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Phylogenetic and morphological analysis of a new cliff-dwelling species reveals a remnant ancestral diversity and evolutionary parallelism in Sonchus (Asteraceae)

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Abstract

We describe a new cliff-dwelling species within Sonchus (Asteraceae): Sonchus boulosii and analyze its systematic position and evolutionary significance; in addition, we provide a key to the species of Sonchus in Morocco. Both morphological and ecological characteristics suggest a close relationship of S. boulosii with taxa of section Pustulati. However, ITS nrDNA and cpDNA matK markers indicate its uncertain position within the genus, but clear genetic differentiation from the remaining major clades. ITS phylogenetic trees show that likely evolutionary shifts to rocky habitat took place at least five times within genus Sonchus and that sect. Pustulati and S. boulosii clades have a clearly independent evolutionary origin. We postulate that the strong resemblance of S. boulosii to other rocky species reflects a phenomenon of homoplasy, probably driven by parallel evolutionary adaptations to the severe ecological constraints of its cliff face habitat. Therefore, a new section is also described, which includes S. boulosii as its sole representative: section Pulvinati. According to phylogenetic trees, the new clade may share its common ancestor with the clade comprising sections Maritimi and Arvenses, from which it is widely divergent in morphology and ecology, with the exception of Sonchus novae-zelandiae. However, the latter is a derived taxon, with high level of polyploidy unlike S. boulosii that shows 2n = 18, basal chromosome number of the genus. Since sections Pulvinati and Pustulati seem to be quite old in Sonchus, we also hypothesize that some similarities, such as fruit morphology, may reflect the persistence of some primitive characteristics.

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References

  • Allan HHB, Moore LB, Edgar E (1961) Flora of New Zealand, vol 1. PD Hasselberg Government Printer, Wellington

    Google Scholar 

  • Arendt J, Reznick D (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23:26–32. https://doi.org/10.1016/j.tree.2007.09.011

    Article  PubMed  Google Scholar 

  • Bailey SF, Rodrigue N, Kassen R (2015) The effect of selection environment on the probability of parallel evolution. Molec Biol Evol 32:1436–1448. https://doi.org/10.1093/molbev/msv033

    Article  CAS  PubMed  Google Scholar 

  • Barnosky A, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471:51–57. https://doi.org/10.1038/nature09678

    Article  CAS  PubMed  Google Scholar 

  • Beuzenberg EJ, Hair JB (1984) Contributions to a chromosome atlas of the New Zealand flora—27. Compositae. New Zealand J Bot 22:353–356

    Article  Google Scholar 

  • Boulos L (1972) Révision systématique du genre Sonchus s.l. I. Introduction et classification. Bot Not 125:287–305

    Google Scholar 

  • Boulos L (1973) Révision systématique du genre Sonchus s.l. IV. Sous-genre 1. Sonchus. Bot Not 126:155–196

    Google Scholar 

  • Boulos L (1974a) Révision systématique du genre Sonchus s.l. V. Sous-genre 2. Dendrosonchus. Bot Not 127:7–37

    Google Scholar 

  • Boulos L (1974b) Révision systématique du genre Sonchus s.l. VI. Sous-genre 3. Origosonchus. Genres Embergeria, Babcockia et Taeckholmia. Species exclusae et dubiae. Index. Bot Not 127:402–451

    Google Scholar 

  • Bragazza L (2009) Conservation priority of Italian Alpine habitats: a floristic approach based on potential distribution of vascular plant species. Biodivers & Conservation 11:2823–2835

    Article  Google Scholar 

  • Carlquist S (1966) The biota of long-distance dispersal. II. Loss of dispersibility in Pacific Compositae. Evolution 20:30–48

    Article  PubMed  Google Scholar 

  • Carlquist S (1967) Anatomy and systematics of Dendroseris (sensu lato). Brittonia 19:99–121

