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Diversity and evolution of the gynoecium in Cuscuta (dodders, Convolvulaceae) in relation to their reproductive biology: two styles are better than one

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Abstract

The gynoecium of 122 species and 14 varieties of Cuscuta (dodders) was investigated by light and scanning electron microscopy to assess its diversity and evolution and to provide a morphological foundation for understanding the different reproductive strategies encountered in the genus. Data were optimized into a consensus tree constructed from three large-scale molecular phylogenies of the genus based on nuclear ITS and plastid trnL-F sequences. The number of styles combined with the stigma shape are the only floral/fruit characters that enable the separation of Cuscuta subgenera. In addition, gynoecium morphology is useful for delimiting species in some clades. The one-style gynoecium of subg. Monogynella is mostly likely ancestral whereas gynoecia with two styles are derived in subgenera Cuscuta and Grammica. Gynoecia with two styles encountered in the latter subgenera provide a greater morphological complexity and flexibility for various reproductive strategies. In subg. Cuscuta, both the equal styles and stigmas continue to elongate and modify their position after the flowers open, until pollination occurs. In subg. Grammica, the two unequal styles may cause a spatial separation of the sexes in the flower, herkogamy, while the two stigmas mature sequentially and have a differential timing of their receptivity for pollen. A nectary consisting of a ring of modified stomata at the base of the ovary, the equivalent of the hypogynous nectary disc present in many Convolvulaceae, was observed for the first time in all Cuscuta species. The vasculature of the styles is reduced, represented mostly by phloem; xylem is present only in subg. Monogynella. Some gynoecial characters, for example papillae diameter, stigma surface area, stigma width, and style width were moderately correlated with pollen volume, pollen polar–equatorial ratio and tectum perforation. Gynoecium features suggest that Cuscuta is allied with the “bifid clade” (Dicranostyloideae) in Convolvulaceae.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Inl 11:36–42

    Google Scholar 

  • Austin DF (1973) The American Erycibeae (Convolvulaceae). Maripa, Dicranostyles and Lysiostyles, I. Systematics. Ann Missouri Bot Gard 60:306–412

    Article  Google Scholar 

  • Austin DF (1994) A new Bonamia (Convolvulaceae) from Nicaragua. Novon 4:319–321

    Article  Google Scholar 

  • Austin DF (1998) Parallel and convergent evolution in the Convolvulaceae. In: Mathews P, Sivadasan M (eds) Biodiversity and taxonomy of tropical flowering plants. Mentor Books, Calicut, pp 201–234

    Google Scholar 

  • Austin DF (2000) A revision of Cressa L. (Convolvulaceae). Bot J Linn Soc 133:27–39

    Article  Google Scholar 

  • Ayensu ES (1967) Aerosol OT solution––an effective softener of herbarium specimens for anatomical study. Stain Technol 42:155–156

    PubMed  CAS  Google Scholar 

  • Beliz T (1986) A revision of Cuscuta sect. Cleistogrammica using phenetic and cladistic analyses with a comparison of reproductive mechanisms and host preferences in species from California, Mexico and Central America. Ph.D. Thesis. University of California, Berkeley

  • Bell J, Hicks G (1976) Transmitting tissue in the pistil of tobacco: light and electron microscope observations. Planta (Berl) 131:187–200

    Article  Google Scholar 

  • Bigazzi M, Selvi F (2000) Stigma form and surface in the tribe Boragineae (Boraginaceae): micromorphological diversity, relationships with pollen, and systematic relevance. Can J Bot 78:388–408

    Google Scholar 

  • Bray DF, Bagu J, Koegler P (1993) Comparison of hexamethyldisilazane (HMDS), Peldri II, and critical-point drying methods for scanning electron microscopy of biological specimens. Microsc Res Tech 26:489–495

    Article  PubMed  CAS  Google Scholar 

  • Caruso JC, Cliff N (1997) Empirical size, coverage and power of confidence intervals for Spearman’s Rho. Ed Psy Meas 57:637–654

    Article  Google Scholar 

  • Chaloner WG (1986) Electrostatic forces in insect pollination and their significance in exine ornament. Linn Soc Symp Ser 12:103–108

    Google Scholar 

  • Choisy JD (1842) De Convolvulaceis dissertatio. Mem Soc Phys Hist Nat Genève 9:261–288

    Google Scholar 

  • Costea M (2007-onward) Digital Atlas of Cuscuta (Convolvulaceae) Wilfrid Laurier University, Ontario, Canada. www.wlu.ca/page.php?grp_id=2147&p=8968. Accessed 05 March 2011

  • Costea M, Stefanović S (2009a) Molecular phylogeny of Cuscuta californica complex (Convolvulaceae) and a new species from New Mexico and Trans-Pecos. Syst Bot 34:570–579

    Article  Google Scholar 

  • Costea M, Stefanović S (2009b) Cuscuta jepsonii (Convolvulaceae), an invasive weed or an extinct endemic? Am J Bot 96:1–7

    Article  Google Scholar 

  • Costea M, Stefanović S (2010) Evolutionary history and taxonomy of Cuscuta umbellata complex (Convolvulaceae): evidence of extensive hybridization from discordant nuclear and plastid phylogenies. Taxon 59:1783–1800

    Google Scholar 

  • Costea M, Tardif FJ (2006) Biology of Canadian weeds. Cuscuta campestris Yuncker, C. gronovii Willd. ex Schult., C. umbrosa Beyr. ex Hook., C. epithymum (L.) L. and C. epilinum Weihe. Can J Pl Sci 86:293–316

    Article  Google Scholar 

  • Costea M, Nesom GL, Tardif FJ (2005) Taxonomic status of Cuscuta nevadensis and C. veatchii (Convolvulaceae). Brittonia 57:264–272

