Major Gene Effects During Weed Evolution:
Phenotypic Characters Cosegregate With
Alleles at the Ray Floret Locus in Senecio
vulgaris L. (Asteraceae)
H. P. Comes
Ray floret length was used as a codominant marker to test for associations with
phenotypic characters in two F2 progenies (F2A and F2B) derived from crosses between the nonweedy, late-developing Senecio vulgaris subsp. denticulatus and its
weedy, early developing derivative subsp. vulgaris var. vulgaris. Variance analytical
tests between the three marker genotype classes indicated that the chromosomal
region associated with the ray floret locus controlled more than 10% of the phenotypic variation of 9 of the 17 characters analyzed in F2B. Particularly pronounced
associations (r 2 5 28–37%) were found between the marker alleles and leaf number,
pedicel length, and number of involucral bracts. In addition, formal linkage analysis
between the ray floret locus and the previously postulated dominant gene affecting
early development was positive (r 5 0.15 6 0.02). Estimates of dominance relationships at individual quantitative trait loci (QTLs) situated near the ray floret locus
indicated directional dominance for a reduction of vegetative and reproductive
structures, because the heterozygote marker class tended to be more similar to
the weedy derivative, var. vulgaris. This may be interpreted as evidence for past
directional selection acting on these characters. Taken together, it is suggested
that a single chromosomal region within S. vulgaris exhibits a substantial proportion of nonadditive gene effects, contrasting strongly with the traditional additivepolygenic model of the genetic basis of evolutionary divergence in the wild.
From the Institut für Spezielle Botanik und Botanischer
Garten, Johannes Gutenberg-Universität Mainz, Bentzelweg 9, 55099 Mainz, Germany. I wish to acknowledge Dr. Kirsten Wolff, Dr. Richard J. Abbott, and Dr.
Andrew J. Lowe (St. Andrews University, Scotland) for
critically reading the manuscript, Prof. Joachim W. Kadereit (Mainz University, Germany) for constructive
comments throughout the study, and two anonymous
reviewers for their critical comments on an earlier
draft of this article. I am also grateful to Dr. François
Bretagnolle ( Neuchâtel University, Switzerland) for detailed statistical advice. This research was supported
by an LGFG doctoral grant from the Land Baden-Württemberg, Germany.
Journal of Heredity 1998;89:54–61; 0022-1503/98/$5.00
54
Understanding the genetic basis of plant
speciation is a primary goal in evolutionary biology. Because the success of taxa
to become reproductively isolated from
each other often depends on the amount
of genetic differences acquired (Mayr
1963), the characterization of the genetic
basis of phenotypic differences between
ecological races or between related species is fundamental for the study of adaptive phenotypic evolution. In particular,
the number of genes controlling a trait,
the magnitude of their effects, and the genomic organization of such genes are critical in understanding the rapidity and
mode of evolutionary change ( Fisher
1958; Hill 1982; Kimura 1983; Mitchell-Olds
and Rutledge 1986).
The point has been made many times
that evolutionary divergence often involves selection acting on quantitative
polygenic systems (Charlesworth 1984;
Coyne and Lande 1985). Empirical support
for multifactorial evolution comes for example from analyses of the genetic architecture of mating system traits that mainly
consists of a rather large number of genes
with relatively small, primarily additive ef-
fects ( Fenster and Ritland 1994, and references therein). Most recently, however,
genome mapping in Mimulus has revealed
genes of large effect controlling floral
traits associated with reproductive isolation ( Bradshaw et al. 1995). Similarly, major genes with large allelic effects influencing components of fitness such as flowering time are being increasingly hypothesized as playing a central role in natural
plant populations (Arabidopsis, MitchellOlds 1996; Senecio, Comes and Kadereit
1996).
Although the genetics of phenotypic differences between ecological races or between related species has received extensive attention from botanists for several
decades (Orr and Coyne 1992), surprisingly little investigation has been devoted to
the genetic basis of phenotypic changes
surrounding the origin of weeds. As already pointed out by Stebbins (1965), valid data can be obtained by the genetic
analysis of synanthropic taxa and their
nonweedy progenitors. Since the synanthropic component is likely to have
evolved only recently, that is, only after
man-made habitats have become avail-
Figure 1. F2 frequency distribution (from two progenies pooled) for time from germination to bud formation and fitted underlying normal distributions, with respective
means designated by arrows. Overlap between the two fitted distributions is 1.5% and represents the probability of phenotype misclassification given a discrimination point
of approximately 42 days. Probable outliers, excluded from the analysis, are indicated by asterisks. See Comes and Kadereit (1996) for more details.
able, the amount of evolutionary divergence following differentiation should be
comparatively low in these model systems. Therefore their genetic analysis
makes it more feasible to identify changes
that occurred during the process of differentiation and not subsequent to it (Macnair and Cumbes 1989).
In this article I focus on the genetics of
a synanthropic subspecies in the genus
Senecio L. sect. Senecio (Asteraceae) and
its nearest nonweedy relative. The two focal taxa are S. vulgaris L. subsp. denticulatus (O. F. Muell.) P. D. Sell and S. vulgaris
L. subsp. vulgaris var. vulgaris ( both 2n 5
4x 5 40). Subspecies denticulatus is a winter annual herb restricted to Atlantic maritime and Mediterranean montane areas in
Europe ( Kadereit 1984b; Perring and Sell
1968) that shows pronounced seed dormancy ( Kadereit 1984b) and normally produces an outer ring of ray florets up to 3
mm long, whereas var. vulgaris is a cosmopolitan weed lacking ray florets. Occasionally seed dormancy can also be found
in Mediterranean var. vulgaris (Ren and
Abbott 1991; Comes 1995a) but otherwise
is absent from this taxon. Based on the
natural geographical distribution of
subsp. denticulatus and its specialized
maritime habitat (at least in western Europe; Comes 1995b), it has been assumed
that subsp. denticulatus is the predecessor
of the weedy var. vulgaris, or close to such
( Kadereit 1984a,b). Both taxa are predominantly self-pollinating and form hybrids
exhibiting up to 73% seed fertility (Comes
1994).