    Article  Google Scholar 

  • Chalouan A, Michard A, El Kadiri K, Negro F, Frizon de Lamotte D, Soto JI, Saddiqi O (2008) The Rif belt. In: Michard A, Saddiqi O, Chalouan A, Frizon de Lamotte D (eds) Continental evolution: the geology of Morocco. Springer, Berlin, pp 203–302

    Chapter  Google Scholar 

  • Chambouleyron M, Bidat M, Léger J-F (2014) Centaurea ibn-tattoui (Asteraceae), a new narrow endemic species from North-Eastern Morocco. Phytotaxa 174:157–164. https://doi.org/10.11646/phytotaxa.174.3.4

    Article  Google Scholar 

  • Chambouleyron M, Bidat M, Ibn-Tattou M, Molero J, Montserrat J-M, Pyke S, Léger J-F (2015a) Contribution à la connaissance de la flore vasculaire du Maroc oriental: plaine de Lamrija et revers nord des monts de Debdou. Bull Inst Sci Rabat 37:1–16

    Google Scholar 

  • Chambouleyron M, Bidat M, Léger J-F (2015b) Sarcocapnos crassifolia subsp. simplicifolia (Papaveraceae, Fumarioideae), a new narrow-endemic taxon from Northeastern Morocco. Ann Bot Fenn 52:205–210

    Article  Google Scholar 

  • Crisp MD, Cook L-G (2012) Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytol 196:681–694. https://doi.org/10.1111/j.1469-8137.2012.04298.x

    Article  PubMed  Google Scholar 

  • Dobignard A (2002) Contributions à la connaissance de la flore du Maroc et de l’Afrique du Nord. Nouvelle série. 1. J Bot 20:5–43

    Google Scholar 

  • Dobignard A, Chatelain C (2011) Index synonymique de la flore d’Afrique du Nord. Dicotyledoneae: Acanthaceae à Asteraceae, vol 2. Conservatoire et Jardin Botaniques Ville de Genève, ECWP, Genève

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fennane M, Ibn Tattou M (1998) Catalogue des plantes vasculaires rares, menacées ou endémiques du Maroc. Bocconea 8:5–243

    Google Scholar 

  • Fennane M, Ibn Tattou M (2005) Flore vasculaire du Maroc, inventaire et chorologie, Pteridophyta, Gymnospermae, Angiospermae p.p., 1. Travaux de l’Institut Scientifique, Série Botanique, no 37, Rabat

  • Fennane M, Ibn Tattou M, El Oualidi J (eds) (2014) Flore Pratique du Maroc, vol. 3. Travaux de l’Institut Scientifique, Série Botanique, no 40, Rabat

  • Frizon de Lamotte D, Zizi M, Missenard Y, Hafid M, El Azzouzi M, Maury RC, Charrière A, Taki Z, Benammi M, Michard A (2008) The atlas system. In: Michard A, Saddiqi O, Chalouan A, Frizon de Lamotte D (eds) Continental evolution: the geology of Morocco. Springer, Berlin, pp 133–202

    Chapter  Google Scholar 

  • García MB, Guzmán D, Goñi D (2002) An evaluation of the status of five threatened plant species in the Pyrenees. Biol Conservation 103:151–161

    Article  Google Scholar 

  • Guo X, Wang RJ, Simmons MP, But PPH, Yu J (2013) Phylogeny of the Asian Hedyotis-Oldenlandia complex (Spermacoceae, Rubiaceae): evidence for high levels of polyphyly and the parallel evolution of diplophragmous capsules. Molec Phylogen Evol 67:110–122. https://doi.org/10.1016/j.ympev.2013.01.006

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • IUCN Standards and Petitions Subcommittee (2017) Guidelines for using the IUCN red list categories and criteria. Version 13. Prepared by the standards and petitions subcommittee. http://www.iucnredlist.org/documents/RedListGuidelines.pdf

  • Johow F (1896) Estudios sobre la flora de las Islas de Juan Fernández. Imprenta Cervantes, Santiago de Chile

