Printer Friendly

Postdispersal selection following mixed mating in Eucalyptus regnans.

The fate of inbred progenies strongly influences the evolution of natural populations undergoing mixed mating. While the response to selection following mixed mating may be quite different to that under random mating (Allard et al. 1968; Wright and Cockerham 1985; Hedrick 1990), inbreeding depression prior to reproduction will reduce the contribution of inbreds to the final mating population. If few self-progeny survive, evolution will effectively follow that of a randomly mating population (Lande et al. 1994). Inbreeding depression has been studied extensively in many plant species (reviewed in Charlesworth and Charlesworth 1987; Husband and Schemske 1996; Ritland 1996; Williams and Savolainen 1996). However, many of these studies have been short term and conducted in greenhouses or gardens, which may underestimate the intensity of inbreeding depression due to the absence of competition (Schmitt and Ehrhardt 1990; Ritland 1996). Further, while early acting inbreeding depression appears to be well documented, there is a lack of information of later-age inbreeding depression in long-lived angiosperms, as noted by Husband and Schemske (1996) and Ritland (1996).

The study of long-lived plants is of particular interest as the rate of mutation per generation may be much higher than for small annual species, suggesting differences in the expression of inbreeding depression (Lande et al. 1994; Husband and Schemske 1996). Long-lived conifers exhibit severe inbreeding depression for seed set and for later age growth and moderate levels for survival in the field and reproductive traits (Husband and Schemske 1996; Williams and Savolainen 1996). However, conifers are wind pollinated and out-crossing rates are generally close to one (Aide 1986). In addition, conifers possess polyembryony, which enables selection against inferior embryos without reducing reproductive output (Sorenson 1982). Here we report on late-acting inbreeding depression and selection in progenies from mixed mating after competition has developed between inbred and outcross progenies of a long-lived forest-tree angiosperm, Eucalyptus regnans Muell.

Eucalyptus regnans is the tallest angiosperm species in the world, attaining heights of up to 90-100 m (Ashton 1981). It is a common dominant of the forests of southeastern Australia, generally forming pure, even-aged stands on rich, fertile soils in high rainfall areas (Ashton 1981). The species is mass flowering, producing up to 1 million small, hermaphroditic, flowers per tree during a single season (Fripp et al. 1987). Pollination occurs via a variety of nonspecific insect and other animal (Ashton 1975; Griffin 1980) vectors. Although individual flowers are protandrous (Griffin and Hand 1979), the flowering phenology provides ample opportunity for selfing via geitonomy (Griffin 1980). Prezygotic self-in-compatibility is not important with equivalent numbers of fertile self and outcross ovules present at 16 wk after controlled pollination (Sedgley et al. 1989). However, lower seed production under controlled self-pollination compared to cross-pollination (Griffin et al. 1987) indicates that self-pollinated ovules suffer inbreeding depression after this date. Moreover, in mixed pollinations, outcross ovules out compete selfs, resulting in higher outcrossing rates than predicted based on the fitness of the cross-types determined from the independent pollination treatments (Griffin et al. 1987). Overall, 18% to 77% of the mature seeds produced by E. regnans under natural pollination are selfs (Fripp et al. 1987; Griffin et al. 1987; Moran et al. 1989), although clearly the rate of actual self-fertilization is much higher.

Mature seed remains stored in woody capsules in the canopy for several years (Ashton 1975), but it is only following wildfire that successful regeneration typically occurs (Ashton 1981). Fire kills the mature canopy, prepares a receptive seed bed, removes competing vegetation, and promotes seed shed (Ashton 1981). The seeds of E. regnans are small (Boland et al. 1980). Seed dispersal is mainly by wind or gravity and is virtually limited to approximately twice the tree height (Cremer 1966). The longevity of seed in the soil is low (Ashton 1979), and seed fall at other times is either removed by ants (Ashton 1979) or is unable to grow under the unfavorable conditions beneath an unburnt mature canopy (Ashton 1981). While millions of seed per hectare are shed following fire, only 10% ([approximately] 200,000 per hectare) of these seeds germinate, and only 0.5-1.0% ([approximately] 20,000 per hectare) produce seedlings (Cunningham 1960). Deaths continue as the stand ages until the density stabilizes between 40-80 stems per hectare (0.002% of the initial seed rain) around 150 years postfire (Ashton 1976). If wildfire is absent for longer than about 300 years, the eucalypts will senesce, thin out, and be eventually replaced by climax temperate rainforest (Jackson 1968). The enormous loss of progeny with stand growth provides the opportunity for the development of intense competition (Barber 1965). This study addresses the dynamics of postdispersal selection and the fate of inbred progenies in the competitive environment of regenerating forests.


