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Variation in the Population Genetic Structure of Two Cyclamen Species on the Island of Corsica

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Variation in the Population Genetic Structure of Two Cyclamen Species on the Island of Corsica Heredity 78(1997) 205—214 Received21 March 1996 Variation in the population genetic structure of two Cyclamen species on the island of Corsica LAURENCE AFFRE & JOHN D. THOM PSON* C.E.F.E.-C.N.R.S., Route de Mende, BP 5051, F-34033 Montpef/ier Cédex 1, France Cyclamen repandum and C. hedenfolium occur in sympatry in many sites across their distribu- tions but flower at different times. A previous controlled pollination experiment on plants of the two species collected on the island of Corsica showed no evidence of inbreeding depression over all measured life cycle stages in C. repandum, whereas C. hederifolium showed inbreeding depression (multiplicative (50.49) on fruit maturation and seed production. This suggests that C. repandum may have a greater history of inbreeding than C. hederifolium. In this paper, we examine whether within-population heterozygosity and among-population differentiation on Corsica are consistent with the hypothesis that C. repandum is more inbred than C. heder- ifolium. Cyclamen hederifolium showed a higher percentage of polymorphic loci, meannumber of alleles per locus and mean observed heterozygosity than C. repandum. Cyclamen repandum showed higher among population differentiation (FST =0.415)than C. hederifolium (FST =0.131).The within-population fixation index was greater in C. repandum (F1 =0.658) than in C. hederifolium (F1 =0.329).Cyclamen repandum thus appears to have a greater history of inbreeding than C. hederifolium. The variation in the mating systemof the two species is discussed in relation to their sympatric occurrence and data from previouswork on the population genetic structure of island populations of other geographically restricted Cycla- men species Keywords:Cyclamen,genetic variation, mating system, population differentiation, Primula- ceae, sympatry. Linhart & Premoli, 1993) and Karron (1987) has Introduction pointed out the difficulty of drawing conclusions Thereis now much evidence that mating system and about such predictions from studies of unrelated geographical distribution are major determinants of taxa. A useful approach to the study of the relation- the amounts and spatial patterns of genetic varia- ship between mating system, geographical distribu- bility in plant species. Geographically widespread, tion and patterns of genetic diversity is thus the outcrossing animal-pollinated species tend to have comparison of closely related taxa. higher levels of genetic variation within populations Within the genus Cyclamen (Primulaceae), C. and to maintain lower levels of differentiation repandum ssp. repandum (hereafter C. repandum) among populations than restricted, inbreeding and C. hederifolium are widely distributed across the species (Hamrick et al., 1979; Loveless & I-Iamrick, northern Mediterranean Basin. Cyclamen repandum 1984; Karron, 1987, 1991; Hamrick & Godt, 1989). occurs from southern France, through Italy, to the Geographically restricted species have also been western side of ex-Yugoslavia (Dalmatia) and found to have higher rates of self-pollination Greece, and C. hedenfolium occurs from southern (Karron, 1987, 1991). France to eastern Bulgaria and southern Turkey and Some restricted species do, however, contain rela- on several Aegean islands. Both species also occur tively high levels of genetic variation (Primack, 1980; on the islands of Corsica, Sardinia and Sicily (Grey- Wilson, 1988). On Corsica, C. repandum and C. *Correspondence E-mail: [email protected] hederifolium are sympatric, occurring in a wide range 1997 The Genetical Society of Great Britain. 205 206 L. AFFRE & J. D. THOMPSON of similar habitats and frequently in the same sites. Materials and methods Nevertheless, the two species flower at different times of the year, C. repandum in the spring and C. Study species hedenfolium in the autumn. Cyclamenrepandum Sibth. & Sm. and C. hederifo- Both C. repandum and C. hedenfolium are fully hum Aiton are long-lived, perennial herbaceous self-compatible but set almost no fruit in the plant species. Cyclamen repandum (2n =20)and C. absence of external pollinating agents (Affre, 1996). hederifolium (2n =34)are both diploid species, In a controlled pollination trial, C. repandum although the latter is known to have polyploid forms showed no evidence of inbreeding depression on in Greece (Bennett & Grimshaw, 1991). In both fruit maturation and seed number (multiplicative species, the flowers are solitary, pendant with estimate of 5=0.14),whereas C. hederifolium reflexed petals, hermaphroditic and do not produce showed a multiplicative estimate of inbreeding nectar. Cyclamen repandum flowers in the spring depression equal to 0.49 (Affre, 1996). These results (March—May), whereas C. hedenfolium flowers in suggest that C. hedenfolium is an outcrossing the autumn (from the end of August until October species, whereas C. repandum appears to be more or occasionally later) before the leaves