Báo cáo khoa học: "Reproduction and gene flow in the genus Quercus"

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Review article and gene flow in the genus Quercus L Reproduction A Ducousso H Michaud R Lumaret 1 INRA, BP 45, 33611 Gazinet-Cestas; 2 CEFE/CNRS, BP 5051, 34033 Montpellier Cedex, France review the characteristics of the floral biology, life cycle and breeding In this paper Summary — we system in the genus Quercus. The species of this genus self-incompatible and have very long are life spans. The focus of our review is on the effects of gene flow on the structuration of genetic varia- tion in these species. We have examined the influence of gene flow in 2 ways: 1) by measuring the physical dispersal of pollen, seed and vegetative organs; and 2) by using nuclear and cytoplasmic markers to estimate genetic parameters (F N These approaches have shown that nuclear (iso- , ). is m zyme markers) as well as cytoplasmic (chloroplastic DNA) gene flow is usually high, so that very low interspecific differentiation occurs. However, intraspecific differentiation is higher for the cytoplasmic DNA than for the nuclear isozyme markers. floral biology / life cycle / breeding system / gene flow / oak Résumé — Système de reproduction et flux de gènes chez les espèces du genre Quercus. Les caractéristiques de la biologie florale, du cycle de vie et du système de reproduction ont été analysées pour les espèces du genre Quercus. Ces espèces sont auto-incompatibles et à très lon- gue durée de vie. Les effets des flux de gènes sur la structuration de la variabilité génétique ont aussi été étudiés de 2 manières. D’une part, grâce aux mesures de la dispersion du pollen, des graines et des organes végétatifs, et, d’autre part, en utilisant des paramètres génétiques (F N ,) is m obtenus à partir des marqueurs nucléaires et cytoplasmiques. Il apparaît que les flux géniques nu- cléaires (isozymes) et cytoplasmiques (ADN chloroplastique) sont en général importants, d’où une faible différenciation interspécifique. Néanmoins la différenciation intraspécifique est plus forte lors- qu’elle est estimée à partir des marqueurs cytoplasmiques que lorsqu’elle l’est à partir des mar- queurs nucléaires. biologie florale / cycle de vie / système de reproduction / flux de gènes / chêne
INTRODUCTION Staminate flowers Male flowers are grouped in catkins which Plant populations show a significant in the axils of either the inner bud develop amount of organization in the genetic vari- scales or the first leaves, in the lower part ation they contain (Wright, 1951). Such or- of the branches produced in the same ganization is significantly influenced by year. Staminate inflorescences are initiat- joint action of mutation, migration, selec- ed in late spring, flowers develop in early tion and genetic drift. In this context, gene summer and meiosis occurs in the follow- flow among plant populations may repre- ing spring, giving rise to binucleate pollen sent a significant factor influencing the grains immediately prior to the emergence maintenance of genetic organization in of catkins (Sharp and Chisman, 1961; plant species populations (Slatkin, 1987). Stairs, 1964; Tucovic and Jovanovic, 1970; Gene flow is generally considered to be Hagman, 1975; Bonnet-Masimbert, 1978; both small enough to permit substantial lo- Merkle et al, 1980). For a given tree, if cal genetic differentiation (Levin and Kerst- weather conditions are suitable, catkin er, 1974), and large enough to introduce growth is achieved 1-2 weeks after bud variability into widely separated popula- opening, and pollination is completed in 2- tions (Loveless and Hamrick, 1984). This 4 days (Sharp and Chisman, 1961; Stairs, is particularly important in outbreeding, 1964; Vogt, 1969; Lumaret et al, 1991).In perennial and iteroparous species, such deciduous oaks, leaf expansion ceases forest trees. as during the release of pollen, which allows In the present paper, the influences of freer movement of pollen (Sharp and Chis- the mating system and factors operating 1961). man, on gene flow at different stages of the life cycle are reviewed in various species of Pistillate flowers the genus Quercus. Female flowers appear in the axils of leaves produced in the same year. They REPRODUCTIVE SYSTEM are produced on a short stalk and become visible a few days after the emergence of the male catkins (Sharp and Sprague, Floral biology 1967). Inflorescence primordia are difficult to distinguish from lateral bud primordia Species of the genus Quercus (the oaks) before late summer, hence the exact time are predominantly monoecious with dis- of the initiation of pistillate inflorescences tinct male and female flowers borne on 2 is difficult to determine. As hermaphrodite types of inflorescences; very occasionally flowers are known to occur occasionally, they bear hermaphroditic flowers or inflo- Bonnet-Masimbert (1978) has hypothe- (Scaramuzzi, 1958; Stairs, sized that their initiation may occur in late rescences 1964; Tucker, 1972; Bonnet-Masimbert, spring, when the staminate inflorescences 1978; Tucker et al, 1980). The characteris- develop. Female flowers develop in late tics of male and female flowers winter or early spring (Bonnet-Masimbert, are sum- marized below. 1978; Merkle et al, 1980). Each flower is
