Download Resource allocation to growth, reproduction and survival in

J. evol.
Biol.
4: 291-307
IOIO-061X/91/02291-17
e 1991 BirkhIuser
(1991)
Resource allocation to growth, reproduction
Gladiolus : The cost of male function
Catherine
Rameau’l 3, and Pierre-Henri
$ 1.50 +0.20/O
Verlag, Base1
and survival
in
Gouyon*
‘Institut National de la Recherche Agronomique, Station d’amtlioration
des plantes
Jlorales, Frejus 83600, France ‘Universite
de Paris&d,
Laboratoire d’evolution et
systematique vtgetales, Bcit.362, 91405 Orsay cedex, France 3Present address: Institut
National de la Recherche Agronomique,
Station de Genetique, Route de St-Cyr,
Versailles 78000. France
Key words:
Resource
allocation;
trade-off;
pollen; Gladiolus
Abstract
Theoretical models of life-history evolution assume trade-offs between present and
future reproduction and/or survival. Models of the evolution of sex assume trade-offs
between male function and female function. Generally, experiments designed to
evaluate the cost of reproduction
on other functions tend to ignore male function.
The present work on Gladiolus takes into account simultaneously
the different
primary functions of the plant and separates sexual reproduction
into one male
component (pollen production)
and one female component (seed production).
The study of environmental (within-clone),
between-clone and genetic correlations
using strains of Gladiolus and principal component analysis show that trade-offs exist
between male function, female function and survival, including both characters of
plant vigour, perennation (corm production)
and vegetative propagation (cormel
production).
Phenotypic correlations,
using different species and species-hybrids,
have been obtained which confirm these results. In particular, these results underline
the importance of the impact of pollen production on the other functions.
Introduction
Theoretical studies of life-history
evolution assume trade-offs between primary
functions,
because of limited resources available to organisms.
Given certain
constraints
(morphological,
physiological,
ecological), life-history
theory predicts
291
292
Rameau
and Gouyon
the optimal age-specific allocation of resources to growth, survival and reproduction (Charlesworth, 1980, p. 237). Bell (1984a) summarizes the different experiments which have attempted to detect and evaluate reproductive cost. He argues
that the results of these experiments are not all relevant. In his own experiments
(Bell, l984a, 1984b), designed to critically evaluate the cost hypothesis, the correlations between present reproduction and future reproduction or survival were zero
or positive in almost all cases. The reproductive cost hypothesis, however, would
imply an overall negative correlation between all functions of the plant. Valuable
criticisms of Bell’s experiments have been provided by Reznick et al. (1986). In
particular, they contend that correlation between the mean values of different clones
(Bell’s “acquired cost”), which is “roughly equivalent” to genetic correlation, is the
only appropriate estimate of reproductive cost. But even this correlation must be
interpreted with caution becauseit includes a between-group environmental component (Falconer, 1981, p. 144). In Bell’s experiment, this component may be high. He
worked on six speciesof invertebrates which all reproduce asexually. The effect of
the shared maternal environment may have contributed to the variance between the
means of different clones.
Bell’s paper concerns experiments on animals. In plants, despite the importance
of trade-offs in the prediction of theoretical models on the evolution of sex
(Charnov, 1982) or on life-cycle evolution, few experimental studies have been
undertaken. Measuring allocation patterns raises many questions, e.g. How can the
investments be estimated : through biomass allocation (Lovett Doust and Cavers,
l982), energy investment (Smith and Evenson, 1978) or mineral allocation (Abrahamson and Caswell. 1982; McKone, 1987)? Which part of the plant should be
considered? It is not always easy to separate reproductive from vegetative parts of
the plant, or to assign a floral structure to either the male or the female function
(Stanton et al., 1986; Stanton and Preston, 1988a). Willson (1983, p. 23) has
discusseddifferent attempts made to estimate reproductive effort in plants.
