tive ﬁtness dropped signiﬁcantly between long-distance cross-
es within Sinharaja to crosses involving separate forest pop-
ulations. This between-forest crossing effect was consistent be-
tween species in spite of the large interspeciﬁc difference in
FERTILITY IN TWO TROPICAL TREE SPECIES
dispersal potential. For both species, variation in fruit set
among maternal trees was least for the between-forest crosses,
suggesting a universal poor interfertility between trees occur-
ring in separate forest reserves.
Mechanisms underlying outbreeding depression may be of
a genetic or an ecological nature (Price and Waser, 1979;
Shields, 1982). Outbreeding depression involving between-
population crosses is most often ascribed to the genetic mech-
anism involving disruption of coadapted gene complexes
(Templeton, 1986). According to this model, intrinsic coad-
aptation involving relatively few loci develops through re-
stricted gene ﬂow among populations and genetic drift within
populations (Templeton, 1981; Schierup and Christiansen,
1996). Crossing disparate genomes results in outbreeding de-
pression through the disruption of coadaptation between ho-
mologous chromosomes in the F
generation and between co-
restricted to between-forest crosses over 12- and 35-km dis-
tances, may be explained in part by disruption of intrinsic co-
adaptation. The observation of hybrid vigor in seedlings of Sh.
In contrast, the ecological mechanism for outbreeding de-
pression involves reduced ﬁtness of wide outcrosses due to
adaptation to local biotic and abiotic conditions, such that wide
outcrossing yields F
progeny with alleles maladapted to either
tion-driven divergence is typically associated with intrapopu-
lation outbreeding depression (e.g., Waser and Price, 1989),
selection-driven divergence between populations seems a plau-
sible contributor to the reduced interfertility between popula-
tions observed in this study. Through direct selection on ﬁtness
traits, habitat heterogeneity will promote genetic differentia-
tion within and among plant populations (Jain and Bradshaw,
1966; Linhart and Grant, 1996). The considerable environ-
mental heterogeneity of southwest Sri Lanka is likely sufﬁ-
cient to cause genetic differentiation of tree populations over
a scale of tens of kilometers. The ridge and valley system of
southwest Sri Lanka comprises elevations ranging from 300
cloudiness, and rainfall (
Ͻ2500–5000 cm) occurs (Gunatilleke
et al., 1998).
The apparent outbreeding depression observed in fruit set
and cumulative ﬁtness for between-forest crosses in both spe-
cies indicates some degree of genetic isolation among tree
populations occupying the separate forest reserves of Sri Lan-
ka’s wet zone. This result is somewhat surprising given the
large stature of the species and the small geographic area in-
volved, and it suggests that conditions favorable for speciation
in tropical trees may arise over a scale of only several to tens
of kilometers. The geographical heterogeneity of southwest Sri
Lanka, however, may be of a ﬁner scale than that of the ma-
jority of tropical forested landscapes (Ashton and Gunatilleke,
1987). It would be desirable to see whether poor cross-fertility
between forests is universal for tree species in the wet zone.
Unfortunately, plans to continue this study in 1998, and to
include other species of Syzygium and Shorea, were thwarted
due to a general lack of ﬂowering in the region that year. From
a conservation perspective, observation of even minor repro-
ductive isolation between forest reserves suggests that even
where tree species are shared among reserves, each forest rep-
resents a singular genetic resource worthy of preservation.
Outbreeding depression was not detected in crosses over
what is presumably the normal range of pollen ﬂow for either
species. The lack of evidence of outbreeding depression within
continuous-forest populations in this study is consistent with
the literature in which examples of between-population out-
breeding depression in plants far outnumber those of within-
population outbreeding depression. Given the recent nature of
deforestation north of Sinharaja, however, delineation of S.
Walankanda Reserves may not accurately reﬂect the recent
demographic history of this species. Walankanda and Sinha-
raja Reserves were part of one continuous forest until only
30–40 yr ago (P. S. Ashton, personal communication, Harvard
University). This is probably less than the generation time for
these trees and indicates the potential for recent genetic con-
nectivity between the two populations. As S. rubicundum is
generally restricted to mid-slope areas, however, it is likely
that this species was not present in abundance in the valley
between Sinharaja and Walankanda Reserves prior to the
clearing of forest in that area (P. S. Ashton, personal com-
munication, Harvard University). Regardless, the two forests
are separated at present by a deforested strip only 4 km wide.
Gene ﬂow between tree populations occupying these forests
since the separation is therefore at least plausible (e.g., White,
Powell, and Boshier, 1998). For these reasons, observation of
outbreeding depression in crosses between tree populations oc-
cupying Sinharaja and Walankanda Reserves is unexpected,
and it indicates that genetic divergence of tree populations can
occur over very short distances even in continuous habitat.
