Advertisement

Plant Systematics and Evolution

, Volume 305, Issue 7, pp 531–547 | Cite as

Morphological and anatomical evidence supports differentiation of new interspecific hybrids from native Spartina maritima and invasive S. densiflora (Poaceae, subfamily Chloridoideae)

  • María D. Infante-Izquierdo
  • Blanca Gallego-TévarEmail author
  • Enrique Sánchez-Gullón
  • F. Javier J. Nieva
  • Brenda J. Grewell
  • Jesús M. Castillo
  • Adolfo F. Muñoz-Rodríguez
Original Article

Abstract

Interspecific hybridization is a major mechanism for generating evolutionary novelty in plants. Halophytic Spartina species are often abundant in coastal salt marshes around the world, and they frequently hybridize. Despite a large body of knowledge on the ecology and evolution of Spartina species, taxonomic resources for distinction of complex taxa in the genus are scarce. The general aim of this study was to characterize parental species S. maritima (native) and S. densiflora (invasive) and their reciprocal hybrids formed in the Gulf of Cadiz (Southwest Iberian Peninsula). Our approach was to quantify and compare morphological and anatomical characters of tufts, culms, leaves and inflorescences and the limits of their variation in different ecological settings. Our results document discriminating trait variables from populations of both hybrids that can be used to distinguish them from their parental species and each other. From these findings and the verification of type specimens, we describe two new nothotaxa, Spartina × onubensis subsp. onubensis and Spartina × onubensis subsp. tartessiana, and develop taxonomic keys for identification of the four studied taxa. Floral traits such as the length of the terminal spike, the spikelet and its glumes and lemma allow us to differentiate S. densiflora (with lower values) from the other three taxa. The presence of exerted stamens, shorter culms and shorter leaf blades separated S. maritima from both hybrids. Each hybrid can also be distinguished since S. × onubensis subsp. onubensis develops more spikes per inflorescence and consistently has longer leaves than S. × onubensis subsp. tartessiana.

Keywords

Cordgrass Gulf of Cadiz Hybridization Invasive species Phenotypic plasticity Salt marsh 

Notes

Acknowledgements

Blanca Gallego-Tévar thanks the University of Seville for a research contract (Plan Propio de Investigación). M.D. Infante-Izquierdo acknowledges to Ministerio de Educación, Cultura y Deporte, Spanish Government, for the FPU Grant (Ref. FPU14/06556). F. Muñoz-Rodríguez thanks Ministerio de Economía, Industria y Competitividad of Spanish Government for the research project CGL2017-85204-C3-3-P. The authors thank the Directorate of the Tinto, Odiel, Piedra and Guadiana Natural Parks for supporting field work conducted in this study. A cooperative agreement between the United State Department of Agriculture, Agricultural Research Service (USDA-ARS) Invasive Species and Pollinator Health Research Unit and the University of Seville facilitated this collaboration.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2019_1591_MOESM1_ESM.pdf (127 kb)
Supplementary material 1 (PDF 127 kb)
606_2019_1591_MOESM2_ESM.pdf (214 kb)
Supplementary material 2 (PDF 213 kb)
606_2019_1591_MOESM3_ESM.pdf (190 kb)
Supplementary material 3 (PDF 189 kb)
606_2019_1591_MOESM4_ESM.pdf (194 kb)
Supplementary material 4 (PDF 193 kb)