The mating design and field trial have been described in Griffin and Cotterill (1988). Thirteen mature E. regnans individuals from two populations of native forest (six from Narracan and seven from Thorpdale; Victoria, Australia) were crossed in two disconnected factorials within populations to produce 12 Thorpdale and nine Narracan families of controlled outcross seedlings (Table 1). Controlled self- and naturally open-pollinated (OP) progeny were also obtained from all parents (Table 1). A field trial was established in August 1979 with families planted as single tree plots in 36 complete randomized replications at a spacing of 2 m by 3 m among seedlings. Survival was recorded at 11 (1 yr), 21 (2 yr), 30 (3 yr), 43 (4 yr), 115 (10 yr), 152 (13 yr), and 176 (15 yr) mo after planting. Diameter at breast height was measured from 3 yr onward and used to calculate individual tree basal area.

The average proportion of planted seedlings surviving at each age (cumulative survival) was calculated for each cross-type (outcross, OP, and self), population, and parent. Differences in overall survival from planting to 15 yr and the rate of mortality among cross-types and populations were tested using chi-square tests. The significance of the interaction between population and cross-type was tested by fitting a generalized linear model with a logit link function with the procedure PROC GENMOD in SAS (SAS Institute 1993). This analysis was also used within cross-types to remove population differences and test whether the progeny from different parents differed in overall survival, and in the case of the factorials, whether the specific combination of parents affected survival. Inbreeding depression in survival was estimated as one minus the relative overall survival of selfs (i.e., 1 - overall survival of selfs/outcrosses; Lande and Schemske 1985).
TABLE 1. Mating design for the production of naturally
open-pollinated (op), controlled self- (s), and outcross (x)
progenies from 13 different Eucalyptus regnans parents (1-13)
sampled from two populations (Narracan and Thorpdale).


[Male]        1       2       3       4       5       6       OP

1             s               x               x       x       op
2                     s       x               x       x       op
3                             s                               op
4                             x       s       x       x       op
5                                             s               op
6                                                     s       op


[Male]       7      8      9     10     11     12     13     OP

7            s                    x      x      x      x     op
8                   s             x      x      x      x     op
9                          s      x      x      x      x     op
10                                s                          op
11                                       s                   op
12                                              s            op
13                                                     x     op

The average proportion of outcrosses in the OP progenies at planting (i.e., outcrossing rate, [t.sub.plant]) was estimated as

[t.sub.plant] = ([W.sub.OP] - [W.sub.Self] / ([W.sub.Out] - [W.sub.Self]), (1)

where [W.sub.out], [W.sub.OP], and [W.sub.Self] were overall survival from planting to 15 yr of the outcross, OP, and self-progenies, respectively (Charlesworth 1988), as was the outcrossing rate for each population and each parent. This method was also used to calculate the average proportion of outcrosses in the OP progenies at each age ([t.sub.n]) by using the survival from each age to 15 yr for the three cross-types, instead of the overall survival from planting to age 15. In addition, [t.sub.n] was also calculated following Ritland (1990) as

[t.sub.n] = [t.sub.plant][W.sub.Out,n] / ([t.sub.plant][W.sub.Out,n] + [S.sub.plant][W.sub.Self,n]), (2)

where [S.sub.plant] was the proportion of selfs in the OP families at planting (i.e., 1 - [t.sub.plant]), and [w.sub.out,n] and [W.sub.self,n] were the cumulative survival from planting to age n of outcross and self-progenies, respectively. Pearson correlations coefficients were used to examine the associations among overall survival of outcross, OP, and self-progenies, and inbreeding depression in overall survival. The calculation of both inbreeding depression due to open-pollination and the proportion of out-crosses in the OP families assumed that (1) selfing is the only form of inbreeding; and (2) the controlled outcrosses are genetically equivalent to the outcrossing that occurs under natural open-pollination within each population. The extent of biparental inbreeding that occurs in eucalypt populations is unknown, however, if inbreeding depression is linear with F, full-sib mating (F = 0.25) would have half the impact of selfing (F = 0.5), whereas half-sib inbreeding (one parent in common, F = 0.125) would only have one-quarter the impact, and therefore levels of biparental inbreeding would have to be substantial to bias our outcrossing estimates.

The effect of cross-type on basal area was examined with a restricted maximum-likelihood (REML) analysis at each age using PROC MIXED in SAS (SAS Institute 1992). This procedure was used to remove population differences, estimate the least square mean basal area for each cross-type, construct confidence intervals (P = 0.05), and undertake pair-wise tests between the cross-type means. The relationship between prior basal area and later-age survival was examined at each age with a second REML analysis that included a survival term in the model specifying if the plant was dead or alive at the next measurement date, as well as a term for the interaction between cross-type and later age survival. The significance of size-dependent mortality was tested by contrasting the levels of the survival term within each cross-type. Relative growth rate (Larocque and Marshall 1993) in basal area was calculated for each individual and the effect of cross-type examined as described above for basal area.