In hermaphroditic plants, experimental studies of trade-off phenomena usually
ignore male function (pollen production), because of the difficulty of quantifying
the male component of fitness (Sutherland and Delph, 1984). Thus, reproductive
effort is most often measured by the ratio of reproductive organ biomass to total
plant biomass, or by seed production. However, the model of Charnov et al. ( 1976)
on sex investment in hermaphrodites emphasizes the importance of male function
since it assumesa trade-off between female function (egg production and seed
maturation) and mate function (pollen donation).
Despite these shortcomings, some interesting results have been obtained from the
few studies conducted on hermaphroditic plants. Primack and Antonovics (1982),
using Plantago,
demonstrated a compensation between vegetative growth and
sexual reproduction. Furthermore, with regard to the cost of male function to other
functions of the plant, it has been shown that female (male-sterile) plants often
produce more seedsthan hermaphrodites (Darwin, 1877; Vear, 1984; Couvet et al.,
1985; Kohn, 1989). Darwin (1877) explained this latter effect of a “compensation
law”, i.e. in male-steriles the resources not invested in pollen production are
reallocated to seed production. This implies that male function has a negative
Growth,
reproduction
and survival
in gladiolus
293
impact on female function. In addition, male function may also have an impact on
survival: Van Damme (1985) noticed in gynodioecious species of Plantago that
survival was significantly greater for male-steriles than for hermaphroditic
individuals. Recently, Couvet et al. (in preparation), using Thymus wfgaris L., have found
a negative between-family correlation between seed set and number of full pollen
grains in a flower, despite a positive within-family
correlation owing to a plant
vigour effect. Although
they merit attention, none of the above studies has
simultaneously
taken into account each of the different functions of interest, i.e.
growth, survival, asexual reproduction, female and male functions. As noted by
Stanton and Preston (3988b), the whole-plant level has to be considered when
studying interactions between male and female allocation. This fact becomes clear
if we bear in mind the following: Imagine a species in which there is genetic
diversity for the system determining
resource allocation to male, female and
survival functions. A study of the male/female allocation ratio which does not take
survival into account would show positive or negative genetic correlations, depending on the relative importance of the variation in reproduction/survival
or male/
studied.
If the variation
in the
female investment
in the population
reproduction/survival
ratio is high compared with the variation in male/female
investment, a positive genetic correlation will be found between male and female
investment. Finally, it should be noted that it will be even more difficult to interpret
the results when studies do not allow clear discrimination
between genetic and
environmental
effects (e.g. Ross, 1984).
It is clearly necessary, therefore, to study the way in which all functions interact,
in order to study the cost of male function. This is the aim of the work reported
here on Gladiolus, a genus chosen because it permits easy measurement of the main
functions of the plant, i.e. growth, survival, asexual reproduction, female and male
functions.
Materials
and methods
In Gladiolus, specific organs are concerned with specific stages of plant development. The corm is an annually replaced, tuberous stem. It is formed by a swelling
of the basal internodes of the flower stalk. After planting, one or two upper buds
on the corm develop into shoots. The apex differentiates into foliage leaves which
have a vegetative function. Later an inflorescence differentiates and enables sexual
reproduction
to occur. Finally, filling of the new corm and of cormels occurs
(cormels are buds formed at the end of stolons, between the old and the new corm,
which allow vegetative reproduction).
It is possible, therefore, to describe the life-history of this plant in two different
ways : (i) as an annual which can reproduce vegetatively (corms, cormels) and
sexually (seeds, pollen); (ii) as a perennial because of the dynamic relationship
between the corm and the aerial part. The corm is in this case an organ of survival.
This perennial plant can reproduce sexually (seeds, pollen) and asexually (cormels).
For the purpose of this paper, we will consider the latter view. Furthermore, in
294
Rameau
and Gouyon
Gladiolus the organ of survival (the corm) and the organs of asexual reproduction
(cormels) are easily identified. Also, stamen sampling and ovule counting are
relatively easy tasks as Gladiolus is an ornamental plant in which artificial selection
has contributed to the existence of large flowers.
Cultivated forms of Gladiolus have been developed from plants originating in the
Mediterranean region and in Africa, which were introduced into Europe during the
18th and 19th centuries. There are two main groups of cultivars: summer hybrids
with large flowers derived from hybridization between African intertropical species,
and spring hybrids derived from crosses between diploid South African species.
