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Reproductive strategy of the invasive Oxalis pes-caprae: distribution patterns of floral morphs, ploidy levels and sexual reproduction

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Abstract

Oxalis pes-caprae, a tristylous flowering plant native to South Africa, is described in the western Mediterranean basin as an asexual—only 5x short-styled morph (5x S-morph) invasive weed losing all mating partners after introduction. The objective of this study was to reassess the patterns of floral morph and cytotype distribution and the sexual reproduction ability in this invaded range. For that, floral morph and cytotype composition were evaluated in 39 populations of O. pes-caprae in a methodical sampling. The reproductive success of natural populations was assessed as fruit and seed production and seed germination for all floral morphs and cytotypes detected. Self- and morph-incompatibility were also studied with controlled hand pollinations. A remarkable diversity in floral morph and cytotype composition was observed. Furthermore, we observed successful sexual reproduction in several localities across the surveyed area. The S-morph is still dominant in this invaded area, and although it was mostly 5x, an additional cytotype (4x) was also recorded. Records of both a mid-styled morph (M-morph) and an area with trimorphic populations of this species are reported here for the first time in the invasive range of the Mediterranean basin. The long-styled morph appears to occur randomly across the surveyed area, while the M-morph is concentrated mainly in Estremadura province (Portugal), where a breakdown in the incompatibility system was observed. These distribution patterns may result from events of sexual reproduction after incompatibility breakdown and/or from multiple introduction events from the native area. The ability to reproduce sexually, undetected so far, may have important impacts in the population dynamics and major consequences for the adaptation and selection potential of O. pes-caprae in this invaded area.

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References

  • Arroyo J, Barrett SCH, Hidalgo R, Cole WW (2002) Evolutionary maintenance of stigma-height dimorphism in Narcissus papyraceus (Amaryllidaceae). Am J Bot 89:1242–1249

    Article  PubMed  Google Scholar 

  • Ater M (2005) Biologie de la reproduction d’Oxalis pes-caprae au Maroc. In: Congresso 2005 de la Sociedad Española de Malherbologia. Malherbologia Ibérica: Soluciones comunes a problemas comunes, Huelva

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–168

    Google Scholar 

  • Barrett SCH (1979) Evolutionary breakdown of tristyly in Eichhornia crassipes (Mart) Solms (Water Hyacinth). Evolution 33:499–510

    Article  Google Scholar 

  • Barrett SCH (1980) Dimorphic incompatibility and gender in Nymphoides indica (Menyanthaceae). Can J Bot 58:1938–1942

    Article  Google Scholar 

  • Barrett SCH (1992) Heterostylous genetic polymorphisms: model systems for evolutionary analysis. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 1–29

    Chapter  Google Scholar 

  • Barrett SCH (2011) Why reproductive systems matter for the invasion biology of plants. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Blackwell Publishing Ltd, Oxford, pp 195–210

    Google Scholar 

  • Barrett SCH, Forno IW (1982) Style morph distribution in New World populations of Eichhornia crassipes (Mart) Solms Laubach (Water Hyacinth). Aquat Bot 13:299–306

    Article  Google Scholar 

  • Barrett SCH, Coberti RI, Eckert CG (2008) Plant reproductive systems and evolution during biological invasion. Mol Ecol 17:373–383

    Article  PubMed  Google Scholar 

  • Castro S, Loureiro J, Santos C, Ater M, Ayensa G, Navarro L (2007) Distribution of flower morphs, ploidy level and sexual reproduction of the invasive weed Oxalis pes-caprae in the western area of the Mediterranean region. Ann Bot 99:507–517

    Article  PubMed  Google Scholar 

  • Charlesworth D (1979) The evolution and breakdown of tristyly. Evolution 33:486–498

    Article  Google Scholar 

  • Colautti RI, White NA, Barrett SCH (2010) Variation of self-incompatibility within invasive populations of purple loosestrife (Lythrum salicaria L.) from eastern North America. Int J Plant Sci 171:158–166

    Article  Google Scholar 

  • Costa J, Ferrero V, Loureiro J, Castro M, Navarro L, Castro S (2013) Sexual reproduction in the invasive pentaploid short-styled Oxalis pes-caprae allows the production of viable offspring. Plant Biology. doi:10.1111/plb.12010

  • Doležel J, Göhde W (1995) Sex determination in dioecious plants Melandrium album and M. rubrum using high-resolution flow cytometry. Cytometry 19:103–106

