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Asteraceae, Lactuceae) of the Western Mediterranean Marı´Aa´ Ngeles Ortiz1*, Karin Tremetsberger1,2, Tod F

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Asteraceae, Lactuceae) of the Western Mediterranean Marı´Aa´ Ngeles Ortiz1*, Karin Tremetsberger1,2, Tod F Journal of Biogeography (J. Biogeogr.) (2009) 36, 1384–1397 SPECIAL Phylogeographic patterns in Hypochaeris ISSUE section Hypochaeris (Asteraceae, Lactuceae) of the western Mediterranean Marı´aA´ ngeles Ortiz1*, Karin Tremetsberger1,2, Tod F. Stuessy2, Anass Terrab1,2, Juan L. Garcı´a-Castan˜o1 and Salvador Talavera1 1Departamento de Biologı´a Vegetal y Ecologı´a, ABSTRACT Universidad de Sevilla, Sevilla, Spain and Aim To analyse phylogeographic patterns in the four species of Hypochaeris sect. 2Department of Systematic and Evolutionary Botany, Faculty Centre Biodiversity, University Hypochaeris, evaluating possible areas of origin and the microevolutionary of Vienna, Vienna, Austria processes that have shaped their morphology, genetics and distribution. Location Western Mediterranean area. Methods We applied amplified fragment length polymorphism (AFLP) markers to a total of 494 individuals belonging to 82 populations of Hypochaeris arachnoidea, H. glabra, H. radicata and H. salzmanniana to determine population structure. Results Populations with the largest proportion of private and rare AFLP fragments were found in Morocco. This region was consequently inferred to be the ancestral area for H. arachnoidea, H. glabra, H. radicata and H. salzmanniana. The Guadalquivir River (southern Spain) was inferred to be an effective dispersal barrier for H. glabra and H. radicata. The Strait of Gibraltar was inferred to be a somewhat weaker barrier than the Guadalquivir River for H. radicata and a much weaker barrier for H. glabra. The main barrier for H. salzmanniana coincides with the extension of the Rif Mountains to the Atlantic coast in Morocco, and the Strait of Gibraltar is a much weaker barrier for this species. Hypochaeris arachnoidea appears to have originated in the Atlas Mountains. Main conclusions The highest levels of genetic variation in La Mamora forest (H. glabra and H. salzmanniana) or the adjacent central Middle Atlas (H. arachnoidea and H. radicata) in Morocco suggest that these areas were a centre of origin of Hypochaeris sect. Hypochaeris. All three potential barriers – the Guadalquivir River, the Strait of Gibraltar, and the Rif Mountains – have been *Correspondence: Marı´aA´ ngeles Ortiz, important in shaping genetic diversity in species of section Hypochaeris. ´ ´ Departamento de Biologıa Vegetal y Ecologıa, Keywords Universidad de Sevilla, Apdo-1095, 41080 Sevilla, Spain. AFLP, Atlas Mountains, Guadalquivir River, Iberian Peninsula, phylogeography, E-mail: [email protected] population genetic variation, rare fragments, Rif Mountains, Strait of Gibraltar. which now separates the old Palaeozoic lands of the Sierra INTRODUCTION Morena to the north from the Tertiary lands of the Betic The western Mediterranean region has undergone dramatic Sierras; the Riffian Corridor occupied the modern Loukos and geomorphological and environmental changes during the past Sebou river valleys in Morocco, which separate the Rif 8 Myr (Thompson, 2003). The principal events were the Mountains to the north from the Atlas ranges to the south. closure of the connection to the Atlantic (7–5.33 Ma) and the These sea channels constituted formidable barriers for the opening of the Strait of Gibraltar (5.33 Ma). migration of plants and animals between North Africa and The pre-Mediterranean sea had two seaway connections Europe. This situation changed dramatically with the closure with the Atlantic Ocean: the Betic and the Riffian corridors. of the two Mediterranean–Atlantic channels (at 7–5.33 Ma), The Betic Corridor became the future Guadalquivir valley, creating the so-called Messinian Salinity Crisis, with the drying 1384 www.blackwellpublishing.com/jbi ª 2009 The Authors doi:10.1111/j.1365-2699.2008.02079.x Journal compilation ª 2009 Blackwell Publishing Ltd Phylogeographic patterns in Hypochaeris section Hypochaeris out of much of the Mediterranean Basin, followed by the 1995, 2008; Weiss et al., 2003; Weiss-Schneeweiss et al., 2003, opening of the Strait of Gibraltar (at around 5.33 Ma). Until 2007, 2008), DNA sequences (Cerbah et al., 1998; Samuel c. 3.2 Ma, the climate of the south-western Mediterranean area et al., 2003; Tremetsberger et al., 2005), AFLP population seems to have been subtropical, although cold and arid analyses (Stuessy et al., 2003; Tremetsberger et al., 2003a,b, conditions were apparently established in North Africa from 2004, 2006; Muellner et al., 2005; Mraz et al., 2007; Ortiz around 3.9 Ma (Estabrook, 2001). A mediterranean-type et al., 2007, 2008) and reproductive biology (Ortiz et al., climate, with warm, wet winters and hot, dry summers, seems 2006). To date, South