The relationship among mortality, stand development (i.e., the aging of the stand independent of mortality effects), and size of an individual were examined by calculating inbreeding depression (of both self- and OP progenies) and the components of phenotypic variation in basal area at each age using (1) the cohort of plants alive at each age; and (2) only the cohort of plants that were alive at the next measurement date. For example, inbreeding depression in basal area at three years was calculated first using all plants alive at age 3, and second using only the cohorts of plants alive at age 4. The effect of mortality could then be examined by comparing the different cohorts at the same age, and the effect of stand development by comparing the exact same cohort at different ages. The components of phenotypic variation within each cross-type were estimated by REML, and phenotypic variance was calculated by summing the variance components. To enable the comparison of variances that differed greatly in mean, coefficients of phenotypic variation were calculated by dividing the square root of phenotypic variation by the least square mean of the basal area. Variation among and within OP families were adjusted in a similar manner.


The survival of self-progenies to 15 yr. (0.18) was significantly poorer ([[[Chi].sup.2].sub.1] = 66.4; P [less than] 0.001) than that of the out-cross progenies (0.55), and inbreeding depression due to selfing was high (0.67) [ILLUSTRATION FOR FIGURE 1 OMITTED]. There appeared to be two stages of selection against self-progenies [ILLUSTRATION FOR FIGURE 2 OMITTED]. The first stage occurred between planting and one year when the rate or mortality of the selfs (0.12) was double that of the outcrosses (0.06) (P [less than] 0.001; [ILLUSTRATION FOR FIGURE 2 OMITTED]). The second stage commenced after age 4, when the rate of mortality of selfs was consistently and significantly (P [less than] 0.001) higher than for outcross progenies, and increased with age [ILLUSTRATION FOR FIGURE 2 OMITTED]. Between ages 1 and 4, there was no significant inbreeding depression in survival, despite high overall rates of mortality in all cross-types.

The response of the OP progenies was intermediate. Overall survival from planting to 15 yr was 0.40 and significantly different from that of both selfs ([[[Chi].sup.2].sub.1] = 28.5; P [less than] 0.001) and outcrosses ([[[Chi].sup.2].sub.1] = 8.3; P [less than] 0.01) [ILLUSTRATION FOR FIGURE 1 OMITTED]. Based on the relative difference in overall survival of the three cross-types, the average proportion of outcrosses in the OP progenies at planting (outcrossing rate) was estimated as 0.59 [ILLUSTRATION FOR FIGURE 3 OMITTED]. If this proportion is adjusted to account for differential survival rates over successive intervals of the self- and outcross progenies ([ILLUSTRATION FOR FIGURE 2 OMITTED]; following Ritland 1990), then the average proportion of outcrosses in the OP families at different ages would be expected to change little between planting and four years, but increase dramatically thereafter to 0.83 by 15 years [ILLUSTRATION FOR FIGURE 3 OMITTED]. This approach modeled well the temporal variation in the genetic composition of the OP progenies, determined using the relative survival from each age to 15 years of the three cross-types (following Charlesworth 1988).

Survival of the outcrossed progenies from Narracan (0.61) was significantly better ([[[Chi].sup.2].sub.1] = 7.6; P [less than] 0.01) than those from Thorpdale (0.50), but no significant population differences in the survival of self- or OP progenies were detected [ILLUSTRATION FOR FIGURE 4 OMITTED]. The level of inbreeding depression in survival differed little between populations (N - 0.70; T = 0.65), and the interaction between cross-type (self vs. outcrosses) and population was not significant (P = 0.23). Failure to detect a significant difference in inbreeding depression despite significant population differences when outcrossed is consistent with inbreeding depression having a much greater impact than population differences on survival. In contrast, the relative difference in overall survival of the three cross-types would suggest that the proportion of outcrosses in the OP families from the Narracan population (0.41) was markedly [TABULAR DATA FOR TABLE 2 OMITTED] less than that in the Thorpdale population (0.79). Estimated outcrossing rate also varied from 1.00 to 0.15 among parents (Table 2).

After population differences were removed, there were significant differences among parents in the overall survival of their selfed and OP offspring after 15 yr (P [less than] 0.001) (Table 2). However, the factorial indicated no significant additive genetic variation among the parents (P (female) = 0.12, P {male} = 0.45) and only small levels of nonadditive variation (P (female*male) [less than] 0.05; Table 2). The correlation between the average overall survival of the OP and outcross progenies from the same parent was poor (r = 0.15; df = 11, P = 0.63), as was the correlation between OP and selfs (r = 0.20; df = 11; P = 0.51) and between OP survival and inbreeding depression (r = -0.18; df = 11; P = 0.56).

From 3 yr onward, there was significant inbreeding depression due to selfing in growth, with OPs again intermediate [ILLUSTRATION FOR FIGURE 5 OMITTED]. Mortality after age 4 was size dependent in all cross-types, with the cohort of those plants that survived to the next measurement date having significantly higher prior mean basal area than those that died (Table 3). Size-dependent mortality resulted in a consistent decrease in inbreeding depression of both self- and OP progenies after age 4 [ILLUSTRATION FOR FIGURE 5 OMITTED], as demonstrated by a reduction in inbreeding depression at the same age in the cohort of plants surviving to the next measurement date compared with the cohort of all plants that were alive at that age. In contrast, inbreeding depression of exactly the same cohort of plants was enhanced with stand development after age 4 [ILLUSTRATION FOR FIGURE 5 OMITTED]. Selfs also exhibited significantly slower growth rates than outcrosses after age 4, although this was not apparent at earlier ages [ILLUSTRATION FOR FIGURE 6 OMITTED].