Summer hybrids are tetraploid while spring hybrids are diploid or triploid. Both
forms frequently show irregular meiosis and sterility.
Two types of material were studied:
1. Clones (vegetatively propagated) of summer Gladiolus (G. grandzjlorus Hort.),
tetraploid (2n = 4x = 60), were planted in two trials described in Table 1. The first
experiment included 13 strains and six hybrids from INRA
Landemeau. The
second experiment included eight clones. Each clone was represented by 12 plants
in two randomized replications. Hand-pollinations
were carried out with a mixture
of pollen removed the same day from flowers of the different clones. Generally,
three flowers on the main spike were pollinated.
2. In a third experiment, a wild species (G. tristis L.) and two hybrids between
wild species from South Africa, diploid (2n = 30), belonging to the genera Gladiolus
and Homoglossum were studied. These two hybrids are called by horticulturists
Homoglad (G. tristis L. x H. watsanium Thunb.) and Christabel (G. tristis L. x G.
uirescens Thunb.). For each species or hybrid, 40 individuals were planted on 13
November 1985 at a density of 40 plants per square meter. Unlike the previous
material, these plants were not clones. Each individual was obtained by vegetative
propagation of an individual derived from a seed. Each flower was also hand-pollinated with pollen removed from flowers of different plants of the same species or
hybrid.
Experiments were conducted in a glasshouse. Plants were grown in ground. They
were irrigated and fertilized as in commercial production.
A minimum temperature of 10” C was maintained throughout the experiments.
Data were recorded plant by plant, usually at the level of the first spike.
Table
1. Description
Planting
date
Planting
density
First flowering
Last flowering
Corm harvest
of experiments
with
summer
Gladiolus
Experiment
1
( 19 clones)
28/01/85
40 plants/m2
End of April
Mid June
End of August
Experiment
2
(8 clones)
12/12/85
20 plants/m2
End of March
Beginning
of May
Beginning
of July
Growth,
Table
PCW:
D:
NF:
SPIKE:
TFL:
HSTEM:
NSTEM:
WLEAF:
NLEAF:
HCW:
GRO:
HKW:
ovu:
NSEED:
WSEED:
POLL:
reproduction
2. Measured
and survival
295
in gladiolus
Characters
planted corm weight
days from planting
to flowering
number of Rowers on the main stem
spike height
total number
of flowers per planted corm
main stem height
total number
of stems
leaf width
number
of leaves
harvested
corm weight
ratio of harvested
corm weight to planted
harvested
cormel weight
number
of ovules per flower
number
of seeds per fruit
seed weight per fruit
number
of full pollen grains per flower
corm
weight
The following characters were recorded (Table 2): weight of the planted corm
(PCW), days from planting to flowering (D), height of the first stem (HSTEM),
number of flowers on the main stem (NF), total number of stems (STEM), total
number of flowers per planted corm (TFL), number and width of leaves (NLEAF,
WLEAF).
The last two characters were not recorded for the diploid material which
has leaves that are too thin and often curly. Characters
of tuberization
were
estimated by the increase in corm weight (GRO), i.e. the ratio of harvested corm
weight to planted corm weight, and also by the harvested cormel weight (HKW).
The full pollen grains in a Bower were counted on each wild individual and on six
individuals per clone for the cultivars. Two of the three stamens of a basal flower
were collected and stored before pollen release. Pollen fertility, that is full pollen
grain percentage, was estimated by acetic carmine staining of pollen. The total
number of pollen grains was determined on a half stamen following the technique
of P. Cour and P. Richard
from the palynology
laboratory
of U.S.T.L.
in
Montpellier.
The last two measurements provide an estimation of the number of
full pollen grains per flower (POLL).
Female function primary characters were
estimated from the number of ovules in a flower (OVU), number of seeds (NSEED)
and seed weight per flower (WSEED).
Correlations
calculated between each pair of characters
were separated into
within-clone
and between-clone
correlations.