    Article  Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006a) Taxonomy of the Cuscuta pentagona complex (Convolvulaceae) in North America. Sida 22:151–175

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006b) Taxonomy of the Cuscuta indecora (Convolvulaceae) complex in North America. Sida 22:209–225

    Google Scholar 

  • Costea M, Nesom GL, Stefanović S (2006c) Taxonomy of the Cuscuta salina-californica complex (Convolvulaceae). Sida 22:176–195

    Google Scholar 

  • Costea M, Aiston F, Stefanović S (2008) Species delimitation, phylogenetic relationships, and two new species in the Cuscuta gracillima complex (Convolvulaceae). Can J Bot 86:670–681

    Article  CAS  Google Scholar 

  • Costea M, Wright MAR, Stefanović S (2009) Untangling the systematics of salt marsh dodders: Cuscuta pacifica a new segregate species from Cuscuta salina (Convolvulaceae). Syst Bot 34:787–795

    Article  Google Scholar 

  • Dafni A, Motte Maués M (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180

    Article  Google Scholar 

  • de Smet I, Chaerle P, Vanneste S, de Rycke R, Inze D, Beeckman T (2004) An easy and versatile embedding method for transverse sections. J Microsc 213:76–80

    Article  PubMed  Google Scholar 

  • Deroin T (1992) Anatomie florale de Humbertia madagascariensis Lam. Contribution à la morphologie comparée de la fleur et du fruit des Convolvulaceae. Adansonia 2:235–255

    Google Scholar 

  • Deroin T (2002) Anatomie florale de Maripa (Convolvulaceae-Erycibeae). Adansonia 24:93–106

    Google Scholar 

  • Deroin T (2004) Anatomie florale comparée de Cardiochlamys et Cordisepalum. Illustration de l’heterobathmie des Convolvulaceae-Cardiochlamyeae. Adansonia 26:199–211

    Google Scholar 

  • Des Moulins C (1853) Etudes organiques sur les cuscutes. Extrait du Compte-rendu de la XIX session (Toulouse) du congres scientifique de France 2:1–180

    Google Scholar 

  • Endress PK (2011) Evolutionary diversification of the flowers in angiosperms. Am J Bot 98:370–396

    Article  PubMed  Google Scholar 

  • Engelmann G (1859) Systematic arrangement of the species of the genus Cuscuta with critical remarks on old species and descriptions of new ones. Trans Acad Sci St Louis 1:453–523

    Google Scholar 

  • Galetto L, Bernardello G (2004) Floral nectaries, nectar production dynamics and chemical composition in six Ipomea species (Convolvulaceae) in relation to pollinators. Ann Bot 94:269–280

    Article  PubMed  CAS  Google Scholar 

  • García MA (2001) A new western Mediterranean species of Cuscuta (Convolvulaceae) confirms the presence of holocentric chromosomes in subgenus Cuscuta. Bot J Linn Soc 135:169–178

    Article  Google Scholar 

  • García MA, Martin MP (2007) Phylogeny of Cuscuta subgenus Cuscuta (Convolvulaceae) based on nrDNA ITS and chloroplast trnL intron sequences. Syst Bot 32:899–916

    Article  Google Scholar 

  • Govil CM (1972) Morphological studies in the family Convolvulaceae. IV. Vascular anatomy of the flower. Proc Ind Acad Sci 75(Sect B):271–282

    Google Scholar 

  • Govil CM, Lavania S (1980) Floral anatomy and embryology of some species of Cuscuta L. Proc Ind Acad Sci (Plant Sci) 89:219–228

    Google Scholar 

  • Hallier H (1893) Versuch einer natürlichen Gliederung der Convolvulaceen auf morphologischer und anatomischer Grundlage. Bot Jahrb Syst 16:453–591

    Google Scholar 

  • Heslop-Harrison Y (1981) Stigma characteristics and angiosperm taxonomy. Nord J Bot 1:401–420

    Article  Google Scholar 

  • Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Ann Bot 41:1233–1258

    Google Scholar 

  • Hintze JL (2007) NCSS 2007: statistical analysis and graphics, user’s Guide. Number Cruncher Statistical Systems, Kaysville, Utah

  • Jayasuriya KMGG, Baskin JM, Geneve RL, Baskin CC (2009) Phylogeny of seed dormancy in Convolvulaceae, subfamily Convolvuloideae (Solanales). Ann Bot 103:45–63

    Google Scholar 

  • Johannsson MH, Stephenson AG (1997) Effects of pollination intensity on the vigor of the sporophytic and gametophytic generation of Cucurbita texana. Sex Plant Reprod 10:236–240

    Article  Google Scholar 

  • Junqueira MER, Simão-Bianchini R (2006) O gênero Evolvulus L. (Convolvulaceae) no município de Morro do Chapéu, BA, Brasil. Acta Bot Bras 20:157–172

    Article  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley

    Google Scholar 

  • Lejoly J, Lisowski S (1982) Le genre Bonamia (Convolvulaceae) au Zaire. Bull Jard Bot Nat Belg 52:133–139

    Article  Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Maddison WP, Donoghue MJ, Maddison DR (1984) Outgroup analysis and parsimony. Syst Zool 33:83–103

    Article  Google Scholar 

  • Martin FW, Ortiz S (1967) Anatomy of the stigma and style of sweet potato. New Phytol 66:109–113

    Article  Google Scholar 

  • McNeal JR, Arumugunathan K, Kuehl JV, Boore JL, de Pamphilis CW (2007) Systematics and plastid genome evolution of the cryptically photosynthetic parasitic plant genus Cuscuta (Convolvulaceae). BMC Biol 5:55

