Historical biogeography of the herbaceous bamboo tribe Olyreae (Bambusoideae: Poaceae)

Abstract

The tribe Olyreae comprises 124 understorey herbaceous bamboos species and almost all of its species are distributed in the Neotropics. Only Buergersiochloa bambusoides is found in New Guinea, and Olyra latifolia has a disjunct distribution in tropical America, Africa and Madagascar. Applying phylogenetic and biogeographical analyses, our aim was to identify the ancestral area and time of divergence of Olyreae, and to elucidate whether the bi-continental distribution of O. latifolia was the result of natural long-distance dispersal or human introduction. Our results confirmed the monophyly of tribe Olyreae, the paraphyly/polyphyly of the genus Olyra, and the sistership of Buergersiochloa bambusoides to the rest of Olyreae. Estimates of divergence time and ancestral range indicate that the Olyreae probably originated in the late Eocene to Oligocene, followed by Miocene diversification. South America+Oceania were recovered as the ancestral area of the tribe, therefore the distribution of B. bambusoides lies within the ancestral area. Our phylogenetic results showed that all O. latifolia samples, both American and African, formed a strongly supported clade. The lack of genetic differentiation indicates that probably the species was introduced to Africa very recently, potentially by humans during colonial times. Based on the widespread distribution of O. latifolia in Africa despite its lack of use by humans, we suggest that this species might possess effective capabilities for dispersal and establishment, both of which would require further study.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Amarilla LD, Chiapella JO, Sosa V, Moreno NC, Anton AM (2015) A tale of North and South America: time and mode of dispersal of the amphitropical genus Munroa (Poaceae, Chloridoideae). Bot J Linn Soc 179:110–125

    Google Scholar 

  2. Bell KL, Rangan H, Fernandes MM, Kull CA, Murphy DJ (2017) Chance long-distance or human-mediated dispersal? How Acacia s.l. farnesiana attained its pan-tropical distribution. Roy Soc Open Sci 4:170105

    Google Scholar 

  3. Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, van der Bank M, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress toward complete tribal and generic level sampling. Molec Phylogenet Evol 47:488–505

    CAS  PubMed  Google Scholar 

  4. Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkinson T (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot J Linn Soc 162:543–557

    Google Scholar 

  5. Burke SV, Clark LG, Triplett JK, Grennan CP, Duvall MR (2014) Biogeography and phylogenomics of new world Bambusoideae (Poaceae), revisited. Amer J Bot 101:886–891

    Google Scholar 

  6. Burke SV, Lin CS, Wysocki WP, Clark LG, Duvall MR (2016) Phylogenomics and plastome evolution of tropical forest grasses (Leptaspis, Streptochaeta: Poaceae). Frontiers Pl Sci 7

  7. Carlson SE, Linder HP, Donoghue MJ (2012) The historical biogeography of Scabiosa (Dipsacaceae): implications for Old World plant disjunctions. J Biogeogr 39:1086–1100

    Google Scholar 

  8. Christenhusz MJ, Chase MW (2012) Biogeographical patterns of plants in the Neotropics–dispersal rather than plate tectonics is most explanatory. Bot J Linn Soc 171:277–286

    Google Scholar 

  9. Clark LG, Londoño X, Ruiz-Sanchez E (2015) Bamboo taxonomy and habitat. In Liese W, Köhl M (eds ) Bamboo: the plant and its uses, Vol. 10. Springer International Publishing, Switzerland, pp 1–30

    Google Scholar 

  10. Clement M, Posada D, Crandall KA (2000) TCS: A computer program to estimate gene genealogies. Molec Ecol 9:1657–1659

    CAS  Google Scholar 

  11. Crisp MD, Trewick SA, Cook LG (2011) Hypothesis testing in biogeography. Trends Ecol Evol 26, 66–72

    PubMed  Google Scholar 

  12. Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nature, Meth 9:772

    CAS  Google Scholar 

  13. Davidse G (1987) Fruit dispersal in Poaceae. In: Sodestrom TR, Hilu KW, Campbell CS, Barkworth ME (eds) Grass systematics and evolution. Washington, DC: Smithsonian Institution Press, pp 143–155

    Google Scholar 

  14. Davidse G, Pohl RW (1974) Chromosome numbers, meiotic behavior, and notes on tropical American grasses (Gramineae). Canad J Bot 52:317–328

    Google Scholar 

  15. Davis CC, Bell CD, Mathews S, Donoghue MJ (2002) Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proc Natl Acad Sci USA:99:6833–6837

    CAS  PubMed  Google Scholar 

  16. Deng T, Chen Y, Wang H, Zhang X, Volis S, Yusupov Z, Qiang H, Sun H (2018) Molecular phylogeny and biogeography of Adenocaulon highlight the biogeographic links between New World and Old World. Frontiers Ecol Evol 5:162

    Google Scholar 

  17. Dick CW, Bermingham E, Lemes MR, Gribel R. 2007. Extreme long-distance dispersal of the lowland tropical rainforest tree Ceiba pentandra L. (Malvaceae) in Africa and the Neotropics. Molec Ecol 16:3039–3049

