Biological Journal of the Linncan Socicly (1993), 49: 239-248. With 3 figures
Interspecfic size and number variation in
pollen grains and seeds
WILLIAM D. J. KIRK
Department of Biological Sciences, Keele Universily, Keele, Slafordshire ST5 5 B G
Rcceiued 31 March 1992, accepled for publication I4 M a y 1992
An interspecific correlation between pollen grain size and seed size is demonstrated by means of the
phylogenetic regression, which allows for phylogenetic bias. The correlation was not explained by
plant size, mass of DNA per cell, style length or breeding system, although the first three of these
factors all correlated with both pollen size and seed size. Two interpretations, involving pollen
competition and flower size, are discussed. There is also an interspecific correlation between pollen
grain number per flower and ovule number per flower. Some consequences of these correlations for
the interpretation of pollen-ovule ratios and sex allocation strategies are considered.
ratio - flower
ADDITIONAL KEY WORDS:-Pollen-ovule
allocation.
CONTENTS
Introduction . . .
Materials and methods
Statistical analysis
Plants
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Flowers . . .
Seeds
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Compositae . .
Cruciferae . .
Results . . . .
Discussion
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Acknowledgements .
References
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sex
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INTRODUCTION
The mean seed size of a species has many repercussions for the reproductive
ecology of plants (Harper, Love11 & Moore, 1970). Seed size is linked with
habitat characteristics such as soil disturbance, shade and drought (Salisbury,
1942; Baker, 1972). It is also linked with dispersal ability and survival in seed
banks (Grime, Hodgson & Hunt, 1988). Taxonomic constraints appear to have
reduced intra-familial variation (Hodgson & Mackey, 1986), while
developmental constraints may be responsible for correlations of seed size with
fruit size, flower size and plant size (Primack, 1987; Silvertown, 1989).
Variation in the mean pollen grain size of a species is less well understood. The
main factor historically linked with pollen size is style length, but the
interpretation remains controversial with evidence for and against a causative
239
0024-4066/93/070239+ 10 ,608.00/0
0 1993 The Linnean
Society of London
240
W. D. J. KIRK
link (Darwin, 1877; Cruden & Lyon, 1985; Williams & Rouse, 1990; Cruzan,
1990), although differences between binucleate and trinucleate pollen may have
caused some confusion (Bertin, 1988). Cruden & Lyon (1985) showed that
pollen size could instead be reflecting stigma depth, the distance a pollen tube
has to grow to reach exogenous resources. If so, the assumption that pollinator
size determines style length and hence pollen size (Taylor & Levin, 1975; Lee,
1978) is considerably weakened. A variety of other influences on inter-specific
differences in pollen size have been suggested. They include: aerodynamic
constraints for wind-pollinated and buzz-pollinated species (Whitehead, 1969;
Muller, 1979), polyploidy (Levin, 1968; Muller, 1979), breeding system
(Pandey, 197 l ) , longevity (Cruzan, 1990), the pollen population effect (Cruden
& Miller-Ward, 1981), pollinator dietary requirements (Baker & Baker, 1979)
and competition between pollen grains (Willson & Burley, 1983).
Seeds and pollen can be considered in the context of evolutionary trade-offs
between size and number (Smith & Fretwell, 1974; Lloyd, 1987, 1988). These
trade-offs cover an enormous size range for plant propagules (Haig & Westoby,
1991). In the British flora, the largest seeds are at least 100000 times as heavy as
the smallest and the largest pollen grains have at least 1000 times the volume of
the smallest. However, investigations of pollen-ovule number ratios (P/Os) in
relation to pollination mechanism and breeding system have generally not taken
into account the direct effect of a size-versus-number trade-off on PI0 variation
(Cruden, 1977; Cruden & Miller-Ward, 1981). Charnov (1982) gives an
equation linking PI0 with pollen size and seed size, assuming size-versus-number
trade-offs and ovule number equal to seed number:
'J
log ( P / O )= log (1-
+ logC*-logC,
where r is the proportion of reproductive resource allocation given to pollen, C, is
the cost of a seed and C,is the cost of a pollen grain. Charnov (1982) pointed out
that, assuming seed size shows no systematic interspecific variation with pollen
size, this equation may be sufficient to explain negative correlations between P I 0
and pollen size (Cruden & Miller-Ward, 1981) and positive correlations between
P/O and seed size (Shaanker & Ganeshaiah, 1984; Preston, 1986). Queller
( 1984) developed Charnov's equation to show that correlations between P/Os
and four pollination and breeding system factors can be interpreted in terms of
evolutionary models of optimal allocation of resources to male and female
functions, rather than in terms of efficiency (see Cruden, 1977; Cruden &
Miller-Ward, 1981).