    Article  PubMed  Google Scholar 

  • Miglia KJ, Freeman DC (1996) The effect of delayed pollination on stigma length, sex expression, and progeny sex ratio in spinach, Spinacia oleracea (Chenopodiaceae). Am J Bot 83:326–332

    Article  Google Scholar 

  • Miller RE, Rausher MD, Manos PS (1999) Phylogenetic systematics of Ipomoea (Convolvulaceae) based on ITS and waxy sequences. Syst Bot 24:209–227

    Article  Google Scholar 

  • Myint T (1966) Revision of the genus Stylisma (Convolvulaceae). Brittonia 18:97–117

    Article  Google Scholar 

  • Myint T, Ward DB (1968) A taxonomic revision of the genus Bonamia (Convolvulaceae). Phytologia 17:121–239

    Google Scholar 

  • O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcarphi Pty Ltd, Melbourne

    Google Scholar 

  • Onus AN (2000) Structure of the stigma and style in Capsicum eximium and the effects of pollination. Turk J Bot 24:337–346

    Google Scholar 

  • Ooststroom SJV (1934) A monograph of the genus Evolvulus. Meded Bot Mus Herb Rijks Univ Utrecht 14:1–267

    Google Scholar 

  • Parker C, Riches CR (1993) Parasitic weeds of the world. Biology and control. CAB International, Wallingford

  • Peter A (1891) Convolvulaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien. IV.3.a, Engelmann, Leipzig, pp 1–40

  • Peterson RL, Hersey RE, Brisson JD (1978) Embedding softened herbarium material in Spurr’s resin for histological studies. Stain Tech 53:1–9

    CAS  Google Scholar 

  • Pfeiffer L (1845) Characteristik der in der Gegend von Kassel beobachteten Gattungen und Arten von Cuscuteen. Bot Ztg 3:673–674

    Google Scholar 

  • Plitmann U, Levin DA (1983) Pollen-pistil relationships in the Polemoniaceae. Evolution 37:957–967

    Article  Google Scholar 

  • Prather LA, Tyrl J (1993) The biology of Cuscuta attenuata Waterfall. Proc Okla Acad Sci 73:7–13

    Google Scholar 

  • Prenner G, Deutsch G, Harvey P (2002) Floral development and morphology in Cuscuta reflexa Roxb. (Convolvulaceae). Stapfia 80:311–322

    Google Scholar 

  • Rodriguez-Pontes M (2009) Seed formation and pollination system in Cuscuta obtusiflora: first record of preanthesis cleistogamy in parasitic plants and some functional inferences. Flora 204:228–237

    Article  Google Scholar 

  • Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, Oxford

    Google Scholar 

  • Schols P, D’hondt C, Geuten K, Merckx V, Jamssens S, Smets E (2004) MorphoCode: coding quantitative data for phlyogenetic analysis. PhyloInformatics 4:1–4

    Google Scholar 

  • Snow AA, Spira TP (1996) Pollen-tube competition and male fitness in Hibiscus moscheutos. Evolution 50:1866–1870

    Article  Google Scholar 

  • Staples GW (2006) Revision of Asiatic Poraneae (Convolvulaceae)–Cordisepalum, Dinetus, Duperreya, Porana, Poranopsis, and Tridynamia. Blumea 51:403–491

  • Staples GW, Austin DF (2009) Revision of Neotropical Calycobolus and Porana (Convolvulaceae). Edinb J Bot 66:133–153

    Article  Google Scholar 

  • Stefanović S, Olmstead RG (2004) Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes. Syst Biol 53:384–399

    Article  PubMed  Google Scholar 

  • Stefanović S, Krueger L, Olmstead RG (2002) Monophyly of the Convolvulaceae and circumscription of their major lineages based on DNA sequences of multiple chloroplast loci. Am J Bot 89:1510–1522

    Article  PubMed  Google Scholar 

  • Stefanović S, Austin DF, Olmstead RG (2003) Classification of Convolvulaceae: a phylogenetic approach. Syst Bot 28:791–806

    Google Scholar 

  • Stefanović S, Kuzmina M, Costea M (2007) Delimitation of major lineages within Cuscuta subgenus Grammica (Convolvulaceae) using plastid and nuclear DNA sequences. Am J Bot 94:568–589

    Article  PubMed  Google Scholar 

  • Stuessy TF (2008) Plant taxonomy: the systematic evaluation of comparative data, 2nd edn. Columbia University Press, New York

    Google Scholar 

  • Taylor TN, Levin DA (1975) Pollen morphology of Polemoniaceae in relation to systematics and pollination systems: scanning electron microscopy. Grana 15:91–112

    Google Scholar 

  • Thiele K (1993) The holy grail of the perfect character: the cladistic treatment of morphometric data. Cladistics 9:275–304

    Article  Google Scholar 

  • Tiagi B (1951) A contribution to the morphology and embryology of Cuscuta hyalina and C. planiflora. Phytomorphology 1:9–21

    Google Scholar 

  • Tiagi B (1966) Floral morphology of Cuscuta reflexa Roxb. and C. lupuliformis Krocker with a brief review of the literature on the genus Cuscuta. Bot Mag Tokyo 79:89–97

    Google Scholar 

  • Welsh M, Stefanović S, Costea M (2010) Pollen evolution and its taxonomic significance in Cuscuta (dodders, Convolvulaceae). Plant Syst Evol 285:83–101

    Article  Google Scholar 

  • Wilkin P (1999) A morphological cladistic analysis of the Ipomoeeae (Convolvulaceae). Kew Bull 54:853–876