    Book  Google Scholar 

  • Kim S-C, Lee C, Mejías JA (2007) Phylogenetic analysis of chloroplast DNA matK gene and ITS of nrDNA sequences reveals polyphyly of the genus Sonchus and new relationships among the subtribe Sonchinae (Asteraceae: Cichorieae). Molec Phylogen Evol 44:578–597. https://doi.org/10.1016/j.ympev.2007.03.014

    Article  CAS  Google Scholar 

  • Kim S-C, Mejías JA, Pesach L (2008) Molecular confirmation of the hybrid origin of the critically endangered western Mediterranean endemic Sonchus pustulatus (Asteraceae: Sonchinae). J Pl Res 121:357–364. https://doi.org/10.1007/s10265-008-0166-8

    Article  CAS  Google Scholar 

  • Kimura M (1980) Simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Molec Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Küpfer P (1974) Recherches sur les liens de parenté entre la flore orophile des Alpes et celle des Pyrénées. Boissiera 23:322

    Google Scholar 

  • Larson DW, Matthes U, Kelly PE (2005) Cliff ecology: pattern and process in cliff ecosystems. Cambridge University Press, Cambridge

    Google Scholar 

  • Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107:505–518

    Article  Google Scholar 

  • Lee C, Kim S-C, Lundy K, Santos-Guerra A (2005) Chloroplast DNA phylogeny of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian Islands. Amer J Bot 92:2072–2085. https://doi.org/10.3732/ajb.92.12.2072

    Article  CAS  Google Scholar 

  • Levan A, Fredga K, Sandberg A (1964) Nomenclature for centromeric position on chromosomes. Hereditas (Lund) 52:201–220

    Article  Google Scholar 

  • Lin TT, Klinkhamer PGL, Vrieling K (2015) Parallel evolution in an invasive plant: effect of herbivores on competitive ability and regrowth of Jacobaea vulgaris. Ecol Lett 18:668–676. https://doi.org/10.1111/ele.12445

    Article  PubMed  Google Scholar 

  • Lindberg H (1932) Itinera Mediterranea. Acta Soc Sci Fenn, Ser B, Opera Biol 1(2):1–178

    Google Scholar 

  • Löve Á, Löve D (1975) Plant chromosomes. J Cramer, Vaduz

    Google Scholar 

  • Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Ann Missouri Bot Gard 84:112–127

    Article  Google Scholar 

  • Mejías JA (1988) Diferencias cariológicas y morfológicas entre Sonchus pustulatus Willk. y Sonchus tenerrimus L. Lagascalia 15(Extra):345–354

    Google Scholar 

  • Mejías JA (2017) Sonchus. In: Talavera S, Buira A, Quintanar A, García MA, Talavera M, Fernández-Piedra P, Aedo C (eds) Flora iberica 16(2). Real Jardín Botánico; CSIC, Madrid, pp 871–891

    Google Scholar 

  • Mejías JA, Andrés C (2004) Karyological studies in Iberian Sonchus (Asteraceae: Lactuceae): S. oleraceus, S. microcephalus and S. asper and a general discussion. Folia Geobot 39:275–291

    Article  Google Scholar 

  • Mejías JA, Valdés B (1988) Karyological studies in Sonchus section Maritimi (Asteraceae) from the Iberian Peninsula. Bot J Linn Soc 98:61–69

    Article  Google Scholar 

  • Michard A, Hoepffner C, Soulaimani A, Baidder L (2008) The Variscan belt. In: Michard A, Saddiqi O, Chalouan A, Frizon de Lamotte D (eds) Continental evolution: the geology of Morocco. Springer, Berlin, pp 65–132

    Chapter  Google Scholar 

  • Moen DS, Irschick DJ, Wiens JJ (2013) Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proc Roy Soc London, Ser B, Biol Sci 280:20132156. https://doi.org/10.1098/rspb.2013.2156

