Biochemical Genetics

, Volume 56, Issue 4, pp 315–340 | Cite as

Phylogeography of the Macaronesian Lettuce Species Lactuca watsoniana and L. palmensis (Asteraceae)

  • Elisabete F. Dias
  • Norbert Kilian
  • Luís Silva
  • Hanno Schaefer
  • Mark Carine
  • Paula J. Rudall
  • Arnoldo Santos-Guerra
  • Mónica Moura
Original Article


The phylogenetic relationships and phylogeography of two relatively rare Macaronesian Lactuca species, Lactuca watsoniana (Azores) and L. palmensis (Canary Islands), were, until this date, unclear. Karyological information of the Azorean species was also unknown. For this study, a chromosome count was performed and L. watsoniana showed 2n = 34. A phylogenetic approach was used to clarify the relationships of the Azorean endemic L. watsoniana and the La Palma endemic L. palmensis within the subtribe Lactucinae. Maximum parsimony, Maximum likelihood and Bayesian analysis of a combined molecular dataset (ITS and four chloroplast DNA regions) and molecular clock analyses were performed with the Macaronesian Lactuca species, as well as a TCS haplotype network. The analyses revealed that L. watsoniana and L. palmensis belong to different subclades of the Lactuca clade. Lactuca watsoniana showed a strongly supported phylogenetic relationship with North American species, while L. palmensis was closely related to L. tenerrima and L. inermis, from Europe and Africa. Lactuca watsoniana showed four single-island haplotypes. A divergence time estimation of the Macaronesian lineages was used to examine island colonization pathways. Results obtained with BEAST suggest a divergence of L. palmensis and L. watsoniana clades c. 11 million years ago, L. watsoniana diverged from its North American sister species c. 3.8 million years ago and L. palmensis diverged from its sister L. tenerrima, c. 1.3 million years ago, probably originating from an African ancestral lineage which colonized the Canary Islands. Divergence analyses with *BEAST indicate a more recent divergence of the L. watsoniana crown, c. 0.9 million years ago. In the Azores colonization, in a stepping stone, east-to-west dispersal pattern, associated with geological events might explain the current distribution range of L. watsoniana.


Azores Canary Islands Divergence time Karyology Lactuca Macaronesia Molecular clock Phylogeography Phylogeny 



We are grateful to Graciete Belo Maciel, José Martins, Fred Rumsey and Orlanda Moreira for collecting some of the samples. We thank the curators of the herbaria of Museu Carlos Machado (AZ), Ruy Telles Palhinha—Universidade dos Açores (AZB), Universidade dos Açores (AZU), Natural History Museum in London (BM), Royal Botanic Gardens Kew (K), Estação Agronómica Nacional (LISE), Muséum National d’ Histoire Naturelle, Paris–France (P), as well, and to the staff of the molecular laboratories at the Natural History Museum in London and Royal Botanic Gardens, Kew, and also Monika Lüchow at the morphological laboratories of Botanic Garden and Botanical Museum of Berlin-Dahlem. Relevant fieldwork permission was obtained, permit numbers: 77/2012/DRA; 63/2013/DRA; 70/2014/DRA; CCPI:032/2013; CCPI:028/2014.


This study was funded by Fundo Regional da Ciência (M3.1.2/F/032/2011) and FEDER funds through the Operational Programme for Competitiveness Factors—COMPETE and by National Funds through FCT—Foundation for Science and Technology under the UID/BIA/50027/2013; POCI-01-0145-FEDER-006821, and also received support from FCT - Foundation for Science and Technology (SFRH/BSAB/1165/2011FCT) and of SYNTHESYS Project (GB-TAF-2363), which is financed by European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area” programme.

