Download Population differentiation in Crepis tectorum (Asteraceae): patterns

Biological Journal of fhe Linnean SocieQ (1993), 49: 185-194. With 2 figures
Population differentiation in Crepis tectorurn
(Asteraceae):patterns of correlation among
characters
STEFAN ANDERSSON
Department of Systematic Botany, University
S-223 61 Lund, Sweden
Lund, 0. Vallgatan 18-20,
of
Received 3 October I S S I , accepled f o r publicafion 20 March I992
This study examines the relationship among traits distinguishing populations of C. fecforum and the
extent to which existing trait associations reflect underlying (genetic) tradeoffs. Highly consistent
trait associations were found in a comparison of 52 populations representing the western part of the
geographical range of the species. In addition to a tight integration of traits reflecting plant stature
and inflorescence development, there were consistent links between vegetative and reproductive
traits; populations characterized by individuals with large leaves and tall stems with terminal
branches usually had larger heads, flowers and fruits (achenes) than those whose individuals had
small leaves and a short stem branched from the base. There was a weak negative relationship
between the extent of leaf dissection and plant stature; short and compact plants had more deeply
lobed leaves than tall plants with terminal branches. Few of these associations were present among
families representing a single population of C. fecforum,but there was remarkable similarity between
the correlations at the between-population level and those obtained in two segregating F2 progenies
of crosses between contrasting populations. Hence, provided that the F2 correlations have a strong
genetic basis, it appears that the course of population divergence has been constrained by the
underlying correlation structure, although some trait associations may also be a result of selection
operating in a correlated fashion on functionally related traits, perhaps leading to linkage
disequilibrium of parental traits in the first segregating generation of a cross between ecologically
differentiated populations.
ADDITIONAL KEY WORDS:-Genetic
adaptation - pleiotropy.
correlations
-
morphology
correlated response
~
-
CONTENTS
Introduction . . . . . . . . .
Materials and methods
. . . . . .
. . . . . . . .
The plant
Comparative studies . . . . . .
Genetic analyses . . . . . . .
Results . . . . . . . . . .
Matrix comparison . . . . . .
Trait associations.
. . . . . .
Genetic correlations . . . . . .
Discussion
. . . . . . . . .
Trait associations and their genetic basis .
Adaptive changes and correlated responses
Acknowledgements . . . . . . .
References
. . . . . . . . .
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1993 The Linnean Society of London
186
S. ANDERSSON
INTRODUCTION
Whether a trait will evolve in response to natural selection depends on its
heritability and the extent to which different traits are affected by the same
genes (pleiotropy) or by different genes in linkage disequilibrium (Falconer,
1981). For instance, the origin of a new trait combination may be retarded if the
sign of the genetic correlation is opposite to the requirement of the habitat
(Antonovics, 1976; Lande, 1982), a common observation in plant populations
(Silander, 1985; Roach, 1986; Weis, Hollenbach & Abrahamson, 1987; Wolff &
Delden, 1987; Geber, 1990; Dorn & Mitchell-Olds, 1991; but see Mitchell-Olds,
1986; Mazer, 1989; Schwaegerle & Levin, 1991). Genetic correlations may also
lead to a non-adaptive change in a trait as a result of selection on another trait,
or facilitate changes in suites of traits that are correlated and selected in the same
direction (Sokal, 1978; Venable & Blirquez, 1990; Armbruster, 1991). Hence,
whether further micro-evolution will be retarded or enhanced depends on the
relationship between trait and fitness and the sign of the genetic correlation.
While reliable estimates of genetic correlations can improve predictions of the
short-term response to selection (Falconer, 198 1; Mitchell-Olds & Rutledge,
1986), it is more difficult to assess the role of genetic tradeoffs in previous
generations. An indirect approach is to search for trait associations at more than
one taxonomic level. For instance, correlations that are manifest both within and
between populations imply that genetic tradeoffs have constrained large-scale
patterns of variation (Sokal, 1978; Venable & Blirquez, 1990; Armbruster,
1991). Evidence for genetic constraints would also support the use of allometric
relationships as null models against which to test adaptation (Midgley, Cowling
& Lamont, 1991) and argue against comparisons based on overall similarity in
morphology; the genetic distance between two taxa may be overestimated if
there are strong genetic correlations among traits used to distinguish the taxa
(Grant, 1975).