    Article  PubMed  Google Scholar 

  • Dulberger R (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 41–84

    Chapter  Google Scholar 

  • Eckert CG, Barrett SCH (1992) Stochastic loss of style morphs from populations of tristylous Lythrum salicaria and Decodon verticillatus (Lythraceae). Evolution 46:1014–1029

    Article  Google Scholar 

  • Eckert CG, Barrett SCH (1993) Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus (Lythraceae). Am J Bot 80:1175–1182

    Article  Google Scholar 

  • Eckert CG, Barrett SCH (1995) Style morph ratios in tristylous Decodon verticillatus (Lythraceae): selection vs historical contingency. Ecology 76:1051–1066

    Article  Google Scholar 

  • Emshwiller E (2002) Ploidy levels among species in the ‘Oxalis tuberosa Alliance’ as inferred by flow cytometry. Ann Bot 89:741–753

    Article  PubMed  Google Scholar 

  • Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell-cycle in intact plant tissues. Science 220:1049–1051

    Article  PubMed  CAS  Google Scholar 

  • Ganders FR (1979) The biology of heterostyly. N Z J Bot 17:607–635

    Google Scholar 

  • Heuch I (1979) Equilibrium populations of heterostylous plants. Theor Popul Biol 15:43–57

    Article  Google Scholar 

  • Hodgins KA, Barrett SCH (2008) Asymmetrical mating patterns and the evolution of biased style-morph ratios in a tristylous daffodil. Genet Res 90:3–15

    Article  Google Scholar 

  • Kohn JR, Barrett SCH (1992) Experimental studies on the functional significance of heterostyly. Evolution 46:43–55

    Article  Google Scholar 

  • Kolař F, Stech M, Travníček P, Rauchová J, Urfuš T, Vít P, Kubešová M, Suda J (2009) Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Ann Bot 103:963–974

    Article  PubMed  Google Scholar 

  • Krejčíková J, Sudová R, Oberlander KC, Dreyer LL, Suda J (2013) Cytogeography of Oxalis pes-caprae in its native range: where are the pentaploids? Biol Invasions. doi:10.1007/s10530-012-0370-2

  • Legendre P, Fortin M-J (1989) Spatial patterns and ecological analysis. Vegetatio 80:107–138

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. 2nd English edition edn. Elsevier Science BV, Amsterdam

  • Lewis D, Jones DA (1992) The genetics of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer-Verlag, Berlin, pp 129–150

  • Loureiro J, Rodriguez E, Doležel J, Santos C (2006) Comparison of four nuclear isolation buffers for plant DNA flow cytometry. Ann Bot 86:679–689

    Article  Google Scholar 

  • Lourteig A (2000) Oxalis L. subgénero Monoxalis (Small) Lourt., Oxalis y Trifidus Lourt. Bradea 7:201–629

    Google Scholar 

  • Luo SX, Zhang DX, Renner SS (2006) Oxalis debilis in China: distribution of flower morphs, sterile pollen and polyploidy. Ann Bot 98:459–464

    Article  PubMed  Google Scholar 

  • Michael P (1964) The indentity and origin of varieties of Oxalis pes-caprae L. naturalized in Australia. Trans R Soc S Aust 88:167–173

    Google Scholar 

  • Morgan MT, Barrett SCH (1988) Historical factors and anisoplethic population structure in tristylous Pontederia cordata: a reassessment. Evolution 42:496–504

    Article  Google Scholar 

  • Mulcahy DL (1964) Reproductive biology of Oxalis priceae. Am J Bot 51:1045–1050

    Article  Google Scholar 

  • Oberlander KC, Emshwiller E, Bellstedt DU, Dreyer LL (2009) A model of bulb evolution in the eudicot genus Oxalis L. Mol Phylogenet Evol 51:54–63

    Article  PubMed  CAS  Google Scholar 

  • O’Brien SP, Calder DM (1989) The breeding biology of Epacris impressa. Is this species heterostylous? Aust J Bot 37:43–54

    Google Scholar 

  • O’Neil P (1992) Variation in male and female reproductive success among floral morphs in the tristylous plant Lythrum salicaria (Lythraceae). Am J Bot 79:1024–1030

    Article  Google Scholar 

  • Ornduff R (1972) Breakdown of trimorphic incompatibility in Oxalis Section Corniculatae. Evolution 26:52–65

    Article  Google Scholar 

  • Ornduff R (1986) The origin of weediness in Oxalis pes-caprae. Am J Bot 73:779–780

    Article  Google Scholar 

  • Ornduff R (1987) Reproductive systems and chromosome races of Oxalis pes-caprae L. and their bearing on the genesis of a noxious weed. Ann Mo Bot Gard 74:79–84

