Reproduction and Gene Flow in the Genus Quercus L

Home , Quercus ilicifolia, Quercus rubra

Review article

Reproduction and gene flow in the genus Quercus L

A Ducousso H Michaud R Lumaret

1 INRA, BP 45, 33611 Gazinet-Cestas; 2 CEFE/CNRS, BP 5051, 34033 Montpellier Cedex, France

Summary — In this paper we review the characteristics of the floral biology, life cycle and breeding system in the genus Quercus. The species of this genus are self-incompatible and have very long life spans. The focus of our review is on the effects of gene flow on the structuration of genetic variation 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 (Fis, Nm). These approaches have shown that nuclear (isozyme 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 (Fis, Nm) 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 lorsqu’elle est estimée à partir des marqueurs cytoplasmiques que lorsqu’elle l’est à partir des marqueurs 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 amount of organization in the genetic vari- develop scales or the first leaves, in the lower part ation they contain (Wright, 1951). Such or- of the branches in the same ganization is significantly influenced by produced Staminate inflorescences are initiat- joint action of mutation, migration, selec- year. 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 and to introduce er, 1974), large enough growth is achieved 1-2 weeks after bud variability into widely separated popula- opening, and pollination is completed in 2- tions and Hamrick, This (Loveless 1984). 4 days (Sharp and Chisman, 1961; Stairs, is in particularly important outbreeding, 1964; Vogt, 1969; Lumaret et al, 1991). In perennial and iteroparous species, such deciduous oaks, leaf expansion ceases as forest trees. 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 man, 1961). on gene flow at different stages of the life are reviewed in various of cycle species Pistillate flowers the genus Quercus.