Previous work has revealed a number of possible constraints in Crepis tectorum,
including a presumably ‘energetic’ tradeoff between offspring size and the
number of flowers (Andersson, 1989b) and a positive correlation between overall
plant size and the size of the floral structures (Andersson, 1989d). However, no
effort has yet been made to elucidate the genetic basis of these correlations in
order to rule out the possibility that associated traits evolved independently of
each other. In the present study, I describe the pattern of correlation among a
wide range of vegetative and reproductive traits and test the hypothesis that the
underlying correlation structure has constrained large-scale patterns of variation
in C. tectorum. Two approaches were used to reveal a genetic basis of existing trait
associations. The first approach was based on data obtained in a previous
quantitative genetic analysis of a natural population (Andersson, 199la), while
the second was based on patterns of character segregation in the F2 generation of
two crosses between widely different populations.
MATERIALS AND METHODS
The plant
Crepis lectorurn L (Asteraceae) is a diploid (2n = 8) weedy plant native to
Eurasia and introduced to North America. The species has undergone
PATlERNS OF CORRELATION IN C. TEC’TORUM
187
considerable morphological divergence, particularly in areas where the weed
type grades into more specialized forms adapted to rocky outcrops (Babcock,
1947; Anderson, 1989a-d, 1990, 1991a, b). Most plants behave as winter
annuals, germinating in the autumn, overwintering as leaf rosettes and flowering
in the following summer. Each inflorescence (‘head’) contains a large number of
ligulate flowers surrounded by protective involucral bracts. Fertilized flowers
develop into one-seeded indehiscent fruits (‘achenes’) as in all composites.
Comparative studies
Morphometric data from individuals from different populations raised in a
greenhouse were obtained with the aim of detecting consistent trait associations
in C. tectorum. I compared 52 populations from the western part of the
geographical range of the species (Europe and Canada) on the basis of the
median for each of 11 quantitative traits (Table I ) , all of which showed
significant among-population variation (P< 0.00 1 ; Kruskal-Wallis tests). I used
the medians rather than the means to reduce the influence of single outliers
(unpublished). Trait associations were expressed in terms of the Spearman rank
correlation coefficient ( rs) instead of the conventional product-moment
correlation coefficient, since transformations sometimes failed to improve
normality (unpublished). For some traits, I extended the analysis to the amongspecies level by using data from an extensive monograph on the genus (Babcock,
1947).
Genetic analyseJ
If genetic tradeoffs have constrained trait combinations in the course of
population divergence, one would expect to find similar associations among
genotypes within populations (Sokal, 1978; Venable & Burquez, 1990;
Armbruster, 1991). This idea was tested by calculating the rank correlations
based on the means of 40 greenhouse-grown families representing a single
population; each family consisted of 20-25 offspring derived from a maternal
TABLE
1. The traits measured in this study. All analyses were based on one measurement
per plant, the only exception being achene length which represents an average of two
achenes
~~~
Trait
Leaf traits:
Leaf dissection
Leaf length
Plant slature:
Plant height
Side branches
Basal branches
Head traits:
Peduncle length
Involucre length
Flowers per head
Ligule length
Head width
Achene length
Description (unit of measurement)
1 -(the smallest width between lobes/the maximum leaf width)
(mm)
(mm)
The proportion of nodes with side branches
The number of basal branches
Length of third side branch from the top (mm)
(mm)
(mm)
(mm)
(mm)
S. ANDERSSON
188
TABLE
2. Information on the parents (P) used in the F2 analyses
~~
~
Locality
Habitat
Cross no. I
P, Filehajdar, island of Gotland, Sweden
P, Bordeaux, France
Cross no. 2
P, Vickleby, island of Oland, Sweden
P, Algutsboda, Srnkland, Sweden
Outcrop
Ruderal weed
Outcrop
Weed in arable field
plant (Andersson, 1991a). Family-mean correlations yield rough estimates of the
extent to which genes have direct effects on more than one trait or are in linkage
disequilibrium with other genes (Falconer, 1981; Mazer, 1989).
Patterns of segregation among F2 progeny of crosses between populations
provided additional information on the extent to which existing trait associations
have a genetic basis (Grant, 1975; Dijk, 1984; Soltis, 1986). Seeds of two
segregating F2 generations were obtained by selfing F1 plants of crosses between
some of the populations used in the comparative study (Table 2). I raised a large
number of F2 plants in the greenhouse, scored the plants for traits that
distinguished the parents (P< 0.001, Mann-Whitney U-test) and calculated the
rank correlation coefficient among traits that segregated in the F2 generation (as
indicated by greater variance in the F2 than in the F1 generation). To examine
whether F2 correlations could reflect environmental responses in the same or in
the opposite direction, I performed a similar analysis of the non-segregating F1
generation to reveal correlations with a strong environmental component.