Phenotypic variation in basal area among the selfs was almost twice that among the outcrosses with OPs intermediate [ILLUSTRATION FOR FIGURE 7 OMITTED]. Size-dependent mortality after age 4 reduced phenotypic variation in all cross-types, but this was enhanced by stand development. The net effect of the two opposing [TABULAR DATA FOR TABLE 3 OMITTED] trends was that the phenotypic variation of the OP progenies, in particular, changed little with time. Variation within the OP families was much greater than variation among families [ILLUSTRATION FOR FIGURE 8 OMITTED]. This was accentuated with age as mortality reduced both among and within family variation, while stand development inflated the variability within families for a given cohort [ILLUSTRATION FOR FIGURE 8 OMITTED].


The ultimate fate of inbred progeny following mixed mating in E. regnans is clearly determined by intense postdispersal selection. While there is strong selection against the products of self-fertilization within the capsule (Griffin et al. 1987; Sedgley et al. 1989), this is not sufficient to remove all inbred seed prior to dispersal (Moran and Bell 1983; Fripp et al. 1987; Griffin et al. 1987; Moran et al. 1989). In this trial, we estimate 59% of the OP progenies at planting were outcrosses, which is consistent with Griffin et. al.'s (1987) allozyme-based estimate of 56% for the same populations. However, our estimate of the relative fitness of selfs and outcrosses at different ages [ILLUSTRATION FOR FIGURE 3 OMITTED], suggests that the proportion of outcrosses increased to 83% after 15 years. In-breeding depression in survival reported here for E. regnans (0.67) is extremely high compared with the average juvenile survival for outcrossing angiosperm species (0.12; predominantly short-lived; Husband and Schemske 1996), and long-term (6-24 yr) field survival of coniferous species (mean 0.14, range 0.03-0.29; Sorensen and Miles 1982; Fowler and Park 1983; Park and Fowler 1984; Williams and Savolainen 1996).

The major phase of postdispersal selection against self-progenies commenced after 4 yr [ILLUSTRATION FOR FIGURE 1 OMITTED], and was coincident with canopy closure. The dynamics of growth over this phase is consistent with the development of strong competition for light and other resources. Competition enhances inbreeding depression through the development of dominance-suppression (Waller 1985; Schmitt and Ehrhardt 1990; Wolfe 1993; Damgaard and Loeschcke 1994), similar to the increase in inbreeding depression observed with stand development in E. regnans [ILLUSTRATION FOR FIGURE 5 OMITTED]. The development of declining size-dependent growth rates after age 4 [ILLUSTRATION FOR FIGURE 6 OMITTED] is also consistent with the onset of competition (Perry 1985; Schmitt et al. 1987; Larocque and Marshall 1993), and indicates that the enhancement of inbreeding depression with stand development is not simply a consequence of exponential growth alone (Sorensen and Miles 1982; Waller 1984). Size-dependent mortality after age 4 (Table 3) suggests that the higher mortality of the selfs at later ages was a result of continual suppression by the dominant outcrosses, eventually leading to death (e.g., Harper 1977; Perry 1985).

The development of strong competition also explained the response of the OP progenies at later ages. The observed increase in variation within OP families with stand development [ILLUSTRATION FOR FIGURE 8 OMITTED] is consistent with dominance-suppression inflating differences between inbreds and outcrossed individuals (e.g., [ILLUSTRATION FOR FIGURE 5 OMITTED]) within OP families. In contrast, size-dependent mortality after age 4 (which appears to be predominantly of the inbreds) operated in the opposite direction, reducing differences among and within families and leading to a reduction in total phenotypic variation. This is similar to the observed reduction in phenotypic and within-plot (residual) variances after artificial culling of the smallest trees in field trials (Matheson and Raymond 1984; Sorensen and White 1988). Thus, the identification of the less vigorous homozygous genotypes by dominance-suppression and the subsequent culling by size-dependent mortality results in an overall reduction in the variation among OP families, but little change in total phenotypic variation with age. Selection against homozygotes has been reported by Muona et al. (1987) in a Pinus sylvestris field trial, and appeared to account for the removal of genetic differences among subpopulations of Liatris cylindracea (Schaal and Levin 1976).

