An Experimental Study of Competitive Performance in Brassica rapa (Cruciferae)
Thomas E. Miller; Douglas W. Schemske
American Journal of Botany, Vol. 77, No. 8. (Aug., 1990), pp. 993-998.
Stable URL:
http://links.jstor.org/sici?sici=0002-9122%28199008%2977%3A8%3C993%3AAESOCP%3E2.0.CO%3B2-J
American Journal of Botany is currently published by Botanical Society of America.
Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at
http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained
prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in
the JSTOR archive only for your personal, non-commercial use.
Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at
http://www.jstor.org/journals/botsam.html.
Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed
page of such transmission.
JSTOR is an independent not-for-profit organization dedicated to and preserving a digital archive of scholarly journals. For
more information regarding JSTOR, please contact support@jstor.org.
http://www.jstor.org
Wed Apr 11 13:22:16 2007
Amer. J. Bot. 77(8): 993-998.
1990.
AN EXPERIMENTAL STUDY OF COMPETITIVE PERFORMANCE
IN BRASSICA RAPA (CRUCIFERAE)'
THOMAS
E. MILLER^ AND DOUGLAS
W. SCHEMSKE~
Department of Ecology and Evolution, Barnes Laboratory, 5630 S. Ingleside,
University of Chicago, Chicago, Illinois 60637
ABSTRACT
Growth chamber experiments with rapid-cycling Brassica rapa were designed to estimate the
signsand magnitudes ofthe genetic correlationsfor plant performance in each ofthree conditions:
no-competition (isolated plants), intraspecific competition, and interspecific competition with
Raphanus sativa. Biomass and flower number were highest in the no-competition treatment,
intermediate under intraspecific competition, and lowest under interspecific competition. Significant among-family variation in biomass and flower number was found under each regime.
The mean family performance (biomass or flower number) in the no-competition treatment
was significantly positively correlated with the performance in only one of the competitive
treatments (for biomass in the intraspecific treatment). For both biomass and flower number
there was a significant positive correlation between family means in the intra- and interspecific
regimes. These correlations were greater in magnitude than those for the comparison between
no-competition and competition (intra- or interspecific) treatments. Our results suggest that the
importance of traits affecting plant performance is environment-dependent; the performance
of a family grown without competition was a poor predictor of performance with competition,
while the performance offamilies grown under intra- and interspecific competition was positively
correlated.
GENETIC
variation for plant performance in
competitive environments has been identified
in agricultural systems (e.g., Sakai, 1955, 1961;
Donald, 1981; Langton, 1985) and in natural
populations (Solbrig and Simpson, 1977; Martin and Harding, l 98 l , 1982; Shaw, l 986; Clay
and Levin, 1986). However, little is known
about how the performance of genotypes
changes with competitive regime. The two extreme possibilities are: 1) specialization for a
particular competitive regime; and 2) generalized adaptation to a broad variety of such
regimes. In the former case, the rankings of
relative fitness for genotypes would vary with
competitive regime, indicating that the performance of a genotype is dependent on the
competitive regime under which it is grown.
In the latter case, the rankings ofrelative fitness
would be relatively stable across regimes and
the ranking of individual genotypes independent of competitive conditions.
l Received for publication 7 April 1989; revision accepted 6 March 1990.
The authors thank A. Winn and S. Tonsor for comments
and discussion and the University of Chicago greenhouse
staff for maintaining plants and providing advice and support.
Corresponding author; current address: Department of
Biological Science B-142, Florida State University, Tallahassee, FL 32306.
Current address: Department of Botany, KB-15, University of Washington, Seattle, WA 98195.
Several previous studies have used analysis
of variance to separate the effects of plant genotype, competition, and the genotype x environment interaction on plant fitness (e.g.,
Kelley and Clay, 1987; Goldberg, 1988). A
significant interaction term indicates that the
relative performance of a genotype varies with
competitive regime (e.g., Gupta and Lewontin,
1982). However, analysis of variance tests the
significance of an interaction term in a linear
model and does not directly address the distinction between specialized and generalized
competitive ability.
