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Evolutionary Ecology

, Volume 20, Issue 5, pp 447–463 | Cite as

The evolutionary potential of invasive Carpobrotus (Aizoaceae) taxa: are pollen-mediated gene flow potential and hybrid vigor levels connected?

  • Carey Meredith Suehs
  • Stéphane Charpentier
  • Laurence Affre
  • Frédéric Médail
Research Article

Abstract

Few studies have addressed the importance of native pollinators in shaping the breeding systems and evolutionary potential of invasive plants. We examined the pollination and gamete production of Carpobrotus affine acinaciformis (L.) L. Bol. and C. edulis (L.) N. E. Br. invading the coasts of southeast France (Provence), and found preliminary evidence that the pollen-mediated gene flow potential (PMGFP) within the four studied populations is positively correlated with their Relative Performance in Hybridization indices (RPH), suggesting a link between pollinator services, gene flow, and Carpobrotus hybridization. Flower density (FD) may be a driver behind pollinator abundance and visitation patterns since it shows a significant, positive relationship with relative pollinator abundance (FR) and a significant negative relationship with per flower visit frequencies (FR/F). In the populations with the highest RPH indices, and therefore high hybrid vigor, both taxa produce similar quantities of ovules and pollen per flower, whose ratios further indicate (facultative) xenogamy. Pollen diameter distributions include ∼25% micro-pollen, and overall viability is less than one half. Viable pollen profiles consist of 3.5% micro, 85.5% normal and 10.9% macro pollen (considered as diplogametes) on average per flower for C. affine acinaciformis, and 0.7% micro, 73.0% normal and 26.2% macro pollen for C. edulis. Given the co-occurrence of (1) (facultative) xenogamic breeding strategies, (2) a significant, positive relationship between RPH and PMGFP, and (3) frequent pollen abnormalities, it is probable that hybrid dysgenesis mediated by the local pollinators occurs in these populations. Furthermore, the unusually high frequency of potentially viable, diploid macro-pollen underlines the evolutionary/polyploid potential of these invasive, introgressed populations. Native pollinator interactions may greatly affect the taxonomic status and evolutionary potential of invasive plant complexes.

Keywords

Diploid gamete Hybrid dysgenesis Hybridization Introgression Pollen to ovule ratio Pollinator service Polyploid potential Relative performance in hybridization index 

