Báo cáo khoa học: "Gene diversity in natural populations of oak species"

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Review article Gene in natural of oak diversity populations species A Kremer RJ Petit INRA, laboratoire de génétique et d’amélioration des arbres forestiers, BP 45, 33610 Gazinet, Cestas, France Summary — This contribution reviews studies of nuclear and organelle gene diversity in oak spe- cies. Studies of allozymes were reported for 33 species belonging to the sections Erythrobalanus, Lepidobalanus and Mesobalanus of the genus Quercus. The extent and organization of gene diver- sity were investigated at 3 hierarchical levels: complex, species and population. Total diversity at the species and population level varies greatly among species (from 0.06 to 0.40). The range of varia- tion among species is as large as that observed in other plant genera. Life history characteristics and evolutionary history are the main explanations for these results. Species with large and conti- nuous distributions such as Q petraea and Q rubra exhibit high levels of gene diversity. Within a complex, most of the nuclear gene diversity is distributed within populations (74%). The remaining diversity is mainly due to species differentiation (23%), while the between-population component is low (3%). Organelle gene diversity has been investigated recently in 2 species complexes in the sec- tion Lepidobalanus (one in North America and one in Europe). Compared to nuclear genes, orga- nelle gene diversity is strikingly different. Contributions of within-stand variation, species differentia- tion and population differentiation to total diversity, are respectively 13%, 11 % and 76%. Trees of a given population generally share the same chloroplast genome. Moreover, trees of different species (with reported introgression) occupying the same stand exhibit a high degree of similarity. Quercus / nuclear gene diversity / organelle gene diversity / gene differentiation Résumé — Diversité génétique dans les populations de chênes. Cette contribution présente une synthèse des résultats obtenus sur la diversité génétique nucléaire et cytoplasmique chez les chênes. À l’heure actuelle, des données existent sur 33 espèces appartenant aux sections Erythro- balanus, Lepidobalanus et Mesobalanus du genre Quercus. Les analyses ont porté sur l’estimation du niveau de diversité et sur la répartition de la diversité entre les 3 niveaux : complexe, espèce et population. La diversité totale au niveau espèce et population montre une variation importante (entre 0,06 et 0,40). L’amplitude de variation entre espèces est aussi importante que celle observée dans d’autres genres. Les caractéristiques biologiques des espèces ainsi que leur histoire évolutive per- mettent d’interpréter ces résultats. Les espèces à large aire de distribution, telles que Q petraea et Q robur manifestent des niveaux élevés de diversité. Au niveau d’un complexe d’espèces, la majeure partie de la diversité réside à l’intérieur des populations (74%); la différenciation entre espèces à l’intérieur du complexe représente 23%, alors que la différenciation entre populations à l’intérieur d’une espèce ne représente plus que 3% de la diversité totale. La diversité génétique cytoplasmique a été étudiée récemment dans 2 complexes de chênes blancs de la section Lepidobalanus (le pre- mier situé en Amérique du Nord, le second en Europe). Les résultats sont très différents de ceux ob- tenus au niveau nucléaire. Les contributions de la différenciation entre arbres (à l’intérieur des popu-
entre populations (à l’intérieur des espèces) et entre espèces sont respectivement de 13, 11 lations), et 76%. Les arbres d’une même population partagent généralement le même génome cytoplasmique. Par ailleurs, les espèces proches, échangeant des gènes et occupant les mêmes peuplements, mani- festent une similarité génétique élevée. Quercus / diversité génétique nucléaire / diversité génétique cytoplasmique / différenciation génétique INTRODUCTION morphisms. Because chloroplasts are ma- ternally and clonally inherited, whereas nu- clear genes undergo recombination and The genus Quercus comprises more than are biparentally inherited, the comparison 300 species spread over Asia, North of the organization of gene diversity in America and Europe (Camus, 1934- these different genomes is of particular in- 1954). On each continent, oak species are terest and will be stressed in this review. sympatric over large areas in which exten- sive gene flow among related species has been reported. Although morphological MATERIALS AND METHODS and ecological boundaries of species are usually well recognized, natural hybridiza- tion has been described in many combina- Nuclear gene diversity tions based on morphological evidence. This suggests that oaks are multispecies Reported studies or large sets of broadly sympatric species and sampling strategies exchanging genes (Van Valen, 1976). Since introgression represents a poten- Table I presents a general survey of gene diver- tially important source of genetic variation sity studies conducted so far on oak species, in natural populations, the multispecies with particular emphasis on sampling schemes. Species are classified according to Camus’s tax- level has to be considered in evaluating onomy (Camus, 1934-1954). Data