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Microcnemum Coralloides (Chenopodiaceae- Salicornioideae): an Example of Intraspecific East-West Disjunctions in the Mediterranean Region

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Microcnemum Coralloides (Chenopodiaceae- Salicornioideae): an Example of Intraspecific East-West Disjunctions in the Mediterranean Region Anales del Jardín Botánico de Madrid Vol. 65(2): 415-426 julio-diciembre 2008 ISSN: 0211-1322 Microcnemum coralloides (Chenopodiaceae- Salicornioideae): an example of intraspecific East-West disjunctions in the Mediterranean region by Gudrun Kadereit1 & Ahmet Emre Yaprak2 1 Institut für Spezielle Botanik und Botanischer Garten, Johannes Gutenberg-Universität Mainz, 55099 Mainz, Germany. Corresponding author: [email protected] 2 Ankara University, Science Faculty, Department of Biology, Besevler/Ankara, Turkey. [email protected] Abstract Resumen Kadereit, G. & A.E. Yaprak. 2008. Microcnemum coralloides Kadereit, G. & A.E. Yaprak. 2008. Microcnemum coralloides (Chenopodiaceae-Salicornioideae): an example of intraspecific (Chenopodiaceae-Salicornioideae): un ejemplo de las disyuncio- East-West disjunctions in the Mediterranean region. Anales Jard. nes intraespecíficas Este-Oeste en la región mediterránea. Anales Bot. Madrid 65(2): 415-426. Jard. Bot. Madrid 65(2): 415-426 (en inglés). Microcnemum is a monotypic genus of Salicornioideae compris- Microcnemum es un género monotípico de Salicornioideae que ing rare, annual, hygrohalophytic herbs growing in hypersaline in- consiste en hierbas higrohalófilas, anuales, raras, que crecen en land lagoons and salt pans. Microcnemum coralloides shows an cuencas endorréicas hipersalinas del interior y salares. Microcne- East-West disjunction in the Mediterranean region: M. coralloides mum coralloides muestran una disyunción Este-Oeste en la región subsp. coralloides occurs in central and eastern Spain while M. mediterránea: M. coralloides subsp. coralloides aparece en el cen- coralloides subsp. anatolicum grows in Turkey, Syria, Armenia and tro y el levante español, mientras que M.coralloides subsp. anato- Iran. We studied the phylogeny, biogeography and morphological licum crece en Turquía, Siria, Armenia e Irán. Estudiamos la filoge- differentiation of M. coralloides. Molecular analyses, using five nia, la biogeografía y la diferenciación morfológica de M. coralloi- western and eight eastern accessions of the species, were based des. Los análisis moleculares, empleando cinco adquisiciones occi- on three different markers (nuclear ITS and plastid atpB-rbcL spac- dentales y ocho orientales de la especie, se basaron en tres er and trnT/F region) analysed with Maximum Parsimony and marcadores distintos (ITS nuclear, espaciadores plástidos atpB- Maximum Likelihood. Estimates of divergence times were calcu- rbcL y región trnT/F) analizados con Máxima Parsimonia y Máxima lated using a Likelihood Ratio Test (LRT) and the Penalized Likeli- Verosimilitud. Las estimaciones de tiempos divergentes se calcula- hood (PL) method. The two subspecies can be clearly distin- ron empleando una Prueba de Verosimilitud (LRT) y el método de guished by their different seed testa surface. Other diagnostic Verosimilitud Penalizada. Las dos subspecies se distinguen clara- characters were not found. The molecular data (ITS and ML analy- mente por la diferencia en la superficie de su envoltura. No se en- sis of the trnT/F region) indicate that M. coralloides subsp. coral- contraron otras características de diferenciación. Los datos mole- loides originated from within M. coralloides subsp. anatolicum culares (ITS y análisis ML de la región trnT/F) indican que M. cora- which implies an East Mediterranean origin and subsequent west- lloides subsp. coralloides originó de dentro de M. coralloides ward dispersal. Age estimates for the split of the two subspecies subsp. anatolicum, lo cual implica un origen en el este del Medite- range from 2.8–0.5 million years ago. Considering the relatively rráneo y su posterior dispersión hacia el oeste. Las estimaciones de low genetic differentiation and the low crown group age (0.7–0.1 edad para la separación de las dos subespecies data desde hace mya) of M. coralloides subsp. coralloides in comparison to M. 2,8 a 0,5 millones de años. En vista de la diferenciación genética, coralloides subsp. anatolicum we favour the hypothesis that the relativamente baja y la reducida edad del grupo terminal (0,7-0,1 Iberian part of the species range was established during cold peri- millones de años) de M. coralloides subsp. coralloides en compa- ods of the Early Pleistocene and that the range of the species was ración con M. coralloides subsp. anatolicum, favorecemos la hipó- fragmented during a warmer period soon after its arrival in Iberia. tesis de que la parte ibérica de la gama de la especie se estableció durante periodos fríos del Bajo Pleistoceno y que la gama de la es- pecie se fragmentó durante un periodo más cálido no mucho des- pués de su llegada a la Península. Keywords: Biogeography, disjunction, Microcnemum, molecu- Palabras clave: Biogeografía, disyunción, Microcnemum, reloj lar clock, East Mediterranean, Spain. molecular, Mediterráneo oriental, España. 