The extent to which competitive performance is specialized or generalized can be
quantified as the genetic correlation between
total fitnesses, or fitness components, under
different competitive conditions (Falconer,
1952; Via, 1984; Via and Lande, 1985).A negative correlation implies the existence of "genetic trade-offs" in which biomass allocation
or other specializations that lead to superior
performance in one competitive environment
adversely affect performance under different
competitive conditions. If there is local variation in the magnitude of competition or in
the identity of competitors within a population, such negative correlations could promote
the coexistence of different genotypes (e.g.,
Schutz, Brims, and Usanis, 1968; Antonovics,
1978; Kelley and Clay, 1987). On the other
994
[VO~.
77
AMERICAN JOURNAL OF BOTANY
TABLE1. Yield of Brassica rapa grown in no-competition and in two competitive environments. The skewness of the
distribution is given by g, (H,: g, = 0). Positive values indicate skewness to the right of the distribution; negative
values indicate skewness to the left
B~ornass(g)
N o . flowen
Mean
S.D.
g,
Mean
S.D.
g,
No-competition
0.687
0.170
0.110
97.90
25.24
0.174
Competition
Intraspecific
Interspecific
0.073
0.012
0.066
0.009
1.195'
2.332b
12.57
0.82
10.99
1.69
0.897'
2.853b
Env~ronment
hand, positive genetic correlations for performance under different competitive conditions
would reflect generalized adaptation to a broad
variety of competitive regimes and would indicate that traits that improve performance under one regime also do so (or are correlated
with traits that do so) under other competitive
conditions. Generalized competitive adaptations may provide greater fitness when the
competitive regime is spatially or temporally
variable (e.g., Hubbell and Foster, 1986).
To establish that competition contributes
significantly to the observed variation in fitness
among individuals requires that the performance of genotypes grown without competition be a poor predictor of their performance
when grown in competitive environments. The
strength of this prediction will be revealed by
the correlation for performance in competitive
and noncompetitive conditions (Martin and
Harding, 1982). A strong positive correlation
would indicate that a genotype favored in noncompetitive conditions also achieves high fitness when grown under competition. A weak
or negative correlation would indicate that a
genotype favored in competitive environments
is not necessarily favored in noncompetitive
environments. Only in the latter case can one
unambiguously treat competition as a distinct
selective force. This kind of analysis should,
therefore, accompany any study that purports
to examine the evolutionary dynamics of plant
competition.
In this paper, we present the results of experiments designed to estimate the genetic correlations for performance of Brassica rapa
grown under three competitive regimes: noncompetition (isolated plants), intraspecific
competition (monocultures of Brassica rapa),
and interspecific competition (two-species
mixtures with Raphanus sativa). Our objectives were to: 1) identify the genetic basis of
competitive performance in this species; and
2) provide a general protocol for investigating
the evolution of competitive performance in
plants.
ATERIA RIALS AND METHODS -Brassica raps L.
(Cruciferae),rape or field mustard, and Raphanus sativa L. (Cruciferae), radish, are cosmopolitan annuals of temperate zones used in agriculture and found as common weeds. Brassica
has an upright growth form, whereas Raphanus
is relatively prostrate or vine-like and has larger leaves and, in our experiments, a more rapid
growth rate. Rapid-cycling stocks of these
species were obtained from the Crucifer Genetics Cooperative at the University of Wisconsin (Brassica, CRCG stock #1, Aaa; Raphanus, CRCG #7, Rrr; Williams, 1985).The stock
for each species was initially derived by combination of diverse early-flowering types, followed by recurrent selection for minimum time
from sowing to flowering, rapid seed maturation, absence of seed dormancy, and high female fertility (Williams and Hill, 1986).Stocks
of both species appear to contain substantial
genetic variation, including isozyme polymorphism (Williams, 1985; Williams and Hill,
1986) and genetic variation for quantitative
characters such as flowering date, ovule number, and trichome density (personal observation). Both species are hermaphroditic and have
sporophytic self-incompatibility systems.
