Hiolo~@al Jiinrnal uf the Linnean Socieg (1989), 37: 345%357. With 2 figures
Estimates of gene flow in forest trees
DIDDAHALLY R. GOVINDARAJU*
Department of Forestry, University of Kentucky, Lexington, KY40546-0073
Krcrirvd
21 .Ipd 1988. acitped f o r publication 30 ,January 1989
Qualitative ;md quantitative estimates of grne flow wcrc obtained for fourteen gymnosperm and
peries. High levels of grnr flow wcrr prrvalrnt among gymnosprrms
while thcsr Irvrls varied from high t o low among angiosperms. In both groups, spcrirs with grcatcr
pollcn dispersal alditics appear to maintain high levrls o f genr flow. A detailrd analysis of
population strurtiirc in relation t o genr flow was rarrird out on a gymnosprrm sprcirs (Pinu.! rigida)
and two angiosperm suhsprcies (Eum!vptus imvin ssp. raesia and ssp. magnn). T h e rrsults suggrstcd
chat pop\ilalions OF many specirs may bc concatcnatcd systrms hound by grrir flow, and thr ovrrall
Irvcls of gcnc flow may br influenced b y either single or rlustrrs of popuiations. I~illrrrntIevrls o f
gcnc flow was found hrtwcrn two rlosrly related species OF 8.cntsin growing uridrr similar rcologiral
conditiotis. suggrsting a plausihlc link brtwrrn pollinator l x h a v i o u r and pollrn flow.
scvrii a ngiospcrm forrs t t r(
K E Y \Z'ORI)S:
mrthods
Population di fkrnt i at i on
~
ratc of immigration
qualitativr arid quantatitivc
~
rarc alleles - angiosperms and conifrrs.
CON'I'EN'I'S
Intrcrductiori .
.
.
.
.
.
.
M;itrri;ils and inctliods.
Ec.ologic;tl katurcs
.
.
Mc.isurcincnts of gcnr flow
Kcsnlrs
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Discussion.
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350
353
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345
346
346
347
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356
356
I N'I'ROD~JC'l'ION
T h e importance of gene flow as a creative a n d a disruptive force in
microevolutionary processes has been studied by various workers (Wright, 1931;
Mayr, 1963; Ehrlich & Raven, 1969; see Slatkin, 1985a, 1987 for reviews).
Wright (1931) in particular, proposed a threshold limit (Wright's Rule; .sen.su
Slatkin, 1985b) to the levels of gene flow that would affect the degree of'
difl'erentiation among local populations. According to him, local populations
would diverge by genetic drift if JVm (number of migrants per generation), the
product of effective population size, J,and the average rate of immigration, m ,
from a source population is less than 1 , but not if JVm is greater than 1. A large
body of da t a has been accumulated in the last two decades on the levels of
* I'rcwnt
aildress: Urp;irtmc*nt of. Biology. ( h s c \Vestern Kcrer\e L.iiivcrsity%Clcvrland, ( ) H 4410(i, I'.S.A.
+
0 0 2 4 ~ ~ ~ O ( i ~ i : H O : 0 8 0 13
~~4
$O:C.OO/O
5
345
((? 1981) 'l'tiv t i m i e m Socict) o f 1 . o t 1 d o 1 1
346
D. COVINDARAJU
genetic variation and differentiation in both plant and animal species (Hamrick,
Linhart & Milton, 1979; Nevo, Beiles & Ben-Shlomo, 1984; Ledig, 1986).
However, information on the levels of gene flow, which in fact influence both
genetic variation and differentiation among populations, is scanty. Direct
estimates of gene flow in natural plant populations are obtained by using pollen
or seed flow or their dispersal vectors (Levin & Kerster, 1974; Levin, 1986;
Smyth & Hamrick, 1987). Accurate estimates of these parameters, however, are
difficult to obtain in natural populations (Slatkin, 1985b, 1987). This has been
attributed largely to the difficulties associated with direct estimation of gene flow
in natural populations (Slatkin, 1985b, 1987). Nonetheless, a few indirect
methods, based on allele frequencies, have been proposed to estimate
approximate levels of gene flow in natural populations (Wright, 1931; Crow,
1986; Slatkin, 1981a, 1985a; Barton & Slatkin, 1986).
