Genomic insights into rapid speciation within the world's largest tree genus Syzygium.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
12 09 2022
12 09 2022
Historique:
received:
14
10
2021
accepted:
10
08
2022
entrez:
12
9
2022
pubmed:
13
9
2022
medline:
15
9
2022
Statut:
epublish
Résumé
Species radiations, despite immense phenotypic variation, can be difficult to resolve phylogenetically when genetic change poorly matches the rapidity of diversification. Genomic potential furnished by palaeopolyploidy, and relative roles for adaptation, random drift and hybridisation in the apportionment of genetic variation, remain poorly understood factors. Here, we study these aspects in a model radiation, Syzygium, the most species-rich tree genus worldwide. Genomes of 182 distinct species and 58 unidentified taxa are compared against a chromosome-level reference genome of the sea apple, Syzygium grande. We show that while Syzygium shares an ancient genome doubling event with other Myrtales, little evidence exists for recent polyploidy events. Phylogenomics confirms that Syzygium originated in Australia-New Guinea and diversified in multiple migrations, eastward to the Pacific and westward to India and Africa, in bursts of speciation visible as poorly resolved branches on phylogenies. Furthermore, some sublineages demonstrate genomic clines that recapitulate cladogenetic events, suggesting that stepwise geographic speciation, a neutral process, has been important in Syzygium diversification.
Identifiants
pubmed: 36097018
doi: 10.1038/s41467-022-32637-x
pii: 10.1038/s41467-022-32637-x
pmc: PMC9468008
doi:
Banques de données
Dryad
['10.5061/dryad.h18931zpw']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
5031Informations de copyright
© 2022. The Author(s).
Références
Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).
pubmed: 19197052
doi: 10.1126/science.1157966
Givnish, T. J. Adaptive radiation versus ‘radiation’and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. N. Phytol. 207, 297–303 (2015).
doi: 10.1111/nph.13482
Rundell, R. J. & Price, T. D. Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394–399 (2009).
pubmed: 19409647
doi: 10.1016/j.tree.2009.02.007
Gittenberger, E. What about non-adaptive radiation? Biol. J. Linn. Soc. 43, 263–272 (1991).
doi: 10.1111/j.1095-8312.1991.tb00598.x
Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).
pubmed: 25686609
doi: 10.1038/nature14181
Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).
pubmed: 16701254
doi: 10.1016/j.tree.2004.01.003
Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348 (2009).
pubmed: 21628192
doi: 10.3732/ajb.0800079
Meudt, H. M. et al. Polyploidy on Islands: its emergence and importance for diversification. Front. Plant Sci. 12, 637214–637214 (2021).
pubmed: 33763097
pmcid: 7982887
doi: 10.3389/fpls.2021.637214
Givnish, T. J. & Sytsma, K. J. Molecular Evolution and Adaptive Radiation (Cambridge University Press, 2000).
Choi, J. Y. et al. Ancestral polymorphisms shape the adaptive radiation of Metrosideros across the Hawaiian Islands. Proc. Natl. Acad. Sci. USA 118, (2021).
Grant, P.R. Evolution on Islands (Oxford University Press, Oxford, 1998).
Lindqvist, C., Motley, T. J., Jeffrey, J. J. & Albert, V. A. Cladogenesis and reticulation in the Hawaiian endemic mints (Lamiaceae). Cladistics 19, 480–495 (2003).
pubmed: 34905854
doi: 10.1111/j.1096-0031.2003.tb00384.x
Wallace, A. R. Alfred Russel Wallace: Letters from the Malay Archipelago (Oxford University Press, 2013).
Ashton, P. S. & Seidler, R. On the Forests of Tropical Asia: Lest the Memory Fade (Kew Publishing, 2014).