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References

  1. Abbott, RJ 1992Plant invasions, interspecific hybridization and the evolution of new plant taxaTrends Ecol Evol7401405CrossRefGoogle Scholar
  2. Abbott, RJ, James, JK, Milne, RI, Gillies, ACM 2003Plant introductions, hybridization and gene flowPhil Trans R Soc Lond B35811231132CrossRefGoogle Scholar
  3. Agren, J, Schemske, DW 1993Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata Evolution47125135CrossRefGoogle Scholar
  4. Ainouche, ML, Baumel, A, Salmon, A, Yannic, G 2003Hybridization, polyploidy and speciation in Spartina (Poaceae)New Phytol161165172CrossRefGoogle Scholar
  5. Albert A, Jahandiez, E (1908) Catalogue des plantes qui croissent naturellement dans le département du Var. Mus. Hist. Nat. Toulon reprints, 1985, ToulonGoogle Scholar
  6. Albert, ME, D’Antonio, CM, Schierenbeck, KA 1997Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California. I. Morphological evidenceAm J Bot84896904CrossRefGoogle Scholar
  7. Arnold, ML 1992Natural hybridization as an evolutionary processAnnu Rev Ecol Syst23237261CrossRefGoogle Scholar
  8. Arnold, ML 1997Natural hybridization and evolutionOxford University PressNew YorkGoogle Scholar
  9. Barrett, SCH 1996Ecology and evolution of plant matingTrends Ecol Evol117379CrossRefGoogle Scholar
  10. Bierzychudek, P 1981Pollinator limitation of plant reproductive effortAm Nat117838840CrossRefGoogle Scholar
  11. Bierzychudek, P 1985Patterns in plant parthenogenesisExperientia4112551264CrossRefGoogle Scholar
  12. Bierzychudek, P 1990The adaptive significance of sexual reproduction in plantsLect Math Life Sci225191Google Scholar
  13. Blake, ST 1969A revision of Carpobrotus and Sarcozona in Australia, genera allied to Mesembryanthemum (Aizoaceae)Contrib Queensl Herb7165Google Scholar
  14. Bretagnolle, F, Felber, F, Calame, FG, Küpfer, P 1998La polyploïdie chez les plantesBot Helv108537Google Scholar
  15. Bretagnolle, F, Thompson, JD 1995Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plantsNew Phytol129122CrossRefGoogle Scholar
  16. Brown, BJ, Mitchell, RJ 2001Competition for pollination: effects of pollen of an invasive plant on seed set of a native congenerOecologia1294349CrossRefGoogle Scholar
  17. Brown, BJ, Mitchell, RJ, Graham, SA 2002Competition for pollination between an invasive species (Purple Loosestrife) and a native congenerEcology8323282336CrossRefGoogle Scholar
  18. Charlesworth, B 1992Evolutionary rates in partially self-fertilizing speciesAm Nat140126148CrossRefPubMedGoogle Scholar
  19. Charlesworth, D 1989Evolution of low female fertility in plants: pollen limitation, resource allocation and genetic loadTrends Ecol Evol4289292CrossRefGoogle Scholar
  20. Charlesworth, D, Morgan, MT, Charlesworth, B 1990Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkageEvolution4414691489CrossRefGoogle Scholar
  21. Chittka, L, Schürkens, S 2001Successful invasion of a floral marketNature411653PubMedCrossRefGoogle Scholar
  22. Cruden, RW 1977Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plantsEvolution313246CrossRefGoogle Scholar
  23. Diadema K (2002) Facteurs génétiques, cytologiques et morphométriques impliqués dans la dynamique d'invasion de Carpobrotus spp. (Aizoaceae) sur litle de Bagaud (Parc National de Port-Cros). DESS Dissertation. Université d'Aix-Marseille III, Marseilles, France. 43pgs.Google Scholar
  24. Ellstrand, NC, Schierenbeck, KA 2000Hybridization as a stimulus for the evolution of invasiveness in plants?Proc Natl Acad Sci USA9770437050PubMedCrossRefGoogle Scholar
  25. Fontdevila, A 2004Introgression and hybrid speciation via transpositionMoya, AFont, E eds. Evolution: from molecules to ecosystemsOxford University PressOxford182194Google Scholar
  26. Gallagher, KG, Schierenbeck, KA, D’Antonio, CM 1997Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California II. Allozyme evidenceAm J Bot84905911CrossRefGoogle Scholar
  27. García-Ramos, G, Rodríguez, D 2002Evolutionary speed of species invasionsEvolution56661668PubMedCrossRefGoogle Scholar
  28. Gouffé la Cour, M 1813Mémoire sur les végétaux exotiques qui peuvent être naturalisés dans les départements méridionaux de la France, suivi de la liste des plantes rares qui ont fleuri et de celles qui ont fructifié dans divers jardins de Marseille principalement dans le jardin de botanique et de naturalisation de cette villeMém l’Acad Marseille11149259Google Scholar
  29. Hänfling, B, Kollman, J 2002An evolutionary perspective of biological invasionsTrends Ecol Evol17545546CrossRefGoogle Scholar
  30. Hartmann, HEK 1993AizoaceaeKubitzki, K eds. The families and genera of vascular plants. II. Flowering plants – dicotyledonsMagnoliid, Hamamelid and Caryophyllid FamiliesBerlin Heidelberg, New York, NY, USA3769Google Scholar
  31. Hurka, H, Bleeker, W, Neuffer, B 2003Evolutionary processes associated with biological invasions in the BrassicaceaeBiol Invasions5281292CrossRefGoogle Scholar
  32. Kearns, CA, Inouye, DW 1993Techniques for pollination biologistsUniversity Press of ColoradoNiwot, ColoradoCrossRefGoogle Scholar