Wright (1931 ) showed that, for selectively neutral alleles, genetic
differentiation among populations, F,,, is inversely related to Nm. O n the other
hand, Slatkin (1981a) proposed a qualitative method to estimate levels of gene
flow from allozyme data, in which the average frequency of rare alleles, p(i)
(conditional average frequency of rare alleles), is used to estimate gene flow; the
frequency distribution of rare alleles depends strongly on the overall levels of
gene flow among populations, but is nearly independent of both mutation rates
and selection intensity. Subsequently, Slatkin (l985a) found that N m is
approximately linearly related to the logarithm of the average frequency of
private alleles p( 1). These indirect methods have been used, either
independently or in combination, to estimate relative amounts of gene flow
among natural populations of various organisms such as Plethodontids (Larson,
Wake & Yanev, 1984), Troglobites (Caccone, 1985), fishes (Waples, 1987),
Drosophila (Singh & Rhomberg, 1987), Triticum dicoccoides (Golenberg, 1987).
However, similar estimates have not been made for large array of forest tree
species with diverse life histories. The objectives of this study are: (a) to estimate
relative amounts of gene flow, using the indirect methods, among temperate and
tropical forest trees, ( b ) to examine patterns associated with estimates of gene
flow within and among tree species, and (c) to compare gene flow rates between
conifers and angiosperms.
MAI'ERIALS AND METHODS
Ecological f e a h r e s
Data on allozyme variation of fourteen gymnosperm (conifer) and seven
angiosperm forest tree species, representing nine genera and diverse ecological
conditions were collected from published and unpublished sources (Table 1).
There was a diverse distribution patterns, sampling strategies employed and
modes of pollination. For example, the widespread distribution of Pinus rigida
(Guries & Ledig, 1982) is characteristic of most conifers in the eastern U.S.;
conversely populations of P.je$reyi (Furnier & Adams, 1986) were obtained from
its two major distributional ranges (Klamath and Sierra Nevada populations,
growing on ultramafic and rich soils, respectively), forming a system of semiisolated populations, typical of some western conifers. Populations of Calocedrus
GENE FLOW I N F O R E S I 'I'KEES
347
decurrens (Harry, 1984) were sampled from four locations within each of the three
mountains (Kilarc basin, Bailey ridge, and Greenhorn summit) in California.
Abies balsamea (Neale & Adams, 1985) populations were obtained from a 500 m
long transect. Among angiosperms, populations varied from semi-isolated
conditions as in Eucahptus to complete isolation in Lissianthus skinnerii (Sytsma &
Schaal, 1985). The studied conifers, and the two oaks (Quercus sp.), are
pollinated by wind, and the rest of the angiosperms are animal-pollinated. T h e
hierarchical mode of distribution/sampling of populations ranging from the
entire distributional range of species (e.g. Pinus rigida) to localized areas (e.g.
Abies balsamea, Lissianthus skinnerii) , provides an opportunity to examine some of
the general patterns and levels of gene flow associated with a broad spectrum of
species.
Measurements
of gene $ow
A minimum of three populations and at least ten individuals per population
were included in the analysis as suggested by Slatkin (1985a). However, his
criterion for number of private alleles to estimate gene flow was not fulfilled for
several species. Estimates of gene flow were obtained using both qualitative
(Slatkin, 1981a) and quantitative (Barton & Slatkin, 1986; Crow, 1986)
methods. The qualitative method is a graphical representation of the conditional
average frequencies of private alleles p(i) against the occupancy rate i/d, whcrc d
is the total number of demes examined and i is the number of demes occupied by
an allele. Barton & Slatkin's (1986) quantitative method utilizes p(i) to provide
an approximate estimate of the level of gene flow ( N m ) according to the
relationship: log p(i) = a log (Nm)+b. The value of a and b for sample sizes
n= 10, 25 and 50 are: a= -0.489, -0.576, and -0.612; b = 0 . 9 5 l , - 1 . 1 1 and
- 1.21 respectively. The ratio between sample sizes, N = 10, 25 or 50 to actual
number of individuals in each population was multiplied by N m to obtain Nm*
values (see Barton & Slatkin, 1986 for details). Because the above method is
relatively insensitive when the number of private alleles is very low, following
Slatkin (personal communication, 1987), G,, values were used to calculate Nm,,
(Crow, 1986) as follows: G,( = [ 4 N m a + 1 ] - ' , where a= [n/n- 112, n is the
number of populations, and G5tis equivalent to a weighted average of Wright's
F,[over all alleles (Nei, 1973). This method provides an alternative approach to
obtain approximate levels of N m , when the requirements for Slatkin's method
are not met (see also Govindaraju, 1988a, b), and provides an opportunity to
compare the similarities and dissimilarities between the two approaches. This
combined approach has been used by Larson el al. (1984) and Waples (1987) on
Plpthodontids and fishes, respectively. In a majority of the cases, the
values
were obtained from the original sources; when unavailable, they were calculated
from gene frequency data according to Nei (1973). It was assumed that allozyme
variation is selectively neutral in the context of the analysis presented in this
study.