Compliance with ethical standards

Permits were obtained from the environmental authorities for plant collection, and samples only included leaves and not complete individuals, particularly in the case of the rare Lactuca watsoniana

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10528_2018_9847_MOESM1_ESM.pdf (452 kb)
Supplementary material 1 (PDF 452 kb)
10528_2018_9847_MOESM2_ESM.pdf (281 kb)
Supplementary material 2 (PDF 280 kb)
10528_2018_9847_MOESM3_ESM.pdf (402 kb)
Supplementary material 3 (PDF 402 kb)
10528_2018_9847_MOESM4_ESM.pdf (290 kb)
Supplementary material 4 (PDF 290 kb)
10528_2018_9847_MOESM5_ESM.pdf (236 kb)
Supplementary material 5 (PDF 235 kb)
10528_2018_9847_MOESM6_ESM.pdf (1.1 mb)
Supplementary material 6 (PDF 1101 kb)


  1. Acebes-Ginovés JR, Garcia A, León Arencibia MC, Rodríguez-Navarro ML, Aguilar MJDA, Gallo AG, Pérez de Paz PL, Delgado OR, Osório VEM, La Torre WW (2010) Pteridophyta, Spermatophyta. In: Arechavaleta M, Rodríguez S, Zurita N, García A (eds) Lista de especies silvestres de Canarias (hongos, plantas y animales terrestres). Gobierno de Canarias, Canary Island, pp 119–172Google Scholar
  2. Ávila SP, Melo C, Berning B, Cordeiro R, Landau B, da Silva CM (2016) Persististrombus coronatus (Mollusca: Strombidae). in the early Pliocene of Santa Maria Island (Azores: NE Atlantic).: palaeoecology, palaeoclimatology and palaeobiogeographic implications on the NE Atlantic Molluscan Biogeographical Provinces. Palaeogeogr Palaeoclimatol Palaeoecol 441:912–923CrossRefGoogle Scholar
  3. Azevedo J (1998) Geologia e Hidrogeologia da Ilha das Flores (Açores—Portugal). PhD Thesis, Universidade de CoimbraGoogle Scholar
  4. Bateman RM, Rudall PJ, Moura M (2013) Systematic revision of Platanthera in the Azorean archipelago: not one but three species including arguably Europe’s rarest orchid. PeerJ 1:e218CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bolle CKA, Seemann EG, Seemann B (1859) Bonplandia- Zeitschrift für die gesammte Botanik: Officielles Organ der KL-C. Akademie der Naturforscher, vol 7. Carl Rümpler, Paris, p 298Google Scholar
  6. Borges Silva L, Sardos J, Menezes de Sequeira M, Silva L, Crawford D, Moura M (2016) Understanding intra and inter-archipelago population genetic patterns within a recently evolved insular endemic lineage. Plant Syst Evol 302:367–384CrossRefGoogle Scholar
  7. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond A (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10:e1003537CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carine M, Schaefer H (2010) The Azores diversity enigma: why are there so few Azorean endemic flowering plants and why are they so widespread? J Biogeogr 37:77–89CrossRefGoogle Scholar
  9. Carine MA, Russell SJ, Santos-Guerra A, Francisco-Ortega J (2004) Relationships of the Macaronesian and Mediterranean floras: molecular evidence for multiple colonizations into Macaronesia and back-colonization of the continent in Convolvulus (Convolvulaceae). Am J Bot 91:1070–1085CrossRefPubMedGoogle Scholar
  10. Caujapé-Castells J (2004) Boomerangs of biodiversity?: the interchange of biodiversity between mainland North Africa and the Canary Islands as inferred from CPDNA RFLPS in genus Androcymbium. Bot Macaronésica 25:53–69Google Scholar
  11. Caujapé-Castells J (2011) Jesters, red queens, boomerangs and surfers: a molecular outlook on the diversity of the Canarian endemic flora. In: Caujapé-Castells J, Bramwell D (eds) The biology of island floras. Cambridge University Press, CambridgeGoogle Scholar