are available levels and organization of gene diversity. on 33 species and originate from 13 references. Questions related to the multispecies These species belong mainly to sections Lepido- concept are: does interfertility between balanus (white oaks) and Erythrobalanus (red species provide higher levels of gene di- oaks) and are distributed over North America, versity than within species which do not Europe and Asia. No data are available on spe- cies belonging to sections Macrobalanus and normally experience introgression? How is Protobalanus. Sampling schemes are extremely diversity distributed among species and variable and in some cases restricted to a few among populations within species? We ad- loci or populations. Among the 33 species only 8 dress these questions by reviewing the assessed had more than 13 loci and 4 popula- scarce literature on gene diversity in oak tions. For a few economically important species species both at the nuclear and organelle (Q petraea, Q alba, Q rubra, Q macrocarpa), in- vestigations were conducted independently by levels. different institutes, leading in some cases to In recent years, allozymes have been substantial differences in the results. Therefore, used to document nuclear variation in species comparisons will only be made when oaks, while restriction-site data on chloro- the same techniques were applied. plast DNA (cpDNA) have provided a Because oak stands are often composed of preliminary insight into organelle poly- several interfertile species, gene diversity in nat-
ural populations should be analyzed at different Estimation of gene diversity parameters hierarchical levels: complexes of species, spe- cies within complexes and populations within Gene diversity was investigated at 3 hierarchical species. To evaluate gene diversity parame- levels (complex, species and population) by ters, species were considered to form a com- computing the following genetic parameters for plex when: 1) they belonged to the same bo- each locus separately (Hamrick and Godt, tanical section, 2) their natural ranges were 1990): 1) mean number of alleles (A): number of largely overlapping and 3) natural hybridization alleles observed at a given hierarchical level (ie, was indicated in the literature in all pairwise species or populations); 2) genetic diversity combinations. In defining a complex, we added (He); 3) effective number of alleles (A A 1/ ; ee = an additional constraint - that the gene fre- )). e (1-H quencies be obtained with the same tech- Additional subscripts indicate the level at niques for all species forming the complex. which these parameters were calculated; for ex- Among the different species listed in table 1, 4 ample A A and A are, respectively, the mean cs , p complexes can be identified using the criteria number of alleles at the complex, species and reported above. population levels. Genetic diversity was calculat- Σ p ; i 2 ed at each different level by: He 1 = - Q rubra complex where p is the mean frequency of allele i over i all units of the next lowest hierarchical level. Val- Two different studies (Manos and Fairbrothers, ues of the genetic parameters were averaged 1987; Guttman and Weight, 1989) have provid- over all loci analyzed. ed data on 6 and 10 species of red oaks, re- The structure of gene diversity was analyzed spectively. According to the aforementioned cri- using Nei’s genetic diversity statistics (1973, teria and the Quercus rubra syngameon 1977) in which the total diversity in a complex (Jensen, 1993), species were clustered in 2 (H was partitioned into 3 components: H H ) T TS complexes (4 species each): complex 1, com- = + D + D where H is the diversity within prised of Q rubra, Q coccinea, Q ilicifolia and Q SG GT ; S populations within species, D is the compo- velutina (Manos and Fairbrothers, 1987); and SG nent of diversity due to subdivision into popula- complex 2, comprised of Q rubra, Q marilandi- tions within species, and D is the component ca, Q phellos and Q velutina (Guttman and GT of diversity due to subdivision into species (with- Weight, 1989). in the complex). Q alba complex These components were further calculated ratios of total diversity (Chakraborty and Lei- as This contains studied by Guttman and species mar, 1988; Kremer et al, 1991), which is differ- clustered in a complex according Weight (1989) ent from the notation of Nei (1973): G + G + S SG to the Q alba syngameon described by Hardin G 1 and G H the coefficient of gene GT SS , T /H = = (1975): Q alba, Q bicolor, Q lyrata, Q macrocar- differentiation among individuals within popula- pa and Q stellata. tions; G D the coefficient of gene dif- SG SG , T /H = ferentiation among populations within species; Q douglasii complex and G D the coefficient of gene differ- GT GT , T /H = entiation among species within a complex. The Two white oaks (Q douglasii and Q lobata) were proportion of gene diversity residing among pop- selected among the 3 species studied by Millar ulations irrespective of species is: GST G + SG = et al (1992). They are sympatric over their entire . GT G distribution in California. Natural hybridization Due to the extremely different sampling has been reported by Tucker (1990). schemes used (table I), genetic parameters systematically calculated for every not were Q robur complex For documentation purposes, we report study. Q petraea and Q robur species are sympatric all the results on a species level, but restrict the most of Europe and their introgression has analysis of organization of gene diversity to the over been extensively documented (Rushton, 1979; cases where more than 13 loci were investigat- ed. Because authors used different genetic pa- letswaart and Feij, 1989). The data analyzed here originated from Müller-Starck et al (1992). rameters or estimation methods, most of the pa-