A detailed analysis of the relationship between gene flow and population
structure was carried out following Slatkin (1985a) on Pinus rzgida and Eu:uca&Lu.r
Sierra Navada
(fertile soils)
California
Yugoslavia
Yugoslavia
California and Baja,
Mexico
Northeastern U S .
Scotland
P. jeffreyi*
P.
P.
P.
P.
P. rigida
P. syloestris
muricata
nigra ssp. austriaca
nisra ssp. dalmalica
radiata
Klamath Mountains
(ultramafic soils)
SW Oregon and
California
British Columbia
Alberta
SW Oregan and
California
Geographical location
of samples
P. jeffreyi*
P. contorta ssp. latifolia
P. contorta var. latfolza
P. jeffreyit
Pinus allenuata
Species
21
16
14
20
4
32
4
20
20
25
18
20
32
No. of
proteins
11
7
6
5
5
6
7
9
5
13
4
Populations
sampled
65
58
86
17
17
95
51
50
73
71
52
77
No. of
alleles
39- 122
13-35
1&30
50-55
14-55
15-53
11-34
41-57
15.0
30-62
11-57
15-50
Range of
sample sizes
TABLE
1. Information o n species used for t h e analysis of gene flow a m o n g populations
Guries & Ledig, 1982
Kinloch, Westfall &
Forest. 1986
Yeh & Layton, 1979
Dancik & Yeh, 1983
Furnier, 1984
and Furnier & Adams,
I986 (excluding S5)
Furnier, 1984
and Furnier & Adams,
I986
Furnier, 1984
and Furnier & Adams,
1986 (excluding S5;
Millar el al., 1988
Nikolic & Tucic, 1983
Nikolic & Tucic, 1983
Millar et a / . , 1988
Millar el al., 1988
References
eC
icl
>
U
z
8f
f;
Central Panama
New Jersey
New Jersey
Lisianlhus sktnneri
Quercus marilandica
Q. uelulina
*Regional populations within the respective species
Southwestern Australia
Southeastern Australia
North Carolina
(t).
New Hampshire
(elevational transect)
California
California
(Kilarr Basin,
California
(Bailey Ridge)
California
(Greenhorn Summit)
Northwestern and
Ontario
Southwestern Australia
Eucalyplu caesia
ssp. raesia
E. caesia ssp. magna
E . pauciff0ra
Ltriodendron tulipif ra
Larix laririna
C. decurren.s*
C'. decurrens*
Calocedrus decurrenst
C. decurrens*
Abies balsamea
6
10
4
4
12
4
4
II
12
II
II
6
6
15
I 5I
21
30
21
24
24
17
26
79
90
121
106
19
25
25
25
25
8
17-2 I
25.0
16-22
27-50
15-30
33-44
28-54
20.0
45-5 1
35-50
35-5 1
42-5 1
22-40
1987
Manos & Fairbrothers,
1987
Sytsma & Schaal, 1985
Manos & Fairbrothers,
Knowles & Perry,
personal communication
.Moran & Hopper, 1983
(excluding Kg:
Moran & Hooper, 1983
Phillips & Brown, 1977
Brotschol, Roberts &
Namkoong, 1986
Harry, 1984
Harry, 1984
Harry, 1984
Harry, 1984
Seale & Adams, 1985
m
r
z
5
m
v!