included ina cupule, which is regarded as fertilized ovule either suppresses the growth of the other fertilized ovules or pre- homologous to a third-order inflorescence branch (Brett, 1964; McDonald, 1979). vents their fertilization. After fertilization, the acorns mature within about 3 months, During elongation of the stalk, 3-5 styles emerge from the cupule and become red- then fall (Sharp, 1958; Corti, 1959). Each year, even when a good acorn crop oc- dish and sticky when receptive (Corti, curs, a large amount (70% or more) of fruit 1959; Sharp and Sprague, 1967; Rushton, abscisses (Williamson, 1966; Feret et al, 1977). Stigma receptivity for a single flow- er may last up to 6 d and 10-14 d for the 1982). pistillate inflorescence as a whole (Pjatni- The of a period of stigma re- occurrence ski, 1947; in Rushton, 1977). Stigma re- than the period of pollen ceptivity longer ceptivity for a given tree was found to be production for an individual tree may diver- roughly 15 days in Q ilex L (Lumaret et al, sify the number of potential partners for a 1991).In annual acorns, eg in the white given tree (Lumaret et al, 1991). oaks section of the genus, meiosis and fer- tilization of ovules occur 1 or 2 months af- ter pollen deposition. In biennial acorns, eg Life cycle in most of the American red oak section, the delay is about 13-15 months (Helmq- Life span and vegetative multiplication vist, 1953; Arena, 1958; Sharp, 1958; Cor- ti, 1959; Stairs, 1964; Brown and Mogen- Several species which possess vegetative sen, 1972). In several species, such as Q multiplication produce rejuvenated stems coccifera L and Q suber L, annual and bi- from root crown, trunk or rhizomes, so that ennial, or even intermediate acorns, occur it becomes impossible to ascertain the age on distinct individual trees (Corti, 1955; Bi- of a given individual. It is, nevertheless, anco and Schirone, 1985). One embryo likely that such oaks are long-lived species sac is usually initiated per spore and this (Stebbins, 1950; Muller, 1951).For exam- develops in the nucellus. Rare cases of ple, Q ilicifolia Wangenh and Q hinckleyi polyembryony, due to the development of Muller have short-lived stems (20-30 yr more than 1 embryo sac per nucellus, or to and 7-9 yr respectively) but they mainly re- the occurrence of 2 nucelli per ovule, have produce via sprouts (Muller, 1951; Wolgast been reported (Helmqvist, 1953; Corti, and Zeide, 1983). This capacity for stump 1959; Stairs, 1964). At fertilization, the pol- sprouting may be present in juveniles and, len tube enters the ovule through the although decreasing with the age of the micropyle (Helmqvist, 1953) after which 1 trunk, may enable oaks to maintain their of the 6 ovules in the ovary develops into a populations even in the absence of acorn seed. This ovular dominance occurs during production (Muller, 1951; Jones, 1959; early embryo growth (Stairs, 1964). Mo- Neilson and Wullstein, 1980; Andersson, gensen (1975) reported that 4 types of 1991. ) abortive ovules occur in Q gambelii Nutt, with an average of 2.7 ovules per ovary that do not develop into seed due to lack of Age and reproduction fertilization. In other cases, ovule abortion was due to zygote or embryo failure, or the The age of first acorn production varies absence of an embryo sac or the occur- with the species, but also with latitude, life rence of an empty one. For these reasons, span, tree density (a low density favors Mogensen (1975) proposed that the first earlier reproductive maturity) and site
stand to be greater than stand-to- (Sharp, 1958; Jones, 1959; Shaw, 1974). same The age of first reproduction also occurs stand or site-to-site variation. Many other earlier for trees in coppiced sites than similar examples have been reported (eg those from seed origin, and range from 3 Jones, 1959; Feret et al, 1982; Hunter and growing seasons old for the short-lived Van Doren, 1982; Forester, 1990; Hails sprouts of Q ilicifolia (Wolgast and Stout, and Crawley, 1991). 