RESULTS
Matrix comparisons
The largest absolute values of the correlations were found between
populations of C. lectorurn (average r, = 0.391) and among species of Crepis
(average r, = 0.323), while trait correlations were weaker among maternal
families in a population of C. tectorum (average r, = 0.248) and among individual
plants in two segregating F2 progenies (average r, = 0.180 and 0.272, for cross
nos 1 and 2, respectively).
A comparison based on the individual correlations revealed great similarity
between the two F2 correlation matrices ( r , = 0.929) and between these and the
among-population correlation matrix (r, > 0.80; Fig. 1). The within-population
correlation matrix was moderately correlated to the among-population and F2
matrices (rs = 0.390-0.555), while only a weak correspondence was found
between the among-species matrix and the other matrices (rs < 0.277). N o
attempt was made to test the significance of these correlations (the data not
being independent).
Trait associations
Many significant correlations were detected in the between-population matrix
(Fig. 2A), although some of these may be an artefact of the large number of tests
performed ( = 55 pairwise correlations). Hence, I focus on correlations that were
PArTERNS OF CORRELATION IN C. TECTORUM
.
‘I
0.
I89
0
0
0
a
P
-1
0
1
F2 correlation
Figure I . The relationship between trait associations at the between-population level and in two
segregating F2 populations. The Spearman correlation coefficient was 0.802 and 0.977 for cross no.
I and 2, respectively.
significant at conservative levels of significance (P< 0.01 or 0.001). Traits
directly related to the development of the inflorescence and the individual
flowers (‘head traits’) were highly integrated, as shown by strong positive
correlations between the length of the branch supporting the head (peduncle
length), the length of the involucral bracts surrounding the flowers, the number
of flowers per head, the size of the flowers (ligule length), the diameter of the
flowering heads, and the size of the fruit associated with each flower (achene
length). Another group of related traits (‘plant stature’) distinguished
populations with a tall stem and terminal branches from those with a short stem
with side branches that have become ‘basal’ branches due to a secondary
shortening of the lowermost internodes (Fig. 2A).
Strong associations were also found between traits in different developmental
categories; populations characterized by the tallest stem and the largest leaves
usually had the largest involucral bracts, the widest heads, the largest flowers
and the largest achenes. The extent of leaf dissection varied independently of leaf
length but showed a weak relationship with plant stature; short and compact
plants had more deeply lobed leaves than tall plants with terminal branches.
There was no tradeoff between achene size and the number of flowers per head
(Fig. 2A).
Most of the trait associations in C. tectorum were also present at a higher
taxonomic level; large-leaved species of Crepis had a taller stem and higher values
of all head traits than those with smaller leaves; species usually exhibited large
(or small) values for several head traits simultaneously (Fig. 2B). However, plant
height was only weakly related to the head traits, contrasting with patterns
observed among populations of C. tectorum (Fig. 2A).
Genetic correlations
Attempts to relate trait associations within and between populations were
hampered by the few significant correlations detected at the within-population
S. A N D E R S O N
190
BETWEEN-POPULATIONCORRELATIONS (N = 62)
Leaf
branch-
F2 CORRELATIONS (CROSS NO 1; N = 186 - 197)
h f
Aehene
length
Achnnr
hngh
bmnchm
A
D
BETWEEN-SPECIES CORRELATIONS (N = 121 .193)
F2 CORRELATIONS (CROSS NO 2; N 31 175 - 185)
Ache-
Iad
khsne
P l ~ t
heisht
Plowon
perherd
branch-
E
B
-
BETWEEN-FAMILY CORRELATIONS (N 40)
Led
dismction
lengh
Achane
width
-
P co.001
-
Plant
height
Pc0.01
P < 0.05
Bad
bnnchm
Peduncle
hngh
C
Figure 2. Diagram showing the pattern of correlation among characters. Positive correlations are
shown with solid lines and negative correlations are shown with dashed lines (only for correlations
significant at the 5% level). Asterisks denote F2 correlations that were statistically significant in the
genetically uniform F1 generation.
level. The major trait association distinguished between families with a tall stem,
wide flower heads and large achenes and those with the opposite features
(Fig. 2C) and corresponds to a similar relationship among populations
(Fig. 2A).