-
2,m
7
I
L
5z
7
m
z
m
0
D. COVINDARAJU
350
'I'ABLE 2. Frequency of private alleles $( l ) , and the parameters of avcragc number of migrants
exchanged between local populations,
N m , in
various species (arranged in decreasing order of
Nm*)
No. of
Privatc
Alleles
Average
sample size
Nm*
~
I
I
20
15
3
8
31
19
2
2
3
2
19
24
4
5
3
17
4
26
3
28
4
5
10
0.009
0.015
0.016
0.019
0.02 1
0.018
0.019
0.019
0.030
0.024
0.030
0.020
0.028
0.025
0.03 1
0.042
0.026
0.049
0.050
0.062
0.057
0.071
0.067
0.080
0.860
Species
~
2 I .83
13.25
9.73
9.41
8.71
7.47
7.43
6.84
6.74
6.66
6.5 I
6.14
4.9 I
4.87
4.55
4.20
4.10
3.61
2.68
2.26
2.24
1.51
1.14
0.76
0.015
4.15"
I .ow
9.00b
4.58"
8.78"
0.58"
1.35h
4.94"
1.35"
I .37h
8.05'
2.06'
4.55b
4.62'
6.81'
I .07"
0.54'
0.76b
0.17"
0.001'
0.02b
52.00
38.00
46.57
36.40
27.75
63.09
46.1 1
48.77
19.33
35.07
20.00
51.20
37.00
44.84
27.00
17.70
50.00
15.00
20.00
14.80
19.33
19.30
38.15
43.1 I
25.00
Pinus nigra ssp. austriaca
Liriodendron tulipifera
Calocedrus decurrens
Pinus contorta var. latijolia
Abies balsamea
Pinus rigida
Calocedrus decurrens (Kilarc populations)
Calocedrus decurrens (Greenhorn populations)
Quercus marilandica
Pinus j e f f r y
Eucalyptus pauciJiora
Pinus nigra ssp. dalmatica
P. attennata
Calocedrus decurrens (Bailey ridge populations)
Pinus .ylueJtris
P. jeffrgi (Sierra Nevada populations)
P. jeffr,yi (Klamath Mountain populations)
P. contorta ssp. latijolia
Larix laricina
Pinus radiata
Quercus uelntina
Pinus muricata
Eucalyptus caesia ssp. niagna
E. caesia ssp. caesta
Lisianthus skinneri
Nm* Barton and Slatkin (1986) corrected for sample size. N m , , , Crow (1986).
"Based on Gs,values computed using the allele frequency data reported by the authors listed in 'I'able I .
hBased on Gs, values reported by the authors listed in Table 1.
caesia ssp. caesia, and ssp. magna, by eliminating one, two or more populations
from the analysis. Changes in the Nm* values upon eliminating one or more of
populations (relative to the average Nm* values for all the populations in the
species' range) provides insights regarding the genetic distinctiveness of the
eliminated population(s).
RESULI'S
Graphical analyses of gene flow in conifers conformed to the trends that are
common to high gene flow species, but the angiosperms were more diverse
(Fig. la-h). These results closely agreed with the quantitative estimation, Nm*
and Nm,,,. A discrepancy between qualitative and quantitative estimates was
found only when the number of private alleles was low. High gene flow
(Nm* > 1 ) was more common in wind-pollinated species (1.5 1 <Nm* < 2 1.83 and
0.54 < Nm,,, < 9.00) than in animal-pollinated species (0.0 15 < Nm* < 13.25 and
0.02 <Nm,,, < 4.94). Although a one-to-one correspondence between Nm* and
Nm,,, was lacking, 7 1 percent of the species ( 15 out of 2 1) that showed high levels
of gene flow ( > 1 .OO) with one approach also showed similar trends using the
G E N E FLOW I N FORE ST TREES
A
-Plnus rigida
-
P. cantorta ssp. iofifolio
1.0-
- P/nus
a
oftenuafo
P. radiofa
-Caiocedrus decurrens ( 01 I)
I
C.decurrens (Kilarc basin)
--- C. decurrenr
P. rnuricafo
0.6 -
--
35 I
(Bailey ridge)
4 - C . decurrens (Green horn summit)
.-
lQ
0.2
-
I .o
1
CI
Pinus sylvesfris
-
P. nigro ssp. ousiriaca
P. nigra ssp. dalrnatica
-
G
- Eucaiypf us coesia ssp. caer/o
E. caesio ssp. magno
_ _ _E. pouclflora
-
I .o
-L arix
0
laricina
- - - Abies bolsomea
-.-
t‘
0.6
L /riodendran tulipifero
L isianthus skinnerii
‘9
- --
Quercus mariiandica
i
’
0.2
,
0.0
0.2
b.