  33. Klak, C, Khunou, A, Reeves, G, Hedderson, T 2003A phylogenetic hypothesis for the Aizoaceae (Caryophyllales) based on four plastid DNA regionsAm J Bot9014331445Google Scholar
  34. Lee, CE 2002Evolutionary genetics of invasive speciesTrends Ecol Evol17386391CrossRefGoogle Scholar
  35. Maron, JL, Vilà, M, Bommarco, R, Elmendorf, S, Beardsley, P 2004Rapid evolution of an invasive plantEcol Monogr74261280Google Scholar
  36. Milne, RI, Abbott, RJ 2000Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British IslesMol Ecol9541556PubMedCrossRefGoogle Scholar
  37. Ortiz, R 1997Occurrence and inheritance of 2n pollen in Musa Ann Bot79449453CrossRefGoogle Scholar
  38. Pappert, RA, Hamrick, JL, Donovan, LA 2000Genetic variation in Pueraria lobata (Fabaceae), an introduced, clonal, invasive plant of the southeastern United StatesAm J Bot8712401245PubMedCrossRefGoogle Scholar
  39. Parker, IM 1997Pollinator limitation of Cytisus scoparius (Scotch Broom), an invasive exotic shrubEcology7814571470CrossRefGoogle Scholar
  40. Parker, IM, Engel, A, Haubensak, KA, Goodell, K 2002Pollination of Cytisus scoparius and Genista monspessulana, two invasive shrubs in CaliforniaMadroño492532Google Scholar
  41. Parker, IM, Haubensak, KA 2002Comparative pollinator limitation of two non-native shrubs: do mutualisms influence invasions?Oecologia130250258Google Scholar
  42. Ramsey, J, Schemske, DW 1998Pathways, mechanisms, and rates of polyploid formation in flowering plantsAnnu Rev Ecol Syst29467501CrossRefGoogle Scholar
  43. Ramsey, J, Schemske, DW 2002Neopolyploidy in flowering plantsAnnu Rev Ecol Syst33589639CrossRefGoogle Scholar
  44. Rieseberg, LH 1997Hybrid origins of plant speciesAnnu Rev Ecol Syst28359389CrossRefGoogle Scholar
  45. Rieseberg, LH, Carney, SE 1998Plant hybridizationNew Phytol140599624CrossRefGoogle Scholar
  46. Rieseberg, LH, Wendel, JF 1993Introgression and its consequences in plantsHarrison, RG eds. Hybrid zones and the evolutionary processOxford University PressNew York71109Google Scholar
  47. Roy, J 1990 In search of the characteristics of plant invadersdi Castri, FHansen, AJDebussche, M eds. Biological invasions in Europe and the Mediterranean BasinKluwer Academic PublishersDordrecht335352Google Scholar
  48. Sakai, AK, Allendorf, FW, Holt, JS, Lodge, DM, Molofsky, J, With, KA, Baughman, S, Cabin, RJ, Cohen, JE, Ellstrand, NC, McCauley, DE, O’Neil, P, Parker, IM, Thompson, JN, Weller, SG 2001The population biology of invasive speciesAnnu Rev Ecol Syst32305332CrossRefGoogle Scholar
  49. Song, K, Lu, P, Tang, K, Osborn, TC 1995Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolutionProc Natl Acad Sci USA9277197723PubMedCrossRefGoogle Scholar
  50. Statsoft (2001) STATISTICA for Windows [Computer program manual] 6.0 edn. Tulsa, OK: Statsoft Inc.Google Scholar
  51. Stout, JC, Kells, AR, Goulson, D 2002Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in TasmaniaBiol Conserv106425434CrossRefGoogle Scholar
  52. Suehs, CM, Affre, L, Médail, F 2004aInvasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: I. Genetic diversity and introgressionHeredity923140CrossRefGoogle Scholar
  53. Suehs, CM, Affre, L, Médail, F 2004bInvasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: II. Reproductive strategiesHeredity92550556CrossRefGoogle Scholar
  54. Suehs, CM, Affre, L, Médail, F 2005Unexpected insularity effects in invasive plant mating systems: the case of Carpobrotus (Aizoaceae) taxa in the Mediterranean BasinBiol J Linn Soc856579CrossRefGoogle Scholar
  55. Suzuki, N 2000Pollinator limitation and resource limitation of seed production in the Scotch broom, Cytisus scoparius (Leguminosae)Plant Sp Biol15187193CrossRefGoogle Scholar
  56. Thompson, JD 1990Spartina anglica, characteristic features or invasive weed of coastal salt marshes?Biologist37912Google Scholar
  57. Totland, Ø, Matthews, I 1998Determinants of pollinator activity and flower preference in the early spring bloomingCrocus vernus Acta Oecol19155165CrossRefGoogle Scholar
  58. Vilà, M, D’Antonio, CM 1998aFitness of invasive Carpobrotus (Aizoaceae) hybrids in coastal CaliforniaEcoscience5191199Google Scholar
  59. Vilà, M, D’Antonio, CM 1998bHybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal CaliforniaEcol Appl811961205Google Scholar
  60. Vilà, M, Weber, E, D’Antonio, CM 1998Flowering and mating system in hybridizing Carpobrotus (Aizoaceae) in coastal CaliforniaCan J Bot7611651169CrossRefGoogle Scholar
  61. Vilà, M, Weber, E, D’Antonio, CM 2000Conservation implications of invasion by plant hybridizationBiol Invasions2207217CrossRefGoogle Scholar
  62. Wendel, JF 2000Genome evolution in polyploidsPlant Mol Biol42225249PubMedCrossRefGoogle Scholar
  63. Wisura, W, Glen, HF 1993The South African species of Carpobrotus (Mesembryanthema – Aizoaceae)Contrib Bolus Herb1576107Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Carey Meredith Suehs
    • 1
  • Stéphane Charpentier
    • 1
  • Laurence Affre
    • 1
  • Frédéric Médail
    • 1
  1. 1.Institut Méditerranéen d’Ecologie et de Paléoécologie (IMEP, UMR CNRS 6116)Université d’Aix-Marseille III, Europôle Méditerranéen de L’ArboisAix-en-ProvenceFrance

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