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Phylogeography of the Invasive Weed Hypochaeris Radicata

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Phylogeography of the Invasive Weed Hypochaeris Radicata Molecular Ecology (2008) 17, 3654–3667 doi: 10.1111/j.1365-294X.2008.03835.x PhylogeographyBlackwell Publishing Ltd of the invasive weed Hypochaeris radicata (Asteraceae): from Moroccan origin to worldwide introduced populations M. Á. ORTIZ,* K. TREMETSBERGER,*† A. TERRAB,*† T. F. STUESSY,† J. L. GARCÍA-CASTAÑO,* E. URTUBEY,‡ C. M. BAEZA,§ C. F. RUAS,¶ P. E. GIBBS** and S. TALAVERA* *Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo-1095, 41080 Sevilla, Spain, †Department of Systematic and Evolutionary Botany, Faculty Center Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria, ‡División Plantas Vasculares, Museo de La Plata, Paseo del Bosque s/n, La Plata, CP 1900, Argentina, §Departamento de Botánica, Universidad de Concepción, Casilla 160-C, Concepción, Chile, ¶Departamento de Biologia Geral, Universidade Estadual de Londrina, Londrina, Paraná, Brazil, **School of Biology, University of St Andrews, Scotland, UK Abstract In an attempt to delineate the area of origin and migratory expansion of the highly successful invasive weedy species Hypochaeris radicata, we analysed amplified fragment length polymorphisms from samples taken from 44 populations. Population sampling focused on the central and western Mediterranean area, but also included sites from Northern Spain, Western and Central Europe, Southeast Asia and South America. The six primer combinations applied to 213 individuals generated a total of 517 fragments of which 513 (99.2%) were polymorphic. The neighbour-joining tree presented five clusters and these divisions were supported by the results of Bayesian analyses: plants in the Moroccan, Betic Sierras (Southern Spain), and central Mediterranean clusters are all heterocarpic. The north and central Spanish, southwestern Sierra Morena, and Central European, Asian and South American cluster contain both heterocarpic (southwestern Sierra Morena) and homocarpic populations (all other populations). The Doñana cluster includes two homocarpic popula- tions. Analyses of fragment parameters indicate that the oldest populations of H. radicata are located in Morocco and that the species expanded from this area in the Late Quaternary via at least three migratory routes, the earliest of which seems to have been to the south- western Iberian Peninsula, with subsequent colonizations to the central Mediterranean area and the Betic Sierras. Homocarpic populations originated in the southwestern Iberian Peninsula and subsequently spread across north and central Spain, Central Europe and worldwide, where they became a highly successful weed. Keywords: AFLP markers, alien species, Asteraceae, genetic diversity, Hypochaeris radicata, phylogeography Received 1 February 2008; revision accepted 13 May 2008 notably due to human activity, and such facilitated Introduction expansions of area can sometimes result in invasive A basic evolutionary phenomenon, particularly in populations. In their natural habitat, the expansion of postglacial Europe, is the gradual expansion of the area of species may be constrained by factors such as competition distribution of species (Hewitt 1999). The spread of many with other taxa, or physical environmental parameters. If species outward from their original area has increased the limits of natural dispersal can be overcome, however, a species may be able to very successfully colonize new habitats in which the plants tend to be more vigorous Correspondence: M. Á. Ortiz, Fax: +0034 954557059; and individuals often more abundant than in their native E-mail: [email protected] area. © 2008 The Authors Journal compilation © 2008 Blackwell Publishing Ltd PHYLOGEOGRAPHY OF HYPOCHAERIS RADICATA 3655 Various authors have noted that there are very few valid low population growth rate. If the population growth is generalizations to explain the extraordinary success of fast, the reduction in heterozygosity is likely to be low, even some invasive species (Daehler & Strong 1993; Blossey & if the number of founders is few. Nötzold 1995; but see review of consequences of reproduc- The family Asteraceae comprises around 8.4% of the tive diversity for plant invasion by Barrett et al. 2008), world flora and around 14.4% of the European flora although various factors have been proposed, such as the (Pyšek 1998). In a study of the alien species in 26 local floras new habitat providing more favourable conditions, the worldwide, Pyšek (1997) concluded that members of the absence of predators (Crawley 1987), or as a consequence Asteraceae were present in all alien floras, with an average of the re-allocation of resources due to trade-offs in biomass contribution of 13.5%, and were the second most repre- allocation (Blossey & Nötzold 1995). Other authors (e.g. sented family, after the Poaceae. Several authors have Neuffer & Hurka 1999) have suggested that invasive species argued that the Asteraceae possess ideal features for colo- are genetically pre-adapted to their new habitats. In recent nizers, i.e. high reproductive rate, specialized dispersal times, the spread of domesticated grazing animals from structures, and a diversity of metabolic products providing Europe to extensive pastures in the Americas and Australia protection from grazing, etc. (Pyšek 1997, 1998; Caño et al. (Baker 1974) has favoured the exchange and establishment 2007). of weeds in areas that had not been previously exposed to Hypochaeris radicata is a very successful colonizing species such grazing pressure. that now has a presence on virtually all continents. Beyond Although the majority of successful invasive plant species its probable native area in the Mediterranean region, where involve self-compatibility or marked vegetative reproduc- it occurs in relatively sparse populations associated with tion (Baker 1974; Rambuda & Johnson 2004), there are humid evergreen woodland, H. radicata is a successful some examples of self-incompatible (SI) species that have invasive weed in Northern and Central Europe, where it is achieved notable colonizing success (Lafuma & Maurice apparently very flexible with regard to soil requirements 2007). Since the major genetic bottlenecks that usually and growth conditions (Turkington & Aarssen 1983), and accompany founding events can cause the total breakdown recent studies in southeastern Australia showed that H. of SI systems, to yield self-compatible individuals (Reinartz radicata is one the most common dicotyledonous plants of & Les 1994), the survival of SI probably requires some temperate perennial pastures (Dellow et al. 2002). Likewise, flexibility in the system (Hiscock 2000). In many SI species, Doi et al. (2006) found H. radicata in all parts of temperate some plants produce a low proportion of seeds from Japan, commonly in grasslands, with a distribution that is self-pollen, a phenomenon called pseudo-self-compatibility still expanding, and this species is also very common in (PSC; Nettancourt 1977), and such PSC may be particularly South America (Cabrera 1971, 1978, 1987) with populations advantageous in small, newly established populations that comprising large numbers of individuals. The timing of have little S-allele diversity (Levin 1996). During founding this remarkable expansion is largely unknown, but it is events, mating may be restricted due to the reduced number likely to have occurred in recent times. In the Flora Brazilensis of S alleles in the initial population (Byers & Meagher 1992; (Eichler 1884), there is no record of H. radicata for Brazil at but see Brennan et al. 2006), and selection may favour the that time, although it is now abundant in the south of this spread of PSC individuals that will allow the population to country, and similar recent colonization events have been increase. Although the offspring of PSC parents may suffer noted for this species in New Zealand (Esler & Astridge the effects of inbreeding depression, this is likely to be 1987) and Lord Crowe Island in the Pacific Ocean (Pickard outweighed by the reproductive assurance achieved (Hiscock 1984). 2000). Subsequently, if the population size and S-allelic Amplified fragment length polymorphisms (AFLPs) diversity increase, as when aided by the arrival of new have been established as useful genetic markers in studies genotypes via recolonization events, or perhaps by mutation, of genetic diversity and biogeographical patterns that have the level of PSC may decline (Levin 1996). This can have been shaped by Quaternary climatic changes in Mediterra- important evolutionary consequences, especially when nean plant species such as Anthyllis montana (Kropf et al. stochastic processes are involved, since in general, PSC 2002), Armeria pungens (Piñeiro et al. 2007), Limonium dufourii populations are likely to have higher fixation probabilities (Palacios et al. 1999), and other coastal plant species (Levin 1996). (Kadereit et al. 2005) and with three South American species The amount of genetic variation in a species and its of Hypochaeris: H. tenuifolia, H. palustris, and H. acaulis distribution among and within populations is determined (Tremetsberger et al. 2003a, b; Muellner et al. 2005), and by a large number of factors, such as the breeding system, also with Hypochaeris salzmanniana, a species of the north- historical events (e.g. habitat availability, population size, western Moroccan–southwestern Iberian Atlantic coast migration between populations), and many ecological (Tremetsberger et al. 2004; Ortiz et al. 2007). factors. Nei et al. (1975) argued that the loss of heterozygosity In the present
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