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Phylogenetic and Morphological Analysis of a New Cliff-Dwelling

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Phylogenetic and Morphological Analysis of a New Cliff-Dwelling Plant Systematics and Evolution (2018) 304:1023–1040 https://doi.org/10.1007/s00606-018-1523-2 ORIGINAL ARTICLE Phylogenetic and morphological analysis of a new clif‑dwelling species reveals a remnant ancestral diversity and evolutionary parallelism in Sonchus (Asteraceae) José A. Mejías1 · Mathieu Chambouleyron2 · Seon‑Hee Kim3 · M. Dolores Infante4 · Seung‑Chul Kim3 · Jean‑François Léger2,5 Received: 23 December 2017 / Accepted: 18 May 2018 / Published online: 19 July 2018 © Springer-Verlag GmbH Austria, part of Springer Nature 2018 Abstract We describe a new clif-dwelling species within Sonchus (Asteraceae): Sonchus boulosii and analyze its systematic position and evolutionary signifcance; 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 diferentiation from the remaining major clades. ITS phylogenetic trees show that likely evolutionary shifts to rocky habitat took place at least fve 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 refects a phenomenon of homoplasy, probably driven by parallel evolutionary adaptations to the severe ecological constraints of its clif 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 morphol- ogy, may refect the persistence of some primitive characteristics. Keywords Homoplasy · Karyogram · matK cpDNA · nrDNA ITS · Parallel evolution · Western Mediterranean Handling Editor: Christoph Oberprieler. Introduction Electronic supplementary material The online version of this Predictions of biodiversity loss associated with the loom- article (https​://doi.org/10.1007/s0060​6-018-1523-2) contains ing sixth mass extinction crisis (van Vuuren et al. 2006; supplementary material, which is available to authorized users. Barnosky et al. 2011; Regnier et al. 2015) have placed an * José A. Mejías increased urgency on taxonomic eforts regarding the dis- [email protected] covery and description of new species. Achieving an acceler- ated rate of taxonomic discovery requires signifcant funding 1 Department of Plant Biology and Ecology, Universidad de Sevilla, Apdo. 1095, 41080 Seville, Spain support (Valdecasas and Camacho 2003; Mora et al. 2011), and also the development of novel and efective taxonomic 2 Emirates Center for Wildlife Propagation, Province de Boulemane, BP 47, 33250, Missour, Morocco strategies (Wägele et al. 2011; Wege et al. 2015), especially within poorly studied areas. In this respect, the initiative of 3 Department of Biological Sciences, Sungkyunkwan University, 2066 Seobu‑ro, Jangan‑Gu, Suwon 16419, Korea the Emirates Center for Wildlife Propagation (ECWP) of promoting botanical feld surveys in regions that have been 4 Department of Integrated Sciences, Universidad de Huelva (Campus El Carmen), 21071 Huelva, Spain highlighted as being under-explored (Dobignard 2002), such as Eastern and Saharan Morocco, as a part of a research 5 Reneco International Wildlife Consultants LLC, Sky Tower, Ofces 3902 & 3903, Al Reem Island, Abu Dhabi, program on natural habitats should be welcomed. To date, United Arab Emirates this research program has yielded its most signifcant results Vol.:(0123456789)1 3 1024 J. A. Mejías et al. ab e f cd g i 12 354 h jmk l Fig. 1 Ecology and morphology of Sonchus boulosii and other clif- a glandular hair; g anthers and style during anthesis; h external fo- dwelling Sonchus species: a clifs in the Debdou Mountains which rets with a purple band on the back; i achenes of S. boulosii (1, Jbel sustain one of the known populations of this new species; b detail of Tsiouant, SEV 286736; 2, Debdou Mts., SEV 286734), S. pustulatus natural habitats of the population in the Debdou Mountains; c vegeta- (3, SEV 120991), S. fragilis (4, SEV 285880) and S. masguindalii (5, tive plant within its natural habitat; d plant from Jbel Tsiouant (Mid- SEV 285890); j–m appearance of several clif-dwelling Sonchus spe- dle Atlas) cultivated in a greenhouse; e capitulum of a plant from cies: S. pustulatus (j), S. fragilis (k), S. masguindalii (l) and S. radi- the Debdou Mountains during the maturation of achenes; f detail of catus (m). Scale bars: 2 mm (1e, g–i), 0.5 mm (1f) 1 3 Sonchus boulosii, remnant diversity in Sonchus 1025 from the Lamrija plain and the Debdou mountains (East- analyze its phylogenetic relations and discuss its system- ern Morocco) with the discovery of three new plant taxa atic position; (3) to address the signifcance of the species (Chambouleyron et al. 2015a) here. Two of these have been within the evolutionary history of the genus; and (4) assess described previously (Chambouleyron et al. 2014, 2015b), the conservation status of the new species according to its with the third, a species of the genus Sonchus L., being pre- rarity. Additionally, we also provide a key to the Sonchus sented here. species of Morocco. The new species was initially detected in the Debdou Mountains, with its presence also being confrmed later in the Middle Atlas and the Eastern High Atlas. It bears clear Materials and methods morphological similarities to the components of Sonchus sect. Pustulati Boulos (Fig. 1), three endemic species from Morphological study the Baetic–Rifan–Tellian region in the western Mediterra- nean (Boulos 1973; Silva et al. 2015a) that constitute a well- Our morphological study was based on measurements taken defned clade within Sonchus (Kim et al. 2007). Similarly from 54 dried specimens of Sonchus boulosii Chamboul., to these, it possesses a typical rupicolous ecology, coloniz- Mejías & J.F.Léger collected in the feld during seven feld- ing rock crevices in (mainly north facing) calcareous clifs work visits to the four currently known populations, respec- (Fig. 1a–c). Therefore, it could be plausibly proposed that tively located within the Oran Meseta mountains (Debdou the new species should be placed within this clade. However, Mountains), Middle Atlas (Jbel Tsiouant) and Eastern High the incorporation of a new component with a distribution Atlas (Bourdim and Chabkat Bou Ghrara) (Online Resource extended to the Atlas System and the mountain massifs of 1). The specimens are kept in the herbariums ECWP, G, the Oran Meseta would force a reinterpretation of the bio- P, RAB, SEV. For measurements of macro-characters an geography of sect. Pustulati, whose disjunctive distribution electronic digital Mitutoyo caliper C107127 was used. is thought to be the result of a tight biogeographical asso- Measurements of micro-characters were completed using ciation with the geologic history of the Baetic–Rif–Tell or a stereoscopic microscope Leica S6D. Pictures of micro- Baetic–Maghrebides orogen (Rosenbaum et al. 2002; Chal- characters were taken using a technical Leica MCD170 HD ouan et al. 2008; Silva et al. 2015a). This geological terrain Photomicroscope. includes most Andalusia (Spain) in the northern side and the Rif Mountains (Morocco) and the Tell Coastal Ranges Molecular sampling, DNA extraction, PCR (Algeria) in the southern side, two regions at present sepa- amplifcation, sequencing and alignment rated by the Mediterranean Sea but with a common geologic origin and high foristic afnities (Valdés 1991; Médail and Fresh leaf tissue samples were collected in the wild and dried Quézel 1997). They seem to be originated on the European in silica gel, with four individuals being taken from each of plate from terrains attached to the Iberian Peninsula and the populations of the Debdou Mountains and Jbel Tsiouant southern France in the Oligocene that migrated and rotated in July 2014, four individuals from the population of Bour- across the western Mediterranean Sea during Alpine orogeny dim in July 2017 and two individuals from Chabkat Bou (Rosenbaum et al. 2002; Chalouan et al. 2008). The Atlas Ghrara population in May 2017. To avoid clonal repetition, Mountains, meanwhile, are an intracontinental, autochtho- plants from which material was collected were distanced at nous system which developed over the crust of the African least 5 m from each other. Total DNA was isolated from sil- plate during the same period of Alpine orogenesis (Frizon ica-gel-dried leaf tissue using DNeasy plant mini kits (QIA- de Lamotte et al. 2008), and the Eastern Morocco mountains GEN, Carlsbad, California, USA). PCR amplifcation of ITS system, which is part of the Oran Meseta, comprises Paleo- of nrDNA and matK gene was the same as described previ- zoic massifs of the cited African plate, located to the south ously (Lee et al. 2005; Kim et al. 2007). PCR products were of the Rif–Tell system (Michard et al. 2008). It should be purifed with the QiaQuick PCR Purifcation kit (QIAGEN). considered whether the morphological
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