References

  1. Abbott RJ (1992) Plant Invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405.  https://doi.org/10.1016/0169-5347(92)90020-C CrossRefGoogle Scholar
  2. Ainouche M, Gray A (2016) Invasive Spartina: lessons and challenges. Biol Invasions 18:2119–2122.  https://doi.org/10.1007/s10530-016-1201-7 CrossRefGoogle Scholar
  3. Ainouche ML, Baumel A, Salmon A, Yannic G (2004) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172.  https://doi.org/10.1046/j.1469-8137.2003.00926.x CrossRefGoogle Scholar
  4. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173.  https://doi.org/10.1007/s10530-008-9383-2 CrossRefGoogle Scholar
  5. An SQ, Gu BH, Zhou CF, Wang ZS, Deng ZF, Zhi YB, Li HL, Chen L, Yu DH, Liu YH (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res 47:183–191.  https://doi.org/10.1111/j.1365-3180.2007.00559.x CrossRefGoogle Scholar
  6. Anttila CK, King AR, Ferris C, Ayres DR, Strong DR (2000) Reciprocal hybrid formation of Spartina in San Francisco Bay. Molec Ecol 9:765–771.  https://doi.org/10.1046/j.1365-294x.2000.00935.x CrossRefGoogle Scholar
  7. Ayres DR, Garcia-Rossi D, Davis HG, Strong DR (1999) Extent and degree of hybridization between exotic (Spartina alterniflora) and native (S. foliosa) cordgrass (Poaceae) in California, USA determined by randomly amplified polymorphic DNA (RAPDs). Molec Ecol 8:1179–1186.  https://doi.org/10.1046/j.1365-294x.1999.00679.x CrossRefGoogle Scholar
  8. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004a) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6:221–231.  https://doi.org/10.1023/B:BINV.0000022140.07404.b7 CrossRefGoogle Scholar
  9. Ayres DR, Zaremba K, Strong DR (2004b) Extinction of a common native species by hybridization with an invasive congener. Weed Technol 18:1288–1291.  https://doi.org/10.1614/0890-037X(2004)018%5b1288:EOACNS%5d2.0.CO;2 CrossRefGoogle Scholar
  10. Ayres DR, Zaremba K, Sloop CM, Strong DR (2008a) Sexual reproduction of cordgrass hybrids (Spartina foliosa × alterniflora) invading tidal marshes in San Francisco Bay. Diversity Distrib 14:187–195.  https://doi.org/10.1111/j.1472-4642.2007.00414.x CrossRefGoogle Scholar
  11. Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, Anttila CK, Strong DR (2008b) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Amer J Bot 95:713–719.  https://doi.org/10.3732/ajb.2007358 CrossRefGoogle Scholar
  12. Baumel A, Ainouche ML, Levasseur JE (2001) Molecular investigations in populations of Spartina anglica C.E. Hubbard (Poaceae) invading coastal Brittany (France). Molec Ecol 10:1689–1701.  https://doi.org/10.1046/j.1365-294X.2001.01299.x CrossRefGoogle Scholar
  13. Baumel A, Ainouche ML, Misset MT, Gourret JP, Bayer RJ (2003) Genetic evidence for hybridization between the native Spartina maritima and the introduced Spartina alterniflora (Poaceae) in South-West France: Spartina × neyrautii re-examined. Pl Syst Evol 237:87–97.  https://doi.org/10.1007/s00606-002-0251-8 CrossRefGoogle Scholar
  14. Bird KA, VanBuren R, Puzey JR, Edger PP (2018) The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytol 220:87–93CrossRefGoogle Scholar
  15. Bortolus A (2006) The austral cordgrass Spartina densiflora Brong.: its taxonomy, biogeography and natural history. Biogeography 33:158–168.  https://doi.org/10.1111/j.1365-2699.2005.01380.x CrossRefGoogle Scholar
