Plant Systematics and Evolution

, Volume 295, Issue 1–4, pp 23–54 | Cite as

Molecular systematics, character evolution, and pollen morphology of Cistus and Halimium (Cistaceae)

  • Laure Civeyrel
  • Julie Leclercq
  • Jean-Pierre Demoly
  • Yannick Agnan
  • Nicolas Quèbre
  • Céline Pélissier
  • Thierry Otto
Original Article


Pollen analysis and parsimony-based phylogenetic analyses of the genera Cistus and Halimium, two Mediterranean shrubs typical of Mediterranean vegetation, were undertaken, on the basis of cpDNA sequence data from the trnL-trnF, and trnS-trnG regions, to evaluate limits between the genera. Neither of the two genera examined formed a monophyletic group. Several monophyletic clades were recognized for the ingroup. (1) The “white and whitish pink Cistus”, where most of the Cistus sections were present, with very diverse pollen ornamentations ranging from striato-reticulate to largely reticulate, sometimes with supratectal elements; (2) The “purple pink Cistus” clade grouping all the species with purple pink flowers belonging to the Macrostylia and Cistus sections, with rugulate or microreticulate pollen. Within this clade, the pink-flowered endemic Canarian species formed a monophyletic group, but with weak support. (3) Three Halimium clades were recovered, each with 100% bootstrap support; all Halimium species had striato-reticulate pollen. Two Halimium clades were characterized by yellow flowers, and the other by white flowers.


TrnL-F TrnS-G Pollen Exine Cistaceae Cistus Halimium 



We are most grateful to curators or keepers of the herbaria G, K, MPU, and P for permitting the examination of specimens and removal of pollen samples. We should like to thank Peter Biggins from CIRAD for revising the English, and also all colleagues of the palynology unit at the R. B. G. Kew for their assistance, the Conservatoire Botanique National de Brest and Robert Page for their help, and Olivier Filippi for cultivating our plants collected on field trips, especially from Morocco and the Canary Islands. We also wish to thank Elise Van Campo, Laurent Chibret, and Renaud Lahaye for their support.


