Conservation Genetics of an Endemic from The

Conserv Genet (2013) 14:963–972 DOI 10.1007/s10592-013-0487-6 RESEARCH ARTICLE Conservation genetics of an endemic from the Mediterranean Basin: high genetic differentiation but no genetic diversity loss from the last populations of the Sicilian Grape Hyacinth Leopoldia gussonei K. Vandepitte • A. S. Gristina • R. De Raedt • I. Roldań-Ruiz • C. Marceno` • S. Sciandrello • O. Honnay Received: 10 October 2012 / Accepted: 2 April 2013 / Published online: 16 April 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract The Mediterranean Basin is a biodiversity Conservation efforts should therefore focus on the preser- hotspot, housing [11.000 narrowly endemic plant species, vation of all sites where L. gussonei still occurs, yet the many of which are declining due to mass tourism and deliberate introduction of diverse material into the smallest agricultural intensification. To investigate the genetic populations seems unneeded as clonality likely mitigated resource impacts of ongoing habitat loss and degradation, genetic drift effects thus far. More generally, our findings we characterized the genetic variation in the last known support the view that endemic plant species with a narrow populations of Leopoldia gussonei, a self-compatible ecological amplitude, as many specialists in Mediterranean endangered Sicilian Grape Hyacinth numbering less than coastal ecosystems, are highly genetically differentiated 3,000 remaining individuals, using AFLP. Results dem- and that conservation of their genetic diversity requires onstrated significant genome-wide genetic differentiation preservation of most, if not all of their extant populations. among all extant populations (UST = 0.05–0.56), and genetic clustering according to geographic location. Gene Keywords Mediterranean Basin Á AFLP Á Asparagaceae Á diversity was fairly constant across population (mean Habitat loss Á Habitat degradation Á Narrow endemics HE = 0.13) and was neither affected by current population size nor by spatial isolation. Vegetation analysis showed the presence of known invasive weeds in a quarter of the Introduction populations, but we found no relation between genetic diversity and plant community composition. The marked The Mediterranean Basin is a biodiversity hotspot, har- genetic differences among populations and the profusion of boring *22,500 vascular plant species, which more than rare and private alleles indicate that any further population quadruples the number found in all the rest of Europe. loss will lead to significant losses of genetic diversity. More than half of these species are endemic to the region, K. Vandepitte (&) Á R. De Raedt Á O. Honnay I. Roldań-Ruiz Plant Conservation and Population Biology, Biology Plant Sciences Unit–Growth and Development, Institute for Department, University of Leuven, Kasteelpark Arenberg 31, Agricultural and Fisheries Research ILVO, Caritasstraat 21, 3001 Heverlee, Belgium 9090 Melle, Belgium e-mail: [email protected] e-mail: [email protected] R. De Raedt ` e-mail: [email protected] C. Marceno Jardıń Botańico Atlantico, University of Oviedo Indurot, O. Honnay Av del Jardıń Botańico, 33394 Gijon, Spain e-mail: [email protected] e-mail: [email protected] A. S. Gristina S. Sciandrello Department of Agro-Environmental Systems, University of Department of Botany, University of Catania, Palermo, Viale delle Scienze, 90128 Palermo, Italy v. A. Longo 19, 95100 Catania, Italy e-mail: [email protected] e-mail: [email protected] 123 964 Conserv Genet (2013) 14:963–972 of which most are narrow endemics confined to a small attention thus far (Palacios et al. 1999; Juan et al. 2004; area, such as to any of the *5,000 islands scattered Palop-Esteban et al. 2007). Here we investigate the con- throughout the Mediterranean Sea (Suc 1984; Greuter servation genetics of Leopoldia gussonei Parl. (Asparaga- 1991; Dallman 1998;Me´dail and Que´zel 1999). Defores- ceae), a self-fertile Grape Hyacinth endemic to Sicily tation over thousands of years has considerably altered the (Italy), whose current conservation status is well-repre- inland vegetation of this region and, over the last century, sentative for many narrow endemics in coastal areas of the the development of mass tourism and agricultural intensi- Mediterranean Basin (Me´dail and Que´zel 1999). Leopoldia fication have also increasingly strained plant diversity in gussonei is now restricted to eight fragmented populations coastal areas, either directly through habitat clearance or along the Southern coast near Gela (Cundari et al. 2003; indirectly through habitat degradation and the spread of Brullo et al. 2011; Fig. 1) but used to be more widespread exotic plant species. Today, a sheer 5 % of the Mediter- in the region (Albo 1919; Garbari