We expect this study underestimates the intensity of post-dispersal selection and the size of later age inbreeding depression in native stands of E. regnans, despite a trial design that maximizes competition among progenies from different cross-types. The high density of plants at a very young age, followed by high rates of mortality in natural stands (Barber 1965), suggests that intense competition would occur at much earlier ages than reported here, and selfs are unlikely to survive to reproductive maturity. Selection against homozygous inbreds in natural forests has been demonstrated in Pinus (Plessas and Strauss 1986; Morgante et al. 1993), and would explain the higher levels of heterozygosity and near zero inbreeding coefficients in mature populations of Eucalyptus compared to the OP seedling populations (Phillips and Brown 1977; Moran and Brown 1980; Hopper and Moran 1981; Fripp 1982; Sampson et al. 1988; Moran et al. 1989). The failure of selfs from the previous generation to contribute to the next generation means evolution will effectively follow that of random mating. Considerable genetic load may accumulate as selection against the self-progeny per se removes the opportunity to purge only the deleterious alleles (Uyenoyama et al. 1993; Lande et al. 1994).

The results of this study suggest that under natural open-pollination, survival of progenies from different parents is not directly related to differences in additive genetic effects or genetic load among parents. Significant variation in the overall survival of OP progeny from different parents was observed, yet there was no significant additive variation among parents for survival (Table 2). In addition, while there was significant variation among parents in the survival of their self-offspring, the survival of OP progeny was not correlated with the survival of selfs from the same parents, nor inbreeding depression in survival. It is unlikely that the variation in OP survival is due to nonrandom outcrossing because SCA effects were only marginally significant (P = 0.04).

Outcrossing rates, rather than additive genetic differences or genetic load, may be an important determinant of parental fitness. The virtual removal of all inbred progeny by post-dispersal selection means that parents with higher outcrossing rates will contribute more progeny to the mating pool of the next generation when the absolute number of progeny each parent produces is the same. A positive association between outcrossing rate and growth has been reported in both E. globulus (Hardner et al. 1996) and E. grandis (Burgess et al. 1996) in studies where outcrossing rates were independently assessed using isozyme markers. In this study, we found a strong correlation between estimated outcrossing rate at planting and OP survival at 15 yr (r = 0.89; df - 11, P [less than] 0.001), but no correlation between estimated outcrossing rate and inbreeding depression of the parent (r = -0.15; df = 11, P = 0.63), although in this case the estimate of outcrossing rate may be confounded with fitness differences among parents.

Given near absolute inbreeding depression and an apparent positive relationship between outcrossing rate and parental fitness, why has complete outcrossing not evolved in this species (c.f. Lloyd 1979; Lande and Schemske 1985; Charlesworth and Charlesworth 1990; Charlesworth et al. 1990)? An evolutionary response to selection for complete outcrossing depends on (1) additive genetic variation for outcrossing rate; and (2) a selective disadvantage to mixed mating relative to outcrossing. Significant among-family variation in the out-crossing rate of individual progenies has been reported in E. regnans (Moran et al. 1989) implying that some genetic variation may exist. However, in E. regnans there may be little selective disadvantage to self-fertilization. First, excess pollen, and large numbers of small simple flowers and seeds, is a very low-cost reproductive strategy (Harper 1977). In addition, the cost of selection against the products of self-fertilization is minimized as large numbers of ovules and progeny shift most of the genetic deaths to early in the life cycle (Haldane 1957; Barber 1965). Third, the presence of self-pollen does not appear to discount outcross reproductive potential, as no reduction in seed per capsule was found in mixed self:outcross pollinations compared to complete out-cross pollinations (Griffin et al. 1987; Ellis and Sedgley 1992). Therefore, geitonomous selfing in E. regnans may merely represent an unavoidable consequence of adaptations to outcrossing (Lloyd 1992) or a phylogenetic constraint to further evolution (Barrett and Eckert 1990). However, in this context, the presence of gynodioecy in a few eucalypt species (Peters et al. 1990; Ellis and Sedgley 1993) suggests new evolutionary opportunities can arise that may allow the shift toward complete outcrossing.

Alternatively, it may be possible that mixed mating is maintained because it has a higher selective value over complete outcrossing. This may occur if the number of outcross progeny contributed by each parent to the next generation is limited by the availability of outcross pollen (Holsinger 1991). Classically, this is considered in terms of isolation (Jarne and Charlesworth 1993), and may arise in E. regnans when later serial stages are reached and mature trees are scattered over a dense rainforest understory. Moreover, controlled outcrossing (i.e., unlimited pollen supply) increases seed set compared to open-pollination in large natural stands of E. regnans (Eldridge and Griffin 1983). This may be a consequence of limits to the number of intertree pollinator flights and the pollen load that vectors can carry (Geber 1985; Harder and Thomson 1989). Eucalyptus regnans trees with more seed per OP capsule tend to be more self-fertile and have lower outcrossing rates (Griffin et al. 1987), suggesting that mixed mating leads to a higher production of seed per parent compared to pure outcrossing. In E. regnans and other fire-dependent species, the mass release of seed following fire may be a strategy to satiate predatory ants (Ashton 1979; O'Dowd and Gill 1984) and available niches. Thus, mixed mating may be a low-cost strategy to increase absolute offspring production (Lloyd 1980), so as to dilute predator and competition pressures on the limited number of outcross seed. Regardless of the frequency of outcross pollinations, selection against the less vigorous inbreds ensures that essentially only the outcross progenies survive to contribute to the next generation (Weins 1984; Charlesworth 1989; Eckert and Barrett 1994; this study).

