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Species Boundaries and Population Divergence in the Pyrenean Endemic Relict Genus Borderea (Dioscoreaceae) As Revealed by Micros

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Species Boundaries and Population Divergence in the Pyrenean Endemic Relict Genus Borderea (Dioscoreaceae) As Revealed by Micros Aliso: A Journal of Systematic and Evolutionary Botany Volume 22 | Issue 1 Article 42 2006 Species Boundaries and Population Divergence in the Pyrenean Endemic Relict Genus Borderea (Dioscoreaceae) as Revealed by Microsatellite (SSR) and Other Hypervariable Markers José Gabriel Segarra-Moragues Universidad de Zaragoza Pilar Catalan Universidad de Zaragoza Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons Recommended Citation Segarra-Moragues, José Gabriel and Catalan, Pilar (2006) "Species Boundaries and Population Divergence in the Pyrenean Endemic Relict Genus Borderea (Dioscoreaceae) as Revealed by Microsatellite (SSR) and Other Hypervariable Markers," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 22: Iss. 1, Article 42. Available at: http://scholarship.claremont.edu/aliso/vol22/iss1/42 Dioscoreales MONOCOTS Comparative Biology and Evolution Excluding Poales Aliso 22, pp. 541-555 iC· 2006, Rancho Santa Ana Botanic Garden SPECIES BOUNDARIES AND POPULATION DIVERGENCE IN THE PYRENEAN ENDEMIC RELICT GENUS BORDEREA (DIOSCOREACEAE) AS REVEALED BY MICROSATELLITE (SSR) AND OTHER HYPERVARIABLE MARKERS JOSE GABRIEL SEGARRA-MORAGUES AND PILAR CATALAN 1 Departamento de Agricultura y Econom{a Agraria, Universidad de Zaragoza, Escuela Politecnica Superior de Huesca, Ctra. Cuarte km. 1, E-22071 Huesca, Spain ([email protected]) 1Corresponding author ([email protected]) ABSTRACT Microsatellite alleles were used to delimit the genetic boundaries and divergence of the two relictual endemic Pyrenean taxa Borde rea chouardii and B. pyrenaica (Dioscoreaceae ), and to infer the different life histories followed by each species. Our study was conducted on the same populations previously analyzed with allozymes and RAPD markers. The three studied data sets were congruent in the inference of a single evolutionary scenario for the split of the two Borderea taxa from a common Tertiary ancestor in the Prepyrenees, thus supporting their taxonomic treatment as separate species. However, the more variable SSR and RAPD data provided better resolution for a stepping-stone model of local colonization of B. pyrenaica populations from southern Prepyrenean refugia to the northern Pyrenees. SSR markers proved to be more robust than RAPD markers in assessing the genetic structure of recently diverged populations of B. pyrenaica and thus qualified as the best molecular markers for fine-scale evolutionary investigations of Dioscoreaceae. Furthermore, microsatellites rendered unique clues to decipher the mechanisms involved in the origin of these relictual species and their genetic background. Borderea was shown to be a tetraploid genus of hybrid origin with a chromosome base number of x = 6. Phylogenetic data, karyological evidence, and our present knowledge based on microsatellite analyses allowed us to speculate that the Pyrenean endemic genus Borderea and its sister taxon, the Mediterranean genus Tamus, represent some of the oldest paleopolyploid lineages of the mostly pantropical yam family. Key words: Borderea chouardii, B. pyrenaica, Dioscoreaceae, microsatellites, molecular divergence, polyploidy, RAPD, SSR. INTRODUCTION derea, other taxa native to geographical regions apart from the Pyrenean range were also transferred to this genus. Thus, The genus Borderea Miegev., endemic to the central Pyr­ enean and Prepyrenean mountain ranges, has been consid­ the Chilean endemic Dioscorea humilis Bert. ex Colla was ered to be a Tertiary relictual lineage of Dioscoreaceae renamed as B. humilis (Bert. ex Colla) Pax. However, this (Gaussen 1965) based on the fact that the vast majority of and two other Andean dwarf endemics show certain distinc­ its family members (more than 600 spp.) show a present tive morphological features within Dioscoreaceae (i.e., the pantropical distribution with only a few taxa growing outside possession of prominent pistillodes in the male flowers, of that range (Knuth 1924; Burkill 1960; Dahlgren et al. round capsules, and strongly emarginate leaves) that favored 1985). their separate treatment as members of the independent ge­ The species of this genus have been subjected to several nus Epipetrum Phil. (Knuth 1924). Milne-Redhead (1963) taxonomic rearrangements throughout history. The two cur­ described from Kenya Dioscorea gilletii Milne-Redh., a tax­ rently accepted taxa (Borderea pyrenaica and B. chouardii; on potentially close to Borderea based on its wingless seeds cf. Heywood 1980; Villar et al. 2001) were first described and other less consistent traits. The extreme taxonomic im­ within the large pantropical genus Dioscorea L. as D. pyr­ portance given to the wingless seed morphological character enaica Bubani & Bordere ex Gren. and D. chouardii Gaus­ moved Huber (1998) to classify the east African D. gilletii sen, respectively (Gaussen 1952, 1965). The name Borderea and the two Pyrenean endemics as the disjunct members