rameters were estimated following the proce- rameters were recalculated when allele frequen- dures of Nei and Chesser (1983) and Nei cies were available. (1987), recommended for low population sample sizes. Organelle gene diversity Two separate studies were conducted indepen- RESULTS dently on North American and European white oaks (Q alba and Q robur complexes), both of them based on chloroplast DNA (table II). The Levels of nuclear gene diversity Q alba complex comprises Q alba, Q macrocar- pa, Q michauxii and Q stellata. The Q robur complex comprises Q petraea, Q pubescens Complex level and Q robur. The theory of organelle gene diver- sity has recently been developed (Birky et al, At the complex level, oaks exhibited a high 1989; Birky, 1991).Ifwe postulate that there is amount of genetic variation (table III). Over no within-tree variation (ie, no variation among the 4 complexes, the average number of different chloroplasts of the same individual), the same A, H and G parameters for nuclear genes alleles was 3.55 and mean genetic diversi- can be calculated for organelle genes. The data ty was 0.273. With one exception, the ma- originated from restriction-site polymorphisms jority of loci in a complex were comprised corresponding to restriction-site gains or losses. of frequent alleles that were common to all The polymorphisms were analyzed at the geno- species. The exception was the Q alba typic level, ie all haplotypes were considered to complex, in which different alleles were of- be different alleles of one locus. The genetic pa-
nating from the 2 data sets; their causes ten fixed in differentspecies (Guttman and probably be attributed to different elec- Weight, 1989). The Q alba complex exhib- can trophoretic techniques used in different la- ited the highest overall diversity. White oak boratories and different species included in complexes (Q alba, Q douglasii, Q robur) each complex. showed higher diversity than the Q rubra complexes. Within the latter, there were The 3 white oak complexes considered striking differences between results origi- broad distribution in North America have a
Europe, except for the Q douglasii Influence of life history characteristics and complex, which is restricted to California. genetic diversity (data from Manos on and Fairbrothers, 1987; Guttman No correlation between the number of spe- cies within a complex and the levels of and Weight, 1989) gene diversity was found, but data were We investigated variation of H in relation es only available on 4 complexes. to several life history characteristics: mean northern latitude of distribution (NL), range of distribution (RD), seed size (SS), tree Species level height (TH), crossability with other species (CR) and life habitat conditions (LHC). Data on levels of gene diversity at the spe- Quantitative data on RD, SS and TH came cies level are summarized in table I. Be- from Aizen and Patterson (1990), NL was cause of the different sampling strategies, estimated from distribution maps in Fow- we restricted comparisons among species ells (1965). Two habitat conditions were to data obtained with the same techniques. Manos and Fairbrothers (1987) analyzed identified (Fowells, 1965): 1) wet soils, riv- gene diversity in 6 red oaks and one white er banks and flood plains; and 2) dry up- lands. Crossability of a given species is de- oak, each represented by 2-3 populations in New Jersey. Guttman and Weight fined as the number of species which were (1989) provided information on 8 white reported to hybridize under natural condi- oaks and 10 red oaks. Although the sam- tions with the species studied. Data on CR ple size per species was small in the latter were obtained from the review of American hybrids by Palmer (1948). For example Q study (table I), the trees were collected across the range of each species; thus the velutina was reported to hybridize with 14 data were appropriate for the species lev- other species, whereas only 3 hybrids el. Five species were common to the 2 were mentioned for Q prinus. studies. When comparing the same spe- cies in the 2 different studies, the levels of gene diversity were always lower in the study of Manos and Fairbrothers, indicat- ing the use of different electrophoretic techniques or different enzymes. Species comparisons of levels of gene diversity were therefore confined within each study. Influence of taxonomy on genetic diversity (data from Guttman and Weight, 1989) There were significant differences in the levels of diversity (A and H between es ) es white (section Lepidobalanus) and red oaks (section Erythrobalanus) in eastern North America (table IV). White oaks ex- hibited higher levels of diversity than red oaks. Among the 80 pairwise comparisons between species of each section (table I), higher levels of H were found for white es oaks in 66 cases.
