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Systematics and Evolution of Australian Seagrasses in a Global Context

  • Michelle Waycott
  • Edward Biffin
  • Donald H. Les
Chapter

Abstract

Seagrasses have evolved independently at least four times throughout their evolutionary history. All seagrasses are members of the monocot order Alismatales. A new molecular phylogenetic analysis, applying a molecular clock based on recently redefined fossil evidence, provides a framework for describing the timing and relationships of seagrass lineage evolution. The deeper time phylogenetic history of the marine monocotyledons dates back approximately 105 million years ago (Ma) to an ancestor from which two significant lineages evolved more recently. The marine Hydrocharitaceae (Enhalus, Thalassia and Halophila) are a tropical globally distributed lineage which include Australian endemic species of Halophila. The Cymodoceaceae lineage and the Zosteraceae/Potamogetonaceae diverged some ~67 Ma but in each lineage the genera arose more recently. Most seagrass species appear to have evolved in the last ~5 Ma, some more recently. The extant distribution of species will not be the result of vicariance but of long distance connectivity at a global scale. The most significant implication of these results to global biogeography is that there must have been, and likely continues to be, ongoing long distance dispersal leading to the current widespread distributions of species and congeners. The Australian seagrass flora represents all the major evolutionary lineages of seagrasses except the northern hemisphere Phyllospadix, a major clade of Zostera and some of the forms of Halophila. Pollination efficiency is a significant potential driver in the evolution of filiform pollen, and is likely associated with the single seeded fruit in water pollinated species of seagrass in the lineages of seagrass that exhibit this character.

References

  1. Ackerman JD (1995) Convergence of filiform pollen morphologies in seagrasses: functional mechanisms. Evol Ecol 9(2):139–153CrossRefGoogle Scholar
  2. Ackerman JD (2006) Sexual reproduction of seagrasses: pollination in the marine context. In: Larkum WD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, DordrechtGoogle Scholar
  3. Arber A (1920) Water plants: A study of aquatic angiosperms. Cambridge University Press, LondonGoogle Scholar
  4. Ascherson P, Graebner P (1907) IV. II. Potamogetonaceae Heft 31 Verlag von H R Engelmann. In: Cramer J (ed) Das Pflanzenreich. A. Engler, Weinheim/Bergstrasse, p 184Google Scholar
  5. Beaulieu JM, O’Meara BC, Crane P, Donoghue MJ (2015) Heterogeneous rates of molecular evolution and diversification could explain the triassic age estimate for angiosperms. Syst Biol 64(5):869–878.  https://doi.org/10.1093/sysbio/syv027CrossRefPubMedGoogle Scholar
  6. Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97(8):1296–1303Google Scholar
  7. Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for bayesian evolutionary analysis. Plos Comput Biol 10(4):e1003537.  https://doi.org/10.1371/journal.pcbi.1003537CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bromham L, Penny D (2003) The modern molecular clock. Nat Rev Genet 4(3):216–224CrossRefPubMedGoogle Scholar
  9. Byng JW, Chase MW, Christenhusz MJM, Fay MF, Judd WS, Mabberley DJ, Sennikov AN, Soltis DE, Soltis PS, Stevens PF, Briggs B, Brockington S, Chautems A, Clark JC, Conran J, Haston E, Moller M, Moore M, Olmstead R, Perret M, Skog L, Smith J, Tank D, Vorontsova M, Weber A, (Angiosperm Phylogeny Group) (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181(1):1–20.  https://doi.org/10.1111/boj.12385CrossRefGoogle Scholar
  10. Chen LY, Chen JM, Gituru RW, Wang QF (2012) Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol Biol 12:30.  https://doi.org/10.1186/1471-2148-12-30CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen LY, Chen JM, Gituru RW, Wang QF (2013) Eurasian origin of Alismatidae inferred from statistical dispersal-vicariance analysis. Mol Phylogenet Evol 67(1):38–42.  https://doi.org/10.1016/j.ympev.2013.01.001CrossRefPubMedGoogle Scholar