The within-clone
correlation matrix
comes from a discriminant
analysis. Genetic correlations
were estimated from
variance and covariance components. The significance of these genetic correlations
was established using a permutation test. According to Scheffe (1959), we adapted
the permutation test to our experiment. Suppose we want to know the significance
of the genetic correlation coefficient between 2 variables X and Y observed on N
296
Rameau
and Gouyon
clones with b plants in each. Let the vector x, be defined as xi = (xi,,. . .,xib), where
xij is the value of variable X measured on individual j in clone i. Let X be the
vector of all values for all clones: X = (x,,. .,x,). Similarly,
one can define
Y, = (Y,lr. * .,ylb) where y,j is the value of variable Y measured on individual j in
clone i and the vector Y = (y,, . . .,yN) of the variable Y observed on the N clones.
The observed genetic correlation coefficient to be tested was calculated from the
two vectors X and Y. The idea of the permutation
test is to calculate a sample of
genetic correlation
coefficients. This sample is obtained by independent random
permutation
of the components
of X respecting the clones structure.
With N
clones, N! distinct permutations
are possible and N! genetic correlation coefficients
may be calculated. Suppose that among these possible N! genetic correlation
coefficients, only n are calculated. If we choose a significance level of 5%, the
observed genetic correlation coefficient is declared significant if less than 5n/lOO of
the calculated correlation
coefficients are greater (in absolute value) than the
observed value.
For many pairs of characters, our data were not balanced. The first step was to
obtain the same number of plants in each clone. We applied the bootstrap method
of resampling to get a data set of the same size in each clone (generally with b = 12
plants per clone). We completed the data set for one clone by sampling within the
experimental data of the clone.
Results
In the first experiment with summer Gladiolus, most of the hand-pollinations
failed because of inadequate hygrometric
conditions in the glasshouse. Therefore
the production
of seeds was not taken into account in the first planting.
1. Correlation
analysis
Tetraploid culthars
The results of the second experiment in which all functions were taken into
account are presented first.
With respect to within-clone
correlations
(Table 3) flowering
time (D) was
negatively correlated with the other variables owing to the effect of the planted
corm weight : for a given clone, the bigger the planted corm, the more vigorous the
plant and the earlier the flowering, and the lower the relative corm growth (there is
a limit to the size of the corm). This created an artificial correlation between these
characters. For the other characters, provided corm weight (PCW) and lateness (D)
were excluded, within-clone
correlations were all positive.
Evidence of trade-offs between the different functions of the plant was examined
by the correlations given in Table 4a and Table 4b. These tables give three types of
correlation coefficients: between-clones
correlation coefficients (Spearman correlation coefficient),
genetic correlation
coefficients calculated on unbalanced data
0.06
- 0.03
-0.35
0.32
-0.07
0.14
D
0.25
-0.40
0.03
-0.04
0.01
0.12
PCW
-0.17
-0.01
-0.28
NLEAF
GRO
ovu
NSEED
WSEED
POLL
-0.23
correlation
0.33
0.31
0.32
D
3. Within-clone
NF
HSTEM
WLEAF
Table
matrix
NF
0.33
0.14
0.56
0.25
0.39
0.21
0.59
0.16
0.24
experiment
HSTEM
0.20
-0.01
0.14
-0.16
0.01
0.07
in the second
summer
WLEAF
- 0.04
-0.27
0.26
0.07
0.03
0.29
with
NLEAF
- 0.06
0.15
0.18
0.14
-0.20
Gladiolus
GRO
0.23
- 0.02
0.16
0.03
ovu
0.17
0.41
-0.02
NSEED
0.69
0.12
WSEED
-0.03
s.
&
5’
ail
Et
0
5
* significant
POLL
WSEED
NSEED
ovu
GRO
NLEAF
WLEAF
HSTEAM
NF
D
at 5% level
0.62
0.49
0.54
0.21
0.26
0.29
0.57
0.46
0.51
0.31
- 0.02
0.04
-0.07
-0.01
-0.07
0.21
0.04
0.34
-0.41
-0.38
-0.49
-0.45
-0.15
- 0.45
-0.21
-0.22
-0.19
D
0.x3*
0.84
0.82’
0.76*
0.65
0.65*
0.60
0.73
0.67*
-0.07
0.22
0.14
0.67
0.46
0.62
-0.64
-0.72
-0.69*
-0.64
-0.84
-0.86*
-0.74*
-0.45
-0.52
NF
0.74*
0.83
0.82*
0.52
0.59
0.60
-0.05
0.25
0.16
0.91*
O.XX
0.88*
-0.48
-0.47
-0.54
-0.60
-0.55
-0.57
-0.79*
-0.78
-0.80*
HSTEM
0.24
0.25
0.21
- 0.43
-0.19
-0.29
0.79.
