Advertisement

Plant Systematics and Evolution

, Volume 305, Issue 10, pp 961–974 | Cite as

Targeted amplicon sequencing of 40 nuclear genes supports a single introduction and rapid radiation of Hawaiian Metrosideros (Myrtaceae)

  • Julian R. DupuisEmail author
  • Yohan Pillon
  • Tomoko Sakishima
  • Chrissen E. C. Gemmill
  • Srikar Chamala
  • W. Brad Barbazuk
  • Scott M. Geib
  • Elizabeth A. StacyEmail author
Original Article
  • 111 Downloads

Abstract

Compared to traditionally used plastid or ribosomal markers, nuclear gene markers provide many advantages for molecular systematics of plants, and high-throughput sequencing technologies are making large nuclear datasets available at an unprecedented rate. We used targeted amplicon sequencing of 44 nuclear genes to construct a time-calibrated phylogeny of genus Metrosideros (Myrtaceae), evaluate recent systematic revisions, and assess whether phylogenetic signal within the Hawaiian Archipelago is correlated with island biogeography or morphological diversification. We generated a final dataset of 40 nuclear genes for 187 specimens, used multiple search heuristics and species-tree analysis to estimate a phylogeny, and incorporated new fossils for the genus to estimate divergence times across the dataset. All analyses supported the monophyly of Metrosideros, including Carpolepis and Tepualia. Hawaiian Metrosideros were monophyletic and dated to 3.1 MYA using new fossils for the genus, which is intermediate to previous estimates based on nuclear ribosomal/chloroplast loci and calibrated with island ages. Within the Hawaiian Metrosideros clade, we observed short branch lengths and unresolved relationships, and phylogenetic patterns were not concordant with biogeographic hypotheses of island progression, or the delineation of taxa or morphotypes. Average nucleotide diversity was relatively consistent across the Hawaiian Islands with the exception of slightly lower diversity on Kauaʻi. These results provide a data-rich estimate of the timing of a single introduction of Metrosideros to Hawai‘i and highlight the need for molecular markers with higher evolutionary rates for resolution of relationships within this recent radiation.

Keywords

Island biogeography Molecular dating Next-generation sequencing Pacific Islands Phylogenomics 

Notes

Acknowledgements

The authors thank J. Johansen and A. Williams for assistance with sample collection and the Hawaiʻi Division of Forestry and Wildlife for permission to collect from state forests. They also thank Laure Barrabé, Abby Cuttriss, Gildas Gâteblé, Melissa Johnson, Jean-Yves Meyer, Greg Plunkett (“Plant and People of Vanuatu” Project), Laurence Ramon, Ravahere Taputuarai, the staff of the national Park of American Samoa, the herbarium NOU, Eve Lucas and the Kew DNA bank for providing DNA samples, and Mark Simmons, for comments on an earlier draft of this manuscript. Fluidigm Access Array amplification and MiSeq sequencing were conducted at the Institute for Bioinformatics and Evolutionary Studies (IBEST) at the University of Idaho. Data processing and analysis were conducted on the moana HPC cluster at the United States Department of Agriculture, Agricultural Research Service, Daniel K. Inouye Pacific Basin Agricultural Research Center. USDA is an equal opportunity employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. Funding was provided by NSF DEB 0954274 and NSF HRD 0833211. Figures were prepared using FigTree v1.4.4 (Rambaut and Drummond 2010) and Inkscape v0.91 (The Inkscape Team 2017).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

Raw reads are provided as a NCBI Sequence Reads Archive (BioProject PRJNA526920, SRA accessions: SRR8737094-SRR8737280), and data input and parameter files are available in the Electronic Supplementary Material.

