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Morphological Differentiation Supports the Genetic Pattern of the Geographic Structure of Juniperus Thurifera (Cupressaceae)

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Morphological Differentiation Supports the Genetic Pattern of the Geographic Structure of Juniperus Thurifera (Cupressaceae) Plant Syst Evol (2013) 299:773–784 DOI 10.1007/s00606-013-0760-7 ORIGINAL ARTICLE Morphological differentiation supports the genetic pattern of the geographic structure of Juniperus thurifera (Cupressaceae) Adam Boratyn´ski • Anna K. Jasin´ska • Katarzyna Marcysiak • Małgorzata Mazur • Angel M. Romo • Krystyna Boratyn´ska • Karolina Sobierajska • Grzegorz Iszkuło Received: 9 August 2012 / Accepted: 21 January 2013 / Published online: 17 February 2013 Ó The Author(s) 2013. This article is published with open access at Springerlink.com Abstract Juniperus thurifera is an important component The morphological differentiation of populations appeared of woodland communities of dry sites within the West similar to that described on the AFLP. The Gibraltar Straight Mediterranean region and is characterised by a strongly appeared to be the most important barrier. disjunctive geographic range. Two subspecies were recog- nised, subsp. thurifera in Europe and subsp. africana in Keywords Biometry Á Geographic differentiation Á Africa. The aim of the study was the comparison of phenetic Juniperus thurifera Á Numerical taxonomy Á Plant diversity to the pattern of AFLP geographic differentiation of morphology Á Plant variation the species described in the literature. The examination of phenetic diversity was based on the biometrical analysis of 17 populations using 12 morphological characters of cone Introduction and seed. The differences among populations were analysed using Student’s t test, analysis of discrimination, UPGMA Juniperus thurifera L. is a tree-like juniper of the section agglomeration and hierarchical analysis of variance. The Sabina (Mill.) Spach. (Farjon 1993, 2005; Adams 2011), majority of morphological characters differentiated at a occurring in the western Mediterranean region (Fig. 1), statistically significant level between populations and where it grows in the continental climate conditions of the between J. thurifera subsp. thurifera and subsp. africana. mountain systems (Achhal et al. 1980; Fromard and Gau- Three groups of populations were detected using multivari- quelin 1993; Romo and Boratyn´ski 2005; Gasto´n Gonza´lez ate statistical analyses. The first, well separated, is subsp. 2006). The present range of J. thurifera covers several, africana, while the following two concern subsp. thurifera. more or less isolated, areas in the Iberian Peninsula, Pyrenees, Alps and Corsica in Europe; and the Middle, High and Anti-Atlas and Aure`s in North Africa (Jalas and A. Boratyn´ski (&) Á A. K. Jasin´ska Á K. Boratyn´ska Á Suominen 1973; Barbero et al. 1988; Lathuillie`re 1994; K. Sobierajska Á G. Iszkuło Gamisans et al. 1994; Gauquelin et al. 1999; Que´zel and Polish Academy of Sciences, Institute of Dendrology, Me´dail 2003; Farjon 2005; Romo and Boratyn´ski 2005). Ko´rnik, Poland The genetic variation of J. thurifera, tested on the ran- e-mail: [email protected] dom amplified polymorphic DNA (RAPD) by Jime´nez K. Marcysiak Á M. Mazur et al. (2003), suggests that the species migrated from the Department of Botany, Kazimierz Wielki University, European mountain systems southward and westward Bydgoszcz, Poland towards Corsica, the Iberian Peninsula and then the Atlas A. M. Romo Mountains in N Africa. The African populations, the most Consejo Superior de Investigaciones Cientificas, isolated from the others, appeared to be the most distant Institute of Botany, Barcelona, Spain genetically and morphologically (Adams et al. 2003; Jime´nez et al. 2003; Romo and Boratyn´ski 2007; Terrab G. Iszkuło Faculty of Biological Sciences, University of Zielona Go´ra, et al. 2008). The morphological differences between Zielona Go´ra, Poland European and African individuals of J. thurifera were the 123 774 A. Boratyn´ski et al. Fig. 1 Distribution of Juniperus thurifera (compiled from: Jalas and algorithm of Euclidean distances among populations revealed by Suominen 1973; Romo and Boratyn´ski 2005; Gasto´n Gonza´lez 2006) Barrier: a between African and European, b between Corsican and and location of sampled populations (acronyms as in Table 1): subsp. Iberian, c between Iberian and north-Iberian–Alpine, and d between thurifera: filled triangle Iberian–Corsican group, filled circle Alpine– north and southern Middle Atlas populations; the thickness of barriers Iberian Group, filled square subsp. africana: morphological bound- is related to its importance aries (a–d) obtained with Monmoniers’s maximum difference reason for the distinguishing of subsp. africana (Maire) and occurs on the sites inaccessible or only weakly Romo et Boratyn´ski, which differs from J. thurifera subsp. accessible