In this paper, I show that seed size does show an interspecific correlation with
pollen size and I investigate several interpretations of the relationship. An
understanding of the links between seed size, seed number, pollen size and pollen
number is relevant to studies of sex allocation strategies in hermaphrodite plants.
MATERIALS AND METHODS
Statistical analysis
The phylogenetic regression of Grafen (1989) was used because it allows for
phylogenetic bias in cross-species data (Page1 & Harvey, 1988) and permits one
POLLEN AND SEEDS
24 I
to control for other variables. The method needs a ‘working phylogeny’. For this
analysis, the phylogeny was constructed from a published classification, with
each of the named taxa in the classification (the genera, families etc.) forming
the nodes in the phylogeny. The distances between nodes (path segment lengths)
were assigned by the ‘taxonomic levels method’. Nodes at successive taxonomic
levels were assigned the numbers 1, 2, 3 etc. and path segment lengths calculated
from the differences in these values. The distances were power transformed and
used to provide a set of variances and covariances for the regression (see Grafen,
1989). Non-independence between species is divided into that which is and that
which is not due to associations represented in the working phylogeny. The
former is dealt with by developing the standard regression and the latter by
using each node of the phylogeny as an independent data point. The error
degrees of freedom depend on the number of nodes in the phylogeny and not the
number of species involved. Generalized least squares lines of fit are plotted.
Values o f ? are quoted to show how much variance is accounted for, but the
implied P-values are not reliable tests of the regression. Results were computed
by means of a program (version 1.03) in GLIM, supplied by A. Grafen (personal
communication, 1991). All sizes and masses were log,,, transformed.
Plants
The analyses of English species were restricted to angiosperm species listed in
the flora of the central English county of Warwickshire (Cadbury, Hawkes &
Readett, 1971). As part of further studies not reported here, species were
excluded that were escapes, introduced, planted, naturalized, casuals, relics of
cultivation or non-native, according to Cadbury et al. (1971), or that were
water-pollinated or exclusively apomictic, according to Faegri & van der Pijl
(1979) or Proctor & Yeo (1973). The full analysis included 610 species in 81
families. The number of species for which data could be obtained are given in
parentheses for each variable below. The classification of genera given by
Cadbury et al. (1971) and of tribe, sub-family, family, order and sub-class given
by Clapham, Tutin & Moore (1987) was used in the phylogenetic regression.
Plant size (584 spp.) was obtained from the mid-range normal fully grown plant
height or stem length given by Clapham et al. (1987). Floating, creeping or
climbing species were not directly comparable and were omitted. DNA content
(191 spp.) was obtained from the mass of 2C DNA per nucleus in root-tip cells
given by Grime et al. (1988).
Flowers
Pollen grain size (559 spp.) was obtained from the length of the long axis of
acetolysed grains in silicone oil recorded by Andrew ( 1984). Volumes could not
be used in the analysis because the lengths of the short axes were not available
for calculating the volumes of the non-spherical grains. The mid-range size was
used for species with more than one size of pollen. Tetrad sizes were divided by
two to obtain grain sizes. Seven species omitted by Andrew were measured from
specimens in the Department of Geography, Keele University and the
Department of Botany, University of Cambridge. Species were categorised by
pollination mechanism according to Faegri & van der Pijl (1979), Proctor & Yeo
W.D. J. KIRK
242
(1973) and Clapham et al. (1987) into wind-pollinated (167 spp.) and insectpollinated (all others) (443 spp.).