    Article  Google Scholar 

  • Winsor JA, Davis LE, Stephenson AG (1987) The relationship between pollen load and fruit maturation and the effect of pollen load on offspring vigor in Cucurbita pepo. Am Nat 129:643–656

    Article  Google Scholar 

  • Wottiez RD, Willemse MTM (1979) Sticking of pollen on stigmas, the factors and a model. Phytomorphology 29:57–63

    Google Scholar 

  • Yu Q, Huang SQ (2006) Flexible stigma presentation assists context-dependant pollination in a wild columbine. New Phytol 169:237–242

    Article  PubMed  Google Scholar 

  • Yuncker TG (1932) The genus Cuscuta. Mem Torr Bot Club 18:113–331

    Google Scholar 

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Acknowledgments

The authors would like to thank the curators and directors of the herbaria AAU, ALTA, ARIZ, ASU, B, BAB, BOL, BRIT, CANB, CAS, CEN, CHR, CHSC, CIIDIR, CIMI, CONC, CORD, CTES, DAO, F, G, GH, H, HUFU, IAC, IEB, IND, J, JEPS, LL, LP, LPB, LPS, K, MEL, MERL, MEXU, MICH, MO, NMC, NY, OAC, OKLA, OSC, OXF, PACA, PRE, QCNE, QFA, P, PACA, RB, RSA, SAM, S, SD, SGO, SI, SPF, TEX, TRT, TRTE, UA, UB, UBC, UCR, UCT, UNB, UNM, UPRRP, UPS, US, USAS, WTU, XAL, and ZEA, for supplying plant material. Two anonymous reviewers kindly provided comments and suggestions that improved the quality of the article. We are also grateful to Ignacio García-Ruiz (CIIDIR-IPN, Jiquilpan, Michoacán) for help with field work in Mexico. This research was supported by a Discovery grant from Natural Sciences and Engineering Research Council (NSERC) of Canada to M. Costea (327013-06) and an American Society of Plant Taxonomists Graduate Student Research Grant to M. Wright.

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  1. Department of Biology, Wilfrid Laurier University, Waterloo, ON, N2L 3C5, Canada

    Michael A. R. Wright, Mark Welsh & Mihai Costea

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  1. Michael A. R. Wright
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  2. Mark Welsh
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  3. Mihai Costea
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Correspondence to Mihai Costea.

Electronic supplementary material

Fig. 5 Evolution of stigma surface in Cuscuta. Stigma surface was optimized on to a summary consensus tree resulting from three molecular phylogenies of Cuscuta based on nuclear ITS and plastid trn-LF sequences (García and Martin 2007; Stefanović et al. 2007; Stefanović and Costea, personal communication) Surface area values were coded using Thiele’s (1993) gap weighting method implemented by Morphocode (Schols et al. 2004), with n = 8; lighter branches indicate taxa with low stigma surface area whereas darker grey-black branches indicate taxa with large stigma surface area. Stigmas with a large surface area have evolved more than once and not in association with a particular type of stigma shape or number of styles

Fig. 6 Comparison of abnormal versus normal gynoecia in subg. Grammica. (a, b) C. microstyla var. bicolor. a Gynoecia with one style as a result of an organogenesis abnormality in some flowers on the same individual. This gynoecium resembles those encountered in subg. Monogynella. b Normal gynoecium with two unequal styles. (c, d) C. australis var. tinei. c Abnormal gynoecium with four styles fused in two pairs. d Normal gynoecium with two unequal styles.

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Appendix

Appendix

List of herbarium vouchers examined for stereomicroscopy, vasculature, and SEM; specimens used for anatomy of ovary, stigma, and style anatomy are indicated with an [A]. Taxa (arranged in alphabetical order), country, collector, collector number, herbarium acronym from Index Herbariorum.