American species have been the focus to have become established during the Pliocene (around of research because they represent the greatest concentration 3.5 Ma), before the onset of the Northern Hemisphere of species diversity. glaciations at around 2.4 Ma. The latter gave rise to oscillating We review available data for Hypochaeris sect. Hypochaeris changes in sea level in the Strait of Gibraltar area that exposed and focus on four biogeographical issues: (1) the possible area and submerged islands in this area during the glacial cycles. Up of origin of this section; (2) the impact of the Strait of to now, relatively few studies have been concerned with the Gibraltar on populations of H. glabra, H. radicata and evolutionary and biogeographical consequences of Pleistocene H. salzmanniana; (3) the impact of the Guadalquivir River glacial cycles on northern African and southern European taxa. in southern Spain on population divergence in H. glabra and There were three important biogeographical barriers for H. radicata; and (4) patterns of genetic divergence in terrestrial plant species in the western Mediterranean area after H. arachnoidea in Morocco. the Messinian age: the Guadalquivir valley, the Strait of Gibraltar, and the Loukos and Sebou valleys in Morocco. The MATERIALS AND METHODS most important bioclimatic changes in the Mediterranean Basin over the last 5 Myr were: (1) the establishment of the Hypochaeris sect. Hypochaeris mediterranean climate during the Pliocene (c. 3.5 Ma), and (2) the glacial periods of the Pliocene and Pleistocene. The onset of Section Hypochaeris is a monophyletic group (Tremetsberger the mediterranean climate caused very dramatic changes in the et al., 2005) composed of four species: H. arachnoidea Poir., woodlands, particularly in the understorey, with selective H. glabra L., H. radicata L. and H. salzmanniana DC. In pressure to shorten plant life cycles, or to modify underground addition to having morphological differences, these species rhizomes to form corms. As a consequence, more than 50% of differ in a range of other parameters: (1) life-form: H. radicata the plant species of the Mediterranean Basin are annuals is perennial whereas H. arachnoidea, H. glabra and H. salz- (Talavera, 1991), and rhizomatous plants are confined to the manniana are annuals; (2) somatic chromosome number: more humid environments (e.g. streams, lagoons and springs) H. glabra has 2n = 10 chromosomes, whereas H. arachnoidea, or to the mesic understorey. The Quaternary glacial periods H. radicata and H. salzmanniana have 2n = 8 chromosomes shaped the expansion and diversification of plant populations (Tremetsberger et al., 2005); and (3) distribution: H. glabra along the western Mediterranean. During glacial periods, the and H. radicata are widespread in the Mediterranean region sea level was lowered, for example by 130 m in the Last Glacial and also occur as weeds world-wide, whereas H. arachnoidea is Maximum, some 20,000 years ago, and the temporarily endemic to North West Africa (Morocco and Algeria) and emergent coastlines occupied by plant populations were used H. salzmanniana is restricted to the Atlantic coast of Morocco as land-bridges for colonization. During interglacials, the sea and south-western Spain (Ca´diz). The natural habitat of the transgressed and coastal populations suffered drastic reduc- former three species is the understorey of open Quercus tions and possibly extinctions. All of these influences have led woodland (although weedy invasive populations of H. glabra to complex evolutionary and biogeographical patterns in the and H. radicata occur in different habitats), but H. salzman- biota of the Mediterranean region, especially in the western niana occurs principally on coastal dunes. All four species can part (Jong, 1998; Ve´la & Benhouhou, 2007). hybridize in the greenhouse, but in nature hybrids have never Further assessment of the impact of these environmental been found in the natural range of the species. However, changes in the western Mediterranean requires the study of Parker (1975) found sterile hybrids between H. glabra and additional groups, such as the genus Hypochaeris, which can H. radicata in England, where both species are non-native. As serve as a model system. The genus consists of c. 58 species with many composites, Hypochaeris species have sporophytic world-wide, with only 15 confined to the Mediterranean self-incompatibility (SSI), requiring obligatory cross-pollina- region, three in Eurasia, and more than 40 in South America. tion (usually mediated by solitary bees) for fruit-set. Within Of those in the Mediterranean area, section Hypochaeris, with section Hypochaeris, SSI is found in H. arachnoidea and four species, is centred in the western Mediterranean. This H. radicata and in most populations of H. salzmanniana, section is monophyletic (Tremetsberger et al., 2005) and whereas H. glabra is
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