Supplementary material

606_2019_1615_MOESM1_ESM.xlsx (29 kb)
Supplementary material 1 (XLSX 28 kb)
606_2019_1615_MOESM2_ESM.phy (1.9 mb)
Supplementary material 2 (PHY 1895 kb)
606_2019_1615_MOESM3_ESM.nex (2 kb)
Supplementary material 3 (NEX 1 kb)
606_2019_1615_MOESM4_ESM.pdf (70 kb)
Supplementary material 4 (PDF 69 kb)
606_2019_1615_MOESM5_ESM.tre (334 kb)
Supplementary material 5 (TRE 333 kb)
606_2019_1615_MOESM6_ESM.txt (339 kb)
Supplementary material 6 (TXT 338 kb)
606_2019_1615_MOESM7_ESM.pdf (468 kb)
Supplementary material 7 (PDF 467 kb)
606_2019_1615_MOESM8_ESM.zip (85 kb)
Supplementary material 8 (ZIP 86 kb)

References

  1. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92.  https://doi.org/10.1038/nrg.2015.28 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bailey CD, Doyle JJ (1999) Potential phylogenetic utility of the low-copy nuclear gene pistillata in Docotyledonous plants: comparison to nrDNA ITS and trnL intron in Sphaeocardamum and other Brassicaceae. Molec Phylogen Evol 13:20–30CrossRefGoogle Scholar
  3. Berger BA, Kriebel R, Spalink D, Sytsma KJ (2016) Divergence times, historical biogeography, and shifts in speciation rates of Myrtales. Molec Phylogen Evol 95:116–136.  https://doi.org/10.1016/j.ympev.2015.10.001 CrossRefPubMedGoogle Scholar
  4. Bess EC, Catanach TA, Johnson KP, Fernández-Palacios JM (2014) The importance of molecular dating analyses for inferring Hawaiian biogeographical history: a case study with bark lice (Psocidae:Ptycta). J Biogeogr 41:158–167.  https://doi.org/10.1111/jbi.12191 CrossRefGoogle Scholar
  5. Biffin E, Lucas EJ, Craven LA, Ribeiro da Costa I, Harrington MG, Crisp MD (2010) Evolution of exceptional species richness among lineages of fleshy-fruited Myrtaceae. Ann Bot (Oxford) 106:79–93.  https://doi.org/10.1093/aob/mcq088 CrossRefGoogle Scholar
  6. Bouckaert R et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537.  https://doi.org/10.1371/journal.pcbi.1003537 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bybee SM et al (2011) Targeted amplicon sequencing (TAS): a scalable next-gen approach to multilocus, multitaxa phylogenetics. Genome Biol Evol 3:1312–1323.  https://doi.org/10.1093/gbe/evr106 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carstens BC, Satler JD (2013) The carniverous plant described as Sarracenia alata contains two cryptic species. Biol J Linn Soc 109:737–746CrossRefGoogle Scholar
  9. Chou J, Gupta A, Yaduvanshi S, Davidson R, Nute M, Mirarab S, Warnow T (2015) A comparative study of SVDquartets and other coalescent-based species tree estimation methods. BMC Genom 16:S2.  https://doi.org/10.1186/1471-2164-16-S10-S2 CrossRefGoogle Scholar
  10. Clague DA, Braga JC, Bassi D, Fullagar PD, Renema W, Webster JM (2009) The maximum age of Hawaiian terrestrial lineages: geological constraints from Kōko Seamount. J Biogeogr 37:1022–1033.  https://doi.org/10.1111/j.1365-2699.2009.02235.x CrossRefGoogle Scholar
  11. Corn CA, Hiesey WM (1973) Altitudinal variation in Hawaiian Metrosideros. Amer J Bot 60:991–1002CrossRefGoogle Scholar
  12. Couper RA (1960) New Zealand mesozoic and cainozoic plant microfossils. Government Printer, WellingtonGoogle Scholar
  13. de Sousa F, Bertrand YJ, Nylinder S, Oxelman B, Eriksson JS, Pfeil BE (2014) Phylogenetic properties of 50 nuclear loci in Medicago (Leguminosae) generated using multiplexed sequence capture and next-generation sequencing. PLoS ONE 9:e109704.  https://doi.org/10.1371/journal.pone.0109704 CrossRefPubMedPubMedCentralGoogle Scholar
  14. DeBoer N, Stacy EA (2013) Divergence within and among 3 Varieties of the Endemic Tree, ‘Ohi’a Lehua (Metrosideros polymorpha) on the Eastern Slope of Hawaiʻi Island. J Heredity 104:449–458.  https://doi.org/10.1093/jhered/est027 CrossRefPubMedGoogle Scholar
