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

Biochemical Genetics volume 56, pages315–340(2018)Cite this article

Abstract

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.

This is a preview of subscription content, access via your institution.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  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 119–172

    Google 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 441:912–923

    Article  Google Scholar 

  3. Azevedo J (1998) Geologia e Hidrogeologia da Ilha das Flores (Açores—Portugal). PhD Thesis, Universidade de Coimbra

  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:e218

    Article  PubMed  PubMed Central  Google 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 298

    Google 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 302:367–384

    Article  Google 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:e1003537

    Article  PubMed  PubMed Central  CAS  Google 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 37:77–89

    Article  Google 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 91:1070–1085

    Article  PubMed  Google 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 25:53–69

    Google 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, Cambridge

    Google 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):9–22

    Article  Google Scholar 

  13. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google 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 39:1001–1023

    Article  Google 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, Madrid

    Google 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, London

    Google Scholar 

  17. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models new heuristics and parallel computing. Nat Methods 9:772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Del Arco Aguilar MJ (2006) Mapa de vegetación de Canarias. Grafcan, Santa Cruz de Tenerife

    Google 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 GTH

  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 300:987–1001

    Article  Google 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 43:133–144

    Article  Google 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. https://doi.org/10.1093/aobpla/plw072

    PubMed  PubMed Central  Article  Google 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 57:732–749

    Article  PubMed  Google 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):1702–1726

    Article  PubMed  Google 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 29:56–83

    Article  Google 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 86:887–899

    Article  PubMed  CAS  Google Scholar 

  27. Drouet H (1866) Catalogue des Iles Açores précédé d’un voyage dans cet archipel. Mém de la Soc Acad Aube 30:81–233

    Google Scholar 

  28. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) PLoS Biol 4:e88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 17. Mol Biol Evol 29:1969–1973

    Article  PubMed  PubMed Central  CAS  Google 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):47–58

    Article  Google Scholar 

  31. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  32. Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966

    Article  PubMed  CAS  Google Scholar 

  33. Feráková V (1977) The genus Lactuca L. Europe. Univerzita Komenského, Bratislava Slovakia, pp 61–62

    Google Scholar 

  34. Fernández Prieto JA, Aguiar C, Dias E (2012) Description of some new syntaxa from the Azores archipelago. Int J Geobot Res 2:111–116

    Article  Google Scholar 

  35. Fernández-Palácios JM, Dias E (2001) Marco biogeografico macaronesico Naturaleza de las Islas Canarias. Ecol y conservacion 45–52

  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):226–246

    Article  Google 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 727–730

  38. França Z, Nunes JC, Cruz JV, Duarte JF, Forjaz VH (2003) Geologia dos Açores: uma perspectiva actual. Açoreana 10(1):11–140

    Google 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 407–431

    Google Scholar 

  40. Gillespie RG, Roderick GK (2014) Evolution: geology and climate drive diversification. Nature 509:297–298

    Article  PubMed  CAS  Google Scholar 

  41. Goldberg J, Trewick SA (2011) Exploring phylogeographic congruence in a continental island system. Insects 2(3):369–399

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hansen H (1970) Beitrage zur flora der inseln Madeira. Porto Santo und Ilheu Chao (Desertas). Bocagiana 25:1–18

    Google Scholar 

  43. Heleno R, Vargas P (2015) How do islands become green? Glob Ecol Biogeogr 24:518–526

    Article  Google 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 210–211:27–39

    Article  CAS  Google Scholar 

  45. IUCN (2017) The IUCN Red List of Threatened Species. Version 2017-3. http://www.iucnredlist.org. 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 179–208

    Google 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 101:1–15

    Article  Google 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 15:104–109

    Article  PubMed  CAS  Google Scholar 

  49. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 84:482–498

    Article  Google 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 344–383

    Google 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. https://doi.org/10.12705/663.9

    Article  Google 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 93:7743–7748

    Article  PubMed  CAS  Google 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):e0132091

    Article  PubMed  PubMed Central  CAS  Google 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):1517–1530

    Article  PubMed  CAS  Google 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):153–164

    Article  Google Scholar 

  56. Lebeda A, Dolezalová I, Feràkovà V, Astkey D (2004) Geographical distribution of wild Lactuca Species (Asteraceae, Lactuceae). Bot Rev 70(3):328–356

    Article  Google Scholar 

  57. Linnaeus C (1753) Species plantarum, 1st edn. The Ray Society, London, pp 795–796

    Google 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 24:3944–3963

    Article  PubMed  CAS  Google Scholar 

  59. Mejias JA (1993) Cytotaxonomic studies on the Iberian taxa of the genus Lactuca (Compositae). Bot Helv 103:113–130

    Google Scholar 

  60. Menezes CA (1914) Flora do Archipelago da Madeira (phanerogamicas e cryptogamicas vasculares). Junta Agrícola da Madeira, Funchal

    Google 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. https://doi.org/10.1002/ece3.3640

    Article  Google 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, LA

  63. Moura M, Silva L, Caujapé-Castells J (2013) Population genetics in the conservation of the Azorean shrub Viburnum treleasei Gand. Plant Syst Evol 299:1809–1817

    Article  Google 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 210:024–046

    Article  Google Scholar 

  65. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  66. Ortega J, Navarro B (1977) Estudios en la flora de Macaronesia: algunos números de cromossomas III. Bot Macaronesia 3:73–80

