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Genetic Variation of the Riparian Pioneer Tree Population Structure

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Genetic Variation of the Riparian Pioneer Tree Population Structure Heredity 77 (1996) 629—637 Received 28 February 1996 Genetic variation of the riparian pioneer tree species Populus nigra L. I. Study of population structure based on isozymes AGNES LEGIONNET*t & FRANOIS LEFEVRE tINRA, Station d'Amé/ioration des Arbres Forestiers, 45160 Ardon and tINRA, Unite de recherches forestières méditerranéennes, Avenue Vivaldi, 84000 Avignon, France Eightpolymorphic isozyme loci were used to describe the level and organization of the genetic diversity in Populus nigra L. over 111 sites in France and among 60 additional individuals from throughout the species range. Best descriptors and estimators of gene diversity and differentia- tion were sought. Overall diversity level was found to be comparable to other widespread species. Differentiation at three geographical scales was low, although local allele fixations indicated limitation of gene flow. Inferences were made on the effect of the natural history of the species on the organization of neutral diversity, and recommendations for collection of genetic resources were derived. Keywords:geneticdiversity, genetic resources, isozymes, population structure, Populus nigra. distinguished for sure from the rare alleles of P Introduction nigra, and thus we will not be able to discuss this TheEuropean black poplar, Populus nigra L., is a question. In this study, we measured gene diversity common pioneer tree in riparian forests, ranging and differentiation of P nigra in France by means of from central and southern Europe to central Asia allozyme variation. We tried to observe the effect of and north Africa (Zsuffa, 1974). Scattered individ- the species singularities on its neutral genetic diver- uals and small stands also occupy upland sites. Some sity, and we discuss the consequences for the clones of P nigra are widely used for ornamental sampling of genetic diversity. purposes, and as screens against wind. Although the use of pure P nigra for wood production is rare, the Materialand methods species is found among the ancestors of 63 per cent of the poplar cultivars registered by the Inter- Thisstudy was carried out on a stool-bed collection national Poplar Commission, mainly in interspecific of individual trees held by INRA in Orleans. Geno- hybrid clones with P deltoides (Viart, 1992). The types were gathered over a period of 20 years by genetic diversity of the species is thought to be different collectors (Teissier du Cros, 1977; Duval et threatened in two different ways. First, the reduction al., 1993). For most of the accessions, cuttings had of perturbed areas arising from the regularization of been collected from adult trees. In other cases, seeds river flows has been decreasing the regeneration of were collected and half-sib families were vegetatively this species all over western Europe (Frison et al., propagated. Only one randomly chosen offspring of 1995). Secondly, gene exchanges between the wild each family was included in the analyses. and the cultivated gene pool may also occur sponta- neously (Cagelli & Lefèvre, 1995), and a wide Collection distribution of a small number of clones, likely to intercross with wild trees, may lead to a reduction of Thesample used was made of (1) 60 individual trees genetic diversity. However, the markers we used representing different countries from the species were not suitable tools for a study of introgression, range, namely Bulgaria (6 individuals), Romania because the alleles from P deltoides could not be (18), Slovakia (7), Hungary (5), Belgium (12) and Italy (12); (2) 111 individuals representing different *Correspondence collecting sites (Fig. 1) in France, and (3) 196 mdi- 1996 The Genetical Society of Great Britain. 629 630 A. LEGIONNET & F. LEFEVRE drainage of Loire and Allier, including the stands Tinte, Pouilly and Les Brocs); (iii) among stands within the region Loire; and (iv) among zones within the stand Tinte. Electrophores/s Twigswere collected in winter and stored at 4°C until extraction. On each individual, one to five dormant buds were crushed with 0.5 mL extraction buffer (Tris-HC1 0.1 M, pH 7.5, 2 per cent PEG, 0.12 per cent EDTA, 4 per cent soluble PVP), 50 mg insoluble PVP and some sand, Extract was absorbed on 4 x 6 mm wicks of Whatman chromatography paper, and stored at —80°C. The same protocol was used for leaf extracts from the two youngest leaves of plants growing in the greenhouse. Electrophoresis was carried out on 12 per cent starch gels, with two different buffer systems: lithium-borate (Scandalios, Fig. 1 Map of the sites sampled in France for the study 1969; modified) and morpholine (Clayton & Tretiak, collection of Populus nigra with locations of the four study 1972). Staining was processed according to Berg- mann (1987) and Second & Trouslot (1980), modi- regions. fied. Each individual was assayed for bud and leaf extracts. The EST system was stained only for leaves, and the DIA and SDH systems only for dormant buds. All other systems gave the same viduals representing