  15. Drake DR (1992) Seed dispersal of Metrosideros polymorpha (Myrtaceae): a pioneer tree of Hawaiian lava flows. Amer J Bot 79:1224–1228CrossRefGoogle Scholar
  16. Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88.  https://doi.org/10.1371/journal.pbio.0040088 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Duarte JM et al (2010) Identification of shared single copy nuclear genes in Arabadopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol Biol 10:61CrossRefGoogle Scholar
  18. Dupuis JR, Bremer FT, Kauwe A, San Jose M, Leblanc L, Rubinoff D, Geib SM (2018) HiMAP: robust phylogenomics from highly multiplexed amplicon sequencing. Molec Ecol Resources 18:1000–1019.  https://doi.org/10.1111/1755-0998.12783 CrossRefGoogle Scholar
  19. Dawson JW, Stemmermann L (1990) Metrosideros (Gaud.). In: Wagner WI, Herbst DR, Sohmer SH (eds) Manual of the flowering plants of Hawai‘i. University of Hawai‘i Press, Honolulu Hawai‘iGoogle Scholar
  20. Gandolfo MA et al (2011) Oldest known Eucalyptus macrofossils are from South America. PLoS ONE 6:e21084.  https://doi.org/10.1371/journal.pone.0021084 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gardner RC, De Lange PJ, Keeling DJ, Bowala T, Brown HA, Wright SD (2004) A late Quaternary phylogeography for Metrosideros (Myrtaceae) in New Zealand inferred from chloroplast DNA haplotypes. Biol J Linn Soc 83:399–412CrossRefGoogle Scholar
  22. Gemmill CE, Allan GJ, Wagner WL, Zimmer EA (2002) Evolution of insular Pacific Pittosporum (Pittosporaceae): origin of the Hawaiian radiation. Molec Phylogen Evol 22:31–42.  https://doi.org/10.1006/mpev.2001.1019 CrossRefGoogle Scholar
  23. Gillespie RG, Baldwin BG (2010) Island biogeography of remote archipelagoes. In: Losos JB, Ricklefs RE (eds) The theory of island biogeography revisited. Princeton University Press, PrincetonGoogle Scholar
  24. Govaerts R et al (2008) World checklist of Myrtaceae. Kew Publishing, Royal Botanical Gardens, Kew, pp 1–455Google Scholar
  25. Graham A (1985) Studies in Neotropical Paleobotany IV. The Eocene communities of Panama. Ann Missouri Bot Gard 72:504–534CrossRefGoogle Scholar
  26. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321.  https://doi.org/10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  27. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018a) UFBoot2: improving the ultrafast bootstrap approximation. Molec Biol Evol 35:518–522.  https://doi.org/10.1093/molbev/msx281 CrossRefPubMedGoogle Scholar
  28. Hoang DT, Vinh LS, Flouri T, Stamatakis A, von Haeseler A, Minh BQ (2018b) MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evol Biol 18:11.  https://doi.org/10.1186/s12862-018-1131-3 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hollingsworth PM et al (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797.  https://doi.org/10.1073/pnas.0905845106 CrossRefGoogle Scholar
  30. Johnson MA, Pillon Y, Sakishima T, Price DK, Stacy EA (2019) Multiple colonizations, hybridization and uneven diversification in Cyrtandra (Gesneriaceae) lineages on Hawai’i Island. J Biogeogr 46:1178–1196.  https://doi.org/10.1111/jbi.13567 CrossRefGoogle Scholar
  31. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589.  https://doi.org/10.1038/nmeth.4285 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molec Biol Evol 30:772–780.  https://doi.org/10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498CrossRefGoogle Scholar
  34. Kress WJ (2017) Plant DNA barcodes: applications today and in the future. J Syst Evol 55:291–307.  https://doi.org/10.1111/jse.12254 CrossRefGoogle Scholar
  35. Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30:3276–3278.  https://doi.org/10.1093/bioinformatics/btu531 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lowrey TK, Quinn CJ, Taylor RK, Chan R, Kimball RT, De Nardi JC (2001) Molecular and morphological reassessment of relationships within the Vittadinia group of Astereae (Asteraceae). Amer J Bot 88:1279–1289CrossRefGoogle Scholar