Maternal seed families for B. rapa were obtained by outcrossing 48 plants raised in a
greenhouse at the University of Chicago. Pollinations were performed for 10 days; on each
day, four different randomly chosen plants were
designated as pollen donors for each maternal
plant. Pollinationswere performed using a small
piece of felt attached to the end of a toothpick,
which was rubbed over the anthers of the four
pollen donors, then the mixed pollen load was
applied to available stigmas on the maternal
plant. Seed was harvested by maternal parent.
On the basis of our pollination procedures, we
expect that the genetic relatedness among progeny from a given maternal parent was approximately that of half-sibs. Additional populations of both species supplied seeds for neighbor
plants in the competition regimes. Bulk seeds
for this purpose were obtained by daily random
August 19901
MILLER AND SCHEMSKE
-COMPETITIVE PERFORMANCE IN BRASSICA
outcrossing of large populations (100 + individuals) ofBrassica and Raphanus in the greenhouse.
Focal individuals of Brassica were grown
from seed under three regimes: no-competition, intraspecific competition and interspecific competition. In the no-competition treatment, nine seeds from each family were sown
individually in separate 8 x 8 x 12-cm deep
plastic pots. In the intraspecific and interspecific treatments, ten seeds from each family
were sown in hexagonal arrays in 52 x 22 x
8-cm deep plastic flats such that each focal
plant was surrounded by six equidistant neighbors derived from the bulk seed collections.
An 8-cm border of nonsampled plants was used
to preclude edge effects. Five flats were used
per treatment (two replicate individuals per
maternal family per flat), and each flat contained a total of 400 individuals (3,500 plants
m-2). Seeds that failed to germinate and seedlings that died within 6 days of planting were
replaced with transplanted individuals to
maintain the uniformity of the competitive regimes, but these individuals were excluded from
the analysis. There was no mortality after the
6th day, and no family was left with less than
six replicates in each competitive regime; most
had eight to ten (mean = 9.3). Each target individual from the half-sib families was surrounded by either six conspecific neighbors
from the rapid-cycling seed stock (intraspecific
competition) or six individuals ofrapid-cycling
Raphanus sativa (interspecific competition).
Mean weight per seed for each family was determined from unused seed weighed in lots of
approximately 20 seeds.
All plants were grown in ProMix BX (a standard soilless mix of sphagnum moss, vermiculite, and perlite) and maintained in a growth
room at the University of Chicago. Plants were
illuminated 24 hr/day with fluorescent lights
(approx. 240 ern-^ s-') at a constant 24.5 C
temperature. The plants were watered as needed to prevent wilting and were fertilized at 18
and 28 days with a weak solution of soluble
fertilizer (20- 19-18, Peter's Peat-Lite). After 38
days, all plants were harvested, censused for
total number of flowers initiated (number of
flowers + developing fruits), dried at 65 C , and
weighed. Although no hand pollinations were
performed, some pollination occurred when
plants bumped together; less than 3% of the
flowers had begun developing seed.
For both plant biomass and flower number,
we used a mixed model analysis of variance to
examine the main effects of treatment (fixed),
family (random), and the treatment x family
interaction (random). The residuals from AN-
995
OVA departed significantly from a normal distribution for these analyses; thus, the significance levels presented should be interpreted
with caution. Our purpose in these analyses
was simply to establish the presence of a genotype x treatment interaction, which was
found to be highly significant for both measures
of plant performance (see below). To evaluate
the variation in biomass and flower number
among families within treatments, we used the
Kruskal-Wallis nonparametric analysis of
variance in the NPAR procedure of SYSTAT
(Wilkinson, 1987). We estimated genetic correlations for performance using pairwise Pearson correlation coefficients (see Via, 1984),calculated from the mean biomass or flower
number per family for plants grown in the three
different competitive regimes. Confidence intervals for correlation coefficients were determined by means of z-transformations (Sokal
and Rohlf, 1981).
RESULTSAND DISCUSSION-Plantsizes differed dramatically among the three treatments.
Individuals in the no-competition regime were
almost an order of magnitude larger than those
grown under intraspecificcompetition and two
orders of magnitude larger than those grown
under interspecific competition (Table 1).