PATTERNS OF CORRELATION IN C. TECTORUM
191
Analysis of segregating F2 progenies revealed a larger number of significant
correlations (Fig. 2D, E), most of which parallel those obtained at the amongpopulation level (Fig. 1). The segregation pattern not only confirms a strong
genetic correlation among traits in the same developmental category, but also
provides evidence for a genetic basis of the numerous links between plant stature
and head traits. The extent of leaf dissection and plant architecture were also
related; F2 plants with deeply lobed leaves were more compact and of shorter
stature than those with weakly lobed leaves. Achene length and the number of
flowers per head showed independent segregation in the F2 generation
(Fig. 2E). Similar results were obtained when flower number was expressed on a
per-plant basis (r, = -0.08, P = 0.27).
Few of the F2 correlations were significant in the F1 generations (marked with
asterisks in Fig. 2D, E), indicating that trait associations in the F2 generation
were largely genetic. However, the result may also reflect differences in statistical
power; the F1 correlations were based on smaller samples ( N = 39-40) than the
F2 correlations ( N = 175-197).
DISCUSSION
Trait associations and their genetic basis
The present study demonstrates consistent correlations among traits
distinguishing populations of C. tectorum. As expected, there were strong positive
correlations among developmentally related traits, particularly those reflecting
plant stature or the size of structures associated with the flower head (see also
Berg, 1960; Armbruster, 1991, but see Venable & Bfirquez, 1990). In addition to
a tight integration of traits related by development, there was a tendency for
populations to have either large or small values of traits reflecting the size of the
leaves, the main stem and the flower heads. Most of these associations also
occurred at the between-species level, the only exception being plant height
which varied more or less independently of the other traits. The link between
vegetative and reproductive features complements similar findings by other
authors (Primack, 1987; Giles & Bengtsson, 1988; Bond & Midgley, 1988;
Midgley & Bond, 1989; Thompson & Rabinowitz, 1989; Venable & Bh-quez,
1990).
A weaker trend distinguished between populations with a prostrate growth
form and deeply lobed leaves from those with a tall stature and weakly lobed
leaves; this correlation largely reflects the unusually short stem and the finely
divided leaves of subsp. pumila on the Baltic island of Oland (Andersson,
1989a, c). More data are needed to examine whether similar associations exist in
other species.
Although comparative studies sometimes provide insights into genetic
constraints on character evolution, only a genetic analysis can exclude the
possibility that associated traits have been integrated due to selection rather than
genetic tradeoffs. Yet, surprisingly few studies have examined the genetic basis of
trait associations above the population level (e.g. Venable & Bh-quez, 1990;
Grant, 1975; Dijk, 1984; Soltis, 1986). In the following, I examine the hypothesis
that underlying (genetic) correlations have constrained large-scale patterns of
variation in C. tectorum.
I92
S. A N D E R S O N
Population divergence should be easiest along the major axis of variation,
since there is a lack of variation for the alternative trait combinations. Hence,
provided that the genetic correlation structure has been stable, one would expect
that the pattern of correlation among a set of populations will be similar to the
pattern of correlation within these populations (Sokal, 1978; Venable &
Bfirquez, 1990; Armbruster, 1991). Genetic data from a single population of
C. tectorum (Andersson, 1991a) lend some support to this idea, but only for some
trait combinations; there were highly significant positive correlations between
plant height and head width and between head width and achene length. Apart
from these conservative associations, there was only a weak relationship between
the two correlation matrices (see also Venable & Blirquez, 1990), a reflection of
population divergence in quantitative genetic parameters (Mitchell-Olds, 1986)
or the use of maternal families; family-mean correlations may be biased for
various reasons (non-additive genetic effects, etc.; Falconer, 1981; Mitchell-Olds
& Rutledge, 1986).
In contrast, there was remarkable similarity between the between-population
correlation matrix and the two F2 correlation matrices; trait associations found
between populations were also detected in segregating progenies of crosses
between some of these populations. This is consistent with results of a detailed
analysis of leaf shape; both comparative and gene& evidence indicated a major
trend distinguishing between plants with lanceolate, wide and deeply lobed
leaves and those with the opposite features (Andersson, 1991b), Hence, provided
that differences among F2 plants have a strong genetic basis and that linkage
due to selection can be ruled out (see below), it seems that the underlying
correlation structure has indeed influenced the present-day pattern of variation
in C. tectorum.
