Plant Systematics and Evolution

, Volume 304, Issue 7, pp 841–851 | Cite as

Phylogenetic relationships among Ananas and related taxa (Bromelioideae, Bromeliaceae) based on nuclear, plastid and AFLP data

  • Sabine Matuszak-RengerEmail author
  • Juraj Paule
  • Sascha Heller
  • Elton M. C. Leme
  • Gerardo M. Steinbeisser
  • Michael H. J. Barfuss
  • Georg Zizka
Original Article


Since the first description of the genus in 1754, the taxonomy of Ananas underwent many fundamental changes and it is still the subject of a vivid debate. We present a phylogeny comprising all seven known Ananas taxa, Pseudananas sagenarius as well as closely related members of Bromelioideae (Aechmea subg. Chevaliera) based on three nuclear markers (agt1, ETS, phyC), five plastid markers (atpB–rbcL, trnL–trnF, matK, two segments of ycf1) and AFLP data. This study reveals a close relationship between Ananas, P. sagenarius, Aechmea tayoensis and Disteganthus basilateralis, and proposes novel relationship of the Ananas clade and Aechmea fernandae. Taxonomic implications of our analysis in particular the recognition of species versus varieties in Ananas are discussed. Furthermore, we could show that the evolution of two traits (scape bracts and the apical coma of the inflorescence) might be interlinked.


Aechmea subg. Chevaliera Bayesian inference Disteganthus Pineapple Pseudananas Stochastic character mapping 



We thank Ingo Michalak (University of Leipzig) for his support with the Shimodaira-Hasegawa test. The study was financially supported by the research funding programme “LOEWE—Landesoffensive zur Entwicklung wissenschaftlich-ökologischer Exzellenz” of Hesse’s Ministry of higher education as well as the “Freunde und Förderer” of Goethe-University Frankfurt and Paul Ungerer-Stiftung. We also acknowledge financial support of the German Research Foundation (DFG ZI 557/6-2 and 7-1, SCHU 2426/1-1).

Supplementary material

606_2018_1514_MOESM1_ESM.xlsx (17 kb)
Online Resource 1. List of species names included in this study, specimen information, and GenBank accession numbers for all sequences.
606_2018_1514_MOESM2_ESM.nex (418 kb)
Online Resource 2. Alignment of studied markers (agt1, atpB–rbcL, ETS, matK, phyC, trnL–trnF, ycf1 pos. 1114-2102 and 4550-5532) and AFLP data.
606_2018_1514_MOESM3_ESM.pdf (178 kb)
Online Resource 3. Primer combinations used for selective AFLP amplifications in initial screening and in final analyses.
606_2018_1514_MOESM4_ESM.pdf (191 kb)
Online Resource 4. Results of the Shimodaira-Hasegawa test as implemented in RAxML. Pairwise comparison of single-ML trees inferred by atpB–rbcL, trnL–trnF, matK, ycf1 pos. 1114-2102 and 4550-5532, agt1, ETS, phyC, and AFLP data to test for topological incongruences.
606_2018_1514_MOESM5_ESM.pdf (1.1 mb)
Online Resource 5. Maximum credibility trees of post-burnin Bayesian analyses, each ran for 30 million generations, based on a. AFLP, b. nuclear (agt1, ETS, phyC) or c. plastid (atpB–rbcL, trnL–trnF, matK, ycf1 pos. 1114-2102 and 4550-5532) data.
606_2018_1514_MOESM6_ESM.xlsx (14 kb)
Online Resource 6. Transition model selection for stochastic character mapping and state frequencies per node for Fig. 2. a. The corrected Akaike information criterion (AICc) was used for model selection. b. Table showing the inferred state frequencies calculated across 1000 stochastically mapped character histories (using ER model) for each node in Fig. 2 for two morphological traits: Apical coma (conspicuous, inconspicuous, missing) and Scape bracts (foliaceous, not foliaceous/often imbricate, lacking).
606_2018_1514_MOESM7_ESM.pdf (290 kb)
Online Resource 7. Overview of the published chromosome numbers in the genus Ananas and Pseudananas.