1977b) to 30-45 years for the long-lived For interannual Forester variation, species Q petraea (Matt) Liebl (Jones, (1990) and Hails and Crawley (1991) have 1959). Acorn yield is often correlated with observed that fruit set in Q roburL is main- tree size, although, fecundity decreases ly a characteristic of individual trees. Simi- with increasing diameter (Sharp, 1958; larly, Sharp (1958) has reported that, in Iketake et al, 1988). white oaks, each tree is fairly consistent in acorn production, at least in years of good acorn crops. In addition, for Q ilicifolia indi- Sex allocation viduals transplanted to a common site, in- dividuals of different origins were not found As oaks are monoecious, individual trees to have the same productivity (Wolgast, may show biased reproductive effort favor- 1978a). In Q pedunculiflora (Enescu and ing one or the other of the sexes. Variabil- Enescu, 1966) and Q alba (Farmer, 1981), ity in flowering abundance among trees substantial clonal control over seed yield within the same year has been reported has been reported. However, in several for Q alba L (Sharp and Chisman, 1961; species of the red oak section, acorn pro- Feret et al, 1982), Q acuta Thumb (Iketake duction can fluctuate widely for a single et al, 1988), Q pedunculiflora C Koch tree over a number of years (Sharp, 1958; (Enescu and Enescu, 1966), Q ilex (Luma- Grisez, 1975). ret et al, 1991) and Q ilicifolia (Aizen and Kenigsten, 1990). Between-year variation in flower abundance for a given tree, eg Mean single sites at production acorn variation in catkin density in Q cerris L and Q ilex, has also been reported (Hails and For single sites as a whole, a consistent Crawley, 1991; Lumaret et al, 1991).In the abundance of flowers from year to year is latter case, variation in male and female usually observed, in marked contrast to the investment concerned 15-20% of the indi- marked fluctuations in acorn production viduals. known to occur (Sharp and Sprague, 1967; Grisez, 1975; Hails and Crawley, 1991). The occurrence of mast years in acorn pro- Acorn production by individual trees duction seems to depend upon many fac- tors and is a problem that remains distinct Variation in acorn production among indi- from the interannual variation in seed pro- vidual trees has been well documented duction that occurs for individual trees. and appears to be a general rule in oak Thus, in red-oak populations, acorn crops species. In each year of a 14-year study can be consistent from one year to the on Quercus alba, massive variation in next, because of variation between individ- acorn yield was observed among the trees (Sharp and Sprague, 1967). In Q ilicifolia, uals each year and variation within individ- Wolgast (1978b) found, for uals between years (Sharp, 1958; Grisez, a given year, interindividual variation in the production of 1975). Because each year’s flowers are initiated independently of the environmen- immature acorns by trees growing in the
tal fluctuations parasite attacks and the vigor of young occurring during flowering the next spring (Bonnet-Masimbert, 1978; seedlings (McComb, 1934; Jarvis, 1963; Crawley, 1985), there is some unpredicta- Fry and Vaughn, 1977; Aizen and Patter- bility in fruit set. It will depend upon the 1990; Forester, 1990; Scarlett and son, success of pollination and compatibility of Smith, 1991). male and female gametes (Farmer, 1981; Stephenson, 1981; Sutherland, 1986), on the amount of resources and water availa- Breeding system ble at the time of flowering and fruiting (Corti, 1959; Sharp and Chisman, 1961; Incompatibility within Wolgast and Stout, 1977a), and will be and between species susceptible to many environmental condi- tions, such as soil fertility (Wolgast and From both direct experimental tests of self- Stout, 1977b), attack by parasites and pollination and crosses between half-sibs weather cues (Wood, 1938; Bonnet- (Lumaret et al, 1991; Kremer and Dau- Masimbert, 1973; Neilson and Wullstein, brée, 1993) and indirect estimates of out- 1980; Feret et al, 1982; Crawley, 1983). crossing rates from electrophoretic data Two strategies have thus been de- (Yacine and Lumaret, 1988; Aas, 1991; scribed for oaks. In the long-lived species Schwartzmann, 1991; Bacilieri et al, 1993; Q robur, Crawley (1985) has found that Kremer and Daubrée, 1993), it has been trees initially allocate resources to vegeta- shown that oak species are highly self- tive development, and once survival has incompatible. Hagman (1975) has stated been ensured, commence acorn develop- that, in oaks, this incompatibility is due to a ment. In the short-lived Q ilicifolia, Wolgast gametophytic control of the pollen-tube and Zeide (1983) have shown that, at the growth in the style. Interspecific crosses juvenile stage, environmental stress which are not rare within the same systematic is not too severe can increase seed pro- section and several cases of hybridization duction, whereas good conditions tend to between sections have been reported augment vegetative