    Article  Google Scholar 

  • Otto F (1992) Preparation and staining of cells for high-resolution DNA analysis. In: Radbruch A (ed) Flow cytometry and cell sorting. Springer, Berlin, pp 101–104

    Google Scholar 

  • Pütz N (1994) Vegetative spreading of Oxalis pes-caprae (Oxalidaceae). Plant Syst Evol 191:57–67

    Article  Google Scholar 

  • Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55

    Article  Google Scholar 

  • Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501

    Article  Google Scholar 

  • Rappa F (1911) Osservazioni sull Oxalis cernua Thunb. Bollettino del Orto Botanico Palermo 10:142–183

    Google Scholar 

  • Ray PM, Chisaki HF (1957) Studies on Amsinckia. Am J Bot 44:529–544

    Google Scholar 

  • Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107

    Article  Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, Do Valle CB, Mendes-Bonato AB (2003) Chromosome number and microsporogenesis in a pentaploid accession of Brachiaria brizantha (Gramineae). Plant Breed 122:136–140

    Article  Google Scholar 

  • Rosenberg MS, Anderson CD (2011) PASSaGE: pattern analysis, spatial statistics, and geographic exegesis. Version 2. Methods Ecol Evol 2:229–232

    Article  Google Scholar 

  • 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 (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Salter TM (1944) The genus Oxalis in South Africa: a taxonomic revision. J S Afr Bot, Supplement 1:1–355

    Google Scholar 

  • Schönswetter P, Suda J, Popp M, Weiss-Schneeweiss H, Brochmann C (2007) Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Mol Phylogenet Evol 42:92–103

    Article  PubMed  Google Scholar 

  • Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101

    Article  Google Scholar 

  • Symon D (1961) The species of Oxalis established in South Australia. Trans R Soc S Aust 84:71–77

    Google Scholar 

  • te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubesova M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109:19–45

    Article  Google Scholar 

  • Turketti SS (2010) A study of tristyly in South African Oxalis. PhD Thesis, University of Stellenbosch

  • Vignoli L (1937) Fenomeni reproduttivi di Oxalis cernua Thunb. Lavori Inst Bot Palermo 8:5–30

    Google Scholar 

  • Vilà M, Bartomeus I, Gimeno I, Traveset A, Moragues E (2006) Demography of the invasive geophyte Oxalis pes-caprae across a Mediterranean Island. Ann Bot 97:1055–1062

    Article  PubMed  Google Scholar 

  • Wang Y, Wang QF, Guo YH, Barrett SCH (2005) Reproductive consequences of interactions between clonal growth and sexual reproduction in Nymphoides peltata: a distylous aquatic plant. New Phytol 165:329–335

    Article  PubMed  Google Scholar 

  • Young D (1968) Oxalis L. In: Tutin T, Heywood V, Burges N et al (eds) Flora Europaea, vol 2. Cambridge University Press, Cambridge, p 193

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Inc., New Jersey

    Google Scholar 

Download references

Acknowledgments

Authors are thankful to Conceição Santos and Eleazar Rodriguez for their support in the preliminary flow cytometric analysis. This research was supported by FEDER funds through the COMPETE Program and by Portuguese Foundation for Science and Technology (FCT) funds in the ambit of the project PTDC/BIA-BIC/110824/2009, by CRUP Acções Integradas Luso-Espanholas 2010 with the project E10/10, by MCI-Programa de Internacionalización de la I + D (PT2009-0068) and by by the Spanish DGICYT (CGL2009-10466), FEDER funds from the European Union, and the Xunta de Galicia (INCITE 09-3103009PR). FCT also supported the work of Sílvia Castro (FCT/BPD/41200/2007) and Joana Costa (CB/C05/2009/209; PTDC/BIA-BIC/110824/2009). Fundación Ramón Areces supported the work of Victoria Ferrero.

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Authors and Affiliations

  1. CFE - Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401, Coimbra, Portugal

    Sílvia Castro, Victoria Ferrero, Joana Costa, Ana João Sousa, Mariana Castro & João Loureiro

  2. Department of Plant Biology, Faculty of Science, University of Vigo, As Lagoas-Marcosende, 36200, Vigo, Spain

    Victoria Ferrero & Luis Navarro

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  1. Sílvia Castro
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Correspondence to Sílvia Castro.

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Castro, S., Ferrero, V., Costa, J. et al. Reproductive strategy of the invasive Oxalis pes-caprae: distribution patterns of floral morphs, ploidy levels and sexual reproduction. Biol Invasions 15, 1863–1875 (2013). https://doi.org/10.1007/s10530-013-0414-2

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