0.4
0.6
0.8
1.0 0.0
0.2
0.4
0.6
0.8
E‘igurr I . Rrpresentation of conditional average frequency (if a n allele p(i) against the occupancy
ratr z/d. T h e patterns in graphs A-F arc typical of high ( H ) gene flow sprcirs; but G and H
reprrsrnt sprcies with high, intrrmediate ( I ) and low (L) levels of gcnc flow.
I .o
“Average number of individuals in the sample.
BL-CR
5
35.8
0.022
7.521
8
63.30
0.015
7.96
WL
5
45.6
0.080
0.716
SC
3
39.4
0.086
0.774
6
65.30
0.0 I 7
6.28
YM
6
46.0
0.073
0.843
CI
3
38.7
0.086
0.750
37.1
0.348
0.079
6
BG-MC
57.60
0.019
5.94
10
HM
ss
WP
38.1
0.065
1.204
40.4
0.125
0.386
2
CT-SC
CD-WC
6
49.8
0.068
0.855
7
YN-WL
62.50
0.017
6.56
9
LL
41.4
0.144
0.301
5
MS-HP
57.20
0.017
7.20
10
EP
31.3
0.060
1.250
BL-CR
CD
4
35.3
0.560
0.038
BG-MC
MS
7
65.50
0.015
7.69
6
BR
eliminating one, two, three, etc. populations in each of the species
65.88
0.018
5.70
8
SC-MS
44.9
0.205
0.156
SC
4
U‘C-CT
49.9
0.082
0.633
46.0
0.144
0.272
HM-YM MS-HM
WL
WL
5
5
65.20
0.016
6.91
9
BG
50.76
0.446
0.039
8
MC-MS
YM-WL
68.11
0.015
7.40
6
BR-BG
66.37
0.018
5.64
SC-BF
MS
8
3. Estimates of$( I ) , and Nm* for various subsets of populations in three species of forest trees. Relative changes in Nm* values were computed upon
A. Pinus rigida ( I 1 populations, 2 I loci, Nm* = 7.47)
Populations
BF
MS
BP
SC
excluded
Number of
8
8
8
8
private alleles
63.89
64.80
63.20
65.50
Sample size”
0.018
0.018
0.018
0.018
PI])
N m*
5.86
5.75
5.92
5.71
Population
BR-BR
SC-BF HM-WP BP-SS
excluded
BG
MS-BP
EP-LL
BR-BG
Number of
7
8
8
5
private alleles
Sample size”
71.75
70.28
46.28
76.14
PII)
0.013
0.018
0.016
0.011
Arm*
8.87
5.32
9.78
11.00
B. Eucalyptus caesia, ssp. caesia (6 populations, 1 I loci, Nm* =0.760)
Population
BG
MC
MS
HP
excluded
Number of private
4
7
5
4
alleles
Sample size”
40.7
41.3
42.5
42.3
PII)
0.090
0.290
0.068
0.092
.Vm*
0.660
0.096
1.000
0.614
C. Eucalyptus caesia ssp. magna (6 populations, I 1 loci, Nm* = 1,140)
Population
BL
CR
CD
WC
excluded
Number of
5
6
6
5
private alleles
Sample size”
38.6
35.8
35.9
40.4
0.010
0.055
0.066
0.056
HI)
“+in*
25.30
1.683
1.245
1.448
.rABLES
W
eC
;a
9
U
8s
z
G
N
VI
GENE FLOW IN FOREST TREES
353
Figurr 2. Locations of Pinus rigida (A; modified from Gurirs & Ledig, 19821, and E u c a l y p s carsia (B)
ssp. raisin (0)
and ssp. rnagna ( 0 ;modified from Moran & Hopper, 1983) populations.
alternative approach. Discrepancies between N m * and N m , , appeared to be
found when the number of private alleles and individuals was low.
The Nm* values were generally higher among closely located populations. For
example, in Abies balsamea, the three sampled populations were within a radius of
500 m. Similarly, the Alberta populations of P. contorta var. latzfolia, showed
higher levels of gene flow than ssp. latzfolia from British Columbia.