growth. In Q ilex and (Cornuz, 1955-1956; Van Valen, 1976). Q pubescens, acorns have been found to Dengler (1941; in Rushton, 1977) and be lighter in years of low production (Bran Rushton (1977) have shown that controlled et al, 1990). A further explanation for be- crosses between Q robur and Q petraea tween-year variation in acorn production is may be successful but with variation ac- that the trees have an "interval clock" cording to the year. (Sharp, 1958; Sharp and Sprague, 1967; Feret et al, 1982; Forester, 1990). The oc- Phenology currence of unpredictable mast-fruiting years may also control populations of seed Oak trees flower during the spring in tem- predators (Forester, 1990; Smith et al, perate regions and during the dry season 1990). Several examples of variation in the in paleotropical areas (Sharp, 1958; Shaw, population dynamics of acorn parasites are 1974; Kaul et al, 1986). It has been shown known in relationship to the abundance of in Spain that up to 85% of Q ilex trees fruit production (eg Smith KG, 1986a,b; Smith KG and Scarlett, 1987; Hails and have a second flowering period during late Crawley, 1991).Relationships have also spring or autumn (Vasquez et al, 1990). Only a few studies of individual tree phe- been demonstrated between acorn size and their dispersal ability, their tolerance to nology have been completed. They have
thors consider this parent-offspring disper- 1) that, among the trees of a given shown: sal as consisting of 2 distinct phases, ie location, perfect synchronization from bud gametic and zygotic dispersal. In plant opening to the flowering stage does not 2) that interannual variation in species which show significant amounts of occur; and vegetative growth, it is necessary to con- time may involve up to 30% of flowering sider this growth as a component of disper- the individuals (Sharp and Chisman, 1961; sal. Combining these several components Rushton, 1977; Fraval, 1986; Du Merle, Gliddon et al (1987) have proposed the fol- 1988; Lumaret et al, 1991). lowing formula: The of natural ulti- success crosses mately depends upon synchronization in flowering phenology between trees and the pattern of resource allocation to repro- ductive functions. In addition, there are no stable reproductive groups of individuals where t is the proportion of pollen and/or from one year to the next which could lead &2amgisp; ovules outcrossed, is the variance in &2amgisv; to homogamy. Such characteristics lead to from flower to flower, is pollen dispersal a diversification of the effective pollen the variance in dispersal of flowers from s a2 nd σ cloud received by each tree for a given the plant base is the seed dispersal year, and for a single tree in different variance from the flower to the site of seed years (Copes and Sniezko, 1991; Lumaret germination. Each of these dispersal com- et al, 1991). ponents is reviewed below. Pollen dispersal GENE FLOW Little information exists concerning oak- Levin and Kerster (1974) have defined ’po- pollen dispersal. The velocity of pollen- tential gene flow’ as the deposition of pol- grain movement is negatively correlated len and seeds from a source according to with grain diameter (McCubbin, 1944; the distance. In contrast, ’actual gene flow’ Levin and Kerster, 1974). Oak species refers to the incidence of fertilization and have relatively small pollen grains (Olsson, establishment of reproductive individuals 1975; Rushton, 1976; Solomon, 1983a,b). as a function of the distance from the Niklas (1985) has shown that a higher re- source. The potential gene flow is a meas- lease point allows more horizontal move- ure of physical dispersal, whereas to ment. The pollen dispersal parameters measure actual gene flow, appropriate ge- calculated for several species in tableI netic markers, eg isozymes and restriction show that the oak species (Q robur) has a fragment length polymorphism relatively high pollen-dispersal potential. are re- quired. The local-mate-competition model devel- oped by Lloyd and Bawa (1984) and Burd and Allen (1988) predicts that taller individ- The physical dispersal uals reduce local-mate competition and (potential gene flow) have less saturating fitness curves due to a wider dispersal of their pollen and a high- The variance in parent-offspring dispersal male investment. All these models er distribution (σ has been separated into ) 2 predict a large dispersal distance for the its different components by Crawford main oak species (Quercus petraea, (1984) and Gliddon et al (1987). These au- Q alba, Q rubra, etc) and a relatively low