Hybrid vigor in Shorea cordifolia—For Sh. cordifolia,
trends observed among treatments for seed germination rate
and seedling height suggest hybrid vigor or luxuriance in prog-
eny derived from between-forest crosses. This ﬁnding is ten-
tative, however, due to the small sample sizes involved with
the between-forest crosses for the seed germination and later
stages. Hybrid vigor in F
progeny is consistent with the model
gene complexes. According to this model, F
hybrid vigor re-
breakdown in the F
generation from the disruption of parental
gametogenesis (Templeton, 1986). It re-
of genetic differentiation between mates without subsequent
breakdown (Shields, 1982). Hybrid vigor in interpopulation
ﬁtness has been reported for
1957; Vickery, 1959; Grant and Grant, 1960; Gottlieb, 1971;
Grant, 1971; Hughes and Vickery, 1974; Price and Waser,
1979). In woody angiosperms, hybrid vigor in interpopulation
crosses has been documented for at least one species, Syzygium
cormiﬂorum, a subcanopy species of Australia’s rainforests
(Crome and Irvine, 1986). Unfortunately, due to the long gen-
eration times of trees, study of F
generations in these species
dence of inbreeding and outbreeding effects decreased be-
tween the stages of fruit set and 1-yr-old seedlings. This ﬁnd-
ing is tentative, however, as the power to detect crossing ef-
fects also declined over the same period. In their review of
the timing of inbreeding depression in plants, Husband and
Schemske (1996) concluded that for outcrossing species, in-
growth and reproduction, and much less important for seed
germination. Results of this study are consistent with the gen-
eral conclusion that embryo abortion is an important, if not
primary, component of inbreeding depression in outcrossing
plants (e.g., Levin, 1984, 1989).
Little is known of the timing of outbreeding depression in
plants. Within the conﬁnes of the ﬁtness measures used in this
study, the results are consistent with the ﬁndings of McCall,
Mitchell-Old, and Waller (1991) of optimal outcrossing in Im-
creased between the stages of mature seeds and offspring sex-
ual maturity. Both studies agree with Husband and Schemske’s
(1996) consensus for inbreeding depression that crossing ef-
fects are most notable at the stage of seed set and less so at
the stages of seed germination and early seedling growth (but
see Waser and Price, 1989). Low inbreeding depression ob-
served in germination and survival might be due to the short
duration of, and few genes involved in, these stages relative
to the stages of seed maturation and reproduction (Husband
and Schemske, 1996).
Viewed together, the theories of inbreeding and outbreeding
depression predict that there should exist some intermediate
crossing distance between mates at which both inbreeding and
outbreeding depression are avoided (i.e., the ‘‘optimal out-
crossing distance’’ of Price and Waser, 1979; and Waser and
Price, 1983). Optimal outcrossing refers to those crosses that
achieve greatest reproductive ﬁtness relative to other crosses
and therefore signal optimal genetic compatibility between
mates. Little is known of optimal outcrossing in woody spe-
cies. Although identifying an optimal outcrossing distance was
not an objective of this study, the results indicate that optimal
outcrossing for canopy species in tropical forests may occur
over a range of roughly one to several kilometers. While track-
ing pollen ﬂow at this spatial scale in continuous forest is
exceedingly difﬁcult, a handful of recent studies have dem-
onstrated at least low levels of natural cross-pollinations over
distances of one, or in some cases, several kilometers in trop-
ical trees (Nason, Herre, and Hamrick, 1996, 1998; Nason and
Hamrick, 1997; Apsit, 1998; White, Powell, and Boshier,
1998). Outcrossing distance alone, however, does not explain
variation in crossing success for the two study species. Similar
outcrossing distances yielded very different results in the two
species (high ﬁtness at 10 km for Sh. cordifolia and very low
ﬁtness at 12 km for S. rubicundum). Rather, for these trees,
the critical determinant of crossing success over long distances
appears to be whether or not mates occur within the same
ka’s wet zone forests, fruit set increased signiﬁcantly with out-
crossing distance, peaking at intermediate-distance within-for-
est crosses (1–10 km depending on species). In crosses be-
tween trees occupying separate forest reserves, however, fruit
set was signiﬁcantly reduced (or nearly so) for both species.
In contrast, seed germination and seedling height at 1 yr for
Sh. cordifolia suggested hybrid vigor in between-forest cross-
es. The effects of nearest-neighbor mating varied among trees
and species; the mean ﬁtness cost of nearest-neighbor mating
relative to mating with moderately more distant neighbors was
45% for S. rubicundum and 0% for Sh. cordifolia. In contrast,
the ﬁtness effects of between-forest crossing were substantial
for both species (52 and 70% relative to within-forest crosses
for the same two species). Crossing effects diminished be-
tween the stages of fruit set and 1-yr-old seedling size; only
the former was signiﬁcant for both species. Results indicate a
strong potential for biparental inbreeding depression within
forest tree populations and partial reproductive isolation
among trees occupying the remaining forest reserves in Sri
Lanka’s wet zone.
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