  12. Caujapé-Castells J, García-Verdugo C, Marrero-Rodrígueza Á, Fernández-Palacios JM, Crawford DJ, Mort ME (2017) Island ontogenies, syngameons, and the origins and evolution of genetic diversity in the Canarian endemic flora. Perspect Plant Ecol Evolut Syst 27(2017):9–22CrossRefGoogle Scholar
  13. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  14. Connor SE, Van Leeuwen JFN, Rittenour TM, Van der Knaap WO, Ammann B, Björck S (2012) The ecological impact of oceanic islands colonization: a paleoecological perspective from Azores. J Biogeogr 39:1001–1023CrossRefGoogle Scholar
  15. Couto MAG (2011) Climate atlas of the Archipelagos of the Canary Islands, Madeira and the Azores. Agencia Estatal de Meteorología, Ministerio de Agricultura, Alimentación y Medio Ambiente, MadridGoogle Scholar
  16. Custódio E, Cabrera MC (2012) The Canary Islands. In: De Stefano L, Llamas MR (eds) Water agriculture and the environment in Spain: can we spare the circle?. CRC Press, LondonGoogle Scholar
  17. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  18. Del Arco Aguilar MJ (2006) Mapa de vegetación de Canarias. Grafcan, Santa Cruz de TenerifeGoogle Scholar
  19. Demand J, Fabriol R, Gerard F, Lundt F, Chovelon P (1982) Prospection géothermique íles de Faial et de Pico (Açores) Rapport géologique geochimique et gravimétrique. Technical report, BRGM 82 SGN 003 GTHGoogle Scholar
  20. Dias EF, Sardos J, Maciel MGB, Silva L, Moura M (2014) Microsatellite markers unravel the population genetic structure of the Azorean Leontodon: implications in conservation. Plant Syst Evol 300:987–1001CrossRefGoogle Scholar
  21. Dias EF, Moura M, Schaefer H, Silva L (2015) Interactions between temperature light and chemical promoters trigger seed germination of the rare Azorean lettuce Lactuca watsoniana (Asteraceae). Seed Sci Technol 43:133–144CrossRefGoogle Scholar
  22. Dias EF, Moura M, Schaefer H, Silva L (2016) Geographical distance and barriers explain population genetic patterns in an endangered island perennial. AoB Plants. PubMedPubMedCentralCrossRefGoogle Scholar
  23. Díaz-Pérez AJ, de Sequeira MM, Santos-Guerra A, Catalán P (2008) Multiple colonizations in situ speciation and volcanism-associated stepping-stone dispersals shaped the phylogeography of the Macaronesian red fescues (Festuca L. Gramineae). Syst Biol 57:732–749CrossRefPubMedGoogle Scholar
  24. Díaz-Pérez AJ, de Sequeira MM, Santos-Guerra A, Catalán P (2012) Divergence and biogeography of the recently evolved Macaronesian red Festuca (Gramineae) species inferred from coalescence-based analyses. Mol Ecol 21(7):1702–1726CrossRefPubMedGoogle Scholar
  25. Doležalová I, Křístková E, Lebeda A, Vinter V (2002) Description of morphological characters of wild Lactuca L spp. genetic resources (English-Czech version). Hortic Sci 29:56–83CrossRefGoogle Scholar
  26. Douzery EJ, Pridgeon AM, Kores P, Linder HP, Kurzweil H, Chase MW (1999) Molecular phylogenetics of Diseae (Orchidaceae): a contribution from nuclear ribosomal ITS sequences. Am J Bot 86:887–899CrossRefPubMedGoogle Scholar
  27. Drouet H (1866) Catalogue des Iles Açores précédé d’un voyage dans cet archipel. Mém de la Soc Acad Aube 30:81–233Google Scholar
  28. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) PLoS Biol 4:e88CrossRefPubMedPubMedCentralGoogle Scholar
  29. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 17. Mol Biol Evol 29:1969–1973CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dziechciarková M, Lebeda A, Doležalová I, Astley D (2004) Characterization of Lactuca spp. germplasm by protein and molecular markers: a review. Plant Soil Environ 50(2):47–58CrossRefGoogle Scholar
  31. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797CrossRefPubMedGoogle Scholar