  1. Alverson WS, Karol KG, Baum DA, Chase MW, Swensen SM, Mccourt R, Sytsma KJ (1998) Circumscription of the Malvales and relationships to other Rosidae: evidence from rbcL sequence data. Am J Bot 85:876–887PubMedCrossRefGoogle Scholar
  2. Arrington JM, Kubitzki K (2003) Cistaceae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants. Malvales, Capparales and non-betalain Caryophyllales, vol 5. Springer, BerlinGoogle Scholar
  3. Ball J (1877) Spicilegium Florae Marocannae. J Linn Soc Bot 16:343–348CrossRefGoogle Scholar
  4. Bañares Á, Blanca G, Güemes J, Moreno JC, Ortiz S (eds) (2008) Atlas y Libro Rojo de la Flora Vascular Amenazada de España. Adenda 2008. Dirección General de Medio Natural y Política Forestal (Ministerio de Medio Ambiente, y Medio Rural y Marino-Sociedad Española de Biología de la Conservación de Plantas). MadridGoogle Scholar
  5. Barquín-Diez E, Voggenreiter V (1988) Prodromus del atlas fitocorológico de las Canarias occidentales. Parte I: Flora autóctona y especies de interés generalGoogle Scholar
  6. Batista F, Bañares A, Caujapé-Castells J, Carqué E, Marrero-Gómez M, Sosa PA (2001) Allozyme diversity in three endemic species of Cistus (Cistaceae) from the Canary Islands: intraspecific and interspecific comparisons and implications for genetic conservation. Am J Bot 88:1582–1592PubMedCrossRefGoogle Scholar
  7. Bayer C, Chase MW, Fay MF (1998) Muntingiaceae, a new family of dicotyledons with malvalean affinities. Taxon 47:37–42CrossRefGoogle Scholar
  8. Borsch T, Quandt D (2009) Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Syst Evol 282:169–199CrossRefGoogle Scholar
  9. Civeyrel L, Le Thomas A, Ferguson IK, Chase MW (1998) Critical reexamination of palynological characters used to delimit Asclepiadaceae in comparison to the molecular phylogeny obtained from plastid matK sequences. Mol Phylogenet Evol 9:517–527PubMedCrossRefGoogle Scholar
  10. Clegg MT, Zurawski G (1992) Chloroplast DNA and the study of plant phylogeny: present status and future prospects. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, pp 1–13Google Scholar
  11. Dansereau P (1939) Monographie du genre Cistus. Boissiera 4:1–90Google Scholar
  12. Dansereau P (1940) Études sur les hybrides de Cistes. Ann Épiphyt 6 (Ser. 2):7–26Google Scholar
  13. Dansereau P (1941) Etudes sur les hybrides de cistes—IV. Corrélation des caractères du C. salviifolius L: VI. Introgression dans la section Ladanium. Anim Biodivers Conserv 38:59–67Google Scholar
  14. Demoly JP (1996) Les hybrides binaires rares du genre Cistus L. (Cistaceae). Anales Jard Bot Madrid 54:241–254Google Scholar
  15. Demoly JP (1998) Notes taxonomiques sur le nothogenre × Halimiocistus Janch. (Cistaceae). J Bot Soc Bot France 6:31–38 (× Halimiocistus humilis Demoly)Google Scholar
  16. Demoly JP (2004) Description d une espèce confondue dans le passé avec Cistus symphytifolius Lam. et, parfois, avec C. ocreatus Chr. Sm. Acta Bot Gallica 151:231–232Google Scholar
  17. Demoly JP, Montserrat P (1993) Cistus. In: Castroviejo S et al (eds) Flora Iberica, vol 3, pp 319–337. Consejo de Investigaciones Cientifícas, MadridGoogle Scholar
  18. Dercourt J, Bassoullet JP, Baud A, Butterlin J, Camoin G, Cavelier C, Cecca F, Enay R, Fourcade E, Guiraud R, Lorenz C, Marcoux J, Masse JP, Orszag F, Philip J (1992) Paeloenvironmental atlas of the Tethys from Permian to recent. In: 29th International geological congress, Kyoto, JapanGoogle Scholar
  19. Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, pp 14–35Google Scholar
  20. Emerson BC (2003) Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria. Anim Biodivers Conserv 26:707–716Google Scholar
  21. Erdtman G (1943) An introduction to pollen analysis. Waltham, MassachusettsGoogle Scholar
  22. Erdtman G (1952) Pollen morphology and plant taxonomy, angiosperms. Almqvist and Wiksell, StockholmGoogle Scholar
  23. Erdtman G (1960) The acetolysis method. A revised description. Svensk Bot Tidskr 54:561–564Google Scholar
