. Aquilegia: the cultivated and wild columbines. Gentes Herbarum. 1946;7:1–150.

Murgha YE, Rouillard JM, Gulari E. Methods for the preparation of large quantities of complex single-stranded oligonucleotide libraries. PLoS ONE. 2014;9:e94752. doi: 10.1371/journal.pone.0094752. PubMed DOI PMC

Nam K, Munch K, Hobolth A, Dutheil JY, Veeramah KR, Woerner AE, Hammer MF, Mailund T, Schierup MH, Great Ape Genome Diversity Project Extreme selective sweeps independently targeted the X chromosomes of the great apes. PNAS. 2015;112:6413–6418. doi: 10.1073/pnas.1419306112. PubMed DOI PMC

Nordborg M, Innan H. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics. 2003;163:1201–1213. PubMed PMC

Novikova PY, Hohmann N, Nizhynska V, Tsuchimatsu T, Ali J, Muir G, Guggisberg A, Paape T, Schmid K, Fedorenko OM, Holm S, Säll T, Schlötterer C, Marhold K, Widmer A, Sese J, Shimizu KK, Weigel D, Krämer U, Koch MA, Nordborg M. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nature Genetics. 2016;48:1077–1082. doi: 10.1038/ng.3617. PubMed DOI

Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI

Pease JB, Haak DC, Hahn MW, Moyle LC. Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLOS Biology. 2016;14:e1002379. doi: 10.1371/journal.pbio.1002379. PubMed DOI PMC

Picard Tools Picard. 2018 http://broadinstitute.github.io/picard/

R Core Team . Vienna, Austria: R Foundation for Statistical Computing; 2014. http://www.R-project.org/

Rabanal FA, Nizhynska V, Mandáková T, Novikova PY, Lysak MA, Mott R, Nordborg M. Unstable inheritance of 45S rRNA genes in Arabidopsis thaliana. G3: Genes, Genomes, Genetics. 2017;7:1201–1209. doi: 10.1534/g3.117.040204. PubMed DOI PMC

Ro K-E, McPheron BA. Molecular phylogeny of the Aquilegia group (Ranunculaceae) based on internal transcribed spacers and 5.8S nuclear ribosomal DNA. Biochemical Systematics and Ecology. 1997;25:445–461.

Ro KE, Keener CS, McPheron BA. Molecular phylogenetic study of the Ranunculaceae: utility of the nuclear 26S ribosomal DNA in inferring intrafamilial relationships. Molecular Phylogenetics and Evolution. 1997;8:117–127. doi: 10.1006/mpev.1997.0413. PubMed DOI

Roa F, Guerra M. Distribution of 45S rDNA sites in chromosomes of plants: structural and evolutionary implications. BMC Evolutionary Biology. 2012;12:225. doi: 10.1186/1471-2148-12-225. PubMed DOI PMC

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

Salamov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Genome Research. 2000;10:516–522. doi: 10.1101/gr.10.4.516. PubMed DOI PMC

Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–593. doi: 10.1093/bioinformatics/btq706. PubMed DOI PMC

Schluter D. The Ecology of Adaptive Radiation. New York: Oxford University Press; 2000.

Schluter D, Conte GL. Genetics and ecological speciation. PNAS. 2009;106 Suppl 1:9955–9962. doi: 10.1073/pnas.0901264106. PubMed DOI PMC

Schumer M, Xu C, Powell DL, Durvasula A, Skov L, Holland C, Blazier JC, Sankararaman S, Andolfatto P, Rosenthal GG, Przeworski M. Natural selection interacts with recombination to shape the evolution of hybrid genomes. Science. 2018;360:656–660. doi: 10.1126/science.aar3684. PubMed DOI PMC

Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, Peichel CL, Saetre GP, Bank C, Brännström A, Brelsford A, Clarkson CS, Eroukhmanoff F, Feder JL, Fischer MC, Foote AD, Franchini P, Jiggins CD, Jones FC, Lindholm AK, Lucek K, Maan ME, Marques DA, Martin SH, Matthews B, Meier JI, Möst M, Nachman MW, Nonaka E, Rennison DJ, Schwarzer J, Watson ET, Westram AM, Widmer A. Genomics and the origin of species. Nature Reviews Genetics. 2014;15:176–192. doi: 10.1038/nrg3644. PubMed DOI

Shu S, Goodstein D, Rokhsar D. PERTRAN: genome-guided RNA-seq read assembler. Cold Spring Harbor Lab Genome Informatics.2013.

Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2015 http://www.repeatmasker.org

Smit A, Hubley R. RepeatModeler Open-1.0. 2015 http://www.repeatmasker.org

Soza VL, Brunet J, Liston A, Smith PS, Di Stilio VS. Phylogenetic insights into the correlates of dioecy in meadow-rues (Thalictrum, Ranunculaceae) Molecular Phylogenetics and Evolution. 2012;63:180–192. doi: 10.1016/j.ympev.2012.01.009. PubMed DOI

Spedicato GA. Discrete Time Markov Chains with R. The R Journal. 2017;09:84–104.

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

Sun H, Ding J, Piednoël M, Schneeberger K. findGSE: estimating genome size variation within human and Arabidopsis using k-mer frequencies. Bioinformatics. 2018;34:550–557. doi: 10.1093/bioinformatics/btx637. PubMed DOI

Svardal H, Jasinska AJ, Apetrei C, Coppola G, Huang Y, Schmitt CA, Jacquelin B, Ramensky V, Müller-Trutwin M, Antonio M, Weinstock G, Grobler JP, Dewar K, Wilson RK, Turner TR, Warren WC, Freimer NB, Nordborg M. Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. Nature Genetics. 2017;49:1705–1713. doi: 10.1038/ng.3980. PubMed DOI PMC

Takahata N. Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics. 1989;122:957–966. PubMed PMC

Taylor RJ. Interspecific hybridization and its evolutionary significance in the genus Aquilegia. Brittonia. 1967;19:374. doi: 10.2307/2805535. DOI

Tiley GP, Ané C, Burleigh JG. Evaluating and characterizing ancient whole-genome duplications in plants with gene count data. Genome Biology and Evolution. 2016;8:1023–1037. doi: 10.1093/gbe/evw058. PubMed DOI PMC

Toups MA, Hahn MW. Retrogenes reveal the direction of sex-chromosome evolution in mosquitoes. Genetics. 2010;186:763–766. doi: 10.1534/genetics.110.118794. PubMed DOI PMC

Valente GT, Nakajima RT, Fantinatti BE, Marques DF, Almeida RO, Simões RP, Martins C. B chromosomes: from cytogenetics to systems biology. Chromosoma. 2017;126:73–81. doi: 10.1007/s00412-016-0613-6. PubMed DOI

Vanneste K, Baele G, Maere S, Van de Peer Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Research. 2014;24:1334–1347. doi: 10.1101/gr.168997.113. PubMed DOI PMC

Vicoso B, Bachtrog D. Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature. 2013;499:332–335. doi: 10.1038/nature12235. PubMed DOI PMC

Wang W, Lu A-M, Ren Y, Endress ME, Chen Z-D. Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data. Perspectives in Plant Ecology, Evolution and Systematics. 2009;11:81–110. doi: 10.1016/j.ppees.2009.01.001. DOI

Weiss-Schneeweiss H, Schneeweiss GM, Stuessy TF, Mabuchi T, Park JM, Jang CG, Sun BY. Chromosomal stasis in diploids contrasts with genome restructuring in auto- and allopolyploid taxa of Hepatica (Ranunculaceae) New Phytologist. 2007;174:669–682. doi: 10.1111/j.1469-8137.2007.02019.x. PubMed DOI

Westergaard M. The mechanism of sex determination in dioecious flowering plants. Advances in Genetics. 1958;9:217–281. PubMed

Whittall JB, Hodges SA. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature. 2007;447:706–709. doi: 10.1038/nature05857. PubMed DOI

Yang JY, Hodges SA. Early inbreeding depression selects for high outcrossing rates in Aquilegia formosa and Aquilegia pubescens. International Journal of Plant Sciences. 2010;171:860–871.

Yant L, Collani S, Puzey J, Levy C, Kramer EM. Molecular basis for three-dimensional elaboration of the Aquilegia petal spur. Proceedings of the Royal Society B: Biological Sciences. 2015;282:20142778. doi: 10.1098/rspb.2014.2778. PubMed DOI PMC

Yeh RF, Lim LP, Burge CB. Computational inference of homologous gene structures in the human genome. Genome Research. 2001;11:803–816. doi: 10.1101/gr.175701. PubMed DOI PMC

The Evolution of Chromosome Numbers: Mechanistic Models and Experimental Approaches

Chromosome Painting Facilitates Anchoring Reference Genome Sequence to Chromosomes In Situ and Integrated Karyotyping in Banana (Musa Spp.)

The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives