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Parallel Evolution of Arborescent Carrots (Daucus) in Macaronesia

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Parallel Evolution of Arborescent Carrots (Daucus) in Macaronesia RESEARCH ARTICLE Parallel evolution of arborescent carrots (Daucus) in Macaronesia Kamil E. Frankiewicz1,7 , Alexei Oskolski2,3, Łukasz Banasiak1, Francisco Fernandes4, Jean-Pierre Reduron5, Jorge-Alfredo Reyes-Betancort6, Liliana Szczeparska1, Mohammed Alsarraf1, Jakub Baczyński1, and Krzysztof Spalik1 Manuscript received 16 September 2019; revision accepted 2 January PREMISE: Despite intensive research, the pathways and driving forces behind the evolution 2020. of derived woodiness on oceanic islands remain obscure. The genus Daucus comprises 1 Department of Molecular Phylogenetics and Evolution, Institute mostly herbs (therophytes, hemicryptophytes) with few rosette treelets (chamaephytes) of Botany, Faculty of Biology, University of Warsaw, Biological and endemic to various Macaronesian archipelagos, suggesting their independent evolution. Chemical Research Centre, Żwirki i Wigury 101, 02-089 Warsaw, Poland To elucidate the evolutionary pathways to derived woodiness, we examined phylogenetic 2 Department of Botany and Plant Biotechnology, University of relationships and the habit and secondary xylem evolution in Daucus and related taxa. Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, METHODS: Sixty taxa were surveyed for molecular markers, life history, and habit traits. South Africa Twenty-one species were considered for wood anatomical characters. A dated phylogeny 3 Botanical Museum, Komarov Botanical Institute, Prof. Popov 2, 197376 St. Petersburg, Russia was estimated using Bayesian methods. The evolution of selected traits was reconstructed 4 Instituto das Florestas e Conservação da Natureza, Quinta Vila using parsimony and maximum likelihood. Passos, R. Alferes Veiga Pestana 15, 9054-505 Funchal, Madeira, RESULTS: Daucus dispersed independently to the Canary Islands (and subsequently to Portugal Madeira), Cape Verde, and the Azores in the late Miocene and Pleistocene. Life span, 5 Via Apia, 10 rue de l'Arsenal, 68100 Mulhouse, France reproductive strategy, and life form were highly homoplastic; the ancestor of Daucus was 6 Jardín de Aclimatación de la Orotava (ICIA), C/Retama no. 2, 38400 probably a monocarpic, biennial hemicryptophyte. Rosette treelets evolved independently Puerto de la Cruz, S/C de Tenerife, Spain in the Canarian-Madeiran lineage and in Cape Verde, the latter within the last 0.13 7 Author for correspondence (e-mail: [email protected]) Myr. Treelets and hemicryptophytes did not differ in wood anatomy. Pervasive axial Citation: Frankiewicz, K. E., A. Oskolski, Ł. Banasiak, F. Fernandes, J.-P. Reduron, J.-A. Reyes-Betancort, L. Szczeparska, et al. 2020. parenchyma in wood occurred more often in polycarpic rather than monocarpic species. Parallel evolution of arborescent carrots (Daucus) in Macaronesia. CONCLUSIONS: Life span and life form in Daucus are evolutionarily labile and may change American Journal of Botany 107(3): 394–412. independently of wood anatomy, which is related to plant reproductive strategy rather doi:10.1002/ajb2.1444 than to life form. Insular woodiness may evolve rapidly (as demonstrated in D. bischoffii), and in Daucus, it does not seem to be an adaptation to lower the risk of xylem embolism. KEY WORDS Apiaceae; Daucinae; habit evolution; insular woodiness; Melanoselinum; molecular dating; Monizia; secondary woodiness; Tornabenea; wood anatomy. Woodiness was most likely ancestral within angiosperms, and the shift herbaceous species favoring taller individuals; Carlquist (1974) postu- from trees and shrubs to herbs has long been considered a major trend lated that moderate climates with low seasonality and/or the absence in the evolution of flowering plants (e.g., Sinnott and Bailey, 1915); of large herbivores may be responsible for the shift; and recently, Lens however, a large body of evidence suggests that the opposite is also pos- et al. (2013b) and Dória et al. (2018) considered drought adaptation sible and that many woody taxa in various angiosperm lineages origi- to be the trigger because derived woody stems have higher embolism nated from herbaceous ancestors (reviewed, e.g., by Dulin and Kirchoff, resistance than herbaceous relatives. Each of those hypotheses has its 2010). Phenomenon of such evolutionary reversal, known as second- limitations; moreover, they are not mutually exclusive. To the contrary, ary or (phylogenetically) derived woodiness, is often associated with a single causal scenario explaining all cases of derived woodiness is insular woodiness, i.e., the tendency of herbaceous plants to evolve into unlikely (Kidner et al., 2015; Carlquist, 2017). Therefore, to explain rosette trees, shrubs, and other arborescent