Flower number displayed a similar pattern
across the three treatments (Table 1). Although
planting densities in the two competitive treatments were equal, interspecific effects on both
biomass and flower number were larger than
intraspecific effects. The two measures of fitness, biomass and number of flowers, were significantly correlated (P < 0.001) in all three
treatments (alone: r = 0.48; intraspecific: r =
0.92; interspecific: r = 0.67).
The three treatments also produced significantly different patterns of variation in biomass and flower number (Table 1). In the nocompetition treatments, both biomass and
flower number were evenly distributed about
the mean and showed no significant skewing
(g,; Sokal and Rohlf, 1981). Significant skewing
was observed in both competitive treatments,
with greater skewing in the more extreme interspecific regime. This result suggests that, as
competitive intensity increases, a smaller
number of individuals will contribute the majority of seeds to the next generation.
There was significant among-family variation in biomass within each treatment (Table
2). Mean biomass within each treatment varied
with family by more than an order of magnitude; for example, mean biomass in the intraspecific treatment ranged from 0.0 11 g to 0.138
g. Mean flower number exhibited similar sig-
996
TABLE
2. Kruskal- Wallis test statistics (H) for effects of
family on plant biomass andflower number (df = 47)
Environment
Biomass
TABLE
3. Analyses of variancefor plant biomass andflower number in Brassica rapa in each environment. All
F values are signzficant at the P < 0.0001 level
No. flowers
Source o f variat~on
Competition
Intraspecific
Interspecific
[Vol. 77
AMERICAN JOURNAL OF BOTANY
85.3"
67.13b
81.5"
50.4
nificant among-family variation except in the
interspecific treatment, where the distribution
of flower number/individual was truncated; the
majority of individuals did not flower.
The treatment x family interaction was
highly significant for both biomass and flower
number (Table 3); the relative performance of
a family depended on the treatment in which
it was growing. The genetic correlation for biomass in the two competitive regimes (intraspecific and interspecific) was significantly
greater than those for biomass in the noncompetitive regime and each competitive treatment (Table 4). Flower number showed a similar but nonsignificant pattern (Table 4); the
low mean and standard deviation in flower
number in the interspecific treatment (Table
1) reduce the likelihood of finding significant
differences between treatments.
These results suggest the presence of a "generalized competitive performance" for the two
competitive regimes used in this study -traits
advantageous in intraspecific competition are
also advantageous in interspecific competition.
However, the correlation coefficients are significantly less than 1 (Table 4), suggesting that
some opportunity exists for evolutionary specialization to each competitive regime.
It is likely that our results are dependent on
the intensity of competition and on the identity
of the limiting resources in this study. For example, competition for light, where light preemption (shading)by early-emerging or rapidly
growing individuals is expected, might lead to
a positive correlation between growth without
competition and growth with competition. We
found a positive, but low, correlation for performance in noncompetitive and competitive
regimes, suggesting that relatively little advantage was conferred simply by the potential for
rapid growth in our competitive treatments.
The significant correlation between family performances in the two competitive treatments
may indicate that similar resources were limiting under the intra- and interspecific conditions used in this experiment. Although the
Biomass/plant
Competitive
regime
Family
Regime x family
Error
Flowers/plant
Competitive
regime
Family
Regime x family
Error
df
2
47
94
1,118
MS
F
59.488 3,021.21
0.028
2.93
0.020
2.03
0.010
2 1,198,609.247 2,591.94
47
641.020
2.84
94
461.280
2.05
1,119
225.490
competition in this study was created by species
with somewhat different growth forms and
competitive intensities (competition with Raphanus created a more severe environment),
other competitive regimes might have produced different results.
Because we used maternal families, we cannot exclude the possibility that some of the
observed differences between families are
caused by maternal genetic and/or environmental effects. One way in which environmental maternal effects appear is through seed
size. Previous research with other species has
shown that the maternal environment can have
a large effect on seed size (e.g., Winn and Werner, 1987),and larger seeds may produce larger
seedlings and adults, especially in competitive
environments (Stanton, 1984; Gross, 1984).In
our study, no significant correlation appeared
between family mean seed mass and plant biomass, or flower number, in the no-competition
or the interspecific treatment (no-competition
treatment: biomass, r = 0.11; flower number,
r = 0.17; interspecific treatment: biomass, r =
0.21; flower number, r = 0.24; all P > 0.05).