Seeds
Seed size classes (403 spp.) were taken from the data of Grime et al. (1988) for
the air-dried mass of a single seed, achene or other indehiscent germinule: 1
( < 0.20 mg), 2 (0.21-0.50 mg), 3 (0.51-1.00 mg), 4 (1.01-2.00 mg), 5
(2.01-10.00 mg), 6 ( > 10 mg). These classes reduce the effect ofoutliers and are
roughly logarithmic.
Compositae
Pollen size (60 spp.), plant size (61 spp.) and mass of DNA (22 spp.) were
obtained as above. Pollen volume was calculated from pollen length, d, with the
,
the grains are spherical or nearly so. Seed mass (29 spp.)
formula ( n / 6 ) d 3 since
was taken from the 'germinule mass' (air-dried) given by Grime et al. (1988).
Style length (63 spp.), from the apex of the ovary to the base of the stigma, was
measured from the botanical drawings of Ross-Craig ( 1960-1 963). Breeding
systems (24 spp.) were divided according to Grime el al. (1988) into three classes:
out-crossing, both selfing and out-crossing, and predominantly selfing, scored 1,
2 and 3, respectively.
Cruciferae
The data of Preston (1986) for 66 Californian taxa were used. Numbers of
ovules and seeds were log,, transformed. Phylogenetic regressions were
performed as above, with the classification into genera and species used by
Preston ( 1986).
RESULTS
The regression of pollen size on seed size class was significant (F,,,35= 38.0,
P < 0.001, N = 375, ?(3,3, = (+)0.10) (Fig. 1). A similar result held within just
0
0
0
'"
6
1
2
3
4
6
6
Seed size class
Figure 1. Pollen grain length plotted against seed size class, log,,T= 0.027 log,,X+ 1.334. Key:
dicots ( 0 )monocots
;
Points have been offset for seed size class to reduce overlap.
(v).
POLLEN AND SEEDS
243
1001 A
1
0.1
':'obc8c\P81.0
W
'
10.0
DNAW
Figure 2. A, Pollen grain length plotted against the mass of 2C DNA per nucleus in root-tip cells,
log,,T = 0.071 log,,X+ 1.378. B, Seed size class plotted against the m a s of 2C DNA, log,,?'= I .016
logI,X+2.73l. Key: dicots (a);monocots (V).
Points have been offset for seed size class to reduce
overlap.
the wind-pollinated species ( F l , 3 3 = 24.0, P < 0.001, N = 107,
= (+)0.20)
and just the insect-pollinated species (F,,%= 21.0, N = 268, P < 0.001, ?(2ss) =
(+)0.08).
Developmental constraints might account for this correlation if plant size
constrains seed size and pollen size, perhaps through a constraint on flower size.
The regression of seed size class on plant size was significant (F,,,,,= 22.2,
P < 0.001, N = 385, r2 383) = (+)0.06), confirming the findings of others (see
Silvertown, 1989), but the regression of pollen size on plant size was only weakly
= 6.0, P = 0.02, N = 537, ?(535) = (+)0.01). The regression of
significant (F1,183
pollen size on seed size class was virtually unchanged by controlling for plant size
(F,,,37= 35.4, P < 0.001, N = 359, ?(356) = (+)omlo).
The amount of DNA per cell might account for the correlation. Polyploid
forms of plants have larger pollen grains (Levin, 1968; Muller, 1979), suggesting
that the amount of DNA constrains pollen size. The regression of pollen size on
= 8.6, P = 0.004, N = 181, ?(179) =
mass of DNA per cell was significant
(+)0.05) (Fig. 2A). Plants with early spring growth have more DNA per cell
(Grime, Shacklock & Band, 1985; Thompson, 1990), and such plants might also
have larger seeds with more endosperm to allow them to grow faster and sooner
(Stanton, 1984). Polyploid seeds also weigh more (Salisbury, 1942). The
regression of seed size class on mass of DNA per cell was also significant
( F I , 6 1 = 12.4, P < 0.001, N = 180, ?(178) = (+)0.07) (Fig. 2B). However, the
W. D.J. KIRK
244
60 O O O L A
f
fBB
0
0.