life forms after dispersal to the evolution of insular woodiness more synthetic studies combining islands. Both phenomena, and especially insular woodiness, have been anatomical and ecological approaches with robust phylogenetic back- extensively discussed since the 19th century, and numerous hypotheses ground are needed. have been proposed to explain them (e.g., Darwin, 1859; Wallace, 1878; Attempts to discover anatomical features that distinguish de- Carlquist, 1974). Darwin suggested increased competition between rived woody plants from ancestral woody ones led to the theory American Journal of Botany 107(3): 394–412, 2020; http://www.wileyonlinelibrary.com/journal/AJB © 2020 The Authors. American Journal of Botany published by Wiley Periodicals, Inc. on behalf of Botanical Society of America. This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, 394 • distribution and reproduction in any medium, provided the original work is properly cited. March 2020, Volume 107 • Frankiewicz et al.—Evolution of arborescence in insular carrots • 395 of paedomorphosis in wood evolution (Carlquist, 1962), which clade (Winter et al., 2008; Magee et al., 2009, 2010). Regardless of the has been extensively studied (Lens et al., 2005, 2007, 2009, 2012a; ancestral condition for subfamily Apioideae, the woody members Neupane et al., 2017) and reviewed in recent years (Carlquist, of Daucinae, as one of its crown groups, are definitely derived from 2009a, b, 2012, 2013; Dulin and Kirchoff, 2010; Lens et al., 2013a). herbaceous ancestors, and this character has been shown to have According to this theory, juvenile or “paedomorphic” traits are a substantial level of homoplasy in various clades of the subfamily expected to persist in the mature wood of derived woody plants. (Calviño et al., 2006; Oskolski and Van Wyk, 2008; Downie et al., However, Lens et al. (2013a) argued that at least some traits usu- 2010; Magee et al., 2010; Banasiak et al., 2016). ally interpreted as being indicators of protracted juvenilism result Recent phylogenetic and taxonomic studies of Daucinae have instead from some distinctive growth forms (rosette trees, stem shown that various woody species that had been previously scat- succulents, and slender-stem shrubs) irrespective of their derived tered among the genera Athamanta, Cryptotaenia, Melanoselinum, or ancestral woodiness. Also, several wood traits not necessarily in- Monizia, Rouya, and Tornabenea are nested within Daucus s.l. and terpreted as juvenile are known to correlate with plant habit (e.g., have been transferred to the latter (Banasiak et al., 2016). The for- Carlquist, 1984; Carlquist and Donald, 1996; Carlquist and DeVore, mer monotypic genera Melanoselinum and Monizia form a clade 1998; Olson and Carlquist, 2001; Carlquist and Grant, 2006; Arévalo (Daucus sect. Melanoselinum) closely related to Daucus s.s. (≡ sect. et al., 2017). Carlquist incorporated this view in his later works, Daucus, which includes the generitype, D. carota), whereas the stud- placing the emphasis of the explanation of protracted juvenilism ied representatives of Tornabenea, as well as Daucus rouyi (≡ Rouya not only with plant evolutionary history, but also with plant growth polygama) and Daucus della-cellae (≡ Athamanta della-cellae), are form (Carlquist, 2009b) and trait function (Carlquist, 2012, 2015a, b, nested within sect. Daucus. However, the phylogenetic positions of 2018). D. elegans from the Canary Islands and D. bischoffii (≡ T. bischoffii), Experimental data on the model plant Arabidopsis thaliana a rosette treelet from Cape Verde, remain obscure. The former was suggest that the gain of a prominent wood cylinder requires small resolved as either the sister to the two Madeiran Daucus species genetic changes (Chaffey et al., 2002; Ko et al., 2004; Melzer et al., (D. decipiens and D. edulis; Spalik and Downie, 2007; Banasiak et al., 2008; Lens et al., 2012b; Rowe and Paul-Victor, 2012; Davin et al., 2013) or included in sect. Daucus as the sister to the remaining spe- 2016); therefore, derived woodiness may evolve in a relatively short cies of sect. Daucus (Banasiak et al., 2016). The phylogenetic position time. However, even though derived woodiness is a widespread of D. bischoffii has never been investigated with molecular data. It is phenomenon found in many families (Park et al., 2001; Barber possible that D. bischoffii is nested within sect. Daucus, like other for- et al., 2002; Francisco-Ortega et al., 2002; Lee et al., 2005; Nürk et al., mer members of Tornabenea. However, as in the case of D. elegans, 2019), the ages of derived and, in particular, insular woody clades it is also possible that the species is related to the Madeiran endemics remain mostly unknown (Kim et al., 2008), obstructing our under- forming sect. Melanoselinum (Fig. 2), a scenario
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