Cuscuta acuta Engelm.: Ecuador, Galapagos Islands, Fagerlind & Wibom 3401 (S); Howell 110140 (G); Wheeler et al. 21 (NY); Howell 10048 (KEW). C. acutiloba Engelm.: Bolivia, Mardon 1481 (G); Peru, Weberbauer 7443 (F); Pennell 13242 (S). C. africana Thumb.: South Africa, Beyers 6968 (NBG) [A]; Muir 156 (GRA); Oliver 11852 (NBG) [A]; Durtz 472 (NBG) [A]. C. americana L.: U.S.A., Florida, Small et al. 11596 (NY); Mexico, Felger 4087 (SD); Colombia, Schneider 999 (S); Billberg 61 (S). C. angulata Engelm.: South Africa, Beyers 12-1985 (NBG); Orchard 460 (NU); Williams 2690 (NBG); Williams 3419 (NBG). C. appendiculata Engelm.: South Africa, Hofmeyr s.n. (GAA) [A]; Bohnen 7827 (NBG) [A]. C. applanata Engelm.: U.S.A., New Mexico, Casteller 7339 (UNM); Mexico, Stewart 1038 (F); Lyle & Wind 754 (S). C. approximata Bab.: U.S.A., California, Abrams 457 (CAS) [A]; U.S.A., Nevada, Kennedy s.n. (CAS); Kennedy 16422 (CAS); Utah, Costea & Wright 2009-01 (WLU) [A]. C. argentinana Yunck.: Argentina, Brücher s.n. (S); Krapovickas & Schinini 36049 (CTES). C. aurea Liebm.: Mexico, Palmer 87 (S); Nesom et al. 5949 (F). C. australis R. Br. var. australis: New Caledonia, Bonati 737 (S); China, Sykes 99 (CHR). C. australis var. tinei (Insenga) Yunck.: Hungary, Simonkai 2635 (NY); Karkovány s.n. (WLU). C. bella Yunck.: Peru, Killip & Smith 21827 (US). C. boldinghii Urb.: Mexico, Ramirez-Amezcua & Steinmann 1158 (IEB); Van Devender 92-31 (ARIZ); Provance 3403 (UCR); Breedlove 37373 (NY). C. boliviana Yunck.: Argentina, Hunzinker 2676 (S); Ruiz Leal 14816 (MERL); Burkart 12503 (CTES). C. brachycalyx Yunck.: U.S.A., California, Ahart 9856 (CHICO); Howell 38877 (NY) Colwell & Coulter AC 04-31 (YM). C. burrelli Yunck.: Brazil, Heringer et al. 43 (UB); Alvarenga–Pereira 766 (RB); Dawson 14278 (NY). C. californica Hook. & Arn.: U.S.A., California, Sanders 25122 (UCR); Munz 7689 (RSA); Gregory 1049 (SD). C. campestris Yunck: U.S.A., Oklahoma, Lipscomb 1894 (SMU); Louisiana, Smith s.n. (SMU); Mexico, Pringle 3111 (S). C. cassytoides Nees.: South Africa, Balkwill 6968 (NU); Alexandre 2407 (NBG); Garland s.n. (NY). C. cephalanthi Engelm.: U.S.A., Illinois, McDonald s.n. (NMS); Steyermark 79977 (MO); Washington, Grant s.n. (RSA). C. chapalana Yunck.: Mexico, García-Ruiz 7942 (CIMI); Machuca 8981 (IBUG); García-Ruiz et al. 8064 (WLU) [A]. C. chilensis Ker Gawl.: Chile, Anderson 84-189 (S); Buchtien 446 (S); Valeutey 94 (S); Laudewer 313 (KEW); Muňoz 5169, 5170 (WLU). C. chinensis Lam.: Australia, Carter 628 (CAN). C. cockerellii Yunck: Argentina, Vargas 2600 (CUS); Vargas 19383 (CUS); Nunez 28 (USM). C. colombiana Yunck.: Colombia, Haught 4535 (KEW). C. compacta Juss.: U.S.A., New Jersey, Moldenke & Moldenke 25129 (AAU); South Carolina, Godfrey & Taylor 1326 (CAS); Maryland, Steele 26022 (CAS). C. corniculata Engelm.: Brazil, Stannard et al. 51861 (G); Colombia, Pennell 1453 (GH). C. coryli Engelm.: U.S.A., Arkansas, Demaree 19603 (CAS); Kansas, Morley 747 (SMU); Maryland, Killip 31293 (NY); Michigan, Hanes 548 (NY); Nebraska, Reynolds 2727 (NY); Tennessee, Rydberg 8179 (NY). C. corymbosa Ruiz & Pav. var. grandiflora Engelm.: Mexico, García-Ruiz et al. 7572 (CIMI, WLU); Iltis & Guzman 29077 (MEXU); Martinez 3295 (MEXU); Mendez & de Lopez 9608 (MICH). C. corymbosa var. stylosa (Choisy) Engelm.: Mexico, Rzedowski 28752 (UCR); Borgeau 3353 (S); Bopp 206 (MEXU); Pringle s.n. (MEXU). C. costaricensis Yunck.: Mexico, Van Devender 98-1789 (ARIZ) [A]; Cházaro et al. 7527 (MICH); García-Ruiz et al. 8052 (CIMI, WLU) [A]. C. cotijana Costea & I. García: Mexico, Carranza et al. 7316 (IEB) [A]; García Ruiz et al. 7557 (CIMI, WLU) [A]. C. cozumeliensis Yunck.: Guatemala, Kellerman 6580 (F); Mexico, Calzade & Nievea 9427 (XAL); Vazquez 176 (MEXU). C. cristata Engelm.: Argentina, Burkart 14000 (SI); Balegna 447 (SMU); Hunzinker 4927 (S). C. cuspidata Engelm.: U.S.A., Arkansas, Demaree 15522 (RSA); Indiana, Deam 33011 (IND); Texas, Higgins 12480 (NY); Runyon 2828 (SMU); U.S.A., Kansas, McGregor 15175 (SMU). C. decipiens Yunck.: Mexico, Henrickson 6362, 13394, 22781 (RSA). C. deltoidea Yunck.: Mexico, Orcutt 4457 (F); Pringle 5350 (NMS). C. dentatasquamata Yunck.: Mexico, Jones s.n. (RSA); U.S.A., Arizona, Lemmon s.n. (UC). C. denticulata Engelm.: U.S.A., Arizona, Peebles & Parker 14793 (NY); California, Thomas 8904 (UC); Nevada, Perish 10299 (CAS); Tiehm 13319 (NY). C. desmouliniana Yunck.: Mexico, Spellenberg et al. 4943 (NMC); Rea 1124 (SD); Spellenberg 4943 (NMS); Van Devender & Reina-G 2002-23 (WLU). C. epilinum Weihe: Sweden, Samuelson 1317 (RSA); Canada, Quebec, Barabe 16914 (DAO); Cayouette s.n. (QUE). C. epithymum (L) L.: Argentina, Bana 14733 (CTES); Australia, Clark 107955-212 (RSA) [A]; Belgium, Meulebrouck s.n. (WLU) [A]; Mexico, Pringle 8514 (S); U.S.A., New York, Ahles 67695 (SMU). C. erosa Yunck.: Mexico, Baja California, Rebman 4275 (UCR); Mexico, Van Devender 2001-737 (NMS). C. europea L.: Finland, Alava et al. s.n. (OSU); Sweden, Holmgren 19784 (SD); Netherlands, Hekking 635 (NY). C. exaltata Engelm.: U.S.A., Texas, Snyder 472 (SMU); Carr 12341 (BRIT); Carter 10584 (MO); Westlund s.n. (CAS). C. floribunda Kunth aff.: Mexico, Ugent & Flores 2440 (SMU). C. flossdorfii Hicken var. pampagrandensis Yunck.: Bolivia, Mendoza & Acebo 919 (MO). C. foetida Kunth. var. foetida: Ecuador, Holm-Neilson & Andrado 18480 (AAU); Holm-Neilson et al. 5181 (AAU); Sparre 16952 (AAU). C. foetida var. pycnantha Yunck.: Peru, Plowman et al. 14291 (F). C. friesii Yunck.: Argentina, Krapovickas et al. 21898 (CTES); Mulgura 1245 (SI). C. glabrior (Engelm.) Yunck.: Mexico, Marsh 1115 (SMU); Henrickson 13676 (RSA); U.S.A., Texas, Palmer 9965 (CAS). C. globiflora Engelm.: Argentina, Mulgura et al. 1199 (MO); Bolivia, Plowman & Davis 5196 (GH); Buchtinen 133 (F). C. globulosa Benth.: Puerto Rico, Stahl 1064 (S); Urban 855 (S); Liogier & Oquendo 180 (UPRRP); Cuba, Ekman 7839 (S). C. glomerata Choisy: U.S.A., Texas, Berkley 13886 (RSA); Wolff 3321 (SMU); Indiana, Dean 39229 (NY). C. goyaziana Yunck.: Brazil, Macedo 3731 (S); Duarte & Mattos 8376 (RB). C. gracillima Engelm.: Mexico, Pringle 6716 (NML); Van Devender 2006-160 (WLU) [A]; Vazquez 511 (UCR); García Ruiz 7334 (CIMI, WLU) [A]. C. grandiflora Kunth.: Argentina, Schinini et al. 34615 (CTES); Hunzinker 1899 (S); Ecuador, Løjtnant et al. 11829 (AAU). C. gronovii Willd. ex Roem. & Schult. var. gronovii: U.S.A., Alabama, Kpeooer et al. s.n. (NY) [A]; Georgia, Mellinger s.n. (SMU); U.S.A., Massachusetts, Gates et al. 14841 (SMU); Canada, Ontario, Wright & Bols 2009-05 (WLU) [A]. C. gronovii var. latifolia Engelm.: Missouri, Brant & Donnell 4810 (MO); U.S.A., Texas, Lundell 11721 (SMU); Connecticut, Hill 17037 (NY). C. gymnocarpa Engelm.: Galapagos Islands, Fagerling & Wibon 3658 (S); Werff 2068 (S). C. harperi Small: U.S.A., Alabama, Churchill 861(CAS); Demaree 46295 (NY); Harper 6479 (SMU); Kral 32878 (SMU). C. haughtii Yunck.: Ecuador, Asplund 15974 (S); Venezuela, Asplund 5618 (F). C. howelliana Rubtzoff: U.S.A., California, True 7407 (DS); Oswald & Ahart 7645 (CHSC). C. hyalina Roth.: India, Pushpauder s.n. (CANB); Namibia, Bosch 25022 (BOL); South Africa, Bosch 25022 (BOL). C. incurvata Prog.: Paraguay, López et al. 243 (CTES); Anisits 2395 (S); Hassler 8170 (S). C. indecora Choisy var. indecora U.S.A., Arizona, Austin 7599 (RSA); U.S.A., Louisiana, Allen 19239 (BRIT); California, Munz 12736 (CAS); Arkansas, Demaree 18050 (CAS). C. indecora var. attenuata (Waterf.) Costea: U.S.A., Oklahoma, Waterfall 17496 (GH); Texas, Whitehouse 16472 (SMU); Mexico, Palmer 333 (F). C. indecora var. longisepala Yunck.: Argentina, Leal 7964 (NY); Burkart s.n. (KEW); U.S.A., Colorado, Ewan 15327 (CAS); Texas, Runyon 2819 (NY). C. jalapensis Schltdl.: Mexico, Waterfall & Wallis 14213 (SMU); Miller 11561 (MEXU); García-Ruiz et al. 7569 (CIMI, WLU). C. japonica Choisy: China, Bartholomew et al. 883 (NY) [A]; Hill 22616 (MO); Japan, Furuse 6890 (RSA) [A]; Brooks 322 (NY) [A]; U.S.A. South Carolina, Hill 20079 (BRIT) [A]. C. jepsonii Yunck.: U.S.A., California, Dudley 1774 (DS); Tracy 2349 (UC). C. killimanjari Oliv.: Malawi, Lacroix 4559 (MO); Tanzania, Scheffler 434 (MEL); Zimbabwe, Eyles 352 (J). C. legitima Costea and Stefanović: U.S.A., Arizona, Felger 