0.73
0.80*
-0.26
-0.21
-0.31
-0.38
-0.13
-0.30
-0.52
-0.46
-0.49
WLEAF
0.62
0.47
0.43
0.24
-0.01
-0.01
-0.83*
-0.76
-0.73*
-0.71*
-0.69
-0.66*
-0.67
-0.55
-0.59
NLEAF
matrix in the second experiment
with summer Gladiolus (8 clones). Spearman
coefficients
without
bootstrap.
Genetic correlation
coefficients
with bootstrap)
-0.52
-0.73
-0.66
0.10
0.14
0.1 I
0.45
0.38
0.41
0.12
0.20
0.25
0.36
0.50
0.44
-0.02
-0.10
-0.18
0.31
0.49
0.20
-0.10
-0.05
0.05
-0.19
-0.29
-0.09
-0.19
-0.17
-0.26
PCW
Table 4a. Correlation
Genetic correlation
-0.24
-0.14
0.05
-0.45
-0.41
-0.43
-0.24
-0.53
-0.51
-0.38
-0.53
-0.54
GRO
correlation
-0.31
0.03
-0.23
-0.55
-0.21
-0.32
-0.60
-0.22
-0.40
ovu
coefficients
0.86*
0.94
0.94*
0.62
0.37
0.44
NSEED
(correlations
0.43
0.16
0.29
WSEED
among
means).
2
9
0.
2
P
5
z
Growth,
reproduction
and
survival
299
in gladiolus
Table 4b. Correlation
matrix
in the second experiment
with fertile
Spearman
correlation
coefficients
(correlations
among means). Genetic
bootstrap.
Genetic correlation
coefficients
with bootstrap)
ovu
POLL
NSEED
-0.10
-0.49
-0.49
-0.10
0.22
0.22
* significant
summer
correlation
gladiolus
(5 clones).
coefficients
without
WSEED
-0.80
-0.83
-0.84’
at 5% level
(without bootstrap), and genetic correlation coefficients calculated on balanced
data (with bootstrap). These three types give similar results.
In this second experiment with summer Gladiolus, pollen fertility analysis
showed that the percentage of full pollen grains was about 60% for three of the
eight clones compared with 100% for the other clones. Female fertility was also
affected for these three clones. Low fertility may be due to interspecific crosses.
Therefore, in the analysis of trade-offs between male and female functions, the
three cultivars with meiotic abnormalities were excluded. In Table 4b, correlations
between characters of sexual reproduction have been calculated on the five fertile
clones.
To test the significance of the genetic correlations by a permutation
test, 5000
permutations with the eight clones (among the 8! = 40320 possible) and all the
5! = 120 possible permutations with the five clones were performed.
Although intra-clone correlations were all positive, negative genetic correlations
(Tables 4a and 4b) were found between seed production (NSEED, WSEED) per
flower and the other variables, and also between the number of full pollen grains
per flower (POLL) and the other variables. Globally, the correlations between the
other variables were significantly positive; these included the correlation between
the number of flowers (NF) and the number of ovules (OVU) which seemed to be
directly associated with the height of the stem (HSTEM).
Of particular interest was
the significant negative genetic correlation
between seed weight per flower
(WSEED) and number of full pollen grains per flower (POLL) (Table 4b).
Turning to the first experiment which involved the 19 clones of summer GludioZus, a similar trend in correlations was found (Table 5), i.e. negative between-clone
correlations between pollen production (POLL) and variables of vegetative vigour
(height of the main stem, corm growth), and positive between-clone correlations for
ovule production and variables of vegetative vigour.