  24. Falchi A, Paolini J, Desjobert JM, Melis A, Costa J, Varesi L (2009) Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL-F and rpl32-trnL sequences of cpDNA. Mol Phylogenet Evol 52:538–543Google Scholar
  25. Farris JS (1969) A successive approximations approach to character weighting. Syst Zool 18:374–385CrossRefGoogle Scholar
  26. Fennane M, Ibn Tattou M, Mathez J, Ouyahya A, El Oualidi J (eds) (1999) Flore Pratique du Maroc, vol 1. Trav Inst Sci 36:I–XVGoogle Scholar
  27. García-Talavera F (1999) La Macaronesia. Consideraciones geológicas, biogegráficas y paleoecológicas. In: Fernández-Palacios JM, Bacallado JJ, Belmonte JA (eds) Ecología y cultura en Canarias, 39–64. Museo de la Ciencia, Cabildo Insular de Tenerife, Santa Cruz de Tenerife, Canary Islands, SpainGoogle Scholar
  28. Gaskin JF, Schaal BA (2003) Molecular phylogenetic investigation of US invasive Tamarix. Syst Bot 28:86–95Google Scholar
  29. Grant OM, McNeilly T, Incoll LD (2006) Genetic diversity of Cistus albidus in south-east Spain does not relate to mesoclimate. Funct Pl Biol 33:247–255CrossRefGoogle Scholar
  30. Greuter W, Raus T (2000) Med-Checklist Notulae, 19. Willdenowia 30:232Google Scholar
  31. Greuter W, Burdet HM, Long G (1984) Med Checklist. A critical inventory of vascular plants of the circum-Mediterranean countries. Conservatoire et Jardin Botanique de la Ville de Genève, GenèveGoogle Scholar
  32. Grosser W (1903) Cistaceae. In: Engler A (éd) Das Pflanzenreieh, Regni vegetabilis conspectus. vol 14, p 161Google Scholar
  33. Guzmán B, Vargas P (2005) Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnL-trnF, and matK sequences. Mol Phylogenet Evol 37:644–660Google Scholar
  34. Guzmán B, Vargas P (2009) Historical biogeography and character evolution of Cistaceae (Malvales) based on analysis of plastid rbcL and trnL-trnF sequences. Org Divers Evol 9:83–99Google Scholar
  35. Guzmán B, Lledó MD, Vargas P (2009) Adaptive radiation in mediterranean Cistus (Cistaceae). PLoS ONE 4(7):e6362. doi: 10.1371/journal.pone.0006362
  36. Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523PubMedGoogle Scholar
  37. Hesse M, Halbritter H, Zetter R, Weber M, Buchner R, Frosch-Radivo A, Ulrich S (2009) Pollen terminology. An illustrated handbook, VI. Springer, WienGoogle Scholar
  38. Heydacker F (1963) Les types polliniques de la famille des Cistaceae. Pollen Spores 5:41–50Google Scholar
  39. Hoernle K, Tilton G, Schminke HU (1991) Sr–Nd–Pb isotopic evolution of Gran Canaria: evidence for shallow enriched mantle beneath the Canary Islands. Earth Planet Sci Lett 106:44–63CrossRefGoogle Scholar
  40. Iversen J, Troels Smith J (1950) Pollenmorfologiske definitioner og typer. Danmarks Geol Unders 3:1–54Google Scholar
  41. Janchen E (1925) Cistaceae. In: Engler A, Prantl K (eds) Die Naturlichen Pflanzenfamilien, 2nd edn., Bd. 21:289–313. W Engelmann, LeipzigGoogle Scholar
  42. Jean MT, Pons A (1962) Une clef de détermination palynologique pour les Cistacées de la flore de France. Naturalia MonspFasc 14:87–92Google Scholar
  43. Jean MT, Pons A (1963) Contibution à l’étude palynologique des Cistacées de la flore de France. Ann Sci Nat Bot Paris 4:159–204Google Scholar
  44. Jiménez-Albarrán MJ (1984) Estudio palinologico del Genero Halimium (Dun.) Spach (Cistaceae). Anal Asoc Pal Lengua Esp 1:21–29Google Scholar
  45. Kress WJ, Prince LM, Williams KJ (2002) The phylogeny and a new classification of the gingers (Zingiberaceae): evidence from molecular data. Am J Bot 89:1682–1696PubMedCrossRefGoogle Scholar
  46. Lahaye R, Klackenberg J, Källersjö M, Van Campo E, Civeyrel L (2007) Phylogenetic relationships within Secamonoideae (Apocynaceae s.l.) based on four chloroplast sequences. Ann Mo Bot Gard 94:378–396CrossRefGoogle Scholar
  47. Márquez J, Diaz-Losada E, Rodríguez-Gracia V, Suàrez-Cervera M (1996) Cistaceae. In: Atlas de Polen de Galicia, pp 113–127, OurenseGoogle Scholar