Biffin, E., Craven, L. A., Crisp, M. D. & Gadek, P. A. Molecular systematics of Syzygium and allied genera (Myrtaceae): evidence from the chloroplast genome. Taxon 55, 79–94 (2006).
doi: 10.2307/25065530
Biffin, E., Harrington, M. G., Crisp, M., Craven, L. A. & Gadek, P. Structural partitioning, paired-sites models and evolution of the ITS transcript in Syzygium and Myrtaceae. Mol. Phylogenet. Evol. 43, 124–139 (2007).
pubmed: 17070713
doi: 10.1016/j.ympev.2006.08.013
Craven, L. A. & Biffin, E. An infrageneric classification of Syzygium (Myrtaceae). Blumea 55, 94–99 (2010).
doi: 10.3767/000651910X499303
Biffin, E. et al. Evolution of exceptional species richness among lineages of fleshy-fruited Myrtaceae. Ann. Bot. 106, 79–93 (2010).
pubmed: 20462850
pmcid: 2889796
doi: 10.1093/aob/mcq088
Beech, E., Rivers, M., Oldfield, S. & Smith, P. GlobalTreeSearch: the first complete global database of tree species and country distributions. J. Sustain. For. 36, 454–489 (2017).
doi: 10.1080/10549811.2017.1310049
Govaerts, R. et al. World Checklist of Myrtaceae (Royal Botanic Gardens, 2008).
McVaugh, R. Nomenclatural notes on Myrtaceae and related families (continuation). Taxon 6, 162–167 (1956).
Nair, K. N. The genus Syzygium: Syzygium cumini and other underutilized species (CRC Press, 2017).
Kochummen, K. M. Myrtaceae. In Tree Flora of Malaya Vol. 3 (ed. Ng, F. S. P.) 119–134 (Longman Malaysia, Kuala Lumpur, 1978).
Boo, C. M., Omar-Hor, K., Ou-Yang, C. L. & Ng, C. K. 1001 Garden Plants in Singapore (National Parks, 2003).
Parnell, J., Craven, L. A. & Biffin, E. Matters of scale: dealing with one of the largest genera of angiosperms. In Reconstructing the Tree of Life: Taxonomy and Systematics of Species Rich Taxa (eds Hodkinson, T. R. & Parnell, J. A. N.) 251–273 (CRC Press LLC, 2007).
Lee, H. et al. Floristic and structural diversity of mixed dipterocarp forest in Lambir Hills National Park, Sarawak, Malaysia. J. Trop. For. Sci. 14, 379–400 (2002).
Craven, L. Unravelling knots or plaiting rope: what are the major taxonomic strands in Syzygium sens. lat. (Myrtaceae) and what should be done with them? In Taxonomy: The Cornerstone of Biodiversity (eds Saw, L. G., Chua, L. S. L. & Khoo, K. C.) 75–85 (Forest Research Institute Malaysia, Kepong, 2001).
Schmid, R. A resolution of the Eugenia–Syzygium controversy (Myrtaceae). Am. J. Bot. 59, 423–436 (1972).
doi: 10.1002/j.1537-2197.1972.tb10113.x
Jain, M., Olsen, H. E., Paten, B. & Akeson, M. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol. 17, 1–11 (2016).
Ruan, J. & Li, H. Fast and accurate long-read assembly with wtdbg2. Nat. Methods 17, 155–158 (2020).
pubmed: 31819265
doi: 10.1038/s41592-019-0669-3
Putnam, N. H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342–350 (2016).
pubmed: 26848124
pmcid: 4772016
doi: 10.1101/gr.193474.115
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
Zimin, A. V. et al. The MaSuRCA genome assembler. Bioinformatics 29, 2669–2677 (2013).
pubmed: 23990416
pmcid: 3799473
doi: 10.1093/bioinformatics/btt476
Stevens, P. F. Angiosperm Phylogeny Website, Version 17 http://www.mobot.org/MOBOT/research/APweb/ (2017).