92-707 (CAS); Spellenberg 12966 (NMS); Mexico, Jones 22633 (UCR), Mexico, Van Devender & Reina-G. 2006-638 (WLU). C. lehmanniana Bunge.: Usbekistan, Vvedensky s.n. (MEL); Drobov 3763 (NY); India, Stewart 21103 (NY); Uzbekistán, Budogoski 817 (NY). C. leptantha Engelm.: Mexico, Wiggins 17125 (MEXU); Lindsay 2928 (SD); Dominguez 3472 (SD); Moran 8669 (SD); Van Devender 2000-933 (WLU); Wiggins 13153 (SD). C. lindsayi Wiggins: Mexico, Wiggins 13185 (MO); García-Ruiz et al. 7569 (CIMI, WLU). C. longiloba Yunck.: Paraguay, Casas & Molero 4384 (MO); Bolivia, Krapovickas & Schinini 13255 (F). C. lucidicarpa Yunck. Peru, Pennell 15067 (GH); Killip & Smith 21858 (US); Killip & Smith 21909 (NY). C. lupuliformis Krock.: Austria, Barta 2004-302 (NY); Netherlands, Lennhouts 2514 (CANB); Hungary, Degen s.n. (RSA); China, Bartholomew et al. 883 (RSA). C. macrocephala W. Schaffn. ex Yunck.: Mexico, Rebman 5743 (SD); Van Devender & Reina-G 2006-872 (WLU); Carter et al. 2186 (F); Moran 18810 (SD). C. mcvaughii Yunck.: Mexico, Hinton et al. 12098 (G). C. micrantha Choisy: Chile, Phillippi 489 (G); Skottsberg 995 (F). C. microstyla Engelm. var. bicolor Hunz.: Argentina, Boelcke et al. 10243 (CTES); Burkart et al. 6968 (SI). C. mitriformis Engelm.: Mexico, Bye 50488 (UCR); Bye 2011 (MEXU); Carranza 5658 (IEB); Moore & Wood 4329 (MICH). C. monogyna Vahl.: Grece, Greuter 11459 (NY); Turkmenistan, Sintenis 1240 (MO); Vietnam, Kung 2024 (NY). C. natalensis Baker: South Africa, Rudatis s.n. (NBG); Rudatis 2412 (NBG). C. nevadensis I.M. Johnst.: U.S.A., California, Raven 12865 (CAS); Peebles 263 (NY); Twisselmann 16318 (CAS); Nevada, Brandegee s.n. (UC), LaRivers & Hancock 164 (NY). C. nitida E. Mey.: South Africa, Compton 15500 (NBG) [A]; Edwards 13 (J); Rogers 17342 (J); Taylor s.n. (NBG) [A]. C. obtusiflora Kunth var. obtusiflora: Argentina, Arbo et al. 7973 (CTES); Bordódon s.n. (CTES). C. obtusiflora var. glandulosa Engelm.: Mexico, Jalisco, García-Ruiz 7752 (WLU) [A]; U.S.A., Texas, Clare 2144 (CAS); Lundell & Lundell 11717 (NY); U.S.A., Delaware, collector illegible (“MC”) s.n. (CAS). C. occidentalis Millsp.: U.S.A., California, Howell 48868 (CAS); Ertter 7326 (NY); Schoolcraft et al. 2220 (NY); Nevada, Tiehm 12257 (NY); Utah, Garrett 2170 (NY). C. odontolepis Engelm.: Mexico, White 2730 (GH); Palmer 412 (F); Van Devender 2006-869 (WLU). C. odorata Ruiz & Pav.: Ecuador, Jaramillo 10372 (AAU); Asplund 7737 (S); Peru, Hitchcock 20320 (GH); Ugent & Ugent 5323 (MO). C. orbiculata Yunck.: Brazil, Alvaregna 93605 (RB); Harley et al. 21452 (AAU). C. ortegana Yunck.: Mexico, Hinton et al. 16294 (MICH); Van Devender et al. 2006-74 (WLU). C. pacifica Costea & Wright: U.S.A., Canada, Kennedy & Ganders 4947 (UBC); U.S.A., California, Dudley 267 (CAS); Eastwood 7971 (CAS); Moldenke 25731 (NY). C. paitana Yunck.: Ecuador, Madsen 63940 (AAU); Peru, Horton 11575 (GH). C. parodiana Yunck.: Argentina, Eyerdam 22423 (MO); Novara 7976 (S); Balegno 447 (SMU); Krapovickas 35879 (G); Novara 7976 (S). C. partita Choisy: Brazil, Eiten & Eiten 3961 (US); Krapovickas et al. 38723 (CTES); Lindman 3481 (S). C. parviflora Engelm. var. elongata Engelm.: Brazil, Filgueiras 1476 (RB); Filgueiras et al. 745 (RB). C. pentagona Engelm.: U.S.A., Alabama, Kral 31225 (SMU); District of Colombia, Buettcher 122 (CAS); Florida, Welch 1633 (NY); Virginia, Herman 10391 (NY). C. planiflora Ten.: Australia, Easkins s.n. (WLU); Howitt & Zaicon-Kunesch s.n. (PERTH); Palestina, Musselman 10461 (RSA); Dorn 5420 (NY). C. plattensis A. Nelson: U.S.A., Wyoming, Nelson 2768 (NY); Nelson 2741 (MO). C. platyloba Prog.: Argentina, Burkart 10554 (CTES); Krapovickas 2911 (KEW); Burkart 14250 (SI); Brazil, Dusen 10005 (S); Paraguay, Montes 16599 (CTES). C. polyanthemos Schaffn. ex Yunck.: Mexico, Wiggins 13153 (SD); Van Devender 2006-809 & Reina (WLU). C. potosina Schaffn. ex Yunck.: var. potosina: Mexico, Rose et al. 9650 (GH); Schaffner 379 (MEXU), Rzedowski 3894 (MEXU). C. potosina var. globifera W. Schaffn.: Mexico, Pringle 6575 (S); Van Devender et al. 96-451 (WLU); U.S.A., Arizona, Gooding 290-61 (ASU). C. prismatica