Table
5. Between-clone
D
-0.50*
-0.25
POLL
ovu
l
Spearman
correlations
coefficient
of correlation,
in the first experiment
with
HSTEM
-0.33
0.23
significant
at 5% level
summer
NF
0.07
0.05’
Gladiolus
(19 clones)
GRO
-0.41
0.30
300
Rameau
and Gouyon
Diploid species and species hybrids
Certain individuals grown in experiment 3 did not flower. This was particularly
true for the cultivar Christabel, one of the two diploid hybrids. Moreover, individuals with a pollen fertility lower than 80% (i.e. showing high sterility owing to their
interspecific origin) were excluded from the analysis. Therefore, correlations
were
calculated on 14 individuals of G. tristis L., 19 individuals of Homoglad and 8
individuals of Christabel.
The correlation between full pollen grain production
and seed weight per flower
was significantly negative in the diploid hybrid Homoglad (r = -0.52, P < 0.05),
nearly significant in the hybrid Cristabel (r = - 0.61, P = 0.0597), and negative,
though not significant, for the species G. tristis L. (r = -0.21, P = 0.5235).
2. Principal
component analysis
The fire fertile clones of summer Gladiolus (second experiment)
Figure 1 shows the plots of initial variables, relative to the first two principal
axes. Data used in the principal component analysis are means per clone. The first
Fig. 1: Plots of initial variables,
relative
analysis on fertile cultivars
of Gladiolus.
to the first
two
principal
axes from
a principal
component
Growth.
reproduction
and survival
301
in gladiolus
two principal components
account for 45% and 33% respectively of the total
variation.
Several groups of variables appear: (i) characters
of male function
(number
of full pollen grains per flower (POLL));
(ii) characters
of female
function (seed-set (NSEED)
and seed weight per flower (WSEED);
(iii) variables
bound to vegetative vigour (stem height (HSTEM),
spike height (SPIKE),
leaf
width (WLEAF));
(iv) characters of perennation and asexual propagation
(corm
growth (GRO),
cormel weight (HKW).
In addition, the number of ovules per
flower (OVU) clustered with the characters of vegetative vigour.
On the first principal component individuals ranked high for male function are
ranked low for female function and vegetative growth.
The second principal
component opposes survival to male function and vegetative vigour, and to a
lesser extent, characters of vigour to characters of female function.
The fertile individuals of the diploid hybrid Homoglad (Fig. 2)
The first principal component accounted for 44% and the second component
for 15% of the total variation. Characters associated with vegetative vigour (total
stem number (NSTEM),
total flower number (TFL)
and weight of harvested
corms (HCW))
were well clustered (Fig. 2). Particularly
evident is the negative
relationship between male function and the other functions, and also the negative
relationship between female function and characters of vigour.
Fig. 2: Plots of initial variables,
relative
to the first
analysis on fertile individuals
of Homoglad.
two
principal
axes from
a principal
component
302
Rameau
and Gouyon
Discussion
Genetic and encironmental
correlations
We can assume that variations in the total,amount
of resources available to an
individual are often due to environmental
variation. When attempts are made to
demonstrate trade-offs between life-history
traits, this variability is likely to hide
genetic variation in resource allocation (Falconer, 1981, pp. 293-284; Primack and
Antonovics,
1982). In two studies on intraspecific
variation for sex allocation
(McKone,
1987; Stanton and Preston, 1988b), pollen production and the components of seed production were measured on several individuals of unknown genetic
origin. In each study, the phenotypic correlations
between pollen and seed productions were weak and highly variable from one population to another. Stanton and
Preston (1988b) concluded that it is necessary to employ quantitative
genetics
methods and progeny analysis to estimate the relative importance of environmental
and genetic variation.
In our experiments, separation into within and between-clone
correlations
indicates that between characters of sexual reproduction
and vegetative characters,
within-clone
correlations are all positive but between-clone correlations, and genetic
correlations which give similar results, are strongly negative. These negative correlations indicate trade-offs.