and Di Martino 1972; ranean Basin is covered by relatively unaffected vegeta- Brullo and Marceno` 1974). Greenhouse agriculture and the tion. Many narrow endemics, which naturally comprise mechanization of vineyard maintenance imperils the per- only a small number of individuals and populations, are sistence of L. gussonei, both directly through habitat currently endangered, if not already extinct (Greuter 1994; destruction, and indirectly through the degradation of Me´dail and Que´zel 1999). adjacent habitats (Brullo et al. 2011). Other immediate An essential component of biodiversity is the genetic threats include tourism infrastructure development, and variation held within and among individuals and popula- grazing by feral livestock. A potential threat in the longer tions of a species. Its maintenance is crucial to sustain term is the invasion of exotic plant species such as the viable populations and to secure the evolutionary potential African Hottentot Fig (Carpobrotus sp.). As a conse- of the species (Reed and Frankham 2003; Jump et al. quence, the species is red-listed as endangered by the 2009). In habitat-specific plant species, habitat destruction IUCN [B2ab(i,ii,iii,iv,v)] and listed as a priority taxon for and the associated loss of populations will immediately conservation in the Habitat Directive 92/43 CEE and the decrease the species’ genetic variation (Young et al. 1996). Bern Convention. Seeds have been collected for ex situ The impact will be especially high when the initial number conservation, yet L. gussonei is currently not included in of populations was already low, as for endemic species, regional or national protection laws or plans (Brullo et al. and if the genetic differences among populations are 2011). marked (Palop-Esteban et al. 2007). The remaining popu- Using Amplified Fragment Length Polymorphism lations, bound to live in spatially isolated habitat remnants markers (AFLP; Vos et al. 1995), we analyzed all known of often degraded quality, may lose genetic variation in a extant L. gussonei populations. We specifically aimed to: more gradual manner. Populations that remain small for (i) quantify the amount and distribution of genome-wide subsequent generations, for instance because suboptimal genetic variation in order to delineate conservation units; habitat conditions continuously hamper sexual recruitment (ii) infer whether ongoing habitat loss and/or degradation or survival (Vergeer et al. 2003; de Vere et al. 2009), are are eroding the adaptive potential of the remaining popu- more likely to lose alleles through genetic drift than large lations by studying how genetic variation is affected by the populations (Wright 1938; Ellstrand and Elam 1993). size, spatial isolation and habitat quality of the populations; When these small populations become spatially isolated (iii) define conservation priorities. due to the loss of nearby populations, gene inflow may no longer replenish the alleles lost and as generations pass, the magnitude of genetic variation will decrease (Ellstrand and Materials and methods Elam 1993; Young et al. 1996). This process, i.e. the accelerated loss of genetic variation due to anthropogenic Species description habitat disturbance, is perceived to occur more rapidly in endemic plant species, which tend to have smaller initial Leopoldia gussonei is a diploid (2n = 2x = 18), bulbous effective population sizes (Gitzendanner and Soltis 2000; geophyte in the Asparagaceae family, subfamily Scilloi- Cole 2003; but see Honnay and Jacquemyn 2007) and very deae. Leaves sprout from underground bulbs in early specific habitat requirements. spring. The single or double stems are 10–30 cm tall and Knowledge of the distribution of genetic variation and the upper halves of stems produce urn-shaped flowers. The of the factors potentially undermining its maintenance is infertile flowers at the top are blue-colored while the fertile hence a critical step towards the adequate long-term in situ flowers lower down are yellow and less ostentatious, as in conservation of endangered endemic species (Haig 1998; the closely related Muscari species. Flowers bloom from Schoen and Brown 2001). Yet the conservation genetics of March to May and set capsular fruits (Garbari and Di coastal Mediterranean endemics has received little Martino 1972). The species is highly self-fertile. The 123 Conserv Genet (2013) 14:963–972 965 Fig. 1 Map of the distribution of Leopoldia gussonei along the Southern coast of Sicily (Italy) fruiting success of bagged individuals in the field was on silica and DNA was extracted using the Nucleospin DNA- *80 %, comparable to the reproductive success of open- extraction kit (Macherey–Nagel, Germany). EcoRI and MseI pollinated

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