  12. Chen LY, Grimm GW, Wang QF, Renner SS (2015) A phylogeny and biogeographic analysis for the Cape-Pondweed family Aponogetonaceae (Alismatales). Mol Phylogenet Evol 82:111–117.  https://doi.org/10.1016/j.ympev.2014.10.007CrossRefPubMedGoogle Scholar
  13. Cox PA, Knox BR (1989) Two-dimensional pollination in hydrophilous plants: Convergent evolution in the genera Halodule (Cymodoceaceae), Halophila (Hydrocharitaceae) Ruppia (Ruppiaceae) and Lepilaena (Zannichelliaceae). Am J Bot 76(2):164–175CrossRefGoogle Scholar
  14. Coyer JA, Hoarau G, Kuo J, Tronholm A, Veldsink J, Olsen JL (2013) Phylogeny and temporal divergence of the seagrass family Zosteraceae using one nuclear and three chloroplast loci. Syst Biodivers 11(3):271–284.  https://doi.org/10.1080/14772000.2013.821187CrossRefGoogle Scholar
  15. Cronquist AC (1981) An integrated system of classification of flowering plants. Columbia University Press, New YorkGoogle Scholar
  16. Dahlgren RMT (1985) The families of the monocotyledons. Springer, BerlinCrossRefGoogle Scholar
  17. den Hartog C (1970) The sea-grasses of the world. North-Holland Publishing Company, AmsterdamGoogle Scholar
  18. den Hartog C (1971) The dynamic aspect in the ecology of seagrass communities. Thalass Jugosl 7(1):101–112Google Scholar
  19. den Hartog C, Kuo J (2006) Taxonomy and biogeography of seagrasses. In: Larkum WD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation, 1st edn. Springer, Dordrecht, p 691Google Scholar
  20. dos Reis M, Donoghue PCJ, Yang Z (2016) Bayesian molecular clock dating of species divergences in the genomics era. Nat Rev Genet 17:71–80.  https://doi.org/10.1038/nrg.2015.8CrossRefPubMedGoogle Scholar
  21. Fawcett JA, Maere S, Van de Peer Y (2009) Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci USA 106(14):5737–5742Google Scholar
  22. Gavryushkina A, Welch D, Stadler T, Drummond AJ (2014) Bayesian inference of sampled ancestor trees for epidemiology and fossil calibration. PLoS Comput Biol 10:e1003919CrossRefPubMedPubMedCentralGoogle Scholar
  23. Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, BerkleyGoogle Scholar
  24. 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(3):307–321.  https://doi.org/10.1093/sysbio/syq010CrossRefPubMedGoogle Scholar
  25. Heath TA, Huelsenbeck JP, Stadler T (2014) The fossilized birth-death process for coherent calibration of divergence-time estimates. PNAS 111(29):E2957–E2966.  https://doi.org/10.1073/pnas.1319091111CrossRefPubMedGoogle Scholar
  26. Hertweck KL, Kinney MS, Stuart SA, Maurin O, Mathews S, Chase MW, Gandolfo MA, Pires JC (2015) Phylogenetics, divergence times and diversification from three genomic partitions in monocots. Bot J Linn Soc 178(3):375–393.  https://doi.org/10.1111/boj.12260CrossRefGoogle Scholar
  27. Iles WJD, Smith SY, Graham SW (2013) Refining our understanding of the phylogenetic backbone of Alismatales. In: Wilkin P, Mayo SJ (eds) Early events in monocot evolution. Systematics Association Special Volume edn. Cambridge University Press, Cambridge, pp 1–28Google Scholar
  28. Iles WJD, Lee C, Sokoloff DD, Remizowa MV, Yadav SR, Barrett MD, Barrett RL, Macfarlane TD, Rudall PJ, Graham SW (2014) Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales). BMC Evol Biol 14:102.  https://doi.org/10.1186/1471-2148-14-102CrossRefPubMedPubMedCentralGoogle Scholar
  29. Iles WJD, Smith SY, Gandolfo MA, Graham SW (2015) Monocot fossils suitable for molecular dating analyses. Bot J Linn Soc 178(3):346–374.  https://doi.org/10.1111/boj.12233CrossRefGoogle Scholar
  30. Ivany LC, Protell RW, Jones DS (1990) Animal-plant relationships and paleobiogeography of an Eocene seagrass community from Florida. Palaios 5:244–258.  https://doi.org/10.2307/3514943CrossRefGoogle Scholar
  31. Jacobs SWL, Les DH, Moody ML (2006) New combinations in Australasian Zostera (Zosteraceae). Telopea 11(2):127–128CrossRefGoogle Scholar
  32. Janssen T, Bremer K (2004) The age of major monocot groups inferred from 800+ rbcL sequences. Bot J Linn Soc 146(4):385–398CrossRefGoogle Scholar