  32. Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966CrossRefPubMedGoogle Scholar
  33. Feráková V (1977) The genus Lactuca L. Europe. Univerzita Komenského, Bratislava Slovakia, pp 61–62Google Scholar
  34. Fernández Prieto JA, Aguiar C, Dias E (2012) Description of some new syntaxa from the Azores archipelago. Int J Geobot Res 2:111–116CrossRefGoogle Scholar
  35. Fernández-Palácios JM, Dias E (2001) Marco biogeografico macaronesico Naturaleza de las Islas Canarias. Ecol y conservacion 45–52Google Scholar
  36. Fernández-Palacios JM, de Nascimento L, Otto R, Delgado JD, García-del-Rey E, Arévalo JR, Whittaker RJ (2011) A reconstruction of Palaeo-Macaronesia, with particular reference to the long-term biogeography of the Atlantic island laurel forests. J Biogeogr 38(2):226–246CrossRefGoogle Scholar
  37. França Z, Nunes JC, Cruz JV, Duarte JF, Forjaz VH (2002) Preliminary study of the Corvo Island volcanism Azores. In: 3° Assembleia Luso-Espanhola de Geodesia e Geofísica (S09), pp 727–730Google Scholar
  38. França Z, Nunes JC, Cruz JV, Duarte JF, Forjaz VH (2003) Geologia dos Açores: uma perspectiva actual. Açoreana 10(1):11–140Google Scholar
  39. Francisco-Ortega J, Crawford DJ, Santos-Guerra A, Jansen RK (1997) Origin and evolution of Argyranthemum (Asteraceae: Anthemideae) in Macaronesia. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University press, Cambridge UK, pp 407–431Google Scholar
  40. Gillespie RG, Roderick GK (2014) Evolution: geology and climate drive diversification. Nature 509:297–298CrossRefPubMedGoogle Scholar
  41. Goldberg J, Trewick SA (2011) Exploring phylogeographic congruence in a continental island system. Insects 2(3):369–399CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hansen H (1970) Beitrage zur flora der inseln Madeira. Porto Santo und Ilheu Chao (Desertas). Bocagiana 25:1–18Google Scholar
  43. Heleno R, Vargas P (2015) How do islands become green? Glob Ecol Biogeogr 24:518–526CrossRefGoogle Scholar
  44. Hildenbrand A, Weis D, Madureira P, Marques FO (2014) Recent plate reorganization at the Azores Triple Junction: evidence from combined geochemical and geochronological data on Faial S Jorge and Terceira volcanic islands. Lithos 210–211:27–39CrossRefGoogle Scholar
  45. IUCN (2017) The IUCN Red List of Threatened Species. Version 2017-3. Accessed 05 Dec 2017
  46. Jardim R, de Menezes Sequeira M (2008) Lista das plantas vasculares (Pteridophyta e Spermatophyta). In: Borges PAV, Abreu C, Aguiar AMF, Carvalho P, Jardim R, Melo I, Oliveira P, Sérgio C, Serrano ARM, Vieira P (eds) A list of the terrestrial fungi flora and fauna of Madeira and Selvagens archipelagos. Direcção Regional do Ambiente da Madeira e Universidade dos Açores Funchal e Angra do Heroísmo, Portugal, pp 179–208Google Scholar
  47. Jones KE, Reyes-Betancort JA, Hiscock SJ, Carine M (2014) Allopatric diversification multiple habitat shifts and hybridization in the Evolution of Pericallis (Asteraceae) a Macaronesian endemic genus. Am J Bot 101:1–15CrossRefGoogle Scholar
  48. Juan C, Emerson BC, Oromi P, Hewitt GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends Ecol Evol 15:104–109CrossRefPubMedGoogle Scholar
  49. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 84:482–498CrossRefGoogle Scholar
  50. Kilian N, Gemeinholzer B, Lack HW (2009) Tribe Cichorieae. In: Funk VA, Susanna A, Stussey TF, Bayer RJ (eds) Systematics, evolution and biogeography of compositae. IAPT, Vienna, pp 344–383Google Scholar