four sampled stands of large results with both kinds of extracts. Eight Mendelian extent: Mallemort (43°44'N, 5°10'E)inthe Durance polymorphic loci were scored: Pgm, Sd/i, Lap, Got-4, valley, 50 individuals; Les Brocs (47°28'N, 2°54'E) in Mdh-1, Dia-2, Idh-1 and Est-r. Inheritance and func- the Loire valley, 32 individuals; Pouilly (47°15'N, tional form of enzymes for loci Lap, Got-4, Mdh-1, 2°58'E) in the Loire valley, 19 individuals; and Tinte Sdh and Pgin have been demonstrated by Rajora (46°50'N, 3°23'E) in the Loire valley, 95 individuals. (1990) using root-tip extracts. Correspondence The stands Tinte and Les Brocs presented sepa- between patterns obtained with different organs and rated geographical zones corresponding to age repeatability of patterns for clones grown in classes: four zones in Tinte (respectively including different conditions were verified by Malvolti et al. 51, 11, 18, and 15 sampled individuals), and two (1991). We verified the Mendelian inheritance of zones in Les Brocs (16 sampled individuals in each). loci for the enzyme systems EST, DIA, IDH. The distribution of trees into geographical zones was confirmed by observation of aerial pictures. In Tinte, Data ages were measured approximately with an auger. In analysis both cases, the youngest age classes were found Allelefrequencies, genetic diversity and differentia- closest to the river bank. Analysis of population tion parameters were computed using different structure was carried out at four hierarchical levels computer packages: s -PLUS(3.0, Statistical Sciences provided by this sampling: (i) among countries Inc., Seattle, 1991), GENEPOP (Raymond & Rousset, within the species range: a set representing France 1995) and BIOSYS (1.7, Swofford & Selander, 1981). made of one randomly chosen genotype per sampled site was compared to the foreign collection; (ii) among regions within France: 249 clones were Allelefrequencies included, originating from the following four Populationallele frequencies iwereestimated by geographical regions: Alps (several drainages in the the sample allele frequencies, and variances were mountains of the northern Alps), Rhône (several estimated including the sample size and the sample drainages on the right bank of the Rhône), Durance genotypic frequency of homozygotes, according to (one drainage in the southern Alps, including the Weir (1990): this estimate is robust for deviations stand Mallemort), Loire (the open and lowland from Hardy—Weinberg equilibrium (HWE). The Genetical Society of Great Britain, Heredity, 77, 629—637. GENETIC VARIATION IN POPULUS NIGRA L. 631 ways of handling unequal sample sizes in the compu- Genetic diversity tation of the differentiation parameter (G1 or 0). Nei'sgene diversity index H (Nei, 1973) originally They showed the adequacy of Weir & Cockerham's described for one locus in one infinite random weighting scheme (in which the subpopulations are mating population was used to compare gene diver- weighted by the sample size) for small values of GST sities. For real populations, an unbiased estimate of (GST<O.Ol) whereas Nei & Chesser's (1983) this parameter, robust to deviation from HWE and scheme, in which all populations are given the same to small sample size is given by Weir (1990). Vari- weight, appeared to be appropriate for greater ance of gene diversity depends on allele frequencies, values of differentiation. In addition, the variation in genotypic frequencies and linkage disequilibrium subpopulation size that occurs in time and space in between loci. As pointed out by Fuerst et al. (1977), real populations causes an important source of diversity indices are expected to vary widely among deviation from Weir & Cockerham's model. In our loci. These authors generated the theoretical case, real population size as defined by the scale of distributionof observed heterozygositiesfor genetic exchange is not easy to estimate, but it different values of the effective population size and seems probable that it will vary between such the mutation rate. In order to detect abnormal loci geographically contrasted sites as the Alps and the or an abnormal distribution of gene diversities, we Loire valley because of restriction to seed and pollen tested the goodness of fit of the observed distribu- flow by natural obstacles such as mountains. Esti- tion of H-values in our study to the theoretical mates and confidence intervals of f F and 0 for distributions with a nonparametrical Smirnov test different subdivision levels were computed with the (Sprent, 1992). DIPLOIDL program (Weir, 1990), which uses Weir & Cockerham's estimators. Estimation of GST was also Hardy— Weinberg equilibrium and genotypic linkage computed following Nei & Chesser (1983). equilibrium These measures were tested within the different groups using the GENEPOP software, provid- Genetic distances Genetic distances summarize ing exact probability values (Louis & Dempster, differences between populations. Nei's genetic 1987; Guo & Thompson, 1992). A 1 per cent prob- distance (1972) and the coancestry distance ability level was used to test hypotheses of (Reynolds et al., 1983; Weir, 1990) are based on equilibrium.
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