  33. 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, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649.  https://doi.org/10.1093/bioinformatics/bts199CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kendrick GA, Waycott M, Carruthers TJB, Cambridge ML, Hovey R, Krauss SL, Lavery PS, Les DH, Lowe RJ, Vidal OMI, Ooi JLS, Orth RJ, Rivers DO, Ruiz-Montoya L, Sinclair EA, Statton J, van Dijk JK, Verduin JJ (2012) The central role of dispersal in the maintenance and persistence of seagrass populations. Bioscience 62(1):56–65.  https://doi.org/10.1525/Bio.2012.62.1.10CrossRefGoogle Scholar
  35. Kumar S, Hedges SB (2016) Advances in time estimation methods for molecular data. Mol Biol Evol 33:863–869.  https://doi.org/10.1093/molbev/msw026CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kuo J, den Hartog C (2006) Taxonomy and biogeography of seagrasses. In: Larkum WD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 1–23Google Scholar
  37. Kuo J, Lee Long W, Coles RG (1993) Occurrence and fruit and seed biology of Halophila tricostata Greenway (Hydrocharitaceae). Aust J Mar Freshw Res 44:43–57Google Scholar
  38. Larkum AWD, den Hartog C (1989) Evolution and biogeography of seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of the seagrasses: a treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp 112–156Google Scholar
  39. Larkum AWD, Waycott M, Conran JG (2016) Chapter 1: evolution and biogeography of seagrasses. In: Larkum AWD, Kendrick GA, Ralph PJ (eds) Seagrasses of Australia. Springer, HeidelbergGoogle Scholar
  40. Les DH (1988) Breeding systems, population structure and evolution in hydrophylous angiosperms. Ann Mo Bot Gard 75:819–835CrossRefGoogle Scholar
  41. Les DH, Haynes RR (1995) Systematics of subclass Alismatidae: a synthesis of approaches. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens, Kew, pp 1–26Google Scholar
  42. Les DH, Tippery NP (2013) In time and with water … the systematics of alismatid monocotyledons. In: Wilkin P, Mayo SJ (eds) Early events in monocot evolution. The Systematics Association Special Volume, vol 83. Cambridge University Press, Cambridge, p 118Google Scholar
  43. Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22(3):443–463CrossRefGoogle Scholar
  44. Les DH, Moody ML, Jacobs SWL, Bayer RJ (2002) Systematics of seagrasses (Zosteraceae) in Australia and New Zealand. Syst Bot 27(3):468–484Google Scholar
  45. Les DH, Crawford DJ, Kimball RT, Moody ML, Landolt E (2003) Biogeography of discontinuously distributed hydrophytes: a molecular appraisal of intercontinental disjunctions. Int J Plant Sci 164(6):917–932CrossRefGoogle Scholar
  46. Li XX, Zhou ZK (2009) Phylogenetic studies of the core Alismatales inferred from morphology and rbcL sequences. Prog Nat Sci 19(8):931–945.  https://doi.org/10.1016/j.pnsc.2008.09.008CrossRefGoogle Scholar
  47. Lohaus R, Van de Peer Y (2016) Of dups and dinos: evolution at the K/Pg boundary. Curr Opin Plant Biol 30:62–69.  https://doi.org/10.1016/j.pbi.2016.01.006CrossRefPubMedGoogle Scholar
  48. McConchie CA, Knox RB, Ducker SC (1982) Ultrastructure and cytochemistry of the hydrophilous pollen of Lepilaena (Zannichelliaceae). Micron (1969) 13(3):339–340.  https://doi.org/10.1016/0047-7206(82)90048-6CrossRefGoogle Scholar
  49. McMahon K, van Dijk K-J, Ruiz-Montoya L, Kendrick GA, Krauss SL, Waycott M, Verduin J, Lowe R, Statton J, Brown E, Duarte CM (2014) The movement ecology of seagrasses. Proc R Soc B-Biol Sci 281(8 October 2014):20140878.  https://doi.org/10.1098/rspb.2014.0878CrossRefGoogle Scholar
  50. Morrone JJ, Crisci JV (1995) Historical biogeography: introduction to methods. Annu Rev Ecol Syst 26:373–401.  https://doi.org/10.1146/annurev.es.26.110195.002105CrossRefGoogle Scholar
  51. Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Bostrom C, Calvert E, Christie H, Granger S, La Lumiere R, Milchakova N, Oudot-Le Secq MP, Procaccini G, Sanjabi B, Serrao E, Veldsink J, Widdicombe S, Wyllie-Echeverria S (2004) North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L. Mol Ecol 13(7):1923–1941.  https://doi.org/10.1111/j.1365-294X.2004.02205.xCrossRefPubMedGoogle Scholar
  52. Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins JW, Jueterbock A, Mraz A, Stam WT, Tice H, Bornberg-Bauer E, Green PJ, Pearson GA, Procaccini G, Duarte CM, Schmutz J, Reusch TBH, Van de Peer Y (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331–335.  https://doi.org/10.1038/nature16548CrossRefPubMedGoogle Scholar