  37. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963.  https://doi.org/10.1093/bioinformatics/btr507 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12CrossRefGoogle Scholar
  39. Moore WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726PubMedGoogle Scholar
  40. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkCrossRefGoogle Scholar
  41. Nepokroeff M, Sytsma KJ, Wagner WL, Zimmer EA (2003) Reconstructing ancestral patterns of colonization and dispersal in the Hawaiian understory tree genus Psychotria (Rubiaceae): a comparison of parsimony and likelihood approaches. Syst Biol 52:820–838.  https://doi.org/10.1080/10635150390251072 CrossRefPubMedGoogle Scholar
  42. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molec Biol Evol 32:268–274.  https://doi.org/10.1093/molbev/msu300 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Oh S-H, Potter D (2003) Phylogenetic utility of the second intron of LEAFY in Neillia and Stephanandra (Rosaceae) and implications for the origin of Stephanandra. Molec Phylogen Evol 29:203–215.  https://doi.org/10.1016/s1055-7903(03)00093-9 CrossRefGoogle Scholar
  44. Olmstead RG, Palmer JD (1994) Chloroplast DNA systematics: a review of methods and data analysis. Amer J Bot 81:1205–1224CrossRefGoogle Scholar
  45. O’Neill EM et al (2013) Parallel tagged amplicon sequencing reveals major lineages and phylogenetic structure in the North American tiger salamander (Ambystoma tigrinum) species complex. Molec Ecol 22:111–129.  https://doi.org/10.1111/mec.12049 CrossRefGoogle Scholar
  46. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420.  https://doi.org/10.1093/bioinformatics/btp696 CrossRefPubMedGoogle Scholar
  47. Percy DM, Garver AM, Wagner WL, James HF, Cunningham CW, Miller SE, Fleischer RC (2008) Progressive island colonization and ancient origin of Hawaiian Metrosideros (Myrtaceae). Proc Royal Soc B 275:1479–1490.  https://doi.org/10.1098/rspb.2008.0191 CrossRefGoogle Scholar
  48. Pigg KB, Stockey RA, Maxwell SL (1993) Paleomyrtinaea, a new genus of permineralized myrtaceous fruits and seeds from the Eocene of British Columbia and Paleocene of North Dakota. Canad J Bot 71:1–9CrossRefGoogle Scholar
  49. Pillon Y (2018) A new species of Metrosideros (Myrtaceae) from Vanuatu and notes on the genus. Phytotaxa 347:197.  https://doi.org/10.11646/phytotaxa.347.2.10 CrossRefGoogle Scholar
  50. Pillon Y et al (2013a) Potential use of low-copy nuclear genes in DNA barcoding: a comparison with plastid genes in two Hawaiian plant radiations. BMC Evol Biol 13:35CrossRefGoogle Scholar
  51. Pillon Y, Johansen JB, Sakishima T, Roalson EH, Price DK, Stacy EA (2013b) Gene discordance in phylogenomics of recent plant radiations, an example from Hawaiian Cyrtandra (Gesneriaceae). Molec Phylogen Evol 69:293–298.  https://doi.org/10.1016/j.ympev.2013.05.003 CrossRefGoogle Scholar
  52. Pillon Y, Johansen J, Sakishima T, Chamala S, Barbazuk WB, Stacy EA (2014) Primers for low-copy nuclear genes in Metrosideros and cross-amplification in Myrtaceae. Appl Pl Sci 2:1400049.  https://doi.org/10.3732/apps.1400049 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pillon Y, Lucas E, Johansen JB, Sakishima T, Hall B, Geib SM, Stacy EA (2015) An expanded Metrosideros (Myrtaceae) to include Carpolepis and Tepualia based on nuclear genes. Syst Bot 40:782–790.  https://doi.org/10.1600/036364415x689249 CrossRefGoogle Scholar
  54. Pole M, Dawson J, Denton T (2008) Fossil Myrtaceae from the Early Miocene of southern New Zealand. Austral J Bot 56:67.  https://doi.org/10.1071/bt07032 CrossRefGoogle Scholar
  55. Portik DM, Smith LL, Bi K (2016) An evaluation of transcriptome-based exon capture for frog phylogenomics across multiple scales of divergence (Class: Amphibia, Order: Anura). Molec Ecol Resources 16:1069–1083.  https://doi.org/10.1111/1755-0998.12541 CrossRefGoogle Scholar