The relationship between gene flow levels, N m * and population structure is
presented in Table 3, Fig. 2. The average N m * for P. rigida was 7.47. Slight
deviations from the average value were obtained upon excluding NM and BR
populations from the analysis, suggesting that these populations may be distinct
from other populations in the species range. Furthermore, elimination of either
HM-WP-KP-LL or BP-SS-BR-BG sets of populations from the analysis led to
substantial deviations in the Nm* values, suggesting two distinct groups of
populations in P. rigida. The trends that were found in pitch pine appear to
dominate in Eucalyptus caesia ssp. caesia, and ssp. magna, but differed in details.
‘The average Nm* value for Eucalyptus caesia ssp. caesia was 0.760, and elimination
of populations, singly or in combinations, indicated low to medium levels of gene
flow. O n the contrary, elimination of populations in ssp. magna made the N m *
values oscillate from low (0.156) to extremely high values (25.30).
DISCUSSION
This study represents a broad range of forest tree species with different
breeding systems, and the gene frequency data were obtained by several
investigators. There is inevitable variation among data sets and sampling
strategies employed; as Harpending ( 1974) pointed out, “one investigator’s
subdivision might be another’s total sample”. Therefore, the results can only
permit certain generalizations on gene flow levels, characteristic of this group of
organisms. Accordingly, gymnosperms and oaks showed high levels of long
distance gene flow irrespective of the sampling strategies employed. High levels
of gene flow through pollen dispersal has been reported by several workers.
354
D COVINUARAJU
Lanner (1966) indicated that pollen dispersal in conifers may cover many miles
under proper environmental conditions. Similarly, Ledig & Fryer ( 1972), based
on their studies of Pinus rigida, noted the importance of long distance migration
in microevolution of forest trees. O n the other hand, the levels of gene flow for
angiosperms differed, as expected. All the angiosperm species (except oaks)
examined are pollinated by birds and insects; thus i t is likely that gene flow levels
would vary depending upon pollinator behaviour. For instance, species such as
Eucalyptus caesia ssp. magna show relatively high gene flow, while populations of
Lisszanthus skinnerii (Sytsma & Schaal, 1985) showed low gene flow levels. Pollen
flow in I,. skinnerii is mediated by insects among flowers, within or among
individuals within populations rather than among populations (Sytsma &
Schaal, 1985) which agrees with the fact that pollinator behaviour is known to
influence pollen dispersal in many animal-pollinated systems (Levin, 1981 ;
Handel, 1983).
The results of this study suggest that a single population or sets of populations
may have gene flow levels distinct from other populations in a species range, and
each species may be a concatenated system of populations bound by gene flow.
For example, Slatkin’s (1985a) approach showed that the H M and BR
populations of Pinus rigida were relatively distinct from others in the species’
range. Additionally, it also detected two major constellations of populations-populations in and around the pine barrens (HM-WP-EP-LL), and
populations located toward the south-western part (BP-SS-BR-BG) of New
Jersey (Fig. 2A). Ledig & Fryer (1972) recognized a pocket of variability for
cone serotiny in P. rigida, which included HM-WP-EP-LL populations, and
reported that gene frequency for cone serotiny (apparently controlled by a single
gene) decreased to zero within 200 miles of these populations. They attributed
the maintenance of a cline for cone serotiny around these populations to long
distance gene flow through pollen and seed dispersal balanced by selection.
Thus, it is likely that, in any given species, one or more populations might be
influencing the overall levels of gene flow in parts or all of the distributional
range. I t has been theoretically demonstrated that differential migration of
groups of related individuals could lead to “disproportionate effects on the
genetic population structure” (Rogers & Jorde, 1987) of a species. Populations,
from an evolutionary viewpoint, are similar to groups (Slatkin, 1981b); thus high
migration rates among subpopulations could lead to intergroup selection
(Harpending & Rogers, 1987). Hypothetically then, disruption of a
concatenated system, or destruction of ‘key’ populations that have dominating
effects on the overall levels of gene flow (e.g. Pinus rigida populations from the
Pine Barrens of New Jersey) may lead to changes in the genetic structure either
in a region or in the entire distribution range of an entire species. This was
demonstrated by artificially removing certain populations from the analyses of
gene flow. T h e effect was more evident in angiosperms than i t was for
gymnosperms. This may be due to the fact that high levels of long distance gene
flow may lead to slight or no apparent differentiation obscuring smaller
differential fitnesses among local populations in gymnosperms (Ledig & Fryer,
1972).