Chanderbali, A. S., Berger, B. A., Howarth, D. G., Soltis, D. E. & Soltis, P. S. Evolution of floral diversity: genomics, genes and gamma. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20150509 (2017).
doi: 10.1098/rstb.2015.0509
Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463 (2007).
pubmed: 17721507
doi: 10.1038/nature06148
Jiao, Y. et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13, 1–14 (2012).
doi: 10.1186/gb-2012-13-1-r3
Myburg, A. A. et al. The genome of Eucalyptus grandis. Nature 510, 356–362 (2014).
pubmed: 24919147
doi: 10.1038/nature13308
Qin, G. et al. The pomegranate (Punica granatum L.) genome and the genomics of punicalagin biosynthesis. Plant J. 91, 1108–1128 (2017).
pubmed: 28654223
doi: 10.1111/tpj.13625
Yuan, Z. et al. The pomegranate (Punica granatum L.) genome provides insights into fruit quality and ovule developmental biology. Plant Biotechnol. J. 16, 1363–1374 (2018).
pubmed: 29271050
pmcid: 5999313
doi: 10.1111/pbi.12875
Feng, C. et al. A chromosome‐level genome assembly provides insights into ascorbic acid accumulation and fruit softening in guava (Psidium guajava). Plant Biotechnol. J. 19, 717–730 (2021).
pubmed: 33098334
doi: 10.1111/pbi.13498
One Thousand Plant Transcriptomes Initiative. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574, 679–685 (2019).
Wang, X. et al. Genome alignment spanning major Poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events. Mol. Plant 8, 885–898 (2015).
pubmed: 25896453
doi: 10.1016/j.molp.2015.04.004
Maurin, O. et al. A nuclear phylogenomic study of the angiosperm order Myrtales, exploring the potential and limitations of the universal Angiosperms353 probe set. Am. J. Bot. 108, 1087–1111 (2021).
Albert, V. A. et al. The Amborella genome and the evolution of flowering plants. Science 342, 1241089 (2013).
doi: 10.1126/science.1241089
Rice, A. et al. The Chromosome Counts Database (CCDB)—a community resource of plant chromosome numbers. N. Phytol. 206, 19–26 (2015).
doi: 10.1111/nph.13191
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Mirarab, S. et al. ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30, i541–i548 (2014).
pubmed: 25161245
pmcid: 4147915
doi: 10.1093/bioinformatics/btu462
Maddison, W. P. Gene trees in species trees. Syst. Biol. 46, 523–536 (1997).
doi: 10.1093/sysbio/46.3.523
Bryant, D. & Moulton, V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol. Biol. Evol. 21, 255–265 (2004).
pubmed: 14660700
doi: 10.1093/molbev/msh018
Burgon, J. D. et al. Phylogenomic inference of species and subspecies diversity in the Palearctic salamander genus Salamandra. Mol. Phylogenet. Evol. 157, 107063 (2021).
pubmed: 33387650
doi: 10.1016/j.ympev.2020.107063
Suh, A., Smeds, L. & Ellegren, H. The dynamics of incomplete lineage sorting across the ancient adaptive radiation of neoavian birds. PLoS Biol. 13, e1002224 (2015).
pubmed: 26284513
pmcid: 4540587
doi: 10.1371/journal.pbio.1002224
Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).
pubmed: 19648217
pmcid: 2752134
doi: 10.1101/gr.094052.109
Lawson, D. J., van Dorp, L. & Falush, D. A tutorial on how not to over-interpret STRUCTURE and ADMIXTURE bar plots. Nat. Commun. 9, 3258 (2018).
Zhang, X. et al. Genomes of the banyan tree and pollinator wasp provide insights into fig-wasp coevolution. Cell 183, 875–889. e17 (2020).
pubmed: 33035453
doi: 10.1016/j.cell.2020.09.043
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
pubmed: 22960212
pmcid: 3522152
doi: 10.1534/genetics.112.145037
Lan, T. et al. Insights into bear evolution from a Pleistocene polar bear genome. Proc. Natl. Acad. Sci. USA 119, e2200016119 (2022).