  56. Price JP, Clague DA (2002) How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proc Royal Soc B 269:2429–2435.  https://doi.org/10.1098/rspb.2002.2175 CrossRefGoogle Scholar
  57. Price JP, Wagner WL (2018) Origins of the Hawaiian flora: phylogenies and biogeography reveal patterns of long-distance dispersal. J Syst Evol 56:600–620.  https://doi.org/10.1111/jse.12465 CrossRefGoogle Scholar
  58. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-projectorg/
  59. Rambaut A, Drummond AJ (2010) FigTree v1.4.4. Institute of Evolutionary Biology, University of Edinburgh. Available at: http://www.treebioedacuk/software/figtree
  60. Romero EJ, Zamaloa MC (1985) Polen de Angiospermas de la formacion Rio Turbio (Eoceno), Provincia de Santa Cruz, Republica Argentina. Ameghiniana 22:43–51Google Scholar
  61. Sang T (2002) Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Molec Biol 37:121–147.  https://doi.org/10.1080/10409230290771474 CrossRefGoogle Scholar
  62. Sayyari E, Mirarab S (2016) Fast coalescent-based computation of local branch support from quartet frequencies. Molec Biol Evol 33:1654–1668.  https://doi.org/10.1093/molbev/msw079 CrossRefPubMedGoogle Scholar
  63. Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction in plants. Austral Syst Bot 17:145–170CrossRefGoogle Scholar
  64. Soltis DE, Soltis PS (1998) Choosing an approach and an appropriate gene for phylogenetic analysis. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer, BostonCrossRefGoogle Scholar
  65. Stacy EA, Sakishima T (2019) Phylogeography of the highly dispersible landscape-dominant woody species complex, Metrosideros, in Hawaii. J Biogeogr (Online First).  https://doi.org/10.1111/jbi.13650 CrossRefGoogle Scholar
  66. Stacy EA, Johansen JB, Sakishima T, Price DK, Pillon Y (2014) Incipient radiation within the dominant Hawaiian tree Metrosideros polymorpha. Heredity 113:334–342.  https://doi.org/10.1038/hdy.2014.47 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Stacy EA, Johansen JB, Sakishima T, Price DK (2016) Genetic analysis of an ephemeral intraspecific hybrid zone in the hypervariable tree, Metrosideros polymorpha, on Hawai‘i Island. Heredity 117:173–183.  https://doi.org/10.1038/hdy.2016.40 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Stallman JK, Funk VA, Price JP, Knope ML (2019) DNA barcodes fail to accurately differentiate species in Hawaiian plant lineages. Bot J Linn Soc 190:374–388.  https://doi.org/10.1093/botlinnean/boz024 CrossRefGoogle Scholar
  69. Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Amer J Bot 99:349–364.  https://doi.org/10.3732/ajb.1100335 CrossRefGoogle Scholar
  70. Sun M, Soltis DE, Soltis PS, Zhu X, Burleigh JG, Chen Z (2015) Deep phylogenetic incongruence in the angiosperm clade Rosidae. Molec Phylogen Evol 83:156–166.  https://doi.org/10.1016/j.ympev.2014.11.003 CrossRefGoogle Scholar
  71. Sur GL, Keating R, Snow N, Stacy EA (2018) Leaf micromorphology aids taxonomic delineation within the hypervariable genus Metrosideros (Myrtaceae) on O‘ahu. Pac Sci 72:345–361.  https://doi.org/10.2984/72.3.6 CrossRefGoogle Scholar
  72. Syring J, Willyard A, Cronn R, Liston A (2005) Evolutionary relationships among Pinus (Pinaceae) subsections inferred from multiple low-copy nuclear loci. Amer J Bot 92:2086–2100CrossRefGoogle Scholar
  73. Tarran M, Wilson PG, Hill RS (2016) Oldest record of Metrosideros (Myrtaceae): fossil flowers, fruits, and leaves from Australia. Amer J Bot 103:754–768.  https://doi.org/10.3732/ajb.1500469 CrossRefPubMedGoogle Scholar
  74. Tarran M, Wilson PG, Macphail MK, Jordan GJ, Hill RS (2017) Two fossil species of Metrosideros (Myrtaceae) from the Oligo-Miocene Golden Fleece locality in Tasmania, Australia. Amer J Bot 104:891–904.  https://doi.org/10.3732/ajb.1700095 CrossRefGoogle Scholar