    Google Scholar 

  18. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem Bull 19:11–15

    Google Scholar 

  19. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed  PubMed Central  Google Scholar 

  20. Fisher AE, Triplett JK, Ho C, Schiller AD, Oltrogge KA, Schroder ES, Kelchner SA, Clark LG (2009) Paraphyly in the bamboo subtribe Chusqueinae (Poaceae: Bambusoideae), and a revised infrageneric classification for Chusquea. Syst Bot 34:673–683

    Google Scholar 

  21. Givnish TJ, Millam KC, Evans TM, Hall J, Pires C, Berry PE, Sytsma KJ (2004) Ancient vicariance or recent long-distance dispersal? inferences about phylogeny and South American–African disjunctions in Rapateaceae and Bromeliaceae based on ndh F sequence data. Int J Pl Sci 165:S35–S54

    CAS  Google Scholar 

  22. Grass Phylogeny Working Group [GPWG] (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Missouri Bot Gard 88:373–457

    Google Scholar 

  23. Guo YY, Luo YB, Liu ZJ, Wang XQ (2012) Evolution and biogeography of the slipper orchids: Eocene vicariance of the conduplicate genera in the Old and New World tropics. PLOS One 7:e38788

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Ho SYW, Phillips MJ (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58:367–380

    PubMed  Google Scholar 

  25. Johnson LA, Porter JM (2017) Fates of angiosperm species following long-distance dispersal: examples from American amphitropical Polemoniaceae. Amer J Bot 104:1729–1744

    Google Scholar 

  26. Judziewicz EJ, Clark LG (2007) Classification and biogeography of New World grasses: Anomochlooideae, Pharoideae, Ehrhartoideae and Bambusoideae. Aliso 23:303–314

    Google Scholar 

  27. Judziewicz EJ, Clark LG, Londoño X, Stern MJ (1999) American bamboos. Washington, DC: Smithsonian Institution

    Google Scholar 

  28. Kelchner SA, Bamboo Phylogeny Group [BPG] (2013) Higher level phylogenetic relationships within the bamboos (Poaceae: Bambusoideae) based on five plastid markers. Molec Phylogenet Evol 67:404–413

    Google Scholar 

  29. Li WJ, Sui XL, Kuss P, Liu YY, Li AR, Guan KY (2016) Long-distance dispersal after the Last Glacial Maximum (LGM) led to the disjunctive distribution of Pedicularis kansuensis (Orobanchaceae) between the Qinghai-Tibetan Plateau and Tianshan region. PLOS One 11:e0165700

    PubMed  PubMed Central  Google Scholar 

  30. Liu XQ, Ickert-Bond SM, Nie ZL, Zhou Z, Chen LQ, Wen J (2016) Phylogeny of the Ampelocissus–Vitis clade in Vitaceae supports the New World origin of the grape genus. Molec Phylogenet Evol 95:217–228

    PubMed  Google Scholar 

  31. 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), 14 November 2010, New Orleans, LA, pp 1–8

  32. Müller J, Müller K, Neinhuis C, Quandt D (2010) PhyDe Phylogenetic Data Editor. Available at www.phyde.de

  33. Niu YT, Ye JF, Zhang JL, Wan JZ, Yang T, Wei XX., Lu LM, Li JH,Chen, ZD (2018) Long-distance dispersal or postglacial contraction? Insights into disjunction between Himalaya–Hengduan Mountains and Taiwan in a cold-adapted herbaceous genus, Triplostegia. Ecol Evol 8:1131–1146

    PubMed  Google Scholar 

  34. Oliveira RP, Clark LG, Schnadelbach AS, Monteiro SHN, Longhi-Wagner HM, van den Berg C (2014) A molecular phylogeny of Raddia (Poaceae, Olyreae) and its allies based on noncoding plastid and nuclear spacers. Molec Phylogenet Evol 78:105–117

    PubMed  Google Scholar 

  35. Porter DM (1974) Disjunct distributions in the New World Zygophyllaceae. Taxon 339–346

  36. Raven PH, Axelrod DI (1974) Angiosperm biogeography and past continental movements. Ann Missouri Bot Gard 61:539–673

    Google Scholar 

  37. Renner S (2004) Plant dispersal across the tropical Atlantic by wind and sea currents. Int J Pl Sci 165:23–33

    Google Scholar 

  38. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804

    CAS  PubMed  Google Scholar 

  39. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  PubMed  Google Scholar 

  40. Ruiz-Sanchez E (2011) Biogeography and divergence time estimates of woody bamboos: insights in the evolution of Neotropical bamboos. Bol Soc Bot México 88:67–75

    Google Scholar 

  41. Ruiz-Sanchez E, Sosa V (2015) Origin and evolution of fleshy fruit in woody bamboos. Molec Phylogenet Evol 91:123–134

    PubMed  Google Scholar 

  42. Simpson MG, Johnson LA, Villaverde T, Guilliams CM (2017) American amphitropical disjuncts: Perspectives from vascular plant analyses and prospects for future research. Amer J Bot 104:1600–1650

    Google Scholar 

  43. Soderstrom TR, Zuloaga FO (1989) A revision of the genus Olyra and the new segregate genus Parodiolyra (Poaceae: Bambusoideae: Olyreae). Smithsonian Contr Bot 69:1–79