Significant correlations were found be- red oaks (Q imbricaria) explain the lack of tween H and NL, RD, SS and TH (table es correlation within this section. V). Because of the small number of spe- Therewas no significant relationship be- cies, correlation was sensitive to extreme crossability and levels of diversity. tween values of H or other covariates. There- es Nor was there any significant difference fore, different calculations were made by between the H values for the 2 cat- es mean removing values for Q prinus, which exhib- egories of habitat conditions. ited extremely high values for H (0.398) es and seed volume (10.5 cm The relation- ). 3 ships detected were stronger in the white level Population oaks than in the red oaks. While the south- In making comparisons among species at ern latitude of distribution is similar to all white and red oaks, the northern latitude the population level, only studies with 13 or varies according to the species. By con- more loci and 4 or more populations were struction, NL and RD are already correlat- included (table I). The results obtained ed. Species distributed along the gulf of show a large range of variation among species in H from 0.057 to 0.275. A Mexico (Q virginiana for the white oaks , ep and Q laurifolia for the red oaks) had low closer analysis revealed that species with the highest level of gene diversity at the H values, respectively 0.149 and 0.146 es (table I). On the other hand, widespread population level were characterized by species (Q alba for the white oaks and Q evenness of allelic frequencies (table VI). In the case of Q petraea, for 33% of the velutina for the red oaks) exhibited higher loci, the frequency of the most common al- es H levels, respectively 0.276 and 0.203. Exceptions to these relationships in the lele was lower than 0.7, whereas this pro-
this discrepancy may be reduced to 5% in Q lobata and species. Again, portion was due to methodological differences. If we Q agrifolia. Higher within- in 0% to discard the results of Manos and Fair- diversities were more closely population associated with differences in frequency brothers, populations from species with profiles than with differences in numbers of large distribution ranges (Q macrocarpa, Q alleles. petraea, Q rubra and Q robur) exhibit con- siderably higher diversity than species with As noted in table I, the data of Manos more restricted distributions (Q agrifolia, Q and Fairbrothers (1987) show lower gene douglasii, Q lobata). diversities than other studies on the same
Levels of organelle gene level (table VII). These values should not diversity be compared to those obtained using allo- zymes, since they refer only to polymor- Preliminary analyses of chloroplast poly- phic sites in the chloroplast genome. In morphisms in the European white oaks comparison to the species level, within- (Q robur complex) were made with 33 dif- population diversity estimates were ex- ferent restriction endonucleases and 2 tremely low (table VII). Among the 91 pop- large Petunia hybrida cp DNA probes rep- ulations analyzed in the Q robur complex, resenting 26% of the Petunia chloroplast all trees within the same populations had genome on a sample of 6 trees belonging the same haplotype except in 15 cases, to 3 different species (Q robur, Q petraea where 2 different genotypes were found. and Q pubescens) (Petit, 1992). A similar Among the 17 populations of the Q alba approach was applied to the American complex, only 4 comprised more than one white oaks (Q alba complex): 15 restriction single haplotype. endonucleases, 7 probes of the Petunia chloroplast genome (73% of the genome), and 45 trees of different origins (Whitte- Organization of nuclear gene diversity more and Schaal, 1991) were used. Six multirestriction-site genotypes were identi- fied in the European oaks and 8 in the level Complex American oaks. With the exception of 3 cases, the different genotypes could be in- complexes, the proportion of Over the 4 terpreted as single restriction-site gains or genetic diversity among populations ac- losses. counted for 26% of the total diversity (table When the analysis was limited to the VIII). A major part of that proportion was polymorphic sites of the genome, high lev- due to differentiation between species, els of diversity were found at the species rather than differentiation among popula-
sampling scheme, G G and G in the Q robur tions within could , S SG ST species, except not be estimated. complex. The proportion of variation due to the differences among species differed among level Species the complexes. In the European white oaks (Q robur complex), differentiation be- When data were available only on a spe- tween the 2 species was extremely low, cies level (table I), differentiation among while in the North American white oaks populations accounted only for a small pro- (Q alba and Q douglasii complexes), it ac- portion of the total diversity, in general less counted for more than 37% of the total di- than 6%, regardless of the species consid- versity. Interestingly, values obtained for ered. the red oaks were of the same magnitude in the 2 different studies, despite the im- portant differences found for A A and , c ec Organization of organelle gene diversity H (table III). ec Differentiation among populations within The 2 reported studies showed remarkably species remained low in all cases (from 1 similar results (table IX). While the total di- to 4%). The coefficient of differentiation versity was rather high (0.664), it was geo- among populations could not be calculated graphically organized. The within-population in the Q alba and Q rubra complexes of component represented only 12% of the American oaks, since each species was total diversity. Moreover, differentiation be- represented by a bulk collection of trees tween species was similar (7%). As a re- sampled across the range of the species sult, interpopulation gene diversity is the (Guttman and Weight, 1989). Due to this major component of the total diversity.