Pleiotropy is usually regarded as the major cause of genetic correlations
among traits (Falconer, 1981), but linkage disequilibrium may also contribute to
trait associations (Grant, 1975; van Dijk, 1984; Soltis, 1986). Genetic linkage
seems likely in C. tectorum, considering the low chromosome number of this
species (2n = 8). The effect of linkage disequilibrium can be substantial in the
first segregating generation(s) of population crosses, particularly if the parental
differences involve a large number of adaptive characters. Hence, the following
discussion contains the caveat that the between-population and F2 correlations
could both arise from selection (see below). Analyses of further generations are
needed to distinguish between these hypotheses and to confirm the idea that
most F2 correlations have a strong genetic component (as suggested by F1 data).
That correlations among populations were of lower magnitude (though still
significant) in the F2 generations may reflect slight differences in growth
conditions; quantitative genetic parameters are valid only for the environment in
which they have been measured (Falconer, 1981).
The observation that large-scale patterns of differentiation can be predicted
from patterns of variation at a lower organizational level also applies to other
kinds of variation. Firstly, morphometric data of C. tectorum raised in a series of
differing environments showed that population divergence in the overall mean
has been greatest in the phenotypically most plastic traits and lowest in the least
plastic traits (Andersson, 1989~).Secondly, there appears to be a positive
correlation between the extent of divergence and the extent of variation among
family groups derived from a single population (Andersson, 1991a). Similarities
PATTERNS OF CORRELATION IN C. TECTORUM
193
in patterns of variation across taxonomic levels combined with evidence that
selection still operates on traits characterizing subsp. pumilu (Andersson, 1992)
support the view that processes acting within populations are sufficient to
account for diversity at higher levels (Sokal, 1978; Davis & Gilmartin, 1985).
Adaptive changes and correlated responses
The major evolutionary trend in C. lectorum reflects adaptation to shallow soil
on rocky outcrops, particularly in the Baltic region, where populations have
undergone considerable reduction in plant size compared with populations in
more mesic habitats (Andersson, 1989a-d, 1991a). While the short stem
probably evolved as a selective response to stressful conditions in the outcrop
habitat (drought, nutrient deficiency and wind exposure; Witte, 1906;
Andersson, 1989c, 1991a), it is more difficult to explain the small flower heads of
some of these populations. For instance, plants of the largely self-sterile subsp.
pumilu have less conspicuous heads than more or less autogamous plants of the
taller weed type (Andersson, 1989d), a surprising result considering the usual
observation that insect-pollinated plants have more attractive structures than
plants capable of automatic self-pollination (Ornduff, 1969). O n the basis of
genetic data (Fig. 2C-E), I suggest that some of the floral reduction in the
outcrop habitat may be a correlated response to selection for a smaller stature.
The small achenes of the decumbent outcrop plants may have a similar ‘non
adaptive’ explanation, although a functional explanation is also possible; small
size of propagules may increase the dispersability or the probability of becoming
incorporated in the seed bank (Andersson, 1990). Another presumably adaptive
association relates leaf shape and plant stature. The extremely dry and exposed
conditions on the Baltic island of Oland favour combinations of traits which
reduce transpiration and overheating, e.g. deeply lobed leaves and a short
stature, two distinctive features of subsp. pumilu (Andersson, 1989a, c). Hence,
the direction of selection and the sign of the genetic correlation (Fig. 2D, E)
probably converge for these traits.
Previous work on C. tectorum in southern Sweden indicated a possible tradeoff
between achene size and the number of flowers (Andersson, 1989b, c). However,
the present study indicates sufficiently independent control of these traits to
allow selection (or drift) to operate independently on them. There was no
correlation between achene size and the number of flowers when a large number
of populations was studied (Fig. 2A), nor was there any tradeoff between these
variables when genetic data were considered (Fig. 2C-E). This illustrates the
importance of genetic analyses or large comparative studies before any broad
generalizations are made regarding life-history ‘tradeoff?.
ACKNOWLEDGEMENTS
I would like to thank K. Ryde for linguistic advice, the staff of various
botanical gardens for providing seed material and M. Lawrence and an
anonymous reviewer for their comments. Technical assistance by Monica
Christiansson and Helena Persson is also acknowledged.
I94
S. ANDEKSSON
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