Pav. ex Choisy: Ecuador, Mille 112 (F); Peru, Pilger et al. s.n. (F). C. punana Costea & Stefanović: Ecuador, Madsen 63850 (AAU). C. purpurata Phil.: Chile, Johnston 5170 (S); Werdermann 852 (S); Rechinger 63509 (B). C. purpusii Yunck.: Mexico, Hendrickson 6608 (RSA); Meyer & Rogers 2878 (UPS). C. racemosa Mart. var. racemosa: Brazil, Hatschbach 64867 (KEW); Pinheiro 55 (SPF); Smith et al. 14478 (F). C. racemosa var. miniata (Mart.) Engelm.: Brazil, Menezes et al. 5100 (CTES); Richon 7835 (S); Arbo et al. 5100 (KEW); Cordeiro et al. 8211 (KEW). C. reflexa Roxb.: India, Cullelt s.n. (MEL) [A]; Kanta s.n. (ASU); Koelz 21955 (NY) [A]. C. rostrata Shuttlw. ex Engelm. & A. Gray: U.S.A., North Carolina, Bozeman et al. 45268 (OSU); Tennessee, Churchill 93217 (CAS); Jennison 2824 (NY); Texas, Lundell 11480 (SMU). C. rugosiceps Yunck.: Mexico, Taylor 21457 (SMU); Lindres 4285 (MEXU); Guatemala, Williams et al. 21950 (NY). C. runyonii Yunck.: U.S.A., Texas, Lundell 9840 (SMU); Runyon 2622 (BRIT); Lundell 9827 (SMU). C. salina Engelm.: U.S.A., Arizona, Hammond 10349 (NY); California, Raven 878 (CAS); Nevada, Tiehm 5991 (CAS). C. sandwichiana Choisy: U.S.A., Hawaii, Stern 8416 (CHICO); Fosberg 14019 (RSA). C. santapaui Banerji & Sitesh Das: Nepal, Nicolson 2796 (MO). C. serrata Yunck.: Brazil, Acevedo & Lopes 848 (RB); Acevedo 757 (RB); Glaziou 21811 (F). C. sidarum Liebm.: Mexico, Palmer 51 (S); Standley 12359 (S); Stevens 20910 (RSA). C. squamata Engelm.: U.S.A., New Mexico, Wooton & Standley 3355 (CAS); Wooton 1894 (S); Texas, Gould 7114 (SMU). C. stenolepis Engelm.: Ecuador, Jaramillo & Caravajal 2307 (AAU); Neilson & Coello 29084 (AAU); Asplund 6678 (S); Tipaz 4636 (MO). C. strobilacea Liebm.: Mexico, Jones s.n. (RSA); Croat & Hannon 65094 (MEXU); Jones 27347 (MICH), Garcìa Ruiz 8071 (WLU) [A]. C. suaveolens Ser.: Australia, Alcock 10415 (RSA); Chile, Eyerdam 24649 (KEW); U.S.A., California, Abrams s.n. (RSA); Dudley s.n. (CAS). C. subinclusa Durand & Hilg.: U.S.A., California, Dudley 1653 (DS); Ewan 11049 (NY); Mason 5766 (NY); Rose 39363 (NMS). C. suksdorfii Yunck.: U.S.A., California, Twisselmann 14603 (SD); Oswald & Ahart 5874 (CHICO); Tracy 18430 (UC); Colwell AC05-213 (UC). C. tasmanica Engelm.: Australia, Barker s.n. (CANB); Walsh 3045 (MEL); Lepschi 909 (MEL). C. tinctoria Mart. ex Engelm.: Mexico, Palmer 87 (S); García Ruiz et al. 7575 (CIMI, WLU); Ventura 4248 (IEB); Rzdowski 34596 (IEB); Van Devender 94-1008 et al. (WLU). C. tuberculata Brandegee: U.S.A., Arizona, Beauchamp 3112 (SD); Mexico, Waterfall 12842 (SMU); Rebman 7638 (SD); Reina 2000-465 (WLU). C. umbellata Kunth: Mexico, Moran 24758 (SD); Nabhan & Rea 167 (ARIZ); U.S.A., Texas, Bernal 37 (SMU); New Mexico, Spellenberg 2902 (NMS). C. umbrosa Beyr. ex Hook.: Canada, Alberta, Allen 150 (DAO); Manitoba, Criddle s.n. (DAO); U.S.A., Utah, Jones s.n. (CAS); Colorado, Jones 571 (RSA); Mulford s.n. (NY). C. veatchii Brandegee: Mexico, Rebman 3189 (SD); Porter 198 (MEXU). C. victoriana Yunck.: Australia, Cowie 9624 (CANB); Glennon 379 (CANB); Lazarides & Palmer 471 (CANB). C. warneri Yunck.: U.S.A., New Mexico, Spellenberg 13890 (WLU); Utah, Warner s.n. (NY). C. werdermanii Yunck.: Chile, Werdermann 880 (SGO). C. woodsonii Yunck.: Guatemala, Heyde et al. 2912 (KEW); Brenckle 47-269 (S); Panama, Davidson 967 (GH). C. xanthochortos Mart. ex Engelm. var. xanthochortos: Argentina, Arbo et al. 6953 (MO); Paraguay, Zardini & Vera 46124 (MO). C. xanthochortos var. carinata Yunck.: Paraguay, Billiet & Jodin 3294 (MO); Bernardi 18758 (MO). C. xanthochortos var. lanceolata Yunck.: Argentina, Schulz 7139 (CTES); Paraguay, Zardini & Villate 46371 (WLU); Jorgensen 3478 (S) . C. yucatana Yunck.: Mexico, Rzedowski 25728 (IEB); Steere 1695 (MICH).

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Wright, M.A.R., Welsh, M. & Costea, M. Diversity and evolution of the gynoecium in Cuscuta (dodders, Convolvulaceae) in relation to their reproductive biology: two styles are better than one. Plant Syst Evol 296, 51–76 (2011). https://doi.org/10.1007/s00606-011-0476-5

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