  16. Bortolus A, Carlton JT, Schwindt E (2015) Reimaging South American coasts: unveiling the hidden invasion history of an iconic ecological engineer. Diversity Distrib 21:1267–1283.  https://doi.org/10.1111/ddi.12377 CrossRefGoogle Scholar
  17. Castellanos EM, Figueroa ME, Davy AJ (1994) Nucleation and facilitation in saltmarsh succession: interactions between Spartina maritima and Arthrocnemum perenne. J Ecol 82:239–248.  https://doi.org/10.2307/2261292 CrossRefGoogle Scholar
  18. Castillo JM, Ayres DR, Leira-Doce P, Baile J, Blum M, Strong DR, Luque T, Figueroa E (2010) The production of hybrids with high ecological amplitude between exotic Spartina densiflora and native S. maritima in the Iberian Peninsula. Diversity Distrib 16:547–558.  https://doi.org/10.1111/j.1472-4642.2010.00673.x CrossRefGoogle Scholar
  19. Castillo JM, Grewell BJ, Pickart A, Bortolus A, Peña C, Figueroa E, Sytsma M (2014) Phenotypic plasticity of invasive Spartina densiflora (Poaceae) along a broad latitudinal gradient on the pacific coast of North America. Amer J Bot 101:448–458.  https://doi.org/10.3732/ajb.1400014 CrossRefGoogle Scholar
  20. Castillo JM, Gallego-Tévar B, Figueroa E, Grewell BJ, Vallet D, Rousseau H, Keller J, Lima O, Dréano S, Salmon A, Aïnouche M (2018) Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America. Ecol Evol 8:4992–5007.  https://doi.org/10.1002/ece3.4063 CrossRefGoogle Scholar
  21. Clayton WD, Renvoize SA (1986) Genera graminarum. Grasses of the world. Kew Bull 13:1–389Google Scholar
  22. Contreras-Cruzado I, Infante-Izquierdo MD, Márquez-García B, Hermoso-López V, Polo A, Nieva FJJ, Cartes-Barroso JB, Castillo JM, Muñoz-Rodríguez A (2017) Relationships between spatio-temporal changes in the sedimentary environment and halophytes zonation in salt marshes. Geoderma 305:173–187.  https://doi.org/10.1016/j.geoderma.2017.05.037 CrossRefGoogle Scholar
  23. Daehler CC, Strong DR (1997) Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. Amer J Bot 84:607–611.  https://doi.org/10.2307/2445896 CrossRefGoogle Scholar
  24. Darby FA, Turner RE (2008) Below- and aboveground biomass of Spartina alterniflora: response to nutrient addition in a Louisiana salt marsh. Estuar Coast 31:326–334.  https://doi.org/10.1007/s12237-008-9037-8 CrossRefGoogle Scholar
  25. Di Bella CE, Striker GG, Escaray FJ, Lattanzi FA, Rodríguez AM, Grimoldi AA (2014) Saline tidal flooding effects on Spartina densiflora plants from different positions of the saltmarsh. Diversities and similarities on growth, anatomical and physiological responses. Environm Exp Bot 102:27–36.  https://doi.org/10.1016/j.envexpbot.2014.02.009 CrossRefGoogle Scholar
  26. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050.  https://doi.org/10.1073/pnas.97.13.7043 CrossRefGoogle Scholar
  27. Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci USA 93:5090–5093.  https://doi.org/10.1073/pnas.93.10.5090 CrossRefGoogle Scholar
  28. Fortune PM, Schierenbeck K, Ayres D, Bortolus A, Catrice O, Brown S, Ainouche ML (2008) The enigmatic invasive Spartina densiflora: a history of hybridizations in a polyploidy context. Molec Ecol 17:4304–4316.  https://doi.org/10.1111/j.1365-294X.2008.03916.x CrossRefGoogle Scholar
  29. Gallego-Tévar B, Rubio-Casal A, de Cires A, Figueroa E, Grewell BJ, Castillo JM (2018a) Phenotypic plasticity of polyploid plant species promotes transgressive behaviour in their hybrids. AoB Plants 10:ply055.  https://doi.org/10.1093/aobpla/ply055 CrossRefGoogle Scholar