  51. Kilian N, Sennikov A, Wang Z-H, Gemeinholzer B, Zhang JW (2017) Sub-Paratethyan origin and Middle to Late Miocene principal diversification of the Lactucinae (Cichorieae, Compositae) inferred from molecular phylogenetics, divergence-dating and biogeographic analysis. Taxon 66(3):675–703. CrossRefGoogle Scholar
  52. Kim S-C, Crawford DJ, Francisco-Ortega J, Santos-Guerra A (1996) A common origin for woody Sonchus and five related genera in the Macaronesian Islands: molecular evidence for extensive radiation. Proc Natl Acad Sci 93:7743–7748CrossRefPubMedGoogle Scholar
  53. Kondraskov P, Schütz N, Schüßler C, Menezes de Sequeira M, Guerra AS, Caujapé-Castells J, Jaén-Molina R, Marrero-Rodríguez A, Koch MA, Linder P, Kovar-Eder J, Thiv M (2015) Biogeography of Mediterranean hotspot biodiversity: re-evaluating the ‘tertiary relict’ hypothesis of Macaronesian laurel forests. PLoS ONE 10(7):e0132091CrossRefPubMedPubMedCentralGoogle Scholar
  54. Koopman WJM, Guetta E, van de Wiel CCM, Vosman B, van den Berg RG (1998) Phylogenetic relationships among Lactuca (Asteraceae) species and related genera based on ITS-1 DNA sequences. Am J Bot 85(11):1517–1530CrossRefPubMedGoogle Scholar
  55. Lebeda A, Doležalová I, Křístková E, Mieslerová B (2001) Biodiversity and ecogeography of wild Lactuca spp. in some European countries. Genet Resour Crop Evol 48(2):153–164CrossRefGoogle Scholar
  56. Lebeda A, Dolezalová I, Feràkovà V, Astkey D (2004) Geographical distribution of wild Lactuca Species (Asteraceae, Lactuceae). Bot Rev 70(3):328–356CrossRefGoogle Scholar
  57. Linnaeus C (1753) Species plantarum, 1st edn. The Ray Society, London, pp 795–796Google Scholar
  58. Mairal M, SanMartín I, Aldasoro JJ, Culshaw V, Manolopoulou I, Alarcón M (2015) Palaeo-islands as refugia and sources of genetic diversity within volcanic archipelagos: the case of the widespread endemic Canarina canariensis (Campanulaceae). Mol Ecol 24:3944–3963CrossRefPubMedGoogle Scholar
  59. Mejias JA (1993) Cytotaxonomic studies on the Iberian taxa of the genus Lactuca (Compositae). Bot Helv 103:113–130Google Scholar
  60. Menezes CA (1914) Flora do Archipelago da Madeira (phanerogamicas e cryptogamicas vasculares). Junta Agrícola da Madeira, FunchalGoogle Scholar
  61. Menezes T, Romeiras M, Sequeira MPSM, Moura M (2017) Phylogenetic relationships and phylogeography of relevant lineages within the complex Campanulaceae family in Macaronesia. Ecol Evolut 2017:1–21. CrossRefGoogle Scholar
  62. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), pp 1–8, New Orleans, LAGoogle Scholar
  63. Moura M, Silva L, Caujapé-Castells J (2013) Population genetics in the conservation of the Azorean shrub Viburnum treleasei Gand. Plant Syst Evol 299:1809–1817CrossRefGoogle Scholar
  64. Moura M, Silva L, Dias EF, Schaefer H, Carine MA (2015) A revision of the genus Leontodon (Asteraceae) in the Azores based on morphological and molecular evidence. Phytotaxa 210:024–046CrossRefGoogle Scholar
  65. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  66. Ortega J, Navarro B (1977) Estudios en la flora de Macaronesia: algunos números de cromossomas III. Bot Macaronesia 3:73–80Google Scholar
  67. Palhinha RT (1966) Catálogo das plantas vasculares dos Açores. Sociedade de Estudos Açorianos Afonso Chaves, LisboaGoogle Scholar
  68. Panero JL, Francisco-Ortega J, Jansen RK, Santos-Guerra A (1999) Molecular evidence for multiple origins of woodiness and a New World biogeographic connection of the Macaronesian Island endemic Pericallis (Asteracea: Senecioneae). Proc Natl Acad Sci 96:13886–13891CrossRefPubMedGoogle Scholar
  69. Park S-J, Korompai EJ, Francisco-Ortega J, Santos-Guerra A, Jansen RK (2001) Phylogenetic relationships of Tolpis (Asteraceae: Lactuceae) based on ndhF sequence data. Plant Syst Evol 226:23–33CrossRefGoogle Scholar