emerge. In autogamous and may show high levels of pollinator- the CEFE—CNRS experimental garden in Montpel- mediated inbreeding in natural populations. The her (France), C. repandum plants produce from one first purpose of this study is thus to compare levels to 11 (mean =5.30.4) vivid carmine-magenta of genetic variation and differentiation within and flowers with narrow, twisting petals. The style is among populations of both species across a range of exserted beyond the mouth of the corolla. Cyclamen sites on Corsica where they are sympatric. Explicitly, hederifolium plants produce from one to 39 we examine whether C. hedenfolium shows higher (mean =9.2 pink flowers with a purple- levels of within-population diversity and heterozygo- magenta blotch forming a V-shape at the base of sity and less among-population differentiation than each corolla lobe. The style is slightly exserted C.repandum. beyond the mouth of the corolla. A recent phylogenetic analysis of Cyclamen species based on morphological and cytological traits (Anderberg, 1993) indicates that C. repandum is Enzymee/ectrophoresis closely related to C. balearicum and C. creticum. OnCorsica, the populations of both studied species Cyclamen hederifolium is in a separate group with were sampled from 10 to 940 m (C. repandum) or to several other related species of more eastern and 1150 m (C. hederifolium). Two or three leaves per central Mediterranean distribution. individual were sampled in eight populations of C. Previous studies of the population genetic struc- repandum in April 1993 and in seven populations of ture of the two species closely related to C. repan- C. hedenfolium in October 1993. Four sites (BF: Bas dum have shown that C. balearicum has a mean Fango (175 m); HF: Haut Fango (350 m); VE: close to 1.00 in most populations and a mean FSTof Vecchio (850 m); and RE: Restonica (940 m)) 0.297±0.059 on theBalearicIslands and contained both species. Four sites contained only C. 0.480±0.101 in southern France (Affre et al., 1997), repandum (P0: Portigliolo (10 m); CA: Capitelle whereas C. creticum has a mean F1 =0.7480.068 (40 m); NI: Nichiareto (90 m); and EV: Evissa and a mean FST of 0.168±0.028 on Crete (Affre & (550m)),and three only C. hederifolium (MA: Thompson, 1997). Cyclamen balearicum and C. creti- Martino (300 m); Al: Aitone (1000 m); and VI: cum have very narrow ranges (C. balearicum occurs Vizzavone (1150 m)). The pedicel of each leaf was on the Balearic Islands and in several isolated sites followed to its insertion on the tuber to be sure that in southern France and C. creticum occurs on Crete closely adjacent leaves were sampled from the same and Karpathos) compared with C. repandum and C. genotype. Horizontal starch gel electrophoresis was hedenfolium. We ask two secondary questions. First, performed on crude protein extracts of leaf tissue. do the two endemic species, C. balearicum and C. Enzyme extraction was carried out by grinding the creticum, exhibit lower levels of genetic variability leaf material with a Tris-HCI extraction buffer than the two widespread species, C. repandum and (Affre, 1996), and centrifuging the homogenate (20 C. hedenfolium? Secondly, because C. balearicum is mm at 15000g). The supernatant was then either the only species of the four capable of spontaneous immediately absorbed on Whatman no. 3 paper self-pollination, does this species exhibit greater wicks (3 x 10 mm) and loaded onto gels, or stored at heterozygote deficiency and genetic differentiation —80°Cprior to electrophoresis. Electrophoresis than C. creticuin, C. repandum and C. hedenfolium? (11—12 per cent w/v) was conducted in a cold The Genetical Society of Great Britain, Heredity, 78, 205—214. GENETIC STRUCTURE OF CYCLAMEN 207 chamber at 4°C on crude protein extract of leaf generation (Nm) we used therelationship tissue (see Affre, 1996). FST =1I(4Nm +1),where N is the local population For 12 enzyme systems investigated, seven (10 size and m is the average rate of immigration enzyme loci) showed reliable results. The 10 enzyme (Wright, 1951; Slatkin, 1987). The proportion of loci analysed were one glutamic-oxaloacetic trans- total (HT) genetic diversity distributed within (F!5) aminase (GOT, EC 2.6.1.1), one malate dehydrogen- and among (GST) populations weighted by the effec- ase (MDH, EC 1.1.1.37), one leucine tive number of individuals was calculated following aminopeptidase (LAP, EC 3.4.11.1), one phospho- Prentice & White (1988). Unbiased genetic distan- glucoisomerase (PGI, EC 5.3.1.9), three phosphoglu- ces among all populations were calculated following comutases (PGM, EC 5.4.2.2), two -esterase Nei (1972, 1973, 1978) and the z2(Balakrishnan& (aEST, EC 3.1.1.2), and one phosphogluconate Sanghvi, 1968) methods because of the presence of dehydrogenase (PGD, EC 1.1.1.44). Nine of these rare alleles. loci were readable for C. repandum (ciEST-2 did not show any bands) and eight were readable for C. hederifoliurn (ca'EST-l and PGM-3 showed no bands). Results Genetic interpretation of electrophoretic variants Allele frequency variation and genetic diversity was based on progeny arrays of controlled crosses (Affre, 1996).
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