Anales del Jardín Botánico de Madrid Vol. 68(2): 175-197 julio-diciembre 2011 ISSN: 0211-1322 doi: 10.3989/ajbm.2260 Genetic and morphological diversity in Armeria (Plumbaginaceae) is shaped by glacial cycles in Mediterranean refugia by Javier Fuertes Aguilar1, Belén Gutiérrez Larena & Gonzalo Nieto Feliner Real Jardín Botánico, CSIC, Plaza de Murillo 2, E-28014 Madrid, Spain 1 [email protected] Abstract Resumen Fuertes Aguilar, J., Gutiérrez Larena, B. & Nieto Feliner, G. 2011. Fuertes Aguilar, J., Gutiérrez Larena, B. & Nieto Feliner, G. 2011. Genetic and morphological diversity in Armeria (Plumbagi- La diversidad genética y morfológica en Armeria (Plumbagi- naceae) is shaped by glacial cycles in Mediterranean refugia. naceae) se debe a los ciclos glaciales en los refugios mediterrá- Anales Jard. Bot. Madrid 68(2): 175-197. neos. Anales Jard. Bot. Madrid 68(2): 175-197 (en inglés). Little is known of the direct effects of Quaternary glaciation- Poco se sabe de los efectos directos de los ciclos de glaciación- deglaciation cycles in plants within southern European refugia. deglaciación del Cuaternario sobre las plantas de los refugios This study, centered in the Sierra Nevada (S Spain), used RAPD glaciales del S de Europa. En el presente estudio, centrado en and morphometric data from 36 populations of Armeria Sierra Nevada (S de España), hemos empleado RAPD y datos (Plumbaginaceae) from five taxa belonging to three species that morfométricos de 36 poblaciones de Armeria (Plumbaginaceae) are endemic to that region: A. filicaulis subsp. nevadensis, A. fi- de cinco táxones pertenecientes a tres especies endémicas de li caulis subsp. trevenqueana, A. filicaulis subsp. alfacarensis, esa región: A. filicaulis subsp. nevadensis, A. filicaulis subsp. tre- A. splendens, and A. villosa subsp. bernisii. The results based on venqueana, A. filicaulis subsp. alfacarensis, A. splendens y A. vil- genetic analyses at the population level (AMOVA, genetic diver- losa subsp. bernisii. Los resultados basados en el análisis genéti- sity, genetic distance) and genetic and morphological analyses co a nivel poblacional (AMOVA, diversidad genética, distancia at individual level (haplotype phenetic distance, PCO, morpho- ge nética) y los análisis genéticos y morfológicos a nivel individual metrics) indicate that: (1) genetic diversity decreases with alti- (distancia fenética genotipo haploide, PCO, morfometría) indi- tude, probably as a result of the postglacial recolonization pro- can que: (1) la diversidad genética se reduce con la altitud, pro- cesses, except in some secondary contact zones between taxa; bablemente como consecuencia de los procesos de colonización (2) gene flow among interspecific populations, most likely facili- posgla ciales, salvo en zonas de contacto entre táxones; (2) el flu- tated by contraction of vegetation belts, led to the formation of jo génico entre poblaciones de distinta especie, probablemente hybrid taxa; (3) genetic distances among populations provide a facilitado por la contracción de los cinturones de vegetación, re- useful basis for studying scenarios with frequent interspecific sultó en la formación de táxones híbridos; (3) la distancia ge- gene-flow since it allows distinguishing eventual cases of intro- nética entre poblaciones nos proporciona una base útil para el gression from hybridogenous taxa. estudio de escenarios con frecuente flujo interespecífico de ge- nes, ya que permite distinguir casos eventuales de introgresión de táxones hibridógenos. Keywords: altitudinal gradient, glacial refugia, hybridization, Palabras clave: gradiente altitudinal, refugios glaciales, hibri- Iberian Peninsula, phylogeography, reticulate evolution, Sierra dización, Península ibérica, filogeografía, evolución reticulada, Nevada. Sierra Nevada. 176 J. Fuertes Aguilar & al. Introduction & Skowronek, 2001) as well as from palynological records in caves and lacustrine sediments (Pons & Glaciations have shaped present-day plant species Reille, 1988; Carrión & al., 2001a). Paleosol studies in distributions in the Northern Hemisphere (Hewitt, periglacial areas reveal that at least three cold Quater- 1996, 2000) through four main direct effects on popu- nary episodes took place in this massif, identified as lations: isolation, expansion, migration and extinction Riss, Würm, and Late Glacial, each one with a de- (Comes & Kadereit, 1998). During glacial periods, creasing glacial activity (Gómez Ortiz & Salvador i species that were adapted to arctic-alpine conditions Franch, 1996; Simón & al., 2000; Schulte, 2002). As a colonized large extensions of tundra and steppe south consequence of its orography, during Quaternary ice- of the ice sheets and alpine enclaves, while those ages the Sierra Nevada paradoxically contained