  70. Press JR, Short MJ (1994) Flora of Madeira. HM Stationery Office, The Natural History Museum, LondonGoogle Scholar
  71. Ramalho RS, Helffrich G, Madeira J, Cosca M, Thomas C, Quartau R, Hipólito A, Rovere A, Hearty PJ, Ávila SP (2017) Emergence and evolution of Santa Maria Island (Azores)—the conundrum of uplifted islands revisited. Geol Soc Am Bull 129:372–390CrossRefGoogle Scholar
  72. Rambaut (2006–2014) Figtree www.treebioedacuk/software/figtree
  73. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v16. www.beastbioedacuk/Tracer
  74. Rijsdijk KF, Hengl T, Norder S, Ávila SP, Férnandez-Palacios JM (2014) Modelling sea level driven change of Macaronesian archipelagos configurations since 120 kyr BP. In: Fernández-Palacios JM, De Nascimento L, Hernández JC, Clemente S, González A, Díaz-González JP (eds) Biogeographic implications of climate change: past present and future perspectives. Servicio de Publicaciones, Universidad de La Laguna, LaLaguna, TenerifeGoogle Scholar
  75. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Helsenbeck JP (2012) MrBayes 32: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  76. Rumeu B, Caujapé-Castells J, Blanco-Pastor JL, Jaén-Molina R, Nogales M, Elias RB, Vargas P (2011) The colonization history of Juniperus brevifolia (Cupressaceae) in the Azores Islands. PLoS ONE 6:e27697CrossRefPubMedPubMedCentralGoogle Scholar
  77. Sánchez-Pinto L, Rodríguez ML, Rodríguez S, Martín K, Cabrera A, Marrero MC (2005) Pteridophyta & Spermatophyta. In: Arechavaleta M, Zurita N, Marrero MC, Martín JL (eds) Lista preliminar de especies silvestres de Cabo Verde (hongos plantas y animales terrestres. Á Consejerıa de Medio Ambiente e Ordenación Territorial Gobierno de Canarias, Canary Island, pp 38–57Google Scholar
  78. Santos-Guerra A (2013) Lactuca palmensis. The IUCN Red List of Threatened Species 2013 eT172087A6821101Google Scholar
  79. Schaefer H (2003) Chorology and diversity of the Azorean flora. Diss Bot 374:1–130Google Scholar
  80. Schaefer H (2005) Flora of the Azores. A field guide, 2nd edn. Margraf Publishers, WeikersheimGoogle Scholar
  81. Schaefer H (2015) On the origin and systematic position of the Azorean goldenrod Solidago azorica (Asteraceae). Phytotaxa 210:047–059CrossRefGoogle Scholar
  82. Schaefer H, Moura M, Maciel MGB, Silva L, Rumsey FJ, Carine MA (2011) The Linnean shortfall in oceanic island biogeography: a case study in the Azores. J Biogeogr 38:1345–1355CrossRefGoogle Scholar
  83. Schönfelder P, Schönfelder I (2005) Kie Kosmos Kanarenflora Über 850 Arten der Kanarenflora und 48 tropische Zierfehölze Kosmos naturführerGoogle Scholar
  84. Shaw KL, Gillespie RG (2016) Comparative phylogeography of oceanic archipelagos: hotspots for inferences of evolutionary process. Proc Natl Acad Sci 113:7986–7993CrossRefPubMedGoogle Scholar
  85. 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 hare III. Am J Bot 94:275–288CrossRefPubMedGoogle Scholar
  86. Sibrant A, Marques FO, Hildenbrand A (2014) Construction and destruction of a volcanic island developed inside an oceanic rift: Graciosa Island, Terceira Rift, Azores. J Volcanol Geotherm Res 284:32–45CrossRefGoogle Scholar
  87. Sibrant ALR, Hildenbrant A, Marques FO, Weiss B, Boulesteix T, Hübscher C, Lüdmannf T, Costa ACG, Catalão JC (2015) Morpho-structural evolution of a volcanic island developed inside an active oceanic rift: S Miguel Island (Terceira Rift Azores). J Volcanol Geotherm Res 301:90–106CrossRefGoogle Scholar
  88. Silva L, Ojeda Land E, Rodríguez Luengo JL (2008) Invasive Terrestrial Flora & Fauna of Macaronesia, TOP 100 in Azores Madeira and Canaries, pp 546. ARENA Ponta DelgadaGoogle Scholar