Female flowers appear in the axils of leaves in the same REPRODUCTIVE SYSTEM produced year. They are produced on a short stalk and become visible a few days after the emergence of the male catkins and Floral biology (Sharp Sprague, 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- rescences (Scaramuzzi, 1958; Stairs, sized that their initiation may occur in late 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 are sum- winter or early spring (Bonnet-Masimbert, marized below. 1978; Merkle et al, 1980). Each flower is included in a cupule, which is regarded as fertilized ovule either suppresses the homologous to a third-order inflorescence growth of the other fertilized ovules or pre- branch (Brett, 1964; McDonald, 1979). vents their fertilization. After fertilization, During elongation of the stalk, 3-5 styles the acorns mature within about 3 months, emerge from the cupule and become red- then fall (Sharp, 1958; Corti, 1959). Each dish and sticky when receptive (Corti, year, even when a good acorn crop oc- 1959; Sharp and Sprague, 1967; Rushton, curs, a large amount (70% or more) of fruit 1977). Stigma receptivity for a single flow- abscisses (Williamson, 1966; Feret et al, er may last up to 6 d and 10-14 d for the 1982). inflorescence as a whole pistillate (Pjatni- The occurrence of a period of stigma re- ski, 1947; in Rushton, 1977). Stigma receptivity longer than the period of pollen for a tree was found to be ceptivity given production for an individual tree may diver- 15 in Q ilex L et roughly days (Lumaret 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 fertilization of ovules occur 1 or 2 months after pollen deposition. In biennial acorns, eg Life cycle in most of the American red oak section, the delay is about 13-15 months (Helmq- vist, 1953; Arena, 1958; Sharp, 1958; Cor- Life span and vegetative multiplication ti, 1959; Stairs, 1964; Brown and Mogen- Several which sen, 1972). In several species, such as Q species possess vegetative coccifera L and Q suber L, annual and bi- multiplication produce rejuvenated stems from root crown, trunk or rhizomes, so that ennial, or even intermediate acorns, occur it becomes to ascertain the on distinct individual trees (Corti, 1955; Bi- impossible age of a individual. It is, nevertheless, anco and Schirone, 1985). One embryo given that such oaks are sac is usually initiated per spore and this likely long-lived species 1950; Muller, exam- develops in the nucellus. Rare cases of (Stebbins, 1951). For Q ilicifolia and Q polyembryony, due to the development of ple, Wangenh hinckleyi Muller have short-lived stems yr more than 1 embryo sac per nucellus, or to (20-30 and 7-9 yr but re- the occurrence of 2 nucelli per ovule, have respectively) they mainly via been reported (Helmqvist, 1953; Corti, produce sprouts (Muller, 1951; Wolgast and This for 1959; Stairs, 1964). At fertilization, the pol- Zeide, 1983). capacity stump be in and, len tube enters the ovule through the sprouting may present juveniles with the of the micropyle (Helmqvist, 1953) after which 1 although decreasing age 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 early embryo growth (Stairs, 1964). Mo- production (Muller, 1951; Jones, 1959; 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 (Sharp, 1958; Jones, 1959; Shaw, 1974). same stand to be greater than stand-to- 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 variation, Forester 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 robur L is main- tree decreases size, although, fecundity 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 Sex allocation acorn crops. In addition, for Q ilicifolia individuals transplanted to a common site, in- As oaks are monoecious, individual trees dividuals of different origins were not found may show biased reproductive effort favor- to have the same productivity (Wolgast, ing one or the other of the sexes. Variabil- 1978a). In Q pedunculiflora (Enescu and ity in flowering abundance among trees Enescu, 1966) and Q alba (Farmer, 1981), within the same year has been reported substantial clonal control over seed yield for Q alba L (Sharp and Chisman, 1961; has been reported. However, in several Feret et al, 1982), Q acuta Thumb (Iketake species of the red oak section, acorn pro- et al, 1988), Q pedunculiflora C Koch duction can fluctuate widely for a single (Enescu and Enescu, 1966), Q ilex (Luma- tree over a number of years (Sharp, 1958; ret et al, 1991) and Q ilicifolia (Aizen and Grisez, 1975). Kenigsten, 1990). Between-year variation in flower abundance for a tree, eg given Mean acorn production at single sites variation in catkin density in Q cerris L and Q ilex, has also been and reported (Hails 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 variation in male and female case, 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). Acorn production by individual trees The occurrence of mast years in acorn production seems to depend upon many fac- Variation in acorn production among indi- tors and is a problem that remains distinct vidual trees has been well documented from the interannual variation in seed pro- and appears to be a general rule in oak duction that occurs for individual trees. species. In each year of a 14-year study Thus, in red-oak populations, acorn crops on Quercus alba, massive variation in can be consistent from one year to the acorn yield was observed among the trees next, because of variation between individ- (Sharp and Sprague, 1967). In Q ilicifolia, uals each year and variation within individ- Wolgast (1978b) found, for a given year, uals between years (Sharp, 1958; Grisez, interindividual variation in the production of 1975). Because each year’s flowers are immature acorns by trees growing in the initiated independently of the environmental fluctuations occurring during flowering parasite attacks and the vigor of young 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 son, 1990; Forester, 1990; Scarlett and 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 1959; and Chisman, 1961; (Corti, Sharp within Wolgast and Stout, 1977a), and will be Incompatibility and between species susceptible to many environmental conditions, such as soil fertility and (Wolgast From both direct tests of self- Stout, 1977b), attack by parasites and experimental pollination and crosses between half-sibs weather cues (Wood, 1938; Bonnet- et Kremer and Dau- Masimbert, 1973; Neilson and Wullstein, (Lumaret al, 1991; brée, and indirect estimates of out- 1980; Feret et al, 1982; Crawley, 1983). 