(Hamrick et al, 1992). Earlier reviews on Whittemore and Schaal (1991) ob- diversity showed that long-lived, out- served for the North American white oaks gene crossing, wind-pollinated species of the (Q alba complex) that, except for the most late stages of succession exhibited higher frequent one, all genotypes were geo- levels of gene diversity (Hamrick and Godt, graphically localized. That is, when spe- 1990). Oak species possess all these char- cies were sampled in the same locality, Moreover, the existence of acteristics. distinctive chloroplast genotypes were large complexes comprising several inter- shared among them. Similar observations fertile sympatric species is an additional were made in white oaks in Europe (Petit, potential source of genetic variation, as 1992). From a subsample of 13 pairs of shown by the high H value on a complex populations (one Q petraea and one Q ro- ec level (0.275). bur) originating from the same or contigu- ous stands, 9 presented the same geno- There is wide heterogeneity among spe- type in each species. cies: levels of gene diversity vary between 0.058 (Q palustris) and 0.376 (Q alba). A significant proportion of this variation ap- DISCUSSION pears to be associated with the range of distribution of the species, particularly the northern latitude of distribution and acorn Nuclear gene diversity size (table V). These characteristics, how- ever, are not independent, as shown by levels of nuclear gene diversi- Aizen and Patterson (1990). According to Oak species among the highest found in long- these authors, large-seeded acorns are ty were preferentially dispersed by animals, partic- lived woody species. Diversity on a spe- ularly birds, and are more successful in cies level (H 0.186, table I) appears to es = site capture, as shown by the positive cor- be higher in the genus Quercus than in relation between acorn size and early Populus (0.127), Acacia (0.125), Abies seedling growth. Thus, large-seeded oak (0.145) or Pinus (0.157); of similar magni- species are considered to be better colo- tude to Eucalyptus (0.187); but inferior to nizers. These results support earlier Pseudotsuga (0.201) or Picea (0.219) con-
divergence (Crawford, 1989), while by Hamrick et al (1992) for clusions drawn zyme gradual speciation through geographic iso- general: that species with tree species in lation results in considerable differentiation distributions and widely dis- widespread among species. On the other hand, natural persed seeds tend to have higher genetic hybridization is frequent within the genus diversities. Surprisingly, we did not find Quercus (Rushton, 1993). Even if hybrid any relationship between crossability and swarms are rare in oaks (Hardin, 1975), level of gene diversity, perhaps because of low gene flow among species may be suffi- imprecise estimates of crossability (table cient to counteract allozyme divergence, V). unless allozymes are differentially selected In addition to life history traits, evolution- in different species. There is some evi- ary history may contribute significantly to dence that the extent of introgression in the current levels of genetic variation, as oaks depends upon site conditions. On shown by the differences observed be- sites optimal to parental species, selection tween the 2 major sections of the genus against F hybrids before they pass on 1 Quercus (table IV). Red oaks are less vari- their genes is thought to be important (Har- able than white oaks. Causes of these dif- din, 1975). On sites less favorable to pa- ferences may be attributed to the original rental species, intermediate phenotypes gene pool of current species or to evolu- are more frequent (Grandjean and Sigaud, tionary forces. Combined data on molecu- 1987). Therefore, the past and present ec- lar and morphological traits suggest that ological opportunities to exchange genes white oaks in northeastern America origi- may result in differences of genetic diffe- nate from multiple lineages covering differ- rentiation among species. ent continents (Nixon et al, Cornell Univer- Population differentiation within oak spe- sity, personal communication). Red oaks cies is in agreement with earlier reviews on are restricted to North America and prob- gene diversity organization in plants which ably stem from a reduced gene pool com- showed that the breeding system has a pre- pared to white oaks. dominant influence on G values (Hamrick ST Species differentiation within