    Article  Google Scholar 

  • Mokhtari N, Mrabet R, Lebailly P, Bock L (2014) Spatialisation des bioclimats, de l’aridité et des étages de végétation du Maroc. Rev Mar Sci Agron Vét 2:50–66

    Google Scholar 

  • Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How many species are there on earth and in the ocean. PLoS Biol 9:e1001127. https://doi.org/10.1371/journal.pbio.1001127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nylander JAA (2004) MrModeltest 22 Computer program and documentation distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala

    Google Scholar 

  • Pearce T (2012) Convergence and parallelism in evolution: a neo-Gouldian account. Brit J Philos Sci 63:429–448. https://doi.org/10.1093/bjps/axr046

    Article  Google Scholar 

  • Pérez-García FJ, Medina-Cazorla JM, Martínez-Hernández F, Garrido-Becerra JA, Mendoza-Fernández AJ, Salmerón-Sánchez E, Mota JF (2012) Iberian Baetic endemic flora and the implications for a conservation policy. Ann Bot Fenn 49:43–54

    Article  Google Scholar 

  • Plata ER, Hernández JE, Lucking R, Staiger B, Kalb K, Cáceres MES (2011) Graphis is two genera: a remarkable case of parallel evolution in lichenized Ascomycota. Taxon 60:99–107

    Google Scholar 

  • Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev Cambridge Philos Soc 90:1248–1262. https://doi.org/10.1111/brv.12154

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v1.5 [computer program]. Available at:http://tgree.bio.ed.ac.uk/software/tracer/. Accessed 28 Aug 2017

  • Regnier C, Achaz G, Lambert A, Cowie RH, Bouchet P, Fontaine B (2015) Mass extinction in poorly known taxa. Proc Natl Acad Sci USA 112:7761–7766. https://doi.org/10.1073/pnas.1502350112

    Article  CAS  PubMed  Google Scholar 

  • Romero Zarco C (1986) A new method for estimating karyotype asymmetry. Taxon 35:526–530

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rosenbaum G, Liste GS, Duboz C (2002) Relative motions of Africa, Iberia and Europe during Alpine orogeny. Tectonophysics 359:117–129

    Article  Google Scholar 

  • Rothfels CJ, Windham MD, Grusz AL, Gastony GJ, Pryer KM (2008) Toward a monophyletic Notholaena (Pteridaceae): resolving patterns of evolutionary convergence in xeric-adapted ferns. Taxon 57: 713–724. http://www.jstor.org/stable/27756703

  • Roux J, Boulos L (1972) Révision systématique du genre Sonchus L. s.l. II. Étude caryologique. Bot Not 125:306–309

    Google Scholar 

  • Silva JL, Lim S-Y, Kim S-C, Mejías JA (2015a) Phylogeography of cliff -dwelling relicts with a highly narrow and disjunct distribution in the Western Mediterranean. Amer J Bot 102:1538–1551

    Article  CAS  Google Scholar 

  • Silva JL, Mejías JA, García MB (2015b) Demographic vulnerability in cliff-dwelling Sonchus species endemic to the Western Mediterranean. Basic App Ecol 16:316–324. https://doi.org/10.3732/ajb.1500152

    Article  CAS  Google Scholar 

  • Skottsberg C (1922) The natural history of Juan Fernández and Easter Island 2: botany, part 2 (7). Almqvist & Wiksells Boktryckeri, Uppsala

    Google Scholar 

  • Stebbins GL (1938) Cytological characteristics associated with the different growth habits in the dicotyledons. Amer J Bot 25:189–198

    Article  Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold, London

    Google Scholar 

  • Steffen S, Kadereit JW (2014) Parallel evolution of flower reduction in two alpine Soldanella species (Primulaceae). Bot J Linn Soc 175:409–422

    Article  Google Scholar 

  • Swofford D (2002) PAUP*. phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford

    Book  Google Scholar 

  • Tjio JH, Levan A (1950) The use of oxyquinoline in chromosome analysis. Anales Estac Exp Aula Dei 2:21–64