1993) 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 allocate resources to initially 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 have shown that, at the (1983) 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 whereas conditions tend to duction, good between sections have been reported In Q ilex and augment vegetative growth. (Cornuz, 1955-1956; Van Valen, 1976). Q acorns have been found to pubescens, (1941; in Rushton, 1977) and be in of low Dengler lighter years 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 occurrence of unpredictable mast-fruiting Phenology years may also control populations of seed predators (Forester, 1990; Smith et al, Oak trees flower during the spring in tem- 1990). Several examples of variation in the perate regions and during the dry season population dynamics of acorn parasites are in paleotropical areas (Sharp, 1958; Shaw, known in relationship to the abundance of 1974; Kaul et al, 1986). It has been shown fruit production (eg Smith KG, 1986a,b; in Spain that up to 85% of Q ilex trees 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). been demonstrated between acorn size Only a few studies of individual tree phe- and their dispersal ability, their tolerance to nology have been completed. They have shown: 1) that, among the trees of a given thors consider this parent-offspring disper- location, perfect synchronization from bud sal as consisting of 2 distinct phases, ie opening to the flowering stage does not gametic and zygotic dispersal. In plant occur; and 2) that interannual variation in species which show significant amounts of flowering time may involve up to 30% of vegetative growth, it is necessary to con- the individuals (Sharp and Chisman, 1961; sider this growth as a component of disper- Rushton, 1977; Fraval, 1986; Du Merle, sal. Combining these several components 1988; Lumaret et al, 1991). Gliddon et al (1987) have proposed the fol- formula: The success of natural crosses ulti- lowing mately depends upon synchronization in flowering phenology between trees and the pattern of resource allocation to reproductive 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 ovules outcrossed, σ2p is the variance in to homogamy. Such characteristics lead to pollen dispersal from flower to flower, σ2v is a diversification of the effective pollen the variance in dispersal of flowers from cloud received by each tree for a given the plant base and2s σ 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 resource. 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 are re- relatively high pollen-dispersal potential. 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 er male investment. All these models distribution (σ2) has been separated into 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 has raised questions concerning how 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 necessary for such range extension are equal to 7 km/generation (Webb, 1986). Mam- mals and birds which eat and thereby disperse 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- for the small in- pollen dispersal species (Q 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 dispersal (Jensen and Nielsen, 1986). Seed- Seed dispersal dispersal distances for squirrels may be several times larger, reaching 150 m for Seed dispersal is easier to observe than seeds of Juglans nigra dispersed by Sciur- pollen dispersal and has thus been the us niger (Stapanian and Smith, 1978), but subject of much research by scientists in is often less than 40 m. The habit of em- excision in white oaks limits seed dis- many different disciplines (eg plant geneti- bryo cists, plant biologists, animal behaviorists). persal compared to the red oak (Wood, The possession of acorns, ie heavy nuts 1938; Fox, 1982). dispersed by gravity, has led to the sug- The second category of animals moves gestion that oaks are K-selected species acorns greater distances but destroys the with low mobility (Harper et al, 1970). In ones they eat. Birds that feed on acorns the absence of biotic dispersal vectors, fall into 3 groups: 1) those which do not large seeds, such as acorns, move shorter cache acorns and destroy them (turkeys, distances than smaller ones (Salisbury, ducks, pheasants, pigeons); 2) those which disperse and cache acorns above lowing long-distance dispersal by jays; 2) the ground (woodpeckers, parids, nut- population settlement following short- hatches); and 3) birds which routinely distance dispersal by small mammals and cache acorns in the soil. The first 2 groups jays. offer virtually no opportunity for effective a small number of dispersal, although very Vegetative dispersal seeds may be dispersed by these birds (Webb, 1986). The third group appears to Vegetative dispersal in the genus Quercus be made up of the American exclusively can occur in two ways (Muller, 1951). The and Recent research on European jays. 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 of oaks and dispersal may help depending upon: 1) rhizome length: from the of explain patterns vegetation-climate 4-20 cm for short rhizomes (Quercus observed to occur after the last equilibria 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 that the mean dis- jay the rhizomes, which may either be juvenile tance between maternal trees and their rhizomes (terminating in a tree-habit, 1-6 seed sites was 1.1 km with a deposition m in Q virginiana) or rhizomes from mature of 100 m to 1.9 km and which could range trees (Q toza or Q ilex). reach 5 km (Johnson and Paterson: in Even with a short rhizome, an individual Darley-Hill and Johnson, 1981). Nuts were can cover large areas (3-15 m in diame- dispersed individually within a few meters ter) due to prolific sprout production. of each other and were always covered with debris or soil. Covering improved ger- In contrast to pollen and acorn disper- mination, rooting and early growth by pro- sal, vegetative propagation is not an important of It tecting the acorns and the radicle from component gene flow. can, how- desiccation and solar insulation, and scat- ever, participate in the maintenance of ter