for other trees (Que´zel and Me´dail 2003). The thurifera by its smaller cone diameter, lower number of adaptation by selection as an important source of pheno- seeds per cone and shorter leaf scales (Romo and Bor- typic differentiation of that species cannot be excluded atyn´ski 2007). Differences between subsp. thurifera and however, but probably had similar influence in various africana have also been found in the biochemical compo- parts of its geographic range (Terrab et al. 2008). sition (Gauquelin et al. 1988, 1999; Lebreton 1990; Akkad The aim of the present study was (1) to determine et al. 2001) and genetic structure (Adams et al. 2001, 2003; morphological dissimilarities between populations by per- Jime´nez et al. 2003; Terrab et al. 2008). The latter study forming a biometrical comparison of morphological char- revealed strong differences between European and African acters of female cones, seeds and shoots, and (2) to populations of J. thurifera, and confirmed subsp. africana evaluate to what extend the multivariate biometrical anal- as a separate taxon. The analysis of European populations ysis would resemble the pattern of variation and differen- showed two different groups, the first including popula- tiation described by Jime´nez et al. (2003) and Terrab et al. tions from the Alps, Pyrenees, northern part of the Iberian (2008) based on RAPDs and AFLP analyses, respectively. Peninsula and Corsica, and the second overlapping those from the central part of the Iberian Peninsula (Terrab et al. 2008). The biometrical examinations of four European Materials and methods populations (Mazur et al. 2005; Marcysiak et al. 2007) revealed the great differences among them, especially Plant material and measuring procedures between one from the Alps and three from the Iberian Peninsula (Mazur et al. 2005). Taking into account the last The material for the study was based on 17 populations of result we hypothesised that J. thurifera’s phenetic diversity J. thurifera (Table 1), which cover almost the entire spe- pattern should be similar to AFLP geographic differentia- cies area of natural distribution (Fig. 1). Populations were tion and is mainly a consequence of the history of the represented by 16–36 individuals (27 in average) except for species. J. thurifera is well adapted to the dry environments MO_02 (see Table 1), where only eight individuals have 123 Morphological differentiation supports the genetic pattern 775 been sampled due to lack of cones on more junipers in that used characters. The STATISTICA (StatSoft) procedures locality. The 441 individuals were biometrically examined, were performed. The frequency distribution of measured each represented by 10 adult cones and 10 young shoots character values was verified using the Shapiro–Wilk’s test to with leaves, all collected from the sunny part of the crown. assess the symmetry and unimodality and, consequently, the However, a few individuals were represented by smaller possibility of conducting the multivariate statistical analyses numbers, because of lack of sufficient number of cones or (Sokal and Rohlf 1997; Zar 1999). The homoscedasticity of destruction of shoots. The cone scales (CSN) were counted data was checked using Brown–Forsythe test as implemented after cone soaking. The seeds were taken off the soaked by STATISTICA (StatSoft) to assess the possibility of use of cones and dried after measuring. The thickness of the parametric statistic tests (Sokal and Rohlf 1997). ultimate lateral branchlet with leaves (ST) was measured The main statistics such as arithmetic means, standard following methods described by Marcysiak et al. (2007). deviations and variation coefficient were calculated for The measurement was performed on dry material. The each population in order to determine the range of their populations were compared on the basis of six characters of variation. The interactions between characters were cones and seeds, two of shoots and leaves, and four pro- checked with Pearson’s correlation coefficient to detect portions (Table 2). possible redundant variables. A stepwise discrimination analysis was performed to: (1) definitively eliminate the Data analysis possible redundant variables, (2) identify the discrimina- tion power of particular characters, and (3) determine the All data were standardised before analysis to avoid the pos- intra- and inter-populational variation (Tabachnik and Fi- sible influence of variation resulting from various types of dell 2007; Sokal and Rohlf 1997). Table 1 Studied populations of Juniperus thurifera; italicized (FR_01 and SP_02, 06 and 07) samples used in previous studies (Mazur et al. 2005; Marcysiak et al. 2007) Taxon Locality Acronym Number of Geographic Altitude specimens coordinates (m) Subsp. thurifera France, Hautes Alpes, St. Cre´pin FR_01 36 N44o560 E06o300 1500 France, Corse, Niolo, Monte Cinto FR_02 21 N42o2200500 E8o5704700 900 France, Corse,
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