Randomization
and small variations
in corm weight
between clones minimize the common environment component of variance. However, because of the effect of the planted corm weight, this component cannot be
eliminated. It may contribute to the variance between means of the clones and thus
may bias between-clone
(and genetic) correlations
by making them more positive
(Reznick et al., 1986). Within-clone
correlations are at least partly due to variation
in the planted corm weight (see above); between-clone correlations
would be even
more negative without this variation.
In wild diploid material, trade-offs between male and female functions have been
demonstrated
in the two diploid hybrids Homoglad
and Christabel,
although
measurements were made on non-cloned material. Referring to the model of Van
Noordwijk
and De Jong (19X6), we can assume that variation in the total amount
of resources available (“resource
acquisition”)
did not hide variation
in the
allocation of resources between the different functions of sexual reproduction.
As for
the tetraploids, the experimental design reduced variation in the total investment.
Strong variation in pollen production and seed production, which gave evidence of
trade-offs in Homoglad and Christabel, may be due to the interspecific origin of these
hybrids. The fact that the correlation
between pollen and seed production
is not
significant in the species G. tristis L. lends support to this last hypothesis.
M&one
(1987) studied the relative maternal and paternal investments in five
bromegrass (Bromus) species. Pollen and seed production
per floret were independent in three species and positively correlated in one species. However,
from the
same data, if we calculate the correlation
between species means of anther length
and seed set per floret, we find a negative and significant correlation (r = -0.975,
P < 1%).
Growth,
reproduction
and survival
303
in gladiolus
The correlations
found in the present study seem to be constant in the genus
Gladiolus since the plots of initial variables obtained with a principal component
analysis are the same for two groups, one belonging to a wild diploid species, the
other being domesticated.
The cost of pollen production
Negative correlations
between full pollen grain production
per flower and seed
production confirm the hypothesis of Charnov et al. (1976) concerning trade-off
phenomena between male and female functions. The correlations
between pollen
production and characters of the vegetative function (foliar system, plant vigour,
tuberization)
together with the high value of regression coefficient, also indicate the
high cost of pollen production to the plant, If we look for the relationship between
these two sets of variables, for instance between pollen production (POLL) and the
height of the main stem (HSTEM),
the relationship
can be expressed by the
equation: HSTEM = -0.75 POLL + 229 (Fig. 3). HSTEM varies from 100 cm to
150 cm in relation with a variation in POLL from 172 to 105 thousands of pollen
grains per flower.
Fig. 3: Plot of pollen production
with summer Gladiolus
(symbol
(POLL)
is value
and height of the stem (HSTEM)
of mean per clone).
in the second
experiment
304
Rameau
and Gouyon
This result was obtained despite a very rough measure of male function
(i.e. number of full pollen grains per flower). This cost seems to have a direct
impact on both seed production
and vegetative organ production.
(A priori,
this may seem very surprising
if we compare, for example, the dry weight of
these organs). Several explanations
can be put forward:
1) Part of the cost of
pollen production
comes from the protein molecule forming the pollen wall
(exine sporopollenin).
This molecule is one of the most resistant in the biosphere and its cost of production
may be very high. 2) the pollen grain has to
contain all the material necessary to permit good germination
and fast growth
of the pollen tube in the style tissues towards
the embryo sac of the ovule.
Expensive nutrients such as nitrogen and phosphorus
could thus be concentrated
in the pollen. 3) It is possible that other characters which have not been measured
are linked with pollen production
(for instance, nectar production
or composition). 4) In hermaphroditic
plants, male function generally begins earlier than
female function. Consequently,
there is stronger competition between male function and vegetative development
than between female function and vegetative
function.
Such a trade-off should have a strong effect in cultivated plants. This has two
implications:
(i) it should be taken into account for plant breeding schemes and
(ii) it should be possible to detect it as a secondary effect in domesticated plants in
which selection on male function has been relaxed. Indeed, such indirect proof
exists. The following examples show the impact of pollen production
(or lack of
pollen production)
on tuberization
and vegetative function in genera other than
Gladiolus.