/
0
v
v
a 10 000
-@
a
d
EiO00
$ 6000&
//
-0
---'
0
ow
0
,a
1
I
I
10.0
1.0
0.1
Seed mass (mg)
60 000
f
v
B
c
(
g 10 000
Q
c
(
&
6000
0
Style length (mm)
0
Style length (mm)
Figure 3. Species in the Compositae. A, Pollen grain volume plotted against seed mass, log,,Y =
0.349 logIJ+4.22l. B, Pollen grain volume plotted against style length, log,,Y = 0.418
log,,X+3.811. C, Seed mass plotted against style length, log,,Y = 1.020 log,,X- 1.168. Key:
;
(V).
Asteroideae ( 0 ) Cichorioideae
regression of pollen size on seed size class remained significant when controlling
= (+)0.10) or
for mass of DNA (F1,77= 14.5, P < 0.001, N = 171,
controlling for plant size and mass of DNA (Fl,75
= 12.1, P < 0.001, N = 166,
'(162)
= (+)o'09)'
Some further factors were examined for the family Compositae. The regression
of pollen volume on seed mass was just significant (Fl,,o= 5.7, P = 0.04, N = 27,
?(25) = (+)0.25) (Fig. 3A).
Style length often correlates with pollen size (see Introduction). The regression
POLLEN AND SEEDS
245
of pollen volume on style length was significant for Compositae (Fl,17
= 6.2,
P = 0.02, N = 60, ?,58, = (+)0.10) (Fig. 3B), as also was the regression of seed
= 6.5, P = 0.03, N = 29, ?(27) = (+)0.22) (Fig. 3C).
mass on style length (Fl,ll
However, the regression of pollen volume on seed mass was still significant when
= 10.6, P = 0.009, N = 27, ?(24) = (+)0.25).
controlling for style length (F,,lo
The relationship between breeding system and pollen and seed sizes is of
particular interest because of the correlation between breeding system and PI0
(see Introduction). The regression of pollen volume on breeding system was not
significant (F,,9= 3.13, P = 0.1 1, N = 23, r2(21)= (+)0.03) and the regression of
seed mass on breeding system was not significant (Fl,l,= 0.34, P = 0.57, N =
24, 8(22)
= (+)0.01). However, the available breeding system data are rather
imprecise.
The relationship between number of pollen grains per flower and number of
ovules per flower was tested with the data of Preston (1986) for 66 crucifer taxa.
Standard regressions, which allow comparison with Preston’s analysis, were
highly significant for 37 self-compatible taxa ( t ( 3 5 )= 5.5, P < 0.001, ?,, =
(+)0.47) and for 29 self-incompatible taxa
= 7.3, P < 0.001, ?(27) =
(+)0.66). Phylogenetic regressions of pollen grains per flower on ovules per
= 11.8, P = 0.006, ?(35) =
flower were also significant for these two groups (Fl,lo
(+)0.29 and F,,6= 62.4, P < 0,001, ?(2,) = (+)0.65 respectively).
DISCUSSION
Pollen size and seed size are positively correlated over a wide range of species.
Although plant size, mass of DNA and style length correlate with both of them,
these factors do not appear to account for much of the pollen-seed size
correlation.
However, caution is needed in interpreting the role of a factor that is not
significant or that does not account for a correlation, since this could be just the
result of few or imprecise data for that factor. This is most likely for the breeding
system data. Better experimental data on the frequency of self-fertilization in
plants would be useful.