1942; Harper et al, 1970). However, the rapid post-glacial migration of oak species raised questions concerning how has acorns are actually dispersed, since it has frequently been observed that distances of up to 300 m per year may occur (Skellam, 1951; Gleason and Cronquist, 1964; Webb, 1966; Johnson and Webb, 1989). The minimum seed-dispersal distances nec- essary for such range extension are equal to 7 km/generation (Webb, 1986). Mam- mals and birds which eat and thereby dis- perse acorns vary in their caching behavior: thus transport distance is highly variable. In North America, at least 90 species of mammals are involved in acorn predation and dispersal (Van Dersal, 1940). These mammals are comprised of 2 groups, each of which has contrasting roles in acorn utili- pollen dispersal for the small species (Q in- zation and dispersal. First are the small kleyi). mammals (eg mice, voles, squirrels and Several factors may act to reduce pollen gophers), which trap food locally, and the dispersal, eg a high vegetation density, larger non-caching animals (eg deer, hare, precipitation and leaf cover (Tauber, wild boar and bear). Mice are known to 1977). Except for the evergreen oaks, flow- move acorns only over tens of metres from ering begins prior to leaf expansion. Dis- the source trees (Orsini, 1979; Sork, 1984; persal over short distances depends upon Jensen and Nielsen, 1986; Miayaki and pollen production which is very variable Kikuzawa, 1988). Rodents appear to be and, in contrast, is constant for long dis- the most important seed predators (Mellan- tance (Tauber, 1977). All this information by, 1967; Vincent, 1977; Vuillemin, 1978; predicts a variable and high pollen- Orsini, 1979; Jensen, 1982; Kikuzawa, dispersal potential. 1988) and can reduce the effect of disper- (Jensen and Nielsen, 1986). Seed- sal dispersal distances for squirrels may be Seed dispersal several times larger, reaching 150 m for seeds of Juglans nigra dispersed by Sciur- Seed dispersal is easier to observe than us niger (Stapanian and Smith, 1978), but pollen dispersal and has thus been the is often less than 40 m. The habit of em- subject of much research by scientists in bryo excision in white oaks limits seed dis- many different disciplines (eg plant geneti- persal compared to the red oak (Wood, cists, plant biologists, animal behaviorists). 1938; Fox, 1982). The possession of acorns, ie heavy nuts The second category of animals moves dispersed by gravity, has led to the sug- greater distances but destroys the gestion that oaks are K-selected species acorns eat. Birds that feed on acorns with low mobility (Harper et al, 1970). In they ones fall into 3 groups: 1) those which do not the absence of biotic dispersal vectors, cache acorns and destroy them (turkeys, large seeds, such as acorns, move shorter pheasants, pigeons); 2) those distances than smaller ones (Salisbury, ducks,
which disperse and cache acorns above lowing long-distance dispersal by jays; 2) population settlement following short- the ground (woodpeckers, parids, nut- distance dispersal by small mammals and hatches); and 3) birds which routinely cache acorns in the soil. The first 2 groups jays. offer virtually no opportunity for effective dispersal, although a very small number of Vegetative dispersal seeds may be dispersed by these birds (Webb, 1986). The third group appears to in the genus Quercus Vegetative dispersal be exclusively made up of the American in two ways (Muller, 1951).The can occur and European jays. Recent research on first is stump sprouting. This phenomenon these birds (Bossema, 1979; Darley-Hill is very common among oak species (eg, and Johnson, 1981; Johnson and Adkis- Quercus rubra, Q virginiana and Q ilex). son, 1985, 1986; Johnson and Webb, The second is rhizomatous sprouting, dif- 1989) provide new insight into long- ferent types of which have been described distance dispersal of oaks and may help depending upon: 1) rhizome length: from explain the patterns of vegetation-climate 4-20 cm for short rhizomes (Quercus equilibria observed to occur after the last hinckleyi) and from 0.3 m to > 1 m for long glaciation. Darley-Hill and Johnson (1981) rhizomes (Q havardii); and 2) the origin of found for the blue jay that the mean dis- the rhizomes, which may either be juvenile tance between maternal trees and their rhizomes (terminating in a tree-habit, 1-6 seed deposition sites was 1.1 km with a m in Q virginiana) or rhizomes from mature range of 100 m to 1.9 km and which could (Q toza or Q ilex). trees reach 5 km (Johnson and Paterson: in Even with short rhizome, individual a an Darley-Hill and Johnson, 1981).Nuts were large areas (3-15 m in diame- can cover dispersed individually within a few meters ter) due to prolific sprout production. of each other and were always covered In contrast to pollen and acorn disper- with debris or soil. Covering improved ger- sal, vegetative propagation is not an impor- mination, rooting and