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Geographical Structure of Gene Diversity in Patterns of Variation

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Geographical Structure of Gene Diversity in Patterns of Variation Heredity 75(1995) 506—517 Received30 March 1995 Geographical structure of gene diversity in Quercus petraea (Matt.) Liebi. I. Monolocus patterns of variation A. ZANETTO & A. KREMER* INRA, Laboratoire de Génetique et d'Amélioration des Arbres Forestiers, BP 45, 33611 Gazinet Cedex, France Agene diversity survey was conducted on a range-wide sample of 81 populations of Quercus petraea. Allele frequencies were calculated at 13 enzyme-coding loci, of which 11 were poly- morphic. There was a clear discrepancy in the levels of diversity at loci controlling enzymes of primary metabolism compared with those involved in secondary metabolism, the latter being more variable than the former. Quercus petraea is a highly variable species as are other long- lived widespread forest species: at the species level, the mean number of alleles per population was 4.77 and the expected heterozygosity 0.265. Populations from the central part of the natural range exhibited fewer alleles but higher heterozygosities than populations from the margins of the distribution. Significant correlations were observed between allele frequencies and longitude for most loci, resulting in a dma! variation of allele frequencies across a continental gradient. The patterns of geographical variation in allele frequencies and levels of diversity were interpreted as a consequence of postglacial migration pathways. Keywords:allozyme,diversity, genetic differentiation, heterozygosity, Quercus petraea, spatial autocorrelation. Introduction range is a continuous distribution, except in the southern limits where stands are scattered. Through- Geographicalvariation in forest trees has been out its distribution, Q. petraea is associated with Q. widely studied in provenance research for morpho- robur resulting in mixed stands where unidirectional logical traits (Wright, 1976). For widespread species hybridization may occur, Q. pet raea preferentially distributed over large latitudinal or continental ran- pollinating Q. robur (Bacilieri et a!., 1995). Prove- ges, clear geographical clinal trends of variation nance tests based on regional population collections have usually been found and important population have been established in several European countries differences have been observed that were attributed (see Kremer et al., 1993 for a review). While to environmental selection pressures. On the other important population differences were discernible hand, allozyme population surveys in widespread for growth and adaptive traits, no clear geographical forest species have resulted in extremely low popula- trends appeared as a result of the limited regional tion differentiation (Hamrick et al., 1992; Kremer, population sampling. 1994), although geographical patterns have been Allozyme diversity studies in oaks (Kremer & detected (Lagercrantz & Ryman, 1990) when range- Petit, 1993) have shown similar patterns of variation wide studies were conducted. In contrast to pheno- to those of other forest tree species (Hamrick et al., typic traits, geographical trends of variation in 1992). A series of papers (Kremer et a!., 1991; ailozyme frequencies have been attributed to evolu- Mülier-Starck & Ziehe, 1991; Müller-Starck et a!., tionary footprints (Strauss et a!., 1992), particularly 1993) has shown that Q. petraea is characterized by recolonization routes. high within-population diversity associated with a Quercus petraea is a widespread species covering low differentiation among populations. These most of Europe from Spain to Russia and from studies, however, failed to reveal any geographical Scotland to Turkey (Kleinschmit, 1993). Its natural pattern in gene frequencies, mostly because they were limited to a regional population sample. It was *Correspondence our objective to address the geographical organiza- 506 1995 The Genetical Society of Great Britain. GENE DIVERSITY IN QUERCUS PETRAEA 507 tion of allozyme diversity over the entire range of Q. the diversity evenly distributed throughout the petraea.Despite its large distribution, early results natural range? Again the sampling strategy was indicated only minor differentiation among popula- designed so that various parameters of diversity tions (Zanetto et a!., 1993). Our focus was to assess could be accurately estimated. Particular attention the geographical delineation of gene frequency and was given to the number of alleles (allelic richness), diversity differences, even if they were small. The a parameter that is more sensitive to frequency pro- population sampling strategy was therefore designed files than heterozygosity. As allozyme frequency pro- so that: (i) minor gene frequency variation could be files in forest trees are generally characterized by detected, and (ii) the geographical distribution of one rather frequent allele and several rare alleles gene frequency and gene diversity could be tested. (Conkle, 1992), a large sample size is required to The strategy consisted of sampling a large number estimate allelic richness. of populations over the whole distribution of the species and of clustering populations in geographical groups so that comparisons could be made between Materials and methods groups. We attempted also to compare the geo- Plant material graphical pattern of gene diversity with evolutionary records of postglacial migrations based on palyno- Eighty-one populations of Q.petraea of putative logical data. native origin were sampled over the natural range of The second objective of this population study was the species from Ireland to Turkey and from the to compare the levels of within-population diversity Pyrenées to Norway. The sample also comprised among populations. The underlying aim was to pro- populations originating from various altitudes rang- vide basic information for conservation strategies. Is ing from sea level (French Brittany) to 1300 m Fig. 1 Geographical distribution of the populations of Quercus petraea. Populations wereclustered in 14 groups according to their geographical proximities. The Genetical Society of Great Britain, Heredity, 75, 506—517. 508 A. ZANETTO & A. KREMER (Alps), although most of the populations came from 0 0 — - cc —— .-i - — altitudes between 100 and 450m(Fig. 1); only six 00 0000 00 00 00 00 00 populations originated from altitudes higher than z 450 m. Geographical data were recorded for each population (latitude, longitude, altitude) and are given elsewhere (Zanetto, 1995, unpublished The- sis). The populations were clustered in 14 groups s.c N\000C according to their geographical proximity (Fig. 1). N-©00 tfl flN \ .CN Several geographical clusterings of populations were I II I I I tested according to proximity. The results of gene 1—ON0 001rN NNC\N©cflN.cn- diversity and differentiation were very similar. The N.- N II'_,- _ - -_ '— - - -, — final choice resulted from a compromise between 0\ trm 00 Nt 00 0\N C\ N 00 N C N constant number of populations per group and geo- N tr - - N graphical proximity. In each stand, where a population was sampled, acorns were collected from the ground over an area rd of 15—20 ha, representing about 50 collecting points t( 0000 QON equally distributed with 100—200 seeds for each N—0ir- N r N \0 I I I I point. Seeds were only harvested when the fruiting I II 4-. was above average (more than 50 per cent of the 00 Nor-00 0 N -N- trees bearing acorns). Seeds of all collection points -_ - — — - were bulked in a single lot. A random sample of 120 s c n 00(r f— N N00 seeds for each population was taken for the study of allozyme variation. In a few cases when collections C.) could be made from single trees, open-pollinated C.) progenies were collected in a stand from the same C - area. Acorns were harvested from at least 10 trees - SCcm 0 CN00 NmO0CO0N-000 per stand (20 acorns for each family) and a random —— .- N —Nkr— — N NN — — subset of 4—12 seeds per family was subsequently I IIIII I I II C00._-l NNrON 00 used for electrophoresis. C 2. — —__ - __ - - '._,N \__— '.—— — . '.CC) 00\ N N C -—N C 'Ic c - m N Starchgel electrophoresis N -C C\ V — — — — — — N( —— Acornswere soaked in water for 24 h and germi- nated on vermiculite in an incubator. When the radi- ..) des were 2—4 cm long, enzymes were extracted from -_NnN C N C C the radicle tissues and separated by standard hori- C.) 00'NN'- ,-IQQ C 00 tfl m N — — NNNN zontal starch gel electrophoresis. Formulations for C.) NcN N II I I I I I C.) 00 N \C) C\ m oc extraction, electrode and gel buffers are given in N N N S 'r N —400.C N .00 Zanetto et al. (1994). Buffer formulations for fl N —f) N Ce — - - - - '—) N — m '—N C.) enzyme stains were adapted from Cheliak et a!. () S-00 N - —N N00 5N C00 C\ N (1984), Conkle et al. (1982) and Vallejos (1983). 00 C IrN S N -\C m C -u Eleven enzymes were analysed for the population C.) survey: acid phosphatase (ACP, EC 3.1.3.2), alanine mr aminopeptidase (AAP, EC 3.4.11.1), diaphorase C.) (DIA, EC 1.8.1.4), glutamate oxaloacetate transami- 00 nase (GOT, EC 2.6.1.1), isocitrate dehydrogenase C (IDH, EC 1.1.1.42), leucine aminopeptidase (LAP, C EC 3.4.11.1), menadione reductase (MR, EC Ce 1.6.99.2), malate dehydrogenase (MDH, EC 1.1.1.37), phosphoglucose isomerase (PGI, EC C.) 5.3.1.9), phosphoglucomutase (PGM, EC 5.4.2.2), 6-phosphogluconatedehydrogenase (6PGD, EC I Ce 1.1.1.44). Segregation analysis (A. Zanetto et al., — aa —— — — — — —— — — — — —— .. The Genetical Society of Great Britain, Heredity, 75, 506—517. GENE DIVERSITY IN QUERCUS PETRAEA 509 unpublished data) showed that these enzymes were population gene diversities. The coefficient of abso- encoded by 13 loci (Acp-C, Aap-A, Dia-A, Got-B, lute gene differentiation G'5 is then: Idh-A, Lap-A, Mr-A, Mdh-B, Mdh-C, Pgi-B, Pgm-A, 6Pgd-A, 6Pgd-B). Because of the continuous Dm G'=St improvement of the methods during the experiment, Ht+Dm the number of loci increased during the experiment from eight to 13 (see Table 1).
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