  1. Aguirre-Santoro J (2017) Taxonomy of the Ronnbergia Alliance (Bromeliaceae: Bromelioideae): new combinations, synopsis, and new circumscriptions of Ronnbergia and the resurrected genus Wittmackia. Pl Syst Evol 303:615–640. CrossRefGoogle Scholar
  2. Aradhya MK, Zee F, Manshardt RM (1994) Isozyme variation in cultivated and wild pineapple. Euphytica 79:87–99. CrossRefGoogle Scholar
  3. Barfuss MHJ (2012) Molecular studies in Bromeliaceae: Implications of plastid and nuclear DNA markers for phylogeny, biogeography, and character evolution with emphasis on a new classification of Tillandsioideae. PhD Thesis, University of Vienna, ViennaGoogle Scholar
  4. Beadle DA (1998) The Bromeliad cultivar registry. The Bromeliad Society International, VeniceGoogle Scholar
  5. Bollback JP (2006) SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7:88. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Molec Ecol 13:3261–3273. CrossRefGoogle Scholar
  7. Brown GK, Gilmartin AJ (1989) Chromosome numbers in Bromeliaceae. Amer J Bot 76:657–665CrossRefGoogle Scholar
  8. Brown GK, Leme EMC (2000) Cladistic analysis in the Nidularioid complex. In: Leme EMC (ed) Nidularium—Bromeliads of the Atlantic Forest. Sexante Artes, Rio de Janeiro, pp 240–247Google Scholar
  9. Butcher D, Gouda EJ (2017) The new bromeliad taxon list. Available at: Accessed 27 Jul 2015
  10. Carlier JD, Coppens d’Eeckenbrugge G, Leitao JM (2007) Pineapple genome mapping and molecular breeding in plants. In: Kole C (ed) Fruits and Nuts. Springer, Berlin, pp 331–342CrossRefGoogle Scholar
  11. Castello LV, Barfuss MHJ, Till W, Galetto L, Chiapella JO (2016) Disentangling the Tillandsia capillaris complex: phylogenetic relationships and taxa boundaries of Andean populations. Bot J Linn Soc 181:391–414. CrossRefGoogle Scholar
  12. Collins JL (1936) A frequently mutating gene in the pineapple. Ananas comosus (L.) Merr. Amer Naturalist 70:467–476. Available at: CrossRefGoogle Scholar
  13. Collins JL (1960) The pineapple, botany, utilization, cultivation. Leonhard Hill, LondonGoogle Scholar
  14. Coppens d’Eeckenbrugge G, Duval MF, Van Miegroet F (1993) Fertility and self-incompatibility in the genus Ananas. Acta Hort 334:45–51. CrossRefGoogle Scholar
  15. Coppens d’Eeckenbrugge G, Leal F (2003) Morphology, anatomy and taxonomy. In: Bartholomew DP, Paull RE, Rohrbach KG (eds) The pineapple: botany, production and uses. CAB International, Wallingford, pp 13–32CrossRefGoogle Scholar
  16. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340. CrossRefPubMedGoogle Scholar
  17. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull Bot Soc Amer 19:11–15Google Scholar
  18. Drábková LZ, Vlček Č (2010) Molecular phylogeny of the genus Luzula DC. (Juncaceae, Monocotyledones) based on plastome and nuclear ribosomal regions: a case of incongruence, incomplete lineage sorting and hybridization. Molec Phylogen Evol 57:536–551. CrossRefGoogle Scholar
  19. Duval MF, Coppens d’Eeckenbrugge G (1993) Genetic variability in the genus Ananas. Acta Hortic 334:27–32. CrossRefGoogle Scholar
  20. Duval MF, Noyer JL, Perrier X, Coppens d’Eeckenbrugge G, Hamon P (2001) Molecular diversity in pineapple assessed by RFLP markers. Theor Appl Genet 102:83–90. CrossRefGoogle Scholar
  21. Duval MF, Buso GSC, Ferreira FR, Noyer JL, Coppens d’Eeckenbrugge G, Hamon P, Ferreira ME (2003) Relationships in Ananas and other related genera using chloroplast DNA restriction site variation. Genome 46:990–1004. CrossRefPubMedGoogle Scholar
  22. Felsenstein J (1985) Phylogenies and the comparative method. Amer Naturalist 125:1–15. CrossRefGoogle Scholar
  23. Fragoso JMV, Huffman JM (2000) Seed-dispersal and seedling recruitment patterns by the last neotropical megafaunal element in Amazonia, the tapir. J Trop Ecol 16:369–385. CrossRefGoogle Scholar