416 G. Kadereit & A.E. Yaprak Introduction anth rudiment which disappears in the fruiting stage represents an autapomorphy and is unique in Sa- Plant species that show an extreme East-West dis- licornioideae (Kadereit & al., 2006). junction in the Mediterranean region have been no- Microcnemum occurs along the shores of flat, step- ticed for a long time (Engler, 1879; Willkomm, 1896; pic lagoons in extremely saline sites. It often grows on Braun-Blanquet & Bolòs, 1957; Davis & Hedge, thick salt crusts together with a few other species that 1971). More recently, also some examples of disjunct- are salt-tolerant and able to cope with extreme hyper- ly distributed lichens were reported in the literature saline conditions during the dry season. Associated (Barreno, 1991; Egea & Alonso, 1996). Additional with Microcnemum coralloides in Turkey are, for ex- striking examples come from studies of cave-dwelling ample, Kalidium foliatum Moq., K. wagenitzii Crustaceae (Brehm, 1947), freshwater zooplankton (Aellen) Freitag & G. Kadereit, Halocnemum strobi- (Miracle, 1982), Coleoptera (Sanmartin, 2003) and laceum M. Bieb., Halimione verrucifera (M. Bieb.) from a detailed survey of the insect fauna of the cen- Aellen and Salicornia L. spp. (all Chenopodiaceae), tral Monegros region of Spain which listed 62 species while M. coralloides in Spain often is associated with showing a disjunct distribution between NE Spain Halopeplis amplexicaulis Ung.-Sternb., Halocnemum and the steppes in the eastern Mediterranean area or strobilaceum M. Bieb., Arthrocnemum macrostachyum Central Asia (Ribera & Blasco-Zumeta, 1998). Al- (Moric.) K. Koch and several species of Sarcocornia though molecular and analytical tools are now avail- A.J. Scott and Salicornia (also all Chenopodiaceae). able to study the origin and age of disjunct distribu- The presence of Microcnemum seems to fluctuate tion patterns, the list of molecular studies which focus from year to year probably in response to seasonal on extreme disjunctions of plant species in the fluctuations in rainfall (E. Yaprak, pers. obs.; B.M. Mediterranean is relatively short (but see: Castro & Crespo, pers. comm.). al., 2002; Carine & al. 2004; Rosselló & al., 2007; Microcnemum coralloides comprises two subspe- Thompson, 1999). cies. Microcnemum coralloides subsp. coralloides is re- Three main explanations have been put forward for stricted to inland salt lakes or salt pans in central and extreme East-West disjunctions in the Mediterranean eastern Spain (Molero, 1986; Blanché & Molero, region: 1. The extant populations have been inter- 1990). For some time after its discovery in 1959, M. preted as relict populations of a formerly (pre-Pleis- coralloides subsp. anatolicum was only known from tocene) continuous or at least wider distribution area, the type locality or nearby (Aellen, 1967). Later it was and probably survived in isoclimatic areas of the also recorded from central and NW Iran, the Syrian Mediterranean (Taberlet & al., 1998) from where Desert, Armenia and several new localities in Turkey some of them again expanded. 2. The extant popula- (Mouterde, 1966; Botschantzev & Barsegjan, 1972; tions in one part of the disjunct distribution area are Gabrielian, 1981; Akhani, 1988; Akhani & Ghorban- the result of colonization through long distance dis- li, 1993; Hamzaoglu & al., 2005; Yaprak, 2008). Apart persal. The direction of dispersal is usually inferred from their disjunct distribution, the two subspecies from the asymmetrical distribution of the specific tax- differ only in the structure of the seed testa, which is on with the newly colonized area having a smaller ex- densely and distinctly papillose in M. coralloides sub- pansion (Davis & Hedge, 1971; Ribera & Blasco- sp. anatolicum (Wagenitz, 1959) but only granulose or Zumeta, 1998; Thompson, 1999). 3. Some taxa are in- slightly papillose in M. coralloides subsp. coralloides terpreted to be early and undocumented introduc- (compare Figs. 1-4 in Molero, 1986). Other differ- tions by man (Willkomm, 1896). ences between the two subspecies have never been Microcnemum is a monotypic genus of Chenopo- identified. The type collection of M. coralloides subsp. diaceae subf. Salicornioideae that shows an extreme anatolicum, how-ever, was incomplete because the East-West disjunction in the Mediterranean region. plant was collected in the fruiting stage only (Wa- Like most members of Salicornioideae it grows in hy- genitz, 1959). grohalophytic habitats and has succulent, apparently A recent molecular systematic study of subf. Sa- leafless, articulated stems and spike-like inflores- licornioideae demonstrated that, based on nuclear cences. Among salicornioidean
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