the adapted to temperate conditions were confined to southernmost glaciers in Europe and at the same time southern refugia (Ferris & al., 1999). In contrast, inter- the surrounding area was a refugial area for plants glacial periods favoured the recolonization of newly (Carrión, 2002; Carrión & al., 2003). open habitats in deglaciated areas, thereby inducing Currently, the Betic and Sub-betic regions in migratory movements towards northern areas that al- Southern Spain form one of the richest centres for lowed the admixture of previously fragmented popu- plant endemism in Europe and the western Medite- lations (Gabrielsen & al., 1997). In some of the south- ern European areas, including high-altitude massifs, a rranean basin (Blanca & al., 2002; Lobo & al., 2001; more complex pattern is added to these latitudinal Médail & Quézel, 1997; Molero Mesa, 1994). Plant refugia dynamics. Due to the great diversity of habitats genera for which the Sierra Nevada region is a diversi- along high-elevation mountains, altitudinal shifts in ty "hot-spot" include Erodium (6 endemic taxa) (Sali- plants induced by climatic changes took place at a nas, 2009), Arenaria (8) (López González, 1990), Cen- much more reduced scale than latitudinal changes taurea (13) (Blanca & al., 2002), and Erysimum (7) (Hewitt, 1999). As a consequence of overlapping lati- (Nieto Feliner, 1993). The subject of our study, the tudinal and altitudinal shifts associated with contrac- Sierra Nevada thrifts (Armeria), is another good ex- tion-expansion cycles, southern refugia became ex- ample of such a diversity pattern (Salazar, 2009). The traordinary arenas for plant evolution that fostered a massif harbours three species of Armeria: A. splen- variety of outcomes including fragmentation, compe- dens (Lag. & Rodr.) Webb, A. filicaulis (Boiss.) Boiss. tition, hybridization and speciation (Brochmann & al., and A. villosa Girard (Table 1). Armeria splendens is a 1998; Steen & al., 2000). Most of the phylogeographic high-altitude (above 2880 m) endemic occurring in and genetic research on European refugia has focused alpine meadows (locally known as "borreguiles"). A. on extinction and recolonization processes in the arc- filicaulis is represented by three endemic subspecies: tic-alpine flora of northern and central glaciated areas A. filicaulis subsp. trevenqueana Nieto Feliner is en- (Abbott & Comes, 2004; Ronikier & al., 2008), the demic to dolomites from Cerro Trevenque and Alayos identification of central and southern European refu- del Dílar, in the western part of the Sierra Nevada gia (Tribsch & Schönswetter, 2003; Schönswetter & (1700 m), A. filicaulis subsp. alfacarensis Nieto Fel., al., 2005), and the pathways of recolonization from Gut. Larena & Fuertes, also occurs on white dolo - such refugia into deglaciated areas (Petit & al., 2003). mitic substrates but in the north-east of the Sierra However, little work has been done on how glaciation- Nevada, on the Sierra de Alfacar and its surroundings, deglaciation cycles affected the plants within the refu- and A. filicaulis subsp. nevadensis Nieto Fel., Rosselló gia of southern Europe (Kropf & al., 2006, 2008; Petit & Fuertes, is restricted to a narrow area on schist be- & al., 2002; Nieto Feliner, 2011). tween 2100-2550 m. A. villosa is represented by A. vil- The Sierra Nevada, the highest massif in the Betic losa subsp. bernisii Nieto Fel., which is endemic to the system (SE Iberian Peninsula), emerged during the eastern Betic mountains, including the Sierra Nevada, Langhian (earliest middle Miocene) and estimations and is the most common taxon of Armeria inhabiting from sedimentary basins indicate that as early as in the Pinus and Quercus forests between 1250 and 2550 m Tortonian-Messinian transition (7.1 Mya), the massif (Blanca & al., 2002; Fuertes Aguilar & al., pers. ob- had already reached 2000 m above sea-level (Braga & servations). al., 2003). Since then, despite erosion forces, it has suf- Previous studies based on trnL-trnF sequences fered a progressive uplift until its present-day highest (Gutiérrez Larena & al., 2002) revealed a shared pat- elevation at the Mulhacén peak (3480 m). Climatic tern of plastid haplotypes among species suggesting oscillations in the Sierra Nevada during the last 5 My an interspecific horizontal transfer in Sierra Nevada, (Tertiary-Quaternary) are well documented from with an initial colonization process being the estab- paleosol evidence within adjacent basins (Günster lishment of Armeria splendens. The study of ITS se- Anales del Jardín Botánico de Madrid 68(2): 175-197, julio-diciembre 2011. ISSN: 0211-1322. doi: 10.3989/ajbm. 2260 Diversity of Armeria in Sierra Nevada 177 Table1. Taxonomic synopsis of Armeria taxa involved in this study. Species Subspecies