early growth by pro- component of gene flow. It can, how- tant tecting the acorns and the radicle from participate in the maintenance of ever, desiccation and solar insulation, and scat- genetic variability within a population (Lu- ter hoarding decreased the concentration maret et al, 1991). of seeds under the parental trees and thus reduced the probability that the seeds would be eaten by other predators (Griffin, Theoretical approach (actual gene flow) 1970; Barnett, 1977; Bossema, 1979; Fo- rester, 1990). The occurrence of numer- ous oak seedlings in jay hoarding sites For most species, the actual movement of and the tendency for jays to hide acorns in genes has been observed to occur over open environments improves the chance distances much smaller than those deter- of survival and indicates that jays facilitate mined according to the mobility of these the colonization of open area by oaks. genes; second, a strong natural selection Bossema (1979) concluded that for sever- can overcome the homogenizing effects of al reasons, jays and oaks can be consid- gene flow and can produce local differenti- ered as co-adapted features of symbiotic ation (McNeilly and Antonovics, 1968). relationship. Several indirect approaches are availa- The oak forest settlement could occur in ble to assess actual gene flow: 1) the cor- 2 phases: 1) the arrival of colonizers fol- relation between variables at different spa-
gotes for Q macrocarpa and Q gambelii tial locations (Moran’s index) which meas- the genetic structuration within a pop- (Schnabel and Hamrick, 1990) Q rubra ures ulation and is independent of any assump- (Sork et al, in press) and Q agrifolia, Q lob- tion regarding population structure; 2) ata and Q douglasii (Millar et al, in press). Wright’s fixation index, F and its deriva- This observed deficit of heterozygotes is tives. F statistic quantifies the deviation of could not be explained by the selfing rate the observed genotypic structure from har- which is very low for all the studied spe- dy-Weinberg proportions in terms of the cies. This result has been explained by: 1) heterozygote deficiency within a population structuration within a stand (Sork et al, for the F and between populations for the 1993) which induces Wahlund’s effect; and is F and gives an estimation of genetic 2) assortative mating (Rice, 1984). st structuration. A deviation of the F from is As indicated in table III, gene flow be- this expected value can be caused by the tween populations or between different combined effects of random drift, selection, species of oak is greater than that ob- mating system, founder effects, assortative served between populations of many other mating and the Wahlund effect. N which m plant species (Govindaraju, 1988) and lim- is the mean number of migrants ex- its the possibility of differentiation because changed among populations is calculated the number of migrants (N is greater ) m using the following formula (Slatkin, 1987): than one (Levin and Kerster, 1974). For mst st st N(1/F (G = F =-1)/4, ). the nuclear genome, the observed differen- As indicated in table II, Wright’s fixation tiation among populations is weak (Yacine index calculated by using enzyme mark- and Lumaret, 1989; Schnabel and Ham- ers, indicates a situation close to random rick, 1990; Kremer et al, 1991; Müller- mating for Quercus ilex (Yacine and Luma- Starck and Ziehe, 1991; Schwarzmann, ret, 1989) and Quercus rubra (Schwarz- 1991; Millar et al, in press; Sork et al, mann, 1991) or a slight deficit of heterozy- 1993). The strong structuration obtained
The conclusion obtained from estimat- by the chloroplast DNA (Whittemore and ing the potential gene flow, ie that the gene Schaal, 1991) and the low structuration flow is very high within and even between observed by isozymes supports the fact oak species, is thus further confirmed by that seeds are less mobile than pollen. assessment of the actual gene flow. Chloroplast DNA variation in oaks does not reflect the species boundaries, but is concordant with the geographical location DISCUSSION of the population. These results suggest that genes are exchanged between spe- history traits of oak species (mat- The life cies, even between pairs of species that ing system, phenology, wind pollination, are distantly related and show limited abili- jay-oak co-evolution, incompatibility, sex ty to hybridize. The genotypes distributed allocation, acorn production and life span) in American (Whittemore and Schaal, lead to significant gene flows. This phe- 1991) and European (Kremer et al, 1991) nomenon is confirmed by the molecular oaks are thus not part of a completely iso- markers which give the highest values ob- lated gene pool, but are actively exchang- tained in the plant world. ing genes.