    Google Scholar 

  44. Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacer ribosomal DNA. Theor Appl Genet 89:26–32

    CAS  PubMed  Google Scholar 

  45. Sungkaew S, Stapleton CMA, Salamin N, Hodkinson TR (2009) Non-monophyly 856 of the woody bamboos (Bambuseae: Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae s.s. J Pl Res 122:95–108

    CAS  Google Scholar 

  46. Thorne RF (1972) Major disjunctions in the geographic ranges of seed plants. Quart Rev Biol 47:365–411

    Google Scholar 

  47. Tiffney BH (1985) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J Arnold Arbor 66:73–94.

    Google Scholar 

  48. Triplett JK, Clark LG, Fisher AE, Wen J (2014) Independent allopolyploidization events preceded speciation in the temperate and tropical woody bamboos. New Phytol 204:66–73

    PubMed  Google Scholar 

  49. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biol 14:2963–2977

    Google Scholar 

  50. Wang W., Chen S., Zhang X (2018) Whole-genome comparison reveals divergent IR borders and mutation hotspots in chloroplast genomes of herbaceous bamboos (Bambusoideae: Olyreae). Molecules 23:1537

    PubMed Central  Google Scholar 

  51. Wen J, Ickert-Bond SM (2009) Evolution of the Madrean–Tethyan disjunctions and the North and South American amphitropical disjunctions in plants. J Syst Evol 47:331–348

    Google Scholar 

  52. Wen J, Nie ZL, Ickert-Bond SM (2016) Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. J Syst Evol 54:469–490

    Google Scholar 

  53. Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644

    PubMed  Google Scholar 

  54. Wolfe JA (1975) Some aspects of plant geography of the Northern Hemisphere during the late Cretaceous and Tertiary. Ann Missouri Bot Gard 62:264–279

    Google Scholar 

  55. Wysocki WP, Clark LG, Attigala L, Ruiz-Sanchez E, Duvall MR (2015) Evolution of the bamboos (Bambusoideae; Poaceae): a full plastome phylogenomic analysis. BMC Evol Biol 15:50

    PubMed  PubMed Central  Google Scholar 

  56. Wysocki WP, Ruiz-Sanchez E, Yin Y, Duvall MR (2016) The floral transcriptomes of four bamboo species (Bambusoideae; Poaceae): support for common ancestry among woody bamboos. BMC Genomics 17:384

    PubMed  PubMed Central  Google Scholar 

  57. Yang T, Lu LM, Wang W, Li JH, Manchester SR, Wen J, Chen ZD (2018) Boreotropical range expansion and long-distance dispersal explain two amphi-Pacific tropical disjunctions in Sabiaceae. Molec Phylogenet Evol 124:181–191

    PubMed  Google Scholar 

  58. Yu Y, Harris AJ, He XJ (2010) S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molec Phylogenet Evol 56:848–850

    PubMed  Google Scholar 

  59. Yu Y, Harris AJ, Blair C, He XJ (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Molec Phylogenet Evol 87:46–49

    PubMed  Google Scholar 

  60. Yule GU (1925) II.—A mathematical theory of evolution, based on the conclusions of Dr. JC Willis, FR S. Philos Trans, Ser B 213:21–87

    Google Scholar 

  61. Zhang W, Clark LG (2000) Phylogeny and classification of the Bambusoideae (Poaceae). In Jacobs SWL, Everert J (eds) Grass systematics and evolution. Melbourne: CSIRO, pp 35–39

    Google Scholar 

  62. Zhang XZ, Zeng CX, Ma PF, Haevermans T, Zhang YX, Zhang LN, Guo ZH, Li DZ (2016) Multi-locus plastid phylogenetic biogeography supports the Asian hypothesis of the temperate woody bamboos (Poaceae: Bambusoideae). Molec Phylogenet Evol 96:118–129

    PubMed  Google Scholar 

Download references

Acknowledgements

We extend our sincere gratitude to Arith Pérez Orozco, Cristina Bárcenas, Maura L. Quezada Aguilar, Wendy Cerrato, Kelvin Bodden, Eydi Yanina Guerrero, Lilian Ferrufino, Claudia Morales, Rodrigo Blanco, Ismael Valdivieso and Regina Cuevas for assistance in the field and laboratory and, Bianca Delfosse for editing the English version of this manuscript. Field work was funded by a grant (215514) from CONACyT (Consejo Nacional de Ciencia y Tecnología), and the Laboratorio Nacional de Identificación y Caracterización Vegetal (CONACyT-UdeG) are also acknowledged.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Eduardo Ruiz-Sanchez.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ruiz-Sanchez, E., Sosa, V., Ortiz-Rodriguez, A.E. et al. Historical biogeography of the herbaceous bamboo tribe Olyreae (Bambusoideae: Poaceae). Folia Geobot 54, 177–189 (2019). https://doi.org/10.1007/s12224-019-09342-7

Download citation

Keywords

  • Africa
  • America
  • herbaceaous bamboos
  • human-mediated dispersal
  • Neotropics
  • Olyra latifolia