  24. French PA, Brown GK, Bayly MJ (2016) Incongruent patterns of nuclear and chloroplast variation in Correa (Rutaceae): introgression and biogeography in south-eastern Australia. Pl Syst Evol 302:447–468. CrossRefGoogle Scholar
  25. Garcia ML (1988) Etude taxinomique du genre Ananas. Utilisation de la variabilite enzymatique. PhD Thesis, University of Science and Technology, Languedoc, MontpellierGoogle Scholar
  26. Gelman A, Rubin D (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–472. CrossRefGoogle Scholar
  27. Gitaí J, Paule J, Zizka G, Schulte K, Benko-Iseppon AM (2014) Chromosome numbers and DNA content in Bromeliaceae: additional data and critical review. Bot J Linn Soc 176:349–368. CrossRefGoogle Scholar
  28. Givnish TJ, Barfuss MHJ, van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Systsma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. Amer J Bot 98:872–895. CrossRefGoogle Scholar
  29. Horres R, Zizka G, Kahl G, Weising K (2000) Molecular phylogenetics of Bromeliaceae: evidence from trnL (UAA) intron sequence of the chloroplast genome. Pl Biol (Stuttgart) 2:306–315. CrossRefGoogle Scholar
  30. Horres R, Schulte K, Weising K, Zizka G (2007) Systematics of Bromelioideae (Bromeliaceae)—evidence from molecular and anatomical studies. Aliso 23:27–43. CrossRefGoogle Scholar
  31. Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52:131–158. CrossRefPubMedGoogle Scholar
  32. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Leal F (1990) On the validity of Ananas monstruosus. J Bromeliad Soc 40:246–249Google Scholar
  34. Leal F, Coppens d’Eeckenbrugge G, Holst BK (1998) Taxonomy of the genera Ananas and Pseudananas—a historical review. Selbyana 19:227–235Google Scholar
  35. Li M, Wunder J, Bissoli G, Scarponi E, Gazzani S, Barbaro E, Saedler H, Varotto C (2008) Development of COS genes as universally amplifiable markers for phylogenetic reconstructions of closely related plant species. Cladistics 24:727–745. CrossRefGoogle Scholar
  36. Louzada RB, Schulte K, Wanderley ML, Silvestro D, Zizka G, Barfuss MHJ, Palma-Silva C (2014) Molecular phylogeny of the Brazilian endemic genus Orthophytum (Bromelioideae, Bromeliaceae) and its implications on morphological character evolution. Molec Phylogen Evol 77:54–64. CrossRefGoogle Scholar
  37. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), San Diego Supercomputer Center, New Orleans, pp 1–8.
  38. Ming R, VanBuren R, Wai CM, Tang H, Schatz MC, Bowers JE, Lyons E, Wang M-L, Biggers E, Zhang J, Huang L, Zhang L, Miao W, Zhang J, Ye Z, Miao C, Lin Z, Wang H, Zhou H, Yim WC, Priest HD, Zheng C, Woodhouse M, Edger PP, Guyot R, Guo H-B, Guo H, Zheng G, Singh R, Sharma A, Min X, Zheng Y, Lee H, Gurtowski J, Sedlazeck FJ, Harkess A, McKain MR, Liao Z, Fang J, Liu J, Zhang X, Zhang Q, Hu W, Qin Y, Wang K, Chen L-Y, Shirley N, Lin Y-R, Liu L-Y, Hernandez AG, Wright CL, Bulone V, Tuskan GA, Heath K, Zee F, Moore PH, Sunkar R, Leebens-Mack J, Mockler T, Bennetzen JL, Freeling M, Sankoff D, Paterson AH, Zhu X, Yang X, Smith JAC, Cushman JC, Paull RE, Yu Q (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47:1435–1442. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pelser PB, Kennedy AH, Tepe EJ, Shidler JB, Nordenstam B, Kadereit J, Watson LE (2010) Patterns and causes of incongruence between plastid and nuclear Senecioneae (Asteraceae) phylogenies. Amer J Bot 97:856–873. CrossRefGoogle Scholar
  40. Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393. CrossRefPubMedGoogle Scholar
  41. Posada D (2008) jModelTest: phylogenetic model averaging. Molec Biol Evol 25:1253–1256. CrossRefPubMedGoogle Scholar
  42. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. CrossRefPubMedGoogle Scholar
  43. R Core Team (2013) R: a language and environment for statistical computing. R Foundation and Statistical Computing, Vienna. Available at:
  44. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. CrossRefGoogle Scholar
  45. Richter W (1978) Zimmerpflanzen von heute und morgen: Bromeliaceen, 4th edn. Neumann Verlag Leipzig, RadebeulGoogle Scholar
  46. Rogstad SH (1992) Saturated NaCl-CTAB solution as a means of field preservation of leaves for DNA analyses. Taxon 41:701–708. CrossRefGoogle Scholar
  47. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. CrossRefPubMedGoogle Scholar
  48. Sass C, Specht CD (2010) Phylogenetic estimation of the core Bromelioids with an emphasis on the genus Aechmea (Bromeliaceae). Molec Phylogen Evol 55:559–571. CrossRefGoogle Scholar
  49. Schulte K, Horres R, Zizka G (2005) Molecular phylogeny of Bromelioideae and its implications on biogeography and the evolution of CAM in the family (Poales, Bromeliaceae). Senckenberg Biol 85:1–13Google Scholar
  50. Schulte K, Barfuss MH, Zizka G (2009) Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily. Molec Phylogen Evol 51:327–339. CrossRefGoogle Scholar
  51. Schulte K, Silvestro D, Kiehlmann E, Vesely S, Novoa P, Zizka G (2010) Detection of recent hybridization between sympatric Chilean Puya species (Bromeliaceae) using AFLP markers and reconstruction of complex relationships. Molec Phylogen Evol 57:1105–1119. CrossRefGoogle Scholar
  52. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molec Biol Evol 16:1114–1116. CrossRefGoogle Scholar
  53. Silva BR (2003) Contributions to the understanding of Andean and Amazonian Aechmea subg. Chevaliera (Bromeliaceae). Selbyana 24:46–63Google Scholar
  54. Silvestro D (2013) Diversification in time and space. Methodological advancement and case studies from the Neotropical plant family Bromeliaceae. PhD Thesis, Goethe University Frankfurt, Frankfurt am MainGoogle Scholar
  55. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity Evol 12:335–337. CrossRefGoogle Scholar
  56. Silvestro D, Zizka G, Schulte K (2014) Disentangling the effects of key innovations on the diversification of Bromelioideae (Bromeliaceae). Evolution 68:163–175. CrossRefPubMedGoogle Scholar
  57. Siqueira-Filho JA, Leme EMC (2006) Fragments of the Atlantic Forest of Northeast Brazil. Andrea Jakobsson Estúdio, Rio de JaneiroGoogle Scholar
  58. Smith LB, Downs RJ (1974) Monograph 14, pitcairnioideae (Bromeliaceae). In: Smith LB, Downs RJ (eds) Flora neotropica. Hafner Press, New YorkGoogle Scholar
  59. Smith L, Downs RJ (1979) Bromelioideae, Bromeliaceae. New York Botanical Garden, New York, pp 2048–2064Google Scholar
  60. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. CrossRefPubMedGoogle Scholar
  61. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680. CrossRefPubMedGoogle Scholar
  63. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414. CrossRefPubMedGoogle Scholar
  64. Wendt T, Canela MBF, de Faria APG, Rios RI (2001) Reproductive biology and natural hybridization between two endemic species of Pitcairnia (Bromeliaceae). Amer J Bot 88:1760–1767CrossRefGoogle Scholar
  65. Xu B, Wu N, Gao X-F, Zhang L-B (2012) Analysis of DNA sequences of six chloroplast and nuclear genes suggests incongruence, introgression, and incomplete lineage sorting in the evolution of Lespedeza (Fabaceae). Molec Phylogen Evol 62:346–358. CrossRefGoogle Scholar
  66. Zhang J, Liu J, Ming R (2014) Genomic analyses of the CAM plant pineapple. J Exp Bot 65:3395–3404. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany and Molecular EvolutionSenckenberg Research Institute and Natural History Museum FrankfurtFrankfurt/MainGermany
  2. 2.Institute for Ecology, Evolution and DiversityGoethe UniversityFrankfurt/MainGermany
  3. 3.Herbarium BradeanumRio de JaneiroBrazil
  4. 4.Department of Botany and Biodiversity Research, Faculty of Life SciencesUniversity of ViennaViennaAustria

Personalised recommendations