Ranunculus asiaticus (Meynet, personal communication)
In Ranunculus, one of the most important ornamental characters is the “doubleness” of flowers which results from a petaloid transformation
of stamens and can
lead to male-sterility
(“double”
flower). The present aim of the breeding program
of I.N.R.A.
is to develop hybrids between inbred clones, one clone being malesterile (double flower), the other one being fertile (simple flower). Each clone is
vegetatively propagated by division of crowns. The male parent (hermaphrodite)
propagates less easily than the female.
Discorea rotundata (Yam)
The yam includes male, female and monoecious plants and produces a tuber.
At the International
Institute of Tropical Agriculture
(IITA),
Tbadan, Nigeria,
a multi-trait
selection for tuber yield, tuber shape and tolerance
to leaf
pathogens has been performed.
Throughout
this selection, it was observed that
the frequency
of female plants tends to increase. In addition, these female
plants have a low fruiting ability (IITA,
unpublished
data, cited by Akoroda
et al., 1984). In the same species, Akoroda
et al. (1984) studied the association
of sex with vegetative characters
and tuber yield in three populations
under
selection. Tuber yield increased in the following
order: male, monoecious
and
female plants.
Growth,
reproduction
Telfairea
and survival
in gladiolus
305
occidentalis
In this dioecious African species, a leaf vegetable, a similar comparison has been
made between male and female plants. Many authors (Tindall, 1965; Phillips, 1973;
Van Epenhuisen, 1974) observed that the female plants produce larger and more
numerous leaves, and over a longer period, than do male plants.
Akoroda et al. (1984) explain this difference between male and female plants by
the sequence of processes involved in vegetative growth compared to processes
involved in sexual reproduction. Male plants begin to flower earlier than female
plants. So male function competes more strongly with the development of foliage,
subsequently with plant vigour, and finally with tuberization, than does female
function.
Orule
and seed production
In Gladiolus,
ovule production per flower is variable. The between-clone correlations are negative between seed-set and vegetative characters, whereas they are
positive between number of ovules per flower and vegetative characters, suggesting
that ovule production relative to seed production is inexpensive for the plant.
In many hermaphroditic species, an overproduction of flowers is observed in
comparison with fruits which mature. Three non-exclusive hypotheses have been
formulated to explain this phenomenon: (i) with an excessof ovules, the plant may
respond to variation in the total amount of available resources (the plant does not
“know” a priori how many ovules it will be able to mature); (ii) the plant may
“choose”, and only the “best” seeds reach maturity (Stephenson, 1983); (iii) the
excess of floral organs and ovules compared with seedsproduced is a consequence
of selection on male function. An increase in number of flowers leads to an increase
in pollen transfer (Queller’s “fleurs du male” syndrome) (Queller, 1983; Couvet et
al., 1985).
It is of interest that one of the conditions required for each of these hypotheses
to be true is that ovule production is inexpensive for the plant, as found in Gladiolus.
Gladiolus
thus shows a high cost of pollen and seed production to the function of
survival (and vegetative propagation) while the ovule cost seemsnegligible. It is
unlikely that this is the case for every plant species. Despite the abundant theoretical literature published on the subject of resource allocation, experimental studies
allowing comparison of different groups of organization (floral, architectural. . .)
are still needed to allow further understanding of the evolution of life-history
patterns.
From the present study, it is possible to conclude that pairwise studies of resource
allocation between different functions of the plant are unlikely to be relevant. Since
vegetative propagation, male and female reproduction and survival all interact in
terms of competition for resources, a general theory is needed taking each of these
different functions into account. In particular, it is probably not realistic to measure
the precise cost of any function without having sufficient information about other
functions of the individual.
306
Rameau
and Gouyon
Acknowledgments
This study
the direction
INRA.
The
grateful to I.
was undertaken
at INRA
in the Frejus Station d’Amelioration
des Plantes florales under
of E. Berninger.
The data-processing
was done at Montpellier
in the CEPE-CNRS
and
authors
are indebted
to these laboratories
for kind help. The authors
are particularly
Small and C. Gliddon
for helpful linguistic comments
and to J. B. Denis for statistical
help.
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Received
29 May 1990;
accepted 29 May 1990.
Corresponding
Editor:
R. Abbott