    Google Scholar 

  • Tremetsberger K, Gemeinholzer B, Zetsche H, Blackmore S, Kilian N, Talavera S (2013) Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. Organisms Diversity Evol 13:1–13. https://doi.org/10.1007/s13127-012-0094-2

    Article  Google Scholar 

  • Valdecasas AG, Camacho AI (2003) Conservation to the rescue of taxonomy. Biodivers & Conservation 12:113–117

    Article  Google Scholar 

  • Valdés B (1991) Andalucia and the Rif. Floristic links and a common flora. Bot Chron (Patras) 10:117–124

    Google Scholar 

  • van Vuuren DP, Sala OE, Pereira, HM (2006) The future of vascular plant diversity under four global scenarios. Ecol Soc 11: 25. http://www.ecologyandsociety.org/vol11/iss2/art25/

  • Wägele H, Klussmann-Kolb A, Kuhlmann M, Haszprunar G, Lindberg D, Koch A, Wägele JW (2011) The taxonomist - an endangered race. A practical proposal for its survival. Frontiers Zool 8: 25. http://www.frontiersinzoology.com/content/8/1/25

    Article  PubMed  PubMed Central  Google Scholar 

  • Wege JA, Thiele KR, Shepherd K, Butcher AR, Macfarlane TD, Coates DJ (2015) Strategic taxonomy in a biodiverse landscape: a novel approach to maximizing conservation outcomes for rare and poorly known flora. Biodivers & Conservation 24:17–32. https://doi.org/10.1007/s10531-014-0785-4

    Article  Google Scholar 

  • Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Rev Ecol Evol Syst 36: 519–539. http://www.jstor.org/stable/30033815

    Article  Google Scholar 

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Acknowledgements

We are grateful to H.H. Sheikh Mohamed bin Zayed Al Nahayan, Crown Prince of Abu Dhabi and Chairman of the International Fund for Houbara Conservation (IFHC), and H.E. Mohamed Al Bowardi, Deputy Chairman of the IFHC, for having provided the main financial support that enabled the collection of data used in this document. We appreciate the help of Herbarium SEV for preserving dry material and the General Greenhouse Service of the University of Seville for the help in plant cultivation. We also thank Dr. Thomas Martin (Reneco International Wildlife Consultants LLC) for reviewing this text, Grégoire Liénart (ECWP) for preparing the map, and the botanical illustrator Rodrigo Tavera for his detailed drawing included as the icon.

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Authors and Affiliations

  1. Department of Plant Biology and Ecology, Universidad de Sevilla, Apdo. 1095, 41080, Seville, Spain

    José A. Mejías

  2. Emirates Center for Wildlife Propagation, Province de Boulemane, BP 47, 33250, Missour, Morocco

    Mathieu Chambouleyron & Jean-François Léger

  3. Department of Biological Sciences, Sungkyunkwan University, 2066 Seobu-ro, Jangan-Gu, Suwon, 16419, Korea

    Seon-Hee Kim & Seung-Chul Kim

  4. Department of Integrated Sciences, Universidad de Huelva (Campus El Carmen), 21071, Huelva, Spain

    M. Dolores Infante

  5. Reneco International Wildlife Consultants LLC, Sky Tower, Offices 3902 & 3903, Al Reem Island, Abu Dhabi, United Arab Emirates

    Jean-François Léger

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Online Resource 1. Collections of Sonchus boulosii for this study.

Online Resource 2. Sequence Alignment of ITS region for the Sonchinae.

Online Resource 3. Sequence Alignment of matk region for the Sonchinae.

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Mejías, J.A., Chambouleyron, M., Kim, SH. et al. Phylogenetic and morphological analysis of a new cliff-dwelling species reveals a remnant ancestral diversity and evolutionary parallelism in Sonchus (Asteraceae). Plant Syst Evol 304, 1023–1040 (2018). https://doi.org/10.1007/s00606-018-1523-2

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