Analysis of gene flow in relation to population structure of Eucalyptus caesia ssp.
caesia and ssp. magna revealed some interesting patterns which agreed with the
ecological and biological peculiarities of these species (Fig. 2B). Both subspecies
G E N E FLOW I N FOREST m E E s
:355
arc bird-pollinated and occur together in isolated clusters among the granitic
outcrops of south-western Australia. However, ssp. magna has slightly larger
flowers atid fruits than ssp. caesia. T h e former subspecies (magna) showed greater
diversity i n the gene flow estimates than the latter, suggesting a possible bias i n
pollen flow within these subspecies. These differences in the relative amounts of
gene flow among populations between two closely related/located subspecies
perhaps could be attributed to variations in pollinator behaviour leading to
difYerential pollen flow. This pattern is consistent with the recent reports on
dinerential pollen flow due to pollinator behaviour in two closely related tropical
herbs, Rizisea spicata and Hausteinia blepharorachis (Linhart et al., 1987).
‘I’he above conclusions are contingent upon the method of analysis. Slatkin’s
(1981a, l98.h) methods are useful for species with a large number of private
alleles. However, as Waples (1987) has pointed out, such ideal conditions are not
always satisfied because of biological peculiarities of species. In such cases,
however, estimation of gene flow using F,, or G,, values could be used as an
alternative (Slatkin personal communication, 1987). Furthermore, i t may be
virtually impossible to distinguish between current levels of gene flow and the
historicity associated with private alleles. This problem is pervasive, not only in
the present investigation but also in previous studies of gene flow (Larson et al.,
1984; Slatkin, 1985a; Caccone, 1985; Waples, 1987; Golenberg, 1987), and in
virtually all studies dealing with the estimation of gene frequencies (Hamrick et
al., 1979; Ledig, 1986). T h e levels of gene flow in this study have been
interpreted on the basis of pollen dispersal abilities. Although this interpretation
in general holds (Govindaraju, 1988a), pollen dispersal abilities measured by
using outcrossing rates may underestimate actual levels of gene flow in natural
plant populations (Govindaraju, 198813).
While the indirect estimates of gene flow in this study provide data for
generalizing the importance of relative measures of gene flow among spccies with
different life histories, they also give insights regarding the relative importance of
population (s) and subtle differences associated with migration patterns among
closely related species and populations. These observations corroborate Handel’s
(1983) view that the pollination biology of a species, particularly the amount of
cross pollination, is not constant among populations: “different sizes, densities
and shapes of populations of the same species can elicit different responses from
pollinators and differences in the amount of pollen that is transferred”.
Slatkin’s approach generally agreed with the previous reports on the
relationship among long-distance dispersal, maintenance of clines and
population differentiation in conifers, particularly in Pinus rigida. T h e results
were also consistent with biological and ecological characteristics in
angiosperms, a s shown in Eucalyptus caesia ssp. caesia and ssp. magna. Longdistance dispersal of up to 10 km was reported by Coyne & Milstead (1987) in
Ilrosophila melanogaster. They postulated that populations of I). melanogaster in
North America consist of demes that are regularly connected by migration,
leading to considerable gene flow among them. Using Slatkin’s approach, Singh
& Rhomberg (1987), working on the same species, reached similar conclusions.
Pine seed is capable of transport to distances of 18 kilometres (Bannister, 1965).
A close relationship between gene flow ( N m ) and dispersal abilities was reported
by Caccone (l98.5), Waples (1987) and Govindaraju (l988a), for cave
arthropods, shore fishes and plants, respectively. Additionally, the present study
356
D. GOVINDARAJU
has indicated that analysis of gene flow at interspecific levels would mask the
gene flow patterns among populations within species, as pointed out by Caccone
(1985). Therefore, a combination of direct and indirect methods coupled with
broad surveys encompassing numerous populations, species and genera will be
useful for a further understanding of the interplay between gene flow and genetic
differentiation in forest tree species.
ACKNOWLEDGEMENTS
My greatest debt rests with all the authors of published papers, and to my
friends for generously sharing their unpublished data used in this study. I am
grateful to Prof M. Slatkin for discussions and suggestions on an earlier draft of
this paper; to Drs Furner and Wagner, and an anonymous reviewer for
comments; and to Ms B. L. Kamala for help during the analysis of data. Mrs
Inda Kidd typed this paper.
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