There were significant correlations between
mean family seed weight and performance under intraspecific competition for both biomass
(r = 0.29, P = 0.04) and flower number (r =
0.42, P = 0.003).
Several previous studies have shown that the
performance of genotypes varies significantly
among different competitive regimes, suggesting specialization to particular competitive environments. Martin and Harding (1 982) used
an experimental design similar to that used in
the present study to investigate the performance of families ofErodium cicutarium when
grown alone, with intraspecificcompetition, or
with interspecific competition. They found sig-
August 19901
MILLER AND SCHEMSKE
-COMPETITIVE PERFORMANCE IN BRASSICA
997
TABLE4. Correlations between mean family performance in each pair of environments. Numbers in parentheses are
95% confidence intervals (after z-transformation, Sokal and Rohlf; 198U
Biomass Intra
No-competition
Intraspecific
0.397=
(0.127-0.6 10)
No. flowen
Inter Intra
0.269
(-0.01-0.514)
0.6 1Ob
(0.399-0.762)
nificant among-family differences in performance in the no-competition and interspecific
competition treatments, indicating that traits
related to performance were heritable. In contrast to the results of our study, they found no
significant correlation between family performances in the two competitive treatments.
However, the Martin and Harding (1982) study
had little statistical power, because of the small
number of families investigated (six) and the
low replication (two plants/family).
Sakai (196 1) found no correlation between
the growth of different rice varieties in weeded
plots (intraspecificcompetition) and unweeded
plots (intra- and interspecific competition),
suggesting that there is specialization for specific types of competitive environments. Turkington and Harper (1979) did find significant
among-clone differences in competitive response of ramets of Trifolium repens to different species of neighboring plants. Aarssen and
Turkington (1985) also found significant differences among genotypes of pasture species in
response to different genotypes of competitors.
Kelly and Clay (1987) measured a similar effect
in Danthonia spicata, but the pattern was not
reciprocal; the competitive performance of
Danthonia spicata depended on both plant genotype and the genotype of the competitor,
Anthoxanthum odoratum, but no such pattern
was found for the competitive performance of
Anthoxanthum when it was grown with Danthonia. Other studies have also found little evidence of specialization (e.g., Goldberg, 1988).
A major purpose of this research was to establish an experimental protocol for evaluating
the role of competitive interactions in the evolution of plant populations. Our approach is
based in large part on the pioneering work of
Sakai (1955, 196 1) and Martin and Harding
(198 1, 1982)which concerned the genetic basis
of competitive performance in plants. In Brassica rapa we found that the genetic correlations
for performance in competitive and noncompetitive conditions were small compared to the
0.219
(-0.070-0.474)
Inter
0.005
(-0.279-0.288)
0.451b
(0.191-0.652)
genetic correlation for performance in intraspecific and interspecific competition treatments. These results suggest that the performance of this species when grown under
competition is due, at least in part, to traits
that confer an advantage only in competitive
environments. In addition, there is little evidence of genetic specialization to particular
competitive environments. We suggest that
these kinds of analyses, once performed for a
number of species in different competitive environments, will aid in our understanding of
the selective effects of competitive interactions
in plants.
LITERATURE CITED
AARSSEN,
L. W., AND R. TURKINGTON.1985. Biotic specialization between neighbouring genotypes in Lobum
perenne and Trifolium repens from a permanent pasture. J. Ecol. 73: 605-614.
ANTONOVICS,
J. 1978. The population genetics of mixtures. In J. R. Wilson [ed.], Plant relations in pastures,
233-252. CSIRO, Melbourne, Australia.
CLAY,K., AND D. A. LEVIN. 1986. Environment-dependent intraspecific competition in Phlox drurnrnond~~.
Ecology 67: 37-45.