Li, H. & Ralph, P. Local PCA shows how the effect of population structure differs along the genome. Genetics 211, 289 (2019).
pubmed: 30459280
doi: 10.1534/genetics.118.301747
Reich, D., Price, A. L. & Patterson, N. Principal component analysis of genetic data. Nat. Genet. 40, 491–492 (2008).
pubmed: 18443580
doi: 10.1038/ng0508-491
Novembre, J. & Stephens, M. Interpreting principal component analyses of spatial population genetic variation. Nat. Genet. 40, 646–649 (2008).
pubmed: 18425127
pmcid: 3989108
doi: 10.1038/ng.139
Slatkin, M. Isolation by distance in equilibrium and non‐equilibrium populations. Evolution 47, 264–279 (1993).
pubmed: 28568097
doi: 10.1111/j.1558-5646.1993.tb01215.x
Wright, S. Isolation by distance. Genetics 28, 114 (1943).
pubmed: 17247074
pmcid: 1209196
doi: 10.1093/genetics/28.2.114
Seeholzer, G. F. & Brumfield, R. T. Isolation by distance, not incipient ecological speciation, explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis, Line‐cheeked Spinetail) despite near threefold body size change across an environmental gradient. Mol. Ecol. 27, 279–296 (2018).
pubmed: 29134710
doi: 10.1111/mec.14429
Barton, N. H. Natural selection and random genetic drift as causes of evolution on islands. Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 351, 785–795 (1996).
doi: 10.1098/rstb.1996.0073
Gavrilets, S. Perspective: models of speciation: what have we learned in 40 years? Evolution 57, 2197–2215 (2003).
pubmed: 14628909
doi: 10.1111/j.0014-3820.2003.tb00233.x
Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005).
doi: 10.1111/j.1461-0248.2004.00715.x
Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009).
pubmed: 19197053
doi: 10.1126/science.1160006
Shafer, A. B. & Wolf, J. B. Widespread evidence for incipient ecological speciation: a meta‐analysis of isolation‐by‐ecology. Ecol. Lett. 16, 940–950 (2013).
pubmed: 23627762
doi: 10.1111/ele.12120
Salojärvi, J. et al. Author Correction: genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat. Genet. 51, 1187–1189 (2019).
pubmed: 31197270
pmcid: 8076037
doi: 10.1038/s41588-019-0442-7
Hu, G. et al. Two divergent haplotypes from a highly heterozygous lychee genome suggest independent domestication events for early and late-maturing cultivars. Nat. Genet. 54, 73–83 (2022).
pubmed: 34980919
pmcid: 8755541
doi: 10.1038/s41588-021-00971-3
Barton, N. H. & Charlesworth, B. Genetic revolutions, founder effects, and speciation. Annu. Rev. Ecol. Syst. 15, 133–164 (1984).
doi: 10.1146/annurev.es.15.110184.001025
Kooyman, R. M. et al. Origins and assembly of Malesian rainforests. Annu. Rev. Ecol. Evol. Systemat. 50, 119–143 (2019).
Matzke, N. J. BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R Scripts. R package version 0.2.1 https://rdrr.io/cran/BioGeoBEARS/ (2013).
Yu, Y., Blair, C. & He, X. RASP 4: ancestral state reconstruction tool for multiple genes and characters. Mol. Biol. Evol. 37, 604–606 (2020).
pubmed: 31670774
doi: 10.1093/molbev/msz257
Thornhill, A. H., Ho, S. Y., Kulheim, C. & Crisp, M. D. Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny. Mol. Phylogenet. Evol. 93, 29–43 (2015).
pubmed: 26211451
doi: 10.1016/j.ympev.2015.07.007
Tarran, M., Wilson, P. G., Paull, R., Biffin, E. & Hill, R. S. Identifying fossil Myrtaceae leaves: the first described fossils of Syzygium from Australia. Am. J. Bot. 105, 1748–1759 (2018).
pubmed: 30276795
doi: 10.1002/ajb2.1163
Hall, R. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J. Asian Earth Sci. 20, 353–431 (2002).