Willson & Burley (1983) have argued that where pollen competition is low,
there should be minimal investment per pollen grain, but where pollen
competition is high, pollen should be investment rich. There is some
experimental evidence that larger pollen grains are more competitive. Larger
grains can have higher rates of tube elongation (Lord & Eckard, 1984; Williams
& Rouse, 1990) and higher rates of ‘post-fertilization siring ability’ (Cruzan,
1990). Such post-fertilization zygotic advantages might even be reflected in
germination rates and seedling growth. Correlations between gametophytic and
sporophytic qualities are already known (Mulcahy, 1983). This suggests a
possible interpretation of the pollen-seed size correlation. For any particular
male/female allocation of resources, if seed number per flower decreases as a
result of selection for larger seeds, then there will be more competition between
pollen grains. The same number of pollen grains would be competing to be the
parents of fewer seeds. If larger grains are more competitive, this could favour
larger pollen when seeds are larger. Unfortunately, there is a paucity of data on
paternal performance (Bertin, 1988) and it is not possible to test this hypothesis
with existing data.
246
W. D. J . KIRK
An alternative interpretation is that seed size and pollen size are constrained
by flower size. Although there was no evidence for a constraint imposed by plant
size, direct measures of flower size would be a much better test. Several could be
tried. Style length is a good measure of floret size in the Compositae, but this size
measure did not account for the pollen-seed size correlation within the
Compositae.
The number of pollen grains per flower (P) and the number of ovules per
flower (0) are highly correlated in the Cruciferae. The same trend is apparent
across ten families in the data of Cruden & Miller-Ward (1981). This number
correlation is likely to be mainly accounted for by the variation in total male/
female resource allocation per flower, rather than by correlated size-versusnumber trade-offs in pollen and seeds. More comprehensive data could elucidate
to what extent either or both of these independent trade-offs are involved.
Increased reproductive resource allocation per flower appears to be manifested
interspecifically by an increased number of pollen grains rather than by an
increase in their size (Cruden & Miller-Ward, 1981). The same may be true for
seeds. However, if the sizes of pollen and seeds were both increased by higher
resource allocation, this could explain the pollen-seed size correlation.
Developmental constraints might do this, as proposed for some other size
correlations (see Introduction). An adaptive interpretation would need to explain
why the optimum seed size and pollen size for a species would be higher when
more resources are available per flower.
Pollen-seed correlations can affect the interpretation of cross-species data.
A strong pollen-seed number correlation would give a high covariance of logP
and logo, which would considerably reduce the variance in log(PI0). If this
covariance arises from variation in total resource allocation, the reduced
variance of log(P/O) would expose variance from other sources, such as maleversus-female or size-versus-number trade-offs. The variance from size-versusnumber trade-offs might also be reduced a little by the pollen-seed size
correlation, since pollen and seed sizes do not vary independently. Reduction of
a large total resource allocation variance and consequent exposure of a maleversus-female trade-off variance probably accounts for Preston’s ( 1986) finding
that log(P/O) was a better indicator of breeding system than logP or log0 alone.
Queller (1984) considered that the data of Cruden & Miller-Ward (1981) could
not be explained by a ‘simple trade-off between pollen size and number’ because
the correlation between logP and log(pol1en size) was not significant, while that
between log(P/O) and log(pol1en size) was. My argument above suggests that in
surveys covering a wide range of total resource allocation per flower, use of
log(P/O) instead of logP could be more, rather than less, likely to expose a sizeversus-number trade-off for pollen. Comprehensive data for the size and number
of pollen grains and seeds for a wide range of species would allow these ideas to
be tested further.
ACKNOWLEDGEMENTS
Facilities were provided by: the Department of Biological Sciences and the
Department of Geography, Keele University; and the Department of Botany,
University of Cambridge. I thank the following for help and advice:
POLLEN AND SEEDS
247
S. A. Corbet, A. Grafen, P. W. Jones, S. Peglar, A. Polwart, A. S. Pullin and
P. A. Thomas. I am grateful for the comments and suggestions of the referees.
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