DONALD,C. M. 1981. Competitive plants, communal
plants, and yield in wheat crops. In L. T. Evans and
W. J. Peacock [eds.], Wheat science-today and tomorrow, 223-247. Cambridge University Press, New
York.
FALCONER,
D. S. 1952. The problem of environment and
selection. Amer. Naturalist 86: 293-298.
GOLDBERG,
D. E. 1988. Response of Solidago canadensis
clones to competition. Oecologia 77: 357-364. GROSS,K. L. 1984. Effects of seed size and growth form
on seedling establishment of six monocarpic perennial
plants. J. Ecol. 72: 369-387.
GUPTA,A. P., AND R. C. LEWONTIN.1982. A study of
reaction norms in natural populations of Drosophila
pseudoobscura. Evolution 36: 934-948.
HUBBELL,
S. P., AND R. B. FOSTER.1986. Biology, chance,
and history and the structure of tropical rain forest
tree communities. In J. Diamondand T. J. Case [eds.],
Community ecology, 3 14-330. Harper and Row, New
York.
KELLEY,S. E., AND K. CLAY. 1987. Interspecific competitive interactions and the maintenance ofgenotypic
998
AMERICAN JOURNAL OF BOTANY
variation within two perennial grasses. Evolution 4 1:
92-103.
LANGTON,
F. A. 1985. Effects of intergenotypic competition on selection within Chrysanthemum progenies. Euphytica 34: 489-497.
MARTIN,M. M., AND J. HARDING. 1981. Evidence for
the evolution of competition between two species of
annual plants. Evolution 35: 975-987.
,AND. 1982. Estimates of fitness in Erodium populations with intra- and interspecific competition. Evolution 36: 1290-1298.
SAKAI,K. I. 1955. Competition in plants and its relation
to selection. Cold Spring Harbor Symposium on
Quantitative Biology 20: 137-1 57.
. 196 1. Competitive ability in plants; its inheritance and some related problems. In F. L. Milthorpe
[ed.], Mechanisms in biological competition. Symposium XV. Society for Experimental Biology, 245263. Academy Press, New York.
SCHUTZ,W. M., C. A. BRIMS,AND S. A. USANIS. 1968.
Intergenotypic competition in plant populations. I.
Feedback systems with stable equilibria in populations of autogamous homozygous lines. Crop Sci. 8:
61-66.
SHAW,R. G. 1986. Response to density in a wild population of the perennial herb Salvia lyrata: variation
among families. Evolution 40: 492-505.
SOKAL,R. R., AND F. J. ROHLF. 1981. Biometry, 2nd ed.
W. H. Freeman, San Francisco.
[Vol. 77
SOLBRIG,
O., AND B. B. SIMPSON.1977. A garden experiment on competition between biotypes of the common dandelion (Taraxacum ominale). J. Ecol. 65:
427-430.
STANTON,
M. L. 1984. Seed variation in wild radish:
effect of seed size on components of seedling and adult
fitness. Ecology 65: 1105-1 112.
TURKINGTON,
R., AND J. L. HARPER.1979. The growth,
distribution and neighbour relationships of Trifolium
repens in a permanent pasture. IV. Fine-scale biotic
differentiation. J. Ecol. 67: 245-254.
VIA, S. 1984. The quantitative genetics of polyphagy in
an insect herbivore. 11. Genetic correlations in larval
performance within and across host plants. Evolution
38: 896-905.
, AND R. LANDE. 1985. Genotype-environment
interaction and the evolution of phenotypic plasticity.
Evolution 39: 505-523.
WILKINSON,L. 1987. Systat: the system for statistics.
Systat, Evanston, IL.
WILLIAMS,
P. H. 1985. CffiC resource book. Department
of Plant Pathology, University of Wisconsin-Madison.
,AND C. B. HILL. 1986. Rapid cycling populations
of Brassica. Science 232: 1385-1 389.
WINN,A. A,, AND P. A. WERNER. 1987. Regulation of
seed yield within and among populations of Prunella
vulgaris. Ecology 68: 1224-1 233.