  48. Marrero-Rodríguez Á, Almeida R, Ríos C (2008) Cistus grancanariae sp. nov. (Cistaceae) una nueva especie para Gran Canaria (Islas Canarias). Bot Macaronésica 27:73–88Google Scholar
  49. Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the mediterranean basin. Ann Mo Bot Gard 84:112–127CrossRefGoogle Scholar
  50. Moreno JC (coord) (2008) Lista Roja 2008 de la flora vascular española. Dirección General de Medio Natural y Política Forestal (Ministerio de Medio Ambiente, y Medio Rural y Marino, y Sociedad Española de Biología de la Conservación de Plantas), MadridGoogle Scholar
  51. Mort ME, Archibald JK, Randle CP, Levsen ND, O’Leary TR, Topalov K, Wiegand CM, Crawford DJ (2007) Inferring phylogeny at low taxonomic levels: utility of rapidly evolving cpDNA and nuclear ITS loci. Am J Bot 94:173–183PubMedCrossRefGoogle Scholar
  52. Nandi OI (1998) Floral development and systematics of Cistaceae. Plant Syst Evol 212:107–134CrossRefGoogle Scholar
  53. Olson ME (2002) Intergeneric relationships within the Caricaceae-Moringaceae clade (Brassicales) and potential morphological synapomorphies of the clade and its families. Int J Plant Sci 163:51–65CrossRefGoogle Scholar
  54. Palacios-Chávez R, Quiroz-García DL, Arreguín-Sánchez MDLL (1999) Morfología de los granos de polen de la familia Cistaceae de México. Acta Botanica Mexicana 49:1–14Google Scholar
  55. Paolini J, Falchi A, Quilichini Y, Desjobert JM, Cian MC, Varesi L, Costa J (2009) Morphological, chemical and genetic differentiation of two subspecies of Cistus creticus L. (C. creticus subsp. eriocephalus and C. creticus subsp. corsicus). Phytochemistry 70:1146–1160PubMedCrossRefGoogle Scholar
  56. Punt W, Blackmore S, Nilsson S, Le Thomas A (1994) Glossary of pollen and spore terminology. LPP Foundation (Laboratory of Paleobotany and Palynology), UtrechtGoogle Scholar
  57. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynology 143:1–81CrossRefGoogle Scholar
  58. Quandt D, Müller K, Stech M, Hilu KW, Frey W, Frahm JP, Borsch T (2004) Molecular evolution of the chloroplast trnL-F region in land plants. Monogr Syst Bot Mo Bot Gard 98:13–37Google Scholar
  59. Raynaud C (1992) Cistaceae. In: Fennane M, Mathez J (eds) Elements pour la Flore pratique du Maroc. Naturalia Monsp, sér. Bot. 56:154–158, 171–220Google Scholar
  60. Reille M (1990) Leçons de Palynologie et d’Analyse pollinique. Editions du CNRS, ParisGoogle Scholar
  61. Saenz De Rivas C (1979) Pollen morphology of Spanish Cistaceae. Grana 18:91–98CrossRefGoogle Scholar
  62. Shaw J, Lickey EB, Beck JT, Farmer SB, Liu WS, Miller J, Siripin KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166PubMedCrossRefGoogle Scholar
  63. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288Google Scholar
  64. Swofford DL (2002) PAUP: phylogenetic analysis using parsimony. Version 4.0b10 for Macintosh. Sinauer Associates, SunderlandGoogle Scholar
  65. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of the chloroplast DNA. Pl Mol Biol 17:1105–1109CrossRefGoogle Scholar
  66. Tan K, Iatrou G (2001) Endemic plants of Greece—the Peloponnese (Halimium voldii). Gads Forlag, Copenhagen, pp 215–217Google Scholar
  67. Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (1968) Flora Europaea, vol 2. Rosaceae to Umbelliferae. Cambridge University Press, CambridgeGoogle Scholar
  68. Ukraintseva VV (1991) The palynological study of the genus Cistus (Cistaceae). Bot J (St. Peterburg). 76:969–985Google Scholar
  69. Ukraintseva VV (1993) Pollen morphology of the family Cistaceae in relation to its taxonomy. Grana 2:33–36CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Laure Civeyrel
    • 1
  • Julie Leclercq
    • 2
  • Jean-Pierre Demoly
    • 3
  • Yannick Agnan
    • 1
  • Nicolas Quèbre
    • 4
  • Céline Pélissier
    • 1
  • Thierry Otto
    • 1
  1. 1.Laboratoire Ecologie Fonctionnelle et EnvironnementUniversité de ToulouseToulouse Cedex 9France
  2. 2.UMR DAP, CIRADMontpellier Cedex 5France
  3. 3.APBFParisFrance
  4. 4.ETH Zentrum, IBZZurichSwitzerland

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