  75. The Inkscape Team (2017) Inkscape v0.91. Available at: https://www.inkscapeorg
  76. Thornhill AH, Ho SY, Kulheim C, Crisp MD (2015) Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny. Molec Phylogen Evol 93:29–43.  https://doi.org/10.1016/j.ympev.2015.07.007 CrossRefPubMedGoogle Scholar
  77. Uribe-Convers S, Settles ML, Tank DC (2016) A phylogenomic approach based on PCR target enrichment and high throughput sequencing: resolving the diversity within the South American species of Bartsia L. (Orobanchaceae). PLoS ONE 11:e0148203.  https://doi.org/10.1371/journal.pone.0148203 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Vasconcelos TNC et al (2017) Myrteae phylogeny, calibration, biogeography and diversification patterns: increased understanding in the most species rich tribe of Myrtaceae. Molec Phylogen Evol 109:113–137.  https://doi.org/10.1016/j.ympev.2017.01.002 CrossRefPubMedGoogle Scholar
  79. Wagner WL, Funk VA (1995) Hawaiian biogeography: evolution on a hot spot archipelago. Smithsonian Institution Press, Washington DCGoogle Scholar
  80. Wagner WL, Herbst DR, Lorence DH (2005) Flora of the Hawaiian Islands website. Available at: http://botany.si.edu/pacificislandbiodiversity/hawaiianflora/index.htm. Accessed Feb 2019
  81. Weitemier K, Straub SC, Cronn RC, Fishbein M, Schmickl R, McDonnell A, Liston A (2014) Hyb-Seq: Combining target enrichment and genome skimming for plant phylogenomics. Appl Pl Sci 2:1400042.  https://doi.org/10.3732/apps.1400042 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis PS, Soltis DE (eds) Molecular systematics of plants II. Kluwer Academic, Dordrecht, pp 265–296CrossRefGoogle Scholar
  83. Wilson PG (2011) Myrtaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol. X. Sapindales, Cucurbitales, Myrtaceae. Springer, Heidelberg, pp 212–271Google Scholar
  84. Wright SD, Yong CG, Dawson JW, Whittaker DJ, Gardner RC (2000) Riding the ice age El Nino? Pacific biogeography and evolution of Metrosideros subg. Metrosideros (Myrtaceae) inferred from nuclear ribosomal DNA. Proc Natl Acad Sci USA 97:4118–4123.  https://doi.org/10.1073/pnas.050351197 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Wright SD, Yong CG, Wichman SR, Dawson JW, Gardner RC (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS + ETS). J Biogeogr 28:769–774CrossRefGoogle Scholar
  86. Zhang C, Rabiee M, Sayyari E, Mirarab S (2018) ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19:153.  https://doi.org/10.1186/s12859-018-2129-y CrossRefPubMedPubMedCentralGoogle Scholar
  87. Zimmer EA, Wen J (2012) Using nuclear gene data for plant phylogenetics: progress and prospects. Molec Phylogen Evol 65:774–785.  https://doi.org/10.1016/j.ympev.2013.01.005 CrossRefPubMedGoogle Scholar
  88. Zimmer EA, Wen J (2015) Using nuclear gene data for plant phylogenetics: Progress and prospects II. Next-gen approaches. J Syst Evol 53:371–379.  https://doi.org/10.1111/jse.12174 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.U.S. Department of Agriculture-Agricultural Research ServiceDaniel K. Inouye U.S. Pacific Basin Agricultural Research CenterHiloUSA
  2. 2.Department of Plant and Environmental Protection ServicesUniversity of Hawaiʻi at MānoaHonoluluUSA
  3. 3.LSTM, IRD, INRA, CIRAD, Montpellier SupAgroUniversity of MontpellierMontpellierFrance
  4. 4.Department of Biology and Tropical Conservation Biology and Environmental Science ProgramUniversity of HawaiʻiHiloUSA
  5. 5.School of Life SciencesUniversity of NevadaLas VegasUSA
  6. 6.School of ScienceUniversity of WaikatoHamilton, AotearoaNew Zealand
  7. 7.Department of BiologyUniversity of FloridaGainesvilleUSA
  8. 8.Department of Pathology, Immunology and Laboratory MedicineUniversity of FloridaGainesvilleUSA

Personalised recommendations