of arose in the mid-nineteenth century (Miegeville 1866) to de­ the small section Borderea within the large genus Dioscorea. scribe specimens from the Pyrenees (B. pyrenaica Bubani A careful examination of the type material for D. gilletii (K! ex Miegev.), which differed from Dioscorea mainly in their H3644/83, H3645/83) revealed several morphologically dis­ dwarf habit and wingless seeds. Karyological analyses of the tinctive features with respect to those exhibited by Borderea two species demonstrated that both taxa shared not only (Segarra-Moragues and Catal<in 2005, unpubl. data), sug­ these remarkable morphological attributes, but also a chro­ gesting that D. gilletii was more closely related to other mosome number of 2n = 24, which was assumed to repre­ Dioscorea species than to Borderea. Recent phylogenetic sent a chromosome base number of x = 12, distinct from studies of Dioscoreaceae (Caddick et al. 2002a) based on that shown for most Dioscorea taxa (x = 10). In turn, this rbcL, atpB, 18S ribosomal DNA (rDNA) sequences, and chromosome value was used as a further argument to clas­ morphological characters demonstrated that Dioscorea s.l. sify both species under the same genus Borderea (Heslot (Huber 1998) is paraphyletic and that the dioecious Dios­ 1953). On the basis of morphological similarities with Bor- coreaceae (i.e., Borderea, Tamus L.) are embedded within a 542 Segarra-Moragues and Catalan ALISO ( ~ i j BcO I \ ~ """~ ~ Fig. 2.- Map of the studied popul ations of Borderea. Be = B. chouardii (BcO I, Sopeira, Huesca, Spajn). Bp = B. pyrenaica (BpO I, La Pl anette, Gavarnie, France; Bp02, Les Roc hers Bl ancs, Gavamie, France; Bp03, Pineta, Huesca, Spai n; Bp04, Ordesa, Huesca, Spain; Bp05, Cotiell a [La Vasa Mora], Hu esca, Spain ; Fig. I.- Habit of Borderea taxa: (a) B. chouardii, male plant and Bp06, Turb6n, Hu esca, Spaj n). detail of fruiting branch of female pl ant; (b) B. py renaica, male pl ant and detail of fruiting branch of female pl ant. Scale bar = I em. and Prepyrenean region (Fig. 2), where it inhabi ts mobile Drawings reproduced by courtesy of M. Saul e ( 199 1). calcareous screes above 1800 m. a.s.l. Its populations are dis­ tributed in three main mountain " islands," the largest one clade of monoecious species. These findings, supported by expanding around the Monte Perdi do massif in the Pyrenean evidence that the putatively distinctive traits of these genera axial divide and two more reduced populati on cores located are not as unique as previously thought, prompted the inc lu­ in the Prepyrenean Coti ell a and Turb6n massifs, respecti vely sion of Borderea and its Mediterranean sister genus Tamus, (Fig. 2). The geographical map di stances among the popu­ within Dioscorea (Schols et aJ . 2001 ; Caddick et al. 2002b). lations of B. pyrenaica growing along the Pyrenean range Regardless of its taxonomic attribution, Borderea repre­ are short (less than 15 km), however, they are separated by sents an evolutionary split from an old Dioscoreaceae line­ some of the hi ghest peaks of this mountain chai n. These age that successfully adapted to and coloni zed the centraJ peaks constitute naturaJ barriers between the more abundant region of the Pyrenees and, as currentl y circumscribed, onl y Spani sh populations on the southern side of the Pyrenees includes two taxa, B. pyrenaica Miegev. and B. chouardii (around the Ordesa and Pineta valleys) and the more spo­ (Gaussen) Heslot (Fig. 1). These two species are endemic of radic populati ons that grow to the north in France around the central Pyrenean and Prepyrenean mountain ranges that the Gavarni e Vall ey. By contrast, the Prepyrenean popula­ present some of the longest Li fe spans reported for herba­ ti ons of B. pyrenaica are located further away, in two iso­ ceous plants (Garcfa and Antor 1995a.; Garcfa 1997; Garcfa lated Spani sh mountain massifs that are separated by deep et al. 2002), including some individuaJs over 300 years old. valleys and by more than 30 km (Coti ell a) and 50 km (Tur­ Both taxa are di oecious geophytes and apparently onl y re­ b6n) from the Pyrenean core, re pecti vely. These geographic produce sexuall y (Garcia and Antor 1995b; Garcfa et al. features currently prevent any gene fl ow between the Pyre­ 1995, 2002). Borderea chouardii is a chasmophyti c species nean and the Prepyrenean populati on cores. On the other that has been classified as " in danger of extincti on" in the hand, the southernmost Prepyrenean B. pyrenaica populati on Annex II of the Habitats Directi ve of the E uropean U ni on of 1\.1rb6n is located at almost the same geographic di stance and as "critically endangered" in the Spanish Red List of from its conspecific Prepyrenean core at Coti ell a (20 km), Endangered Nati onaJ Plants (Garcfa 1996; Varios Autores as from its congener B. chouardii at Sopeira (25 km) (Fi g. 2000; Moreno-Saiz et aJ. 2003). It is onl y known from a 2). Populati ons of B. pyrenaica are somewhat larger-some single population of approximately 2000 individuals (Garcfa comprising more than 10,000 reproducti ve individuals that et al. 2002), located in one of the southernmost Spani sh Pre­ inhabit wide, almost pristine hi gh-mountain areas.
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