a complex and Godt, 1990). Oaks are largely outcross- substantially among the different varies ing species with extensive gene flow among complexes. In the broadly sympatric Euro- populations (Ducousso et al, 1993), thereby pean white oaks, species differentiation is reducing differentiation between popula- even lower than geographic differentiation tions. On the average, G (equivalent to SG (among populations within species), G in other papers) was 6% in oaks, with ST whereas in the North American white oaks extreme values of 1-17% (table I). Sam- 37-51% of the total diversity within a com- pling of populations was too low in most plex is due to species differentiation. In species to further analyze species variation general, most frequent alleles are common of G values. SG to the majority of species forming a com- plex. Time and rates of speciation and im- portance of gene flow between species Organelle gene diversity constitute 2 complementary hypotheses for interpreting our observations. According to Axelrod (1983), oaks proliferated and dif- Because the chloroplast genome was thought to be highly conserved within a ferentiated rapidly during periods of ex- species, studies on cpDNA have mainly fo- treme climatic changes during the middle cused on interspecific relationships. None- to late Tertiary period. Rapid speciation is associated in most cases with low allo- theless, large surveys over several popula-
tions have demonstrated the existence of also found in poplars (Keim et al, 1989; intraspecific variation in cpDNA (Wagner Smith and Systma, 1990). The role of the et al, 1987 in Pinus banksiana and Pinus occurrence of chloroplast capture through- contorta; Neale et al, 1988 in Hordeum; out the evolutionary history is still an open Soltis et al, 1989 in Tolmiea menziesii ; debate. Is ancient hybridization and intro- see Harris and Ingram, 1991, for a re- gression occurring concurrently with coloni- view). Combined inter- and intraspecific zation, or is continuing gene flow responsi- assessments of cpDNA polymorphisms in ble for the maintenance of low species oaks show intriguing features in gene di- differentiation of cpDNA polymorphism? versity organization. Within oak species, differentiation among Patterns of intraspecific variation are accounts for the populations major portion similar in sympatric species in both Ameri- of gene diversity as compared to within pop- can and European white oaks. Different ulation variation. These results were expect- species share identical genotypes that are ed from the neutral theory applied to orga- confined to geographic areas. This has nelle genomes (Birky et al, 1983, 1989; been qualified as chloroplast ’capture’ by Birky, 1991).First, organelle genes are Rieseberg and Soltis (1991).Other woody sensitive to genetic drift than nuclear more plant species showing similar trends are genes, since their effective population size poplars (Smith and Systma, 1990) and wil- is approximately one half that of nuclear lows (Rieseberg and Soltis, 1991).Chloro- genes in monoecious species. Second, if plast capture is attributed by these authors we postulate that organelle genes are only to active gene flow between species. Hy- maternally inherited, their migration is lower bridization and introgression have been than for nuclear genes. Increase of genetic suggested to be important evolutionary drift and decrease of migration leads to forces in oaks (Burger, 1975; Van Valen, greater fixation of genes within populations 1976). However, capture of a maternally in- and, result, to important interpopulation as a herited genome from a donor species by a differentiation. Biological features of fruiting receptive species requires, after hybridiza- and seed dispersal in oaks reinforce theo- a series of unidirectional backcrosses. tion, retical expectations of population differentia- Preferential pollination between the pollen tion. Fruiting in oak stands is extremely het- of the receptive species and the ovule of erogeneous through time and space. As a the hybrids is a prerequisite to the final in- result, some stands may originate from a re- clusion of the chloroplast genome of the do- stricted number of ’mother’ trees. On the nor species into the receptive species. In other hand, seed dispersion is limited (Sork, European oaks, experiments with controlled 1984). Even if transported long distances by crosses show that pollination of peduncu- jays or rodents (Darley-Hill