  30. Gallego-Tévar B, Curado G, Grewell BJ, Figueroa ME, Castillo JM (2018b) Realized niche and spatial pattern of native and exotic halophyte hybrids. Oecologia 188:849–862.  https://doi.org/10.1007/s00442-018-4251-y CrossRefGoogle Scholar
  31. Groves H, Groves J (1880) Spartina × townsendii Nobis. Rep Bot Exch Club Soc Brit Isles 1:37Google Scholar
  32. Hall RJ, Hastings A, Ayres DR (2006) Explaining the explosion: modelling a hybrid invasion. Proc Biol Sci 273:1385–1389.  https://doi.org/10.1098/rspb.2006.3473 CrossRefGoogle Scholar
  33. Hegarty MJ, Hiscock SJ (2005) Hybrid speciation in plants: new insights from molecular studies. New Phytol 165:411–423.  https://doi.org/10.1111/j.1469-8137.2004.01253.x CrossRefGoogle Scholar
  34. Hulme PR, Backer S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Pyšek P, Roques A, Sol D, Solarz W, Vilà M (2008) Grasping at routes of biological invasion: a framework for integrating pathways into policy. J Appl Ecol 45:403–414.  https://doi.org/10.1111/j.1365-2664.2007.01442.x CrossRefGoogle Scholar
  35. Kern VG, Guarise NJ, Vegetti AC (2008) Inflorescence structure in species of Spartina Schreb. (Poaceae: Chloridoideae: Cynodonteae). Pl Syst Evol 273:51–61.  https://doi.org/10.1007/s00606-008-0009-z CrossRefGoogle Scholar
  36. Lee AK, Ayres DR, Pakenham-Walsh MR, Strong DR (2016) Responses to salinity of Spartina hybrids formed in San Francisco Bay, California (S. alterniflora × foliosa and S. densiflora × foliosa). Biol Invasions 18:2207–2219.  https://doi.org/10.1007/s10530-015-1011-3 CrossRefGoogle Scholar
  37. Lovett Doust L, Lovett Doust J (1982) The battle strategies of plants. New Sci 91:81–84Google Scholar
  38. Mallet J (2007) Hybrid speciation. Nature 446:279–283CrossRefGoogle Scholar
  39. Marchant CJ (1967) Evolution in Spartina (Gramineae) I. The history and morphology of the genus in Britain. Bot J Linn Soc 60:1–24.  https://doi.org/10.1111/j.1095-8339.1967.tb00076.x CrossRefGoogle Scholar
  40. Marchant CJ (1968a) Evolution in Spartina (Gramineae). II. Chromosomes, basic relationships and the problem of Spartina × townsendii agg. Bot J Linn Soc 60:381–409.  https://doi.org/10.1111/j.1095-8339.1968.tb00096.x CrossRefGoogle Scholar
  41. Marchant CJ (1968b) Evolution in Spartina (Gramineae) III. Species chromosome numbers and their taxonomic significance. Bot J Linn Soc 60:411–417.  https://doi.org/10.1111/j.1095-8339.1968.tb00097.x CrossRefGoogle Scholar
  42. Maricle BR, Koteyeva NK, Voznesenskaya EV, Thomasson JR, Edwards GE (2009) Diversity in leaf anatomy, and stomatal distribution and conductance, between salt marsh and freshwater species in the C4 genus Spartina (Poaceae). New Phytol 184:216–233.  https://doi.org/10.1111/j.1469-8137.2009.02903.x CrossRefGoogle Scholar
  43. Mobberley DG (1953) Taxonomy and distribution of the genus Spartina. Retrospective theses and dissertations 12794. Iowa State University Digital Repository. Available at: https://lib.dr.iastate.edu/rtd/12794Google Scholar
  44. Mobberley DG (1956) Taxonomy and distribution of the genus Spartina. Iowa State Coll J Sci 30:471–564Google Scholar
  45. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451.  https://doi.org/10.1073/pnas.091093398 CrossRefGoogle Scholar
  46. Partridge TR (1987) Spartina in New Zealand. New Zealand J Bot 25:567–575CrossRefGoogle Scholar