In summary, although mixed mating is consistently reported in many eucalypt species (e.g., Moran 1992) and other genera (Barrett and Eckert 1990), this study has identified that postdispersal selection can be a major factor leading to virtual complete inbreeding depression by reproductive maturity. In this context, eucalypts can be considered to be primary selfers (outcrossing rate at fertilization [less than] 0.5), but secondary outcrossers. Mixed mating in E. regnans appears to be a robust compromise among numerous factors including high genetic load, severe inbreeding depression, low selective cost of self-fertilization, evolutionary constraints, and limitation in outcross pollen supply.


We would like to thank A. R. Griffin for his foresight in initiating this trial, and CSIRO Division of Forestry, and Australian Paper Manufacturers for establishing the trial and allowing us access to data. We also thank J. B. Reid and R. Vaillancourt for their comments on the manuscript.


AIDE, T. M. 1986. The influence of wind and animal pollination on variation in outcrossing rates. Evolution 40:434-435.

ALLARD, R. W., S. K. JAIN, AND P. L. WORKMAN. 1968. The genetics of inbreeding populations. Adv. Genet. 14:55-131.

ASHTON, D. H. 1975. Studies of the flowering behaviour in Eucalyptus regnans F. Muell. Aust. J. Bot. 23:399-411.

-----. 1976. The development of even aged stands in Eucalyptus regnans F. Muell. in central Victoria. Aust. J. Bot. 24:397-414.

-----. 1979. Seed harvesting by ants in forests of Eucalyptus regnans F. Muell. in central Victoria* Aust. J. Ecol. 4:265-277.

-----. 1981. Tall open-forests. Pp. 121-151 in R. H. Groves, ed. Australian vegetation* Cambridge Univ. Press, Cambridge.

BARBER, H. N. 1965. Selection in natural populations. Heredity 20:551-572.

BARRETT, S.C. H., AND C. G. ECKERT. 1990. Variation and evolution of plant mating systems. Pp. 229-254 in S. Kawano, ed. Biological approaches and evolutionary trends in plants. Academic Press, New York.

BOLAND, D. J., M. I. H. BROOKER, J. W. TURNBULL, AND D. A. KLEINIG. 1980. Eucalyptus seed. CSIRO, Melbourne, Australia.

BURGESS, I. P., E. R. WILLIAMS, J. C. BELL, C. E. HARWOOD, AND J. V. OWEN. 1996. The effect of outcrossing rate on the growth of selected families of Eucalyptus grandis. Silvae Genet. 45:97-100.

CHARLESWORTH, D. 1988. A method for estimating outcrossing rates in natural populations of plants. Heredity 61:469-471.

-----. 1989. Why do plants produce so many more ovules than seed? Nature 338:21-22.

CHARLESWORTH, D., AND B. CHARLESWORTH. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237-268.

-----. 1990. Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evolution 44:870-888.

CHARLESWORTH, D, M. T. MORGAN, AND B. CHARLESWORTH. 1990. Inbreeding depression, genetic load, and the evolution of out-crossing rates in a multilocus system with no linkage. Evolution 44:1469-1489.

CREMER, K. W. 1966. Dissemination of seed from Eucalyptus regnans. Aust. For. 29:252-262.

CUNNINGHAM, T. M. 1960. The natural regeneration of Eucalyptus regnans. Bulletin No. 1. School of Forestry, Univ. of Melbourne, Australia.

DAMGAARD, C., AND V. LOESCHCKE. 1994. Inbreeding depression and dominance-suppression competition after inbreeding in rapeseed (Brassica napus). Theor. Appl. Genet. 88:321-323.

ECKERT, C. G., AND S.C. H. BARRETT. 1994. Inbreeding depression in partially self-fertilizing Decodon verticillatus (Lythraceae): Population-genetic and experimental analyses. Evolution 48: 952-964.

ELDRIDGE, K. G., AND A. R. GRIFFIN. 1983. Selfing effects in Eucalyptus regnans. Silvae Genet. 32:216-221.

ELLIS, M. F., AND M. SEDGLEY. 1992. Floral morphology and breeding system of three species of Eucalyptus, section Bisectaria (Myrtaceae). Aust. J. Bot. 40:249-262.

-----. 1993. Gynodioecy and male sterility in Eucalyptus leucoxylon F. Muell. (Myrtaceae). Int. J. Plant Sci. 154:314-324.

FOWLER, D. P., AND Y. S. PARK. 1983. Population studies of white spruce. I. Effects of self-pollination. Can. J. For. Res. 13:11331138.

FRIPP, Y. J. 1982. Allozyme variation and mating system in two populations of Eucalyptus kitsoniana (Luehm.) Maiden. Aust. For. Res. 13:1-10.

FRIPP, Y. J., A. R. GRIFFIN, AND G. F. MORAN. 1987. Variation in allele frequencies in the outcross pollen pool of Eucalyptus regnans F. Muell. throughout a flowering season. Heredity 59:161-171.