doi: 10.1016/S1367-9120(01)00069-4
Hall, R. Late Jurassic–Cenozoic reconstructions of the Indonesian region and the Indian Ocean. Tectonophysics 570, 1–41 (2012).
doi: 10.1016/j.tecto.2012.04.021
Toussaint, E. F. et al. The towering orogeny of New Guinea as a trigger for arthropod megadiversity. Nat. Commun. 5, 1–10 (2014).
doi: 10.1038/ncomms5001
Cannon, C. H., Morley, R. J. & Bush, A. B. The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proc. Natl Acad. Sci. USA 106, 11188–11193 (2009).
pubmed: 19549829
pmcid: 2708749
doi: 10.1073/pnas.0809865106
Stelbrink, B. A Biogeographic View on Southeast Asia's History. 271 (Humboldt-Universität zu Berlin, Lebenswissenschaftliche Fakultät, 2015).
PAGES, P. I. W. G. O. Interglacials of the last 800,000 years. Rev. Geophys. 54, 162–219 (2016).
doi: 10.1002/2015RG000482
Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. Version 3.61 http://mesquiteproject.org (2019).
Vasconcelos, T. N. C., Lucas, E. J., Conejero, M., Giaretta, A. & Prenner, G. Convergent evolution in calyptrate flowers of Syzygieae (Myrtaceae). Bot. J. Linn. Soc. 192, 498–509 (2019).
doi: 10.1093/botlinnean/boz105
Gorchov, D. L., Cornejo, F., Ascorra, C. F. & Jaramillo, M. Dietary overlap between frugivorous birds and bats in the Peruvian Amazon. Oikos 74, 235–250 (1995).
Hodgkison, R., Balding, S. T., Zubaid, A. & Kunz, T. H. Fruit Bats (Chiroptera: Pteropodidae) as seed dispersers and pollinators in a lowland Malaysian rain Forest1. Biotropica 35, 491–502 (2003).
doi: 10.1111/j.1744-7429.2003.tb00606.x
Teixeira, R. C., Corrêa, C. E. & Fischer, E. Frugivory by Artibeus jamaicensis (Phyllostomidae) bats in the Pantanal, Brazil. Stud. Neotrop. Fauna Environ. 44, 7–15 (2009).
doi: 10.1080/01650520802692283
Kalko, E. K. & Condon, M. Echolocation, olfaction and fruit display: how bats find fruit of flagellichorous cucurbits. Funct. Ecol. 12, 364–372 (1998).
doi: 10.1046/j.1365-2435.1998.00198.x
Stocker, G. & Irvine, A. Seed dispersal by cassowaries (Casuarius casuarius) in North Queensland’s rainforests. Biotropica 15, 170–176 (1983).
Michael, T. P. et al. High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat. Commun. 9, 1–8 (2018).
doi: 10.1038/s41467-018-03016-2
Li, H. seqtk Toolkit for processing sequences in FASTA/Q formats. GitHub 767, 69 (2012).
Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27, 737–746 (2017).
pubmed: 28100585
pmcid: 5411768
doi: 10.1101/gr.214270.116
Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Laetsch, D. R. & Blaxter, M. L. BlobTools: interrogation of genome assemblies. F1000Research 6, 1287 (2017).
doi: 10.12688/f1000research.12232.1
Roach, M. J., Schmidt, S. A. & Borneman, A. R. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinform. 19, 1–10 (2018).
doi: 10.1186/s12859-018-2485-7
Robertson, G. et al. De novo assembly and analysis of RNA-seq data. Nat. Methods 7, 909–912 (2010).
pubmed: 20935650
doi: 10.1038/nmeth.1517
Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).
pubmed: 23845962
doi: 10.1038/nprot.2013.084
Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).
pubmed: 25690850
pmcid: 4643835
doi: 10.1038/nbt.3122
Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Gilbert, D. G. Genes of the pig, Sus scrofa, reconstructed with EvidentialGene. PeerJ 7, e6374 (2019).
pubmed: 30723633
pmcid: 6361002
doi: 10.7717/peerj.6374
Tarailo‐Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinform. 25, 4.10.1–4.10.14 (2009).