and Johnson, late oak (Q robur) by sessile oak (Q pe- 1981; Kanazawa, 1982; Miyaki and Kiku- traea) is more successful than that of the zawa, 1988), acorns can rapidly lose their reciprocal cross (Steinhoff, 1993). Similar viability either by predation or storage under results were found in a natural stand com- unfavorable conditions. prised of both species (Bacilieri et al, 1993). Preferential backcrosses between hybrids and one of their parental species have CONCLUSION been reported in a study of introgression between Quercus prinus L and Quercus The contrasting patterns of gene diversity alba (Ledig et al, 1969). Unidirectional gene organization between nuclear and orga- flow resulting in chloroplast capture was nelle DNA may be unique to Quercus, due
essentially to the asymmetry of seed and Axelrod DI (1983) Biogeography of oaks in the Arcto-Tertiary province. Ann Mi Bot Gard 70, pollen dispersal in this genus. Nuclear 629-657 gene diversity is of similar magnitude and Bacilieri R, Roussel G, Ducousso A (1993) Hy- distributed as in most other woody plant bridization and mating system in a mixed genera. Although only scarce data exist for stand of sessile and pedunculate oak. Ann organelle genes, expectations for most Sci For 50 (suppl 1), 122s-127s tree species are that they should be less Birky CW (1991) Evolution and population ge- geographically structured. In most conifers, netics of organelle genomes: mechanisms chloroplasts are predominantly paternally and models. In: Evolution at the Molecular inherited (Neale and Sederoff, 1988) and Level (Selander RK, Clarck AG, Whittam TS, cpDNA variation is expected to be more eds) Sinauer Associates, Sunderland, MA, 112-134 evenly distributed over the range of the species, as shown in Pinus banksiana and Birky CW, Maruyama T, Fuerst P (1983) An ap- proach to population genetic theory for genes Pinus contorta (Wagner et al, 1987). In in mitochondria and chloroplasts, and some other angiosperm woody species, wider results. Genetics 103, 513-527 seed dispersal than in oaks will probably Birky CW, Fuerst P, Maruyama T (1989) Orga- limit population differentiation of cp DNA. nelle gene diversity under migration, muta- As more species are studied for organelle tion, and drift: equilibrium expectation, ap- diversity, interesting comparisons will be- proach to equilibrium, effects of heteroplasmic come possible between potential seed flow cells, and comparison to nuclear genes. Ge- and cpDNA (or mitochondrial DNA) diffe- netics 121, 613-627 rentiation among populations. Burger WC (1975) The species concept in Quer- Taxon 24, 45-50 Comparison of nuclear and organelle cus. gene diversity on a range-wide basis will Camus A (1934-1954) Les chênes. Monograph- ie du genre Quercus. Editions Paul Le Chev- afford interesting insight into the evolution- alier, Paris, 3 vol, 1314 p ary history of oak species, especially as re- Chakraborty R, Leimar O (1988) Genetic varia- gards recolonization after the last glacia- tion within a subdivided population. In: Popu- tions. Maternal lineages may be traced lation Genetics and Fishery Management from suspected refugia to present distribu- (Ryman N, Utter F, eds) University of Wash- tions via cpDNA polymorphisms. Gametic ington Press, Seattle, 89-120 disequilibria between nuclear and cytoplas- Crawford DJ (1989) Enzyme electrophoresis mic genes in mixed stands will clarify the and plant systematics. In: Enzyme Electro- importance of hybridization as an evolu- phoresis and Plant Systematics (Soltis DE, tionary force in oak species. Soltis PS, eds) Chapman and Hall, London, 146-164 Darley-Hill S, Johnson WC (1981) Acorn disper- sal by the blue jay (Cyanocitta cristata). ACKNOWLEDGMENTS Oecologia (Berl) 50, 231-232 We are grateful to C Millar, G Müller-Starck and Daubree JB (1990) Comparaison de la structure ZS Kim for providing their data on allele frequen- génétique du chêne rouge dans son aire na- cies of oak species. turelle et dans aire d’introduction. These son d’ingénieur, I’ENITEF, Nogent-sur-Vernisson, France, 43 p Ducousso A, Michaud H, Lumaret R (1993) Re- REFERENCES production and gene flow in the genus Quer- cus. Ann Sci For 50 (suppl 1), 91s-106s Aizen MA, Patterson WA (1990) Acorn size and geographical range in the North American Fowells HA (1965) Sylvics of Forest Trees of the oaks (Quercus L). J Biogeogr 17, 327-332 USA. US Dept Agric Handb No 271, 762 p
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