GEBER, M. A. 1985. The relationship of plant size to self-pollination in Mertensia ciliata. Ecology 66:762-772.

GRIFFIN, A. R. 1980. Floral phenology of a stand of mountain ash (Eucalyptus regnans F. Muell.) in Gippsland, Victoria. Aust. J. Bot. 28:393-404.

GRIFFIN, A. R., AND P. P. COTTERILL. 1988. Genetic variation in growth of outcrossed, selfed and open-pollinated progenies of Eucalyptus regnans and some implications for breeding strategy. Silvae Genet. 37:124-131.

GRIFFIN, A. R., AND F. C. HAND. 1979. Post-anthesis development of flowers of Eucalyptus regnans F. Muell. and the timing of artificial pollination. Aust. For. Res. 9:9-15.

GRIFFIN, A. R., G. F. MORAN, AND Y. J. FRIPP. 1987. Preferential outcrossing in Eucalyptus regnans F. Muell. Aust. J. Bot. 35: 465-475.

HALDANE, J. B. S. 1957. The cost of natural selection. J. Genet. 55:511-524.

HARDER, L. D., AND J. D. THOMSON. 1989. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. Am. Nat. 133:323-344.

HARDNER, C. M., R. E. VAILLANCOURT, AND B. M. POTTS. 1996. Stand density influences outcrossing rate and growth of open-pollinated families of Eucalyptus globulus. Silvae Genet. 45: 226-228.

HARPER, J. L. 1977. Population biology of plants. Academic Press, London.

HEDRICK, P. W. 1990. Mating systems and evolutionary genetics. Pp. 83-114 in K. Worhmann and S. K. Jain, eds. Population biology. Springer, Berlin, Germany.

HOLSINGER, K. E. 1991. Mass action models of plant mating systems: The evolutionary stability of mixed mating systems. Am. Nat. 138:606-622.

HOPPER, S. D., AND G. F. MORAN. 1981. Bird pollination and the mating system of Eucalyptus stoatei. Aust. J. Bot. 29:625-638.

HUSBAND, B.C., AND D. W. SCHEMSKE. 1996. Evolution of the magnitude and timing of inbreedlag depression in plants. Evolution 50:54-70.

JACKSON, W. D. 1968. Fire, air, water and earth - An elemental ecology of Tasmania. Proc. Ecol. Soc. Aust. 3:9-16.

JARNE, P., AND D. CHARLESWORTH. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annu. Rev. Ecol. Syst. 24:441-466.

LANDE, R., AND D. W. SCHEMSKE. 1985. The evolution of self-fertilization and inbreedlag depression in plants. I. Genetic models. Evolution 39:24-40.

LANDE, R., D. W. SCHEMSKE, AND S. T. SCHULTZ. 1994. High in-breeding depression, selective interference among loci, and the threshold selfing-rate for purging recessive lethal mutations. Evolution 48:965-978.

LAROCQUE, G. R., AND e. L. MARSHALL. 1993. Evaluating the impact of competition using relative growth rate in red pine (Pinus resinosa Ait.) stands. For. Ecol. Manage. 58:65-83.

LLOYD, D. G. 1979. Some reproductive factors affecting selection of self-fertilization in plants. Am. Nat. 113:67-79.

-----. 1980. Demographic factors and mating patterns in angiosperms. Pp. 67-88 in O. T. Solbrig, ed. Demography and evolution in plant populations. Blackwell, Oxford, U.K.

-----. 1992. Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int. J. Plant Sci. 153:370-380.

MATHESON, A. C., AND C. A. RAYMOND. 1984. Effects of thinning in progeny tests on estimates of genetic parameters in Pinus radiata. Silvae Genet. 33:125-128.

MORAN, G. F. 1992. Patterns of genetic diversity in Australian tree species. New For. 6:49-66.

MORAN, G. F., AND J. C. BELL. 1983. Eucalyptus. Pp. 423-441 in S. D. Tanksley and T. J. Orton, eds. Isozymes in plant genetics and breeding. Elsevier Science Publishers B.V., Amsterdam.

MORAN, G. F., AND A. H. D. BROWN. 1980. Temporal heterogeneity of outcrossing rates in alpine ash (Eucalyptus delegatensis R.T. Bak.). Theor. Appl. Genet. 57:101-105.

MORAN, G. F., J. C. BELL, AND A. R. GRIFFIN. 1989. Reduction in levels of inbreeding in a seed orchard of Eucalyptus regnans F. Muell. compared with natural populations. Silvae Genet. 38:3236.

MORGANWE, M., G. G. VENDRAMIN, P. ROSSI, AND A.M. OLIVIERI. 1993. Selection against inbreds in early life cycle phases in Pinus leucodermis Ant. Heredity 70:622-627.

MUONA, O., R. YAZDANI, AND D. RUDIN. 1987. Genetic change between life stages in Pinus sylvestris: Allozyme variation in seeds and planted seedlings. Silvae Genet. 36:39-42.