Keilwagen, J., Hartung, F. & Grau, J. GeMoMa: homology-based gene prediction utilizing intron position conservation and RNA-seq data. Methods Mol. Biol. 1962, 161–177 (2019).
pubmed: 31020559
doi: 10.1007/978-1-4939-9173-0_9
Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic acids Res. 31, 5654–5666 (2003).
pubmed: 14500829
pmcid: 206470
doi: 10.1093/nar/gkg770
Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, 1–22 (2008).
doi: 10.1186/gb-2008-9-1-r7
Lyons, E. et al. Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol. 148, 1772–1781 (2008).
pubmed: 18952863
pmcid: 2593677
doi: 10.1104/pp.108.124867
Joyce, B. L. et al. FractBias: a graphical tool for assessing fractionation bias following polyploidy. Bioinformatics 33, 552–554 (2017).
pubmed: 27794557
Team, R. C. R: A Language and Environment For Statistical Computing (Team, R. C., 2013).
Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).
doi: 10.21105/joss.01686
Hadley, W. Ggplot2: Elegrant Graphics for Data Analysis (Springer, 2016).
Neuwirth, E. RColorBrewer: ColorBrewer Palettes. R package version 1.1-2 https://cran.r-project.org/web/packages/RColorBrewer/index.htmlPackage (2014).
Wilke, C. O. Ridgeline plots in ‘ggplot2’[R Package Ggridges Version 0.5.3] https://cran.r-project.org/web/packages/ggridges/index.html (2021).
Aphalo, P. J. et al. ggpmisc: Miscellaneous Extensions to “ggplot2”. R package version 0.3.6 https://cran.r-project.org/web/packages/ggpmisc/index.html (2020).
Wilkie, P., Poulsen, A. D., Harris, D. & Forrest, L. L. The collection and storage of plant material for DNA extraction: the teabag method. Gardens’ Bull. Singap. 65, 4 (2013).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv preprint arXiv:1303.3997 (2013).
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 2832824
doi: 10.1093/bioinformatics/btq033
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Rambaut, A. FigTree v1.4 http://tree.bio.ed.ac.uk/software/figtree/ (2012).
Levy, D. & Pachter, L. The neighbor-net algorithm. Adv. Appl. Math. 47, 240–258 (2011).
doi: 10.1016/j.aam.2010.09.002
Huson, D. & Huson, D. H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics (Oxford, Engl.) 14, 68–73 (1998).
doi: 10.1093/bioinformatics/14.1.68
Lockhart, P. J., Steel, M. A., Hendy, M. D. & Penny, D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11, 605–612 (1994).
pubmed: 19391266
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242
pmcid: 6137996
doi: 10.1093/bioinformatics/bty191
Toolkit, P. GitHub Repository http://broadinstitute.github.io/picard (Broad Institute, 2019).
Neph, S. et al. BEDOPS: high-performance genomic feature operations. Bioinformatics 28, 1919–1920 (2012).
pubmed: 22576172
pmcid: 3389768
doi: 10.1093/bioinformatics/bts277
Bonfield, J. K. et al. HTSlib: C library for reading/writing high-throughput sequencing data. Gigascience 10, giab007 (2021).
Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).
pubmed: 33590861
pmcid: 7931819
doi: 10.1093/gigascience/giab008
Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).
pubmed: 16862161
doi: 10.1038/ng1847
Salojärvi, J. et al. Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat. Genet. 49, 904–912 (2017).
pubmed: 28481341
doi: 10.1038/ng.3862
Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).
pubmed: 21753753
pmcid: 3154645
doi: 10.1038/nature10231
Popescu, A.-A., Huber, K. T. & Paradis, E. ape 3.0: new tools for distance-based phylogenetics and evolutionary analysis in R. Bioinformatics 28, 1536–1537 (2012).
pubmed: 22495750
doi: 10.1093/bioinformatics/bts184