    Google Scholar 

  67. Palhinha RT (1966) Catálogo das plantas vasculares dos Açores. Sociedade de Estudos Açorianos Afonso Chaves, Lisboa

    Google 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 96:13886–13891

    Article  PubMed  CAS  Google 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 226:23–33

    Article  CAS  Google Scholar 

  70. Press JR, Short MJ (1994) Flora of Madeira. HM Stationery Office, The Natural History Museum, London

    Google 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 129:372–390

    Article  Google 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, Tenerife

    Google 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 61:539–542

    Article  PubMed  PubMed Central  Google 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:e27697

    Article  PubMed  PubMed Central  CAS  Google 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 38–57

    Google Scholar 

  78. Santos-Guerra A (2013) Lactuca palmensis. The IUCN Red List of Threatened Species 2013 eT172087A6821101

  79. Schaefer H (2003) Chorology and diversity of the Azorean flora. Diss Bot 374:1–130

    Google Scholar 

  80. Schaefer H (2005) Flora of the Azores. A field guide, 2nd edn. Margraf Publishers, Weikersheim

    Google Scholar 

  81. Schaefer H (2015) On the origin and systematic position of the Azorean goldenrod Solidago azorica (Asteraceae). Phytotaxa 210:047–059

    Article  Google 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 38:1345–1355

    Article  Google Scholar 

  83. Schönfelder P, Schönfelder I (2005) Kie Kosmos Kanarenflora Über 850 Arten der Kanarenflora und 48 tropische Zierfehölze Kosmos naturführer

  84. Shaw KL, Gillespie RG (2016) Comparative phylogeography of oceanic archipelagos: hotspots for inferences of evolutionary process. Proc Natl Acad Sci 113:7986–7993

    Article  PubMed  CAS  Google 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 94:275–288

    Article  PubMed  CAS  Google 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 284:32–45

    Article  CAS  Google 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 301:90–106

    Article  CAS  Google 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 Delgada

  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 116

  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 117–146

    Google Scholar 

  91. Silvertown J (2004) The ghost of competition past in the phylogeny of island endemic plants. J Ecol 92:168–173

    Article  Google Scholar 

  92. Sjögren E (2000) Aspects on the biogeography of Macaronesia from a botanical point of view. Arquipélago. Life Mar Sci 2:1–9

    Google Scholar 

  93. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771

    Article  Google Scholar 

  94. Stebbins GL, Jenkins JA, Walters MS (1953) Chromosomes and phylogeny in the Compositae tribe Cichorieae. Univ Calif Publ Bot 26:401–430

    Google Scholar 

  95. Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7

    Article  Google Scholar 

  96. Suda J, Kyncl T, Freiová R (2003) Nuclear DNA amounts in Macaronesian angiosperms. Ann Bot 92:153–164

    Article  PubMed  PubMed Central  Google Scholar 

  97. Sunding P (1979) Origins of the Macaronesian flora. In: Bramwell D (ed) Plants and islands. Academic Press, London, pp 13–40

    Google Scholar 

  98. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods) version 4.0 β version. Sinauer Associates, Sunderland, MA

    Google 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 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  100. Trelease W (1897) Botanical observations on the Azores. Mo Bot Gard Annu Rep 8:77–220

    Google 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 13:1–13

    Article  Google Scholar 

  102. Van Den Bogaard P (2013) The origin of the Canary Island Seamount Province-New ages of old seamounts. Sci Rep 3:2107

    Article  PubMed  PubMed Central  Google Scholar 

  103. Vargas P (2007) Are Macaronesian islands refugia of relict plant lineages?: a molecular survey. Phylogeography of southern European refugia. Springer, Dordrecht, pp 297–314

    Google 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:e82692

    Article  PubMed  PubMed Central  CAS  Google 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 358

    Google 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 64:55–71

    Article  Google Scholar 

Download references

Acknowledgements

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.

Funding

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), http://www.synthesys.info/ which is financed by European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area” programme.

Author information

Affiliations

  1. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos Açores, Universidade dos Açores, Rua da Mãe de Deus, Apartado, 1422, 9501-801, Ponta Delgada, Açores, Portugal

    Elisabete F. Dias, Luís Silva & Mónica Moura

  2. Botanic Garden and Botanical Museum Berlin, Freie Universität Berlin, Königin-Luise-Straße 6-8, 14195, Berlin, Germany

    Norbert Kilian

  3. Plant Biodiversity Research, Technische Universität München, 85354, Freising, Germany

    Hanno Schaefer

  4. Department of Life Sciences, The Natural History Museum, London, UK

    Mark Carine

  5. Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK

    Paula J. Rudall

  6. Calle Guaidil 16, Urbanización Tamarco, Tegueste, 38280, Tenerife, Canary Islands, Spain

    Arnoldo Santos-Guerra

Authors
  1. Elisabete F. Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norbert Kilian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luís Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hanno Schaefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mark Carine
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paula J. Rudall
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Arnoldo Santos-Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mónica Moura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisabete F. Dias.

Ethics declarations

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.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dias, E.F., Kilian, N., Silva, L. et al. Phylogeography of the Macaronesian Lettuce Species Lactuca watsoniana and L. palmensis (Asteraceae). Biochem Genet 56, 315–340 (2018). https://doi.org/10.1007/s10528-018-9847-8

Download citation

Keywords

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