  47. Peterson PM, Romaschenko K, Johnson G (2010) A classification of the Chloridoideae (Poaceae) based on multi-gene phylogenetic trees. Molec Phylogen Evol 55:580–598.  https://doi.org/10.1016/j.ympev.2010.01.018 CrossRefGoogle Scholar
  48. Raybould AF, Gray AJ, Lawrence MJ, Marshall DF (1991) The evolution of Spartina anglica C.E. Hubbard (Gramineae): origin and genetic variability. Biol J Linn Soc 43:111–126.  https://doi.org/10.1111/j.1095-8312.1991.tb00588.x CrossRefGoogle Scholar
  49. Renny-Byfield S, Ainouche M, Leitch IJ, Lim KY, Le Comber SC, Leitch AR (2010) Flow cytometry and GISH reveal mixed ploidy populations and Spartina nonaploids with genomes of S. alterniflora and S. maritima origin. Ann Bot (Oxford) 105:527–533.  https://doi.org/10.1093/aob/mcq008 CrossRefGoogle Scholar
  50. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372.  https://doi.org/10.1038/sj.hdy.6886170 CrossRefGoogle Scholar
  51. Saarela JM (2012) Taxonomic synopsis of invasive and native Spartina (Poaceae, Chloridoideae) in the Pacific Northwest (British Columbia, Washington and Oregon), including the first report of Spartina × townsendii for British Columbia, Canada. PhytoKeys 10:25–82.  https://doi.org/10.3897/phytokeys.10.2734 CrossRefGoogle Scholar
  52. Sloop CM, Ayres DR, Strong DR (2009) The rapid evolution of self-fertility in Spartina hybrids (Spartina alterniflora × foliosa) invading San Francisco Bay, CA. Biol Invasions 11:1131–1144.  https://doi.org/10.1007/s10530-008-9385-0 CrossRefGoogle Scholar
  53. Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annual Rev Ecol Evol Syst 44:389–410.  https://doi.org/10.1146/annurev-ecolsys-110512-135803 CrossRefGoogle Scholar
  54. Thompson JD (1990) Morphological variation among natural populations of Spartina anglica. In: Gray AJ, Benham PEM (eds) Spartina anglica—a research review. Institute of Terrestrial Ecology, London, pp 26–33Google Scholar
  55. Thompson JD (1991) The biology of an invasive plant. What makes Spartina anglica so successful? Bioscience 41:393–401.  https://doi.org/10.2307/1311746 CrossRefGoogle Scholar
  56. Tilman D, Wedin D (1991) Plant traits and resource reduction for five grasses growing on a nitrogen gradient. Ecology 72:685–700.  https://doi.org/10.2307/2937208 CrossRefGoogle Scholar
  57. Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber W-H Li DZ, Marhold K, May TW, McNeill J, Monro AM, Prado J, Price MJ, Smith GF (eds) (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Koeltz Botanical Books, GlashüttenGoogle Scholar
  58. Vila M, Weber E, D’Antonio CM (2000) Conservation implications by plant hybridization. Biol Invasions 2:207–217.  https://doi.org/10.1023/A:1010003603310 CrossRefGoogle Scholar
  59. Yao H, Dogra Gray A, Auger DL, Birchler JA (2013) Genomic dosage effects on heterosis in triploid maize. Proc Natl Acad Sci 110:2665–2669.  https://doi.org/10.1073/pnas.1221966110 CrossRefGoogle Scholar
  60. Yoo MJ, Liu X, Pires JC, Soltis PS, Soltis DE (2014) Nonadditive gene expression in polyploids. Annual Rev Genet 48:485–517.  https://doi.org/10.1146/annurev-genet-120213-092159 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Dpto. de Ciencias IntegradasUniversidad de HuelvaHuelvaSpain
  2. 2.Dpto. Biología Vegetal y EcologíaUniversidad de SevillaSevilleSpain
  3. 3.Paraje Natural Marismas del OdielHuelvaSpain
  4. 4.USDA-ARS Invasive Species and Pollinator Health Research Unit, Department of Plant Sciences MS-4University of CaliforniaDavisUSA

Personalised recommendations