O'DOWD, D. J., AND A.M. GILL. 1984. Predator satiation and site alteration following fire: Mass reproduction of alpine ash (Eucalyptus delegatensis) in southeastern Australia. Ecology 65: 1052-1066.

PARK, Y. S., AND D. P. FOWLER. 1984. Inbreeding in black spruce (Picea mariana (Mill.) B.S.P.): Self-fertility, genetic load, and performance. Can. J. For. Res. 14:17-21.

PERRY, D. A. 1985. The competition process in forest stands. Pp. 481-506 in M. G. R. Cannell and J. E. Jackson, eds. Attributes of trees as crop plants. Institute of Terrestrial Ecology, Abbots Ripton, Huntingdon, U.K.

PETERS, G. B., J. S. LONIE, AND G. F. MORAN. 1990. The breeding system, genetic diversity and pollen sterility in Eucalyptus pub verulenta, a rare species with small disjunct populations. AuNt. J. Bot. 38:559-570.

PHILLIPS, M. A., AND A. H. D. BROWN. 1977. Mating system and hybridity in Eucalyptus paucifiora. AuNt. J. Biol. Sci. 30:337344.

PLESSAS, M. E., AND S. H. STRAUSS. 1986. Allozyme differentiation among populations, stands, and cohorts in monterey pine. Can. J. For. Res. 16:1155-1164.

RITLAND, K. 1990. Inferences about inbreeding depression based on changes of the inbreeding coefficient. Evolution 44:12301241.

-----. 1996. Inferring the genetic basis of inbreeding depression in plants. Genome 39:1-8.

SAMPSON, J. F., S. D. HOPPER, AND S. H. JAMES. 1988. Genetic diversity and the conservation of Eucalyptus crucis. Maiden. Aust. J. Bot. 36:447-460.

SAS INSTITUTE. 1992. SAS technical report P-229, SAS/STAT software: Changes and enhancements. Rel. 6.07. SAS Institute, Cary, NC.

-----. 1993. SAS technical report P-243, SAS/STAT software: The GENMOD procedure. Rel. 6.09. SAS Institute, Cary, NC.

SCHAAL, B. A., AND D. A. LEVIN. 1976. The demographic genetics of Liartris cylindracea Michx. (Compositae). J. Hered. 110:191206.

SCHMITT, J., AND D. W. EHRHARDT. 1990. Enhancement of inbreeding depression by dominance and suppression in Impatiens capensis. Evolution 44:269-278.

SCHMITT, J., J. ECCLESTON, AND D. W. EHRHARDT. 1987. Dominance and suppression, size-dependent growth and self-thinning in a natural Impatiens capensis population. J. Ecol. 75:651-665.

SEDGLEY, M., F. C. HAND, R. M. SMITH, AND A. R. GRIFFIN. 1989. Pollen tube growth and early seed development in Eucalyptus regnans F. Muell. (Myrtaceae) in relation to ovule structure and preferential outcrossing. Aust. J. Bot. 37:397-411.

SORENSON, F. 1982. The role of polyembryony and embryo viability in the genetic system of conifers. Evolution 36:725-733.

SORENSEN, F. C., AND R. S. MILES. 1982. Inbreeding depression in height, height growth, and survival of douglas-fir, ponderosa pine, and noble fir to 10 years of age. For. Sci. 28:283-292.

SORENSEN, F. C., AND T. L. WHITE. 1988. Effect of natural inbreeding on variance structure in tests of wind-pollination douglas-fir progenies. For. Sci. 34:102-118.

UYENOYAMA, M. K., K. E. HOLSINGER, AND D. M. WALLER. 1993. Ecological and genetic factors directing the evolution of self-fertilization. Oxf. Surv. Evol. Biol. 9:327-338.

WALLER, D. M. 1984. Differences in fitness between seedlings derived from cleistogamous and chamogamous flowers in Impatiens capensis. Evolution 38:427-440.

-----. 1985. The genesis of size hierarchies in seedling populations of Impatiens capensis. New Phytol. 100:243-260.

WEINS, D. 1984. Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64: 47-53.

WILLIAMS, C. G., AND O. SAVOLAINEN. 1996. Inbreeding depression in conifers: Implications for breeding strategy. For. Sci. 41:102-117.

WOLFE, L. M. 1993. Inbreeding depression in Hydrophyllum appendiculatum: Role of maternal effects, crowding, and parental mating history. Evolution 47:374-386.

WRIGHT, A. J., AND C. C. COCKERHAM. 1985. Selection with partial selfing. I. Mass selection. Genetics 109:585-597.
COPYRIGHT 1997 Society for the Study of Evolution
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 1997 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Hardner, Craig M.; Potts, Bradley M.
Date:Feb 1, 1997
Previous Article:Reciprocal transplant experiments.
Next Article:Ecological history and evolution in a novel environment: habitat heterogeneity and insect adaptation to a new host plant.

Terms of use | Privacy policy | Copyright © 2022 Farlex, Inc. | Feedback | For webmasters |