  89. Silva L, Martins M, Maciel G, Moura M (2009) Azores vascular flora – priorities in conservation. Amigos dos Açores Associação Ecológica & Centro de Conservação e Protecção do Ambiente Ponta Delgada, pp 116Google Scholar
  90. Silva L, Moura M, Schaefer H, Rumsey F, Dias EF (2010) Lista das plantas vasculares (Tracheobionta). In: Borges PAV, Costa A, Cunha R, Gabriel R, Gonçalves V, Martins AF, Melo I, Parente M, Raposeiro P, Rodrigues P, Santos RS, Silva L, Vieira P, Vieira V (eds) A list of the terrestrial and marine biota from the Azores. Princípia Cascais, Parede, pp 117–146Google Scholar
  91. Silvertown J (2004) The ghost of competition past in the phylogeny of island endemic plants. J Ecol 92:168–173CrossRefGoogle Scholar
  92. Sjögren E (2000) Aspects on the biogeography of Macaronesia from a botanical point of view. Arquipélago. Life Mar Sci 2:1–9Google Scholar
  93. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771CrossRefGoogle Scholar
  94. Stebbins GL, Jenkins JA, Walters MS (1953) Chromosomes and phylogeny in the Compositae tribe Cichorieae. Univ Calif Publ Bot 26:401–430Google Scholar
  95. Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7CrossRefGoogle Scholar
  96. Suda J, Kyncl T, Freiová R (2003) Nuclear DNA amounts in Macaronesian angiosperms. Ann Bot 92:153–164CrossRefPubMedPubMedCentralGoogle Scholar
  97. Sunding P (1979) Origins of the Macaronesian flora. In: Bramwell D (ed) Plants and islands. Academic Press, London, pp 13–40Google Scholar
  98. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods) version 4.0 β version. Sinauer Associates, Sunderland, MAGoogle Scholar
  99. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefPubMedGoogle Scholar
  100. Trelease W (1897) Botanical observations on the Azores. Mo Bot Gard Annu Rep 8:77–220Google Scholar
  101. Tremetsberger K, Gemeinholzer B, Zetzsche H, Blackmore S, Kilian N, Talavera S (2013) Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. Org Divers Evol 13:1–13CrossRefGoogle Scholar
  102. Van Den Bogaard P (2013) The origin of the Canary Island Seamount Province-New ages of old seamounts. Sci Rep 3:2107CrossRefPubMedPubMedCentralGoogle Scholar
  103. Vargas P (2007) Are Macaronesian islands refugia of relict plant lineages?: a molecular survey. Phylogeography of southern European refugia. Springer, Dordrecht, pp 297–314CrossRefGoogle Scholar
  104. Wang ZH, Peng H, Kilian N (2013) Molecular phylogeny of the Lactuca alliance (Cichorieae subtribe Lactucinae; Asteraceae) with focus on their Chinese centre of diversity detects potential events of reticulation and chloroplast capture. PLoS ONE 8:e82692CrossRefPubMedPubMedCentralGoogle Scholar
  105. Watson HC (1870) Notes on the botany of the Azores. In: Godman FC (ed) The natural history of the Azores or Western Islands. John Van Yoorbt Paternoster Row, London, p 358Google Scholar
  106. Wei Z, Zhu S, Van den Berg RG, Bakker FT, Schranz ME (2015) Phylogenetic relationships within Lactuca L. (Asteraceae) including African species based on chloroplast DNA sequence comparisons. Genet Resour Crop Evol 64:55–71CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos AçoresUniversidade dos AçoresPonta DelgadaPortugal
  2. 2.Botanic Garden and Botanical Museum Berlin, Freie Universität BerlinBerlinGermany
  3. 3.Plant Biodiversity ResearchTechnische Universität MünchenFreisingGermany
  4. 4.Department of Life SciencesThe Natural History MuseumLondonUK
  5. 5.Royal Botanic Gardens, KewRichmondUK
  6. 6.Calle Guaidil 16, Urbanización TamarcoTenerifeSpain

Personalised recommendations