hoarding decreased the concentration genetic variability within a population (Lu- of seeds under the parental trees and thus maret et al, 1991). reduced the probability that the seeds would be eaten by other predators (Griffin, 1970; Barnett, 1977; Bossema, 1979; Fo- Theoretical approach (actual gene flow) 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 spatial locations (Moran’s index) which meas- gotes for Q macrocarpa and Q gambelii ures the genetic structuration within a pop- (Schnabel and Hamrick, 1990) Q rubra 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, Fis and its deriva- This observed deficit of heterozygotes 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 Fis and between populations for the 1993) which induces Wahlund’s effect; and Fst and gives an estimation of genetic 2) assortative mating (Rice, 1984). structuration. A deviation of the from Fis As indicated in table III, gene flow be- this value can be caused the expected by tween populations or between different combined effects of random drift, selection, species of oak is greater than that ob- founder assortative mating system, effects, served between populations of many other mating and the Wahlund effect. Nm which 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 (Nm) is greater the formula using following (Slatkin, 1987): than one (Levin and Kerster, 1974). For Nm = (1/Fst-1)/4, (Gst =st). F 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 by the chloroplast DNA (Whittemore and The conclusion obtained from estimat- Schaal, 1991) and the low structuration ing the potential gene flow, ie that the gene observed by isozymes supports the fact flow is very high within and even between that seeds are less mobile than pollen. oak species, is thus further confirmed by Chloroplast DNA variation in oaks does assessment of the actual gene flow. not reflect the species boundaries, but is concordant with the geographical location of the population. These results suggest DISCUSSION that genes are exchanged between species, even between pairs of species that The life history traits of oak species (mat- are distantly related and show limited abili- ing system, phenology, wind pollination, ty to hybridize. The genotypes distributed jay-oak co-evolution, incompatibility, sex in American (Whittemore and Schaal, allocation, acorn production and life span) 1991) and European (Kremer et al, 1991) lead to significant gene flows. This phe- oaks are thus not part of a completely iso- nomenon is confirmed by the molecular lated gene pool, but are actively exchang- markers which give the highest values ob- ing genes. tained in the plant world. 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 persability than those in more advanced or of organisms that are actually or potentially stable habitats (Levin and Kerster, 1974). interbreeding is not applicable to the genus This generality appears to hold for different Quercus because it relies on a total isola- oak species. For example, if we compare tion between species. Using morphologi- Quercus robur and Q petraea, it can be cal, ecological or physiological characters, seen that in the former, physiological several authors (Burger, 1975; Hardin, characters such as a high light require- 1975; Van Valen, 1976) have discussed ment (Jones, 1959; Horn, 1975; Wigston, this problem. A model more appropriate to 1975; Duhamel, 1984) high pollen disper- oaks is that which considers species as sal due to small pollen diameter, and wide adaptative peaks, in which interspecific acorn dispersal due to their being the gene flow is balanced by selection for one European jay’s preferred food (Bossema, or several groups of co-adapted and linked 1979), convey a high colonizing ability. alleles (Whittemore and Schaal, 1991). Q petraea, however, is the species which This theory could explain how sympatric is more commonly found in climax commu- species are able to remain distinct despite nities due to its shade tolerance and its considerable gene exchange. 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). raphy of natural populations could be used During its lifetime, a population passes to determine the limits and the amplitude through different stages: colonization, es- of seed-collection zones and genetic re- tablishment, succession and extinction. source reserves. Slatkin (1978) has devel- a which Although one local population may thus oped model Govindaraju (1990) be in disequilibrium, the collection of local has applied to 2 species of pine. Such a model could also be used for the different populations (ie a metapopulation) may be at equilibrium (Levins, 1971; Olivieri et al, oak species. 1990). During these phases, the inter- Falk (1990) suggests that the loss of and intrapopulation gene-flow intensity dispersability (ie gene flow) could induce and pattern varies (Thiébaut et al, 1990). the decline of a species and may explain First, during the colonization stage, the the situation of several endangered oak trees are scattered and the pollen (Tau- species (Q inckleyi, Q tardifolia). On the ber, 1977) and acorns travel over large contrary, maintaining gene flow mainly im- distances (Bossema, 1979; Darley-Hill proves the chance of survival for species and Johnson, 1981). The slight differentia- facing habitat fragmentation (deforestation, tion observed in the northern populations urbanization) and global change. The ac- of Q rubra (Sork et al, 1993) confirms this tivity of jays in transporting and hoarding because since the last glaciation, the acorns provides one hopeful sign that the number of generations has been low and main oak species may be able to shift loca- structuration has not yet had time to de- tion relatively quickly. velop. Second, during the later stages, pollen and seed dispersal are low and differentiation is more marked. The southern ACKNOWLEDGMENT 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. REFERENCES Brett DW (1964) The inflorescence of Fagus and Castanea, and the evolution of cupules of the Fagaceae. New Phytol 63, 96-118 Aas G mit Stiel- und (1991) Kreuzungsversuche Brown RC, Mogensen HL (1972) Late ovule and Traubeneichen robur L und Q pe- (Quercus early embryo development in Quercus gam- traea Forst (Matt) Liebl). Allg Jagdztg 162, belii. 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