Species occupying disturbed or tran- The concept of a biological species ad- sient habitats usually have a greater dis- vocated by Mayr (1942, 1963) as a group of organisms that are actually or potentially persability than those in more advanced or interbreeding is not applicable to the genus stable habitats (Levin and Kerster, 1974). Quercus because it relies on a total isola- This generality appears to hold for different tion between species. Using morphologi- oak species. For example, if we compare cal, ecological physiological characters, Quercus robur and Q petraea, it can be or several authors (Burger, 1975; Hardin, seen that in the former, physiological 1975; Van Valen, 1976) have discussed characters such as a high light require- this problem. A model more appropriate to (Jones, 1959; Horn, 1975; Wigston, ment oaks is that which considers species as 1975; Duhamel, 1984) high pollen disper- adaptative peaks, in which interspecific sal due to smallpollen diameter, and wide gene flow is balanced by selection for one dispersal due to their being the acorn or several groups of co-adapted and linked European jay’s preferred food (Bossema, alleles (Whittemore and Schaal, 1991). 1979), convey a high colonizing ability. This theory could explain how sympatric Q petraea, however, is the species which species are able to remain distinct despite is more commonly found in climax commu- considerable gene exchange. nities due to its shade tolerance and its ability to replace Q robur during succes- The pattern of gene flow, the assess- sional forest development (Rameau, ment of selection pressure and the demog- 1987). of natural populations could be used raphy to determine the limits and the amplitude During its lifetime, a population passes of seed-collection zones and genetic re- through different stages: colonization, es- source reserves. Slatkin (1978) has devel- tablishment, succession and extinction. oped a model which Govindaraju (1990) Although one local population may thus has applied to 2 species of pine. Such a be in disequilibrium, the collection of local model could also be used for the different populations (ie a metapopulation) may be oak species. at equilibrium (Levins, 1971; Olivieri et al, 1990). During these phases, the inter- Falk (1990) suggests that the loss of dispersability (ie gene flow) could induce and intrapopulation gene-flow intensity the decline of a species and may explain and pattern varies (Thiébaut et al, 1990). the situation of several endangered oak First, during the colonization stage, the species (Q inckleyi, Q tardifolia). On the trees are scattered and the pollen (Tau- contrary, maintaining gene flow mainly im- ber, 1977) and acorns travel over large proves the chance of survival for species distances (Bossema, 1979; Darley-Hill facing habitat fragmentation (deforestation, and Johnson, 1981).The slight differentia- urbanization) and global change. The ac- tion observed in the northern populations tivity of jays in transporting and hoarding of Q rubra (Sork et al, 1993) confirms this acorns provides one hopeful sign that the because since the last glaciation, the main oak species may be able to shift loca- number of generations has been low and tion relatively quickly. structuration has not yet had time to de- velop. Second, during the later stages, pollen and seed dispersal are low and dif- ACKNOWLEDGMENT ferentiation is more marked. The southern populations of red oak, where the number of generations is higher, show such a pat- We thank Dr J Thomson for useful comments on tern. the manuscript.
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