  53. Petersen G, Seberg O, Cuenca A, Stevenson DW, Thadeo M, Davis JI, Graham S, Ross TG (2016) Phylogeny of the Alismatales (Monocotyledons) and the relationship of Acorus (Acorales?). Cladistics 32(2):141–159.  https://doi.org/10.1111/cla.12120CrossRefGoogle Scholar
  54. Posluszny U, Charlton WA, Les DH (2000) Modularity in helobial flowers. In: Wilson KD, Morrison D (eds) Systematics and evolution of monocots. CSIRO Publishing, Victoria, pp 63–74Google Scholar
  55. Robertson EL (1984) Seagrasses. In: Womersley HBS (ed) Volume 1: the marine benthic flora of southern Australia. Government Printer, Adelaide, pp 57–122Google Scholar
  56. Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst Biol 46:195–203.  https://doi.org/10.1093/sysbio/46.1.195CrossRefGoogle Scholar
  57. Ross TG, Barrett CF, Soto Gomez M, Lam VKY, Henriquez CL, Les DH, Davis JI, Cuenca A, Petersen G, Seberg O, Thadeo M, Givnish TJ, Conran J, Stevenson DW, Graham SW (2016) Plastid phylogenomics and molecular evolution of Alismatales. Cladistics 32(2):160–178.  https://doi.org/10.1111/cla.12133CrossRefGoogle Scholar
  58. Schulte P, Alegret L, Arenillas I, Arz JA, Barton PJ, Bown PR et al (2010) The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327(5970):1214–1218.  https://doi.org/10.1126/science.1177265CrossRefPubMedGoogle Scholar
  59. Sculthorpe CD (1967) The biology of aquatic vascular plants. Edward Arnold Publishers, LondonGoogle Scholar
  60. Soltis DE, Soltis PS, Endress PK, Chase MW (2005) Phylogeny and evolution of angiosperms. Sinauer Associates, Sunderland, MassGoogle Scholar
  61. Thorne RF (1992) An updated phylogenetic classification of the flowering plants. Aliso 13(2):365–390CrossRefGoogle Scholar
  62. Tomlinson PB (1982) Helobiae (Alismatidae). In: Metcalfe CR (ed) Anatomy of the monocotyledons, vol VII. Clarendon Press, OxfordGoogle Scholar
  63. Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K (2009) The flowering world: a tale of duplications. Trends Plant Sci 14(12):680–688Google Scholar
  64. van Dijk KJ, van Tussenbroek BI, Jimenez-Duran K, Marquez-Guzman JG, Ouborg J (2009) High levels of gene flow and low population genetic structure related to high dispersal potential of a tropical marine angiosperm. Mar Ecol Prog Ser 390:67–77.  https://doi.org/10.3354/meps08190CrossRefGoogle Scholar
  65. van Tussenbroek BI, Santos MGB, Wong JGR, van Dijk JK, Waycott M (2010) A guide to the tropical seagrasses of the Western Atlantic. Universidad Nacional Autónoma de MéxicoGoogle Scholar
  66. Vanneste K, Baele G, Maere S, Van de Peer Y (2014) Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res 24(8):1334–1347.  https://doi.org/10.1101/gr.168997.113CrossRefPubMedPubMedCentralGoogle Scholar
  67. Waisel Y (1972) Biology of halophytes. Academic Press, LondonGoogle Scholar
  68. Waycott M, Les DH (2000) Current perspectives on marine angiosperm evolution. Biol Mar Mediterr 7(2):160–163Google Scholar
  69. Waycott M, McMahon KM, Mellors JE, Calladine A, Kleine D (2004) A guide to tropical seagrasses of the Indo-West Pacific. James Cook University, TownsvilleGoogle Scholar
  70. Waycott M, Procaccini G, Les DH, Reusch TBH (2006) Seagrass evolution, ecology and conservation: a genetic perspective. In: Larkum WD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 25–50Google Scholar
  71. Waycott M, McMahon K, Lavery P (2014) A guide to southern temperate seagrasses. CSIRO Publishing, MelbourneGoogle Scholar
  72. Wiley EO (1988) Vicariance Biogeography. Annu Rev Ecol Syst 19:513–542.  https://doi.org/10.1146/annurev.es.19.110188.002501CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Michelle Waycott
    • 1
    • 2
    • 3
  • Edward Biffin
    • 3
  • Donald H. Les
    • 4
  1. 1.School of Biological SciencesThe University of AdelaideAdelaideAustralia
  2. 2.Environment InstituteThe University of AdelaideAdelaideAustralia
  3. 3.State Herbarium of South Australia, Department of Environment, Water and Natural ResourcesAdelaideAustralia
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA

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