Data from previous genetic studies (e.g.,
Hull 1974; Trow 1912) have established
that the presence or absence of ray florets
in S. vulgaris is controlled by a single, incompletely dominant locus, with the longrayed subsp. denticulatus homozygous for
the dominant R allele, the discoid var. vulgaris homozygous for the recessive r allele, and their short-rayed F1 hybrids heterozygous for both alleles. More recently
it was reported that taxon differences in
speed of development can also be attributed to hereditary factors (Comes and
Kadereit 1996). In these studies crosses
between the early developing var. vulgaris
and the late developing subsp. denticulatus
produced an F2 that had an early:late ratio
not significantly different from that expected under a single gene model of inheritance, with early development dominant over late. Accurate discrimination between early and late F2 phenotypic classes
was possible due to a small overlap between two underlying normal distributions fitted to the data ( Figure 1). Another
character which is known to show discrete disomic and dominant inheritance in
crosses between the taxa is the absence
of seed dormancy ( Kadereit 1984b). Taken
together, it thus appears that the initial
ecological shift from the weedy to the nonweedy condition in S. vulgaris is due to selection for (1) loss of seed dormancy, (2)
early flowering, and (3) loss of ray florets,
with each of the three traits being controlled by a single gene.
Given the simple nature of intraspecific
capitulum variation in S. vulgaris and its
suitability for serving as a marker polymorphism (e.g., Abbott 1986; Abbott et al.
1992), I examine here the association patterns between the polymorphism for capitulum type and a number of quantitative
characters, analyzing F2 progenies of a
cross between subsp. denticulatus and var.
vulgaris. However, in contrast to previous
investigations into quantitative variation
associated with capitulum type in S. vulgaris (reviewed by Abbott 1986; Oxford et
al. 1996), capitulum type is scored here as
a quantitative gene effect via the expression of ray floret length, and not as a qualitative, dominant gene effect via the presence [RR, Rr] or absence [rr] of ray florets.
This approach has the advantage of utilizing the ray floret gene as a codominant
marker locus, with genotypes [TrTr],
[TrTn], and [TnTn] for long-rayed, shortrayed, and discoid plants, respectively
(see Hull 1974 for allele designation); it
thus allows complete classification of genotypes in F2 progenies, and consequently
permits examination of dominance relationships at individual quantitative trait
Comes • Cosegregation in Senecio vulgaris 55
loci (QTLs) putatively linked to the ray floret marker.
Explicitly the following questions have
been addressed. (1) Are there significant
associations between the ray floret locus
and character variation distinguishing the
weedy derivative and its nonweedy progenitor? (2) If significant associations exist, what is the genetic architecture of the
suite of characters, that is, are genes of
small additive effect involved or ones of
large, nonadditive effect? (3) What is the
linkage relationship between the previously identified major gene controlling speed
of development and the ray floret locus?
Materials and Methods
Plant Materials
One population from each taxon was chosen for study and collected for achenes:
(1) a long-established winter annual population of subsp. denticulatus on Jersey
(Channel Islands, Les Quennevais, North
of La Pulente), restricted to carbonate-rich
and nutrient-poor soils of open, stabilized
dunes and open turf (Comes 1995b); (2) a
population of var. vulgaris in the Botanic
Garden, Heidelberg University, Germany.
Crossing Design and Characters Scored
Two F2 progenies (A and B) were generated by self-pollinating two F1 half-sibs
from crosses between a single plant of var.
vulgaris (used as female parent) and two
plants of subsp. denticulatus. Further F1
progeny were produced at the same time.
All crosses were produced by Alexander’s
(1979) emasculation technique, which has
been shown to reduce the degree of residual selfing to less than 4% (Comes and
Kadereit 1996). F1 hybrids were verified by
the presence of short, stubby ray florets.
Parental stocks of subsp. denticulatus and
var. vulgaris were maintained by random
selfing of individuals within each taxon.
F2 progenies were grown simultaneously
with parental and F1 samples. Plants were
grown in 10 cm plastic pots under outdoor
conditions using six randomized blocks.
Two-way analysis of variance (ANOVA)
comparison revealed that the two F2 progenies (A and B) were significantly (P , .01)
different from each other for a number of
traits studied, so their data were not
pooled. This analysis also revealed that
block (i.e., local environmental) factors
and family 3 block effects (i.e., gene-environment interactions) were generally insignificant (data not shown). If not indicated otherwise, only the recordings for
56 The Journal of Heredity 1998:89(1)
Table 1. Description of traits analyzed in Senecio, with code designations appearing in Tables 2 and 3
No.
Trait
Code
Measured at anthesis of first capitulum
1.
Stem height (cm)
2.
No. of leaves on main stem
3.
Pedicel length of first capitulum (mm)
STH
NL
PL
Measured at fruiting of first capitulum
4.
No. of lateral branches from main stem
5.
Longest internode length on main stem
6.
Longest leaf length (cm)
7.
Longest leaf width (cm)
8.
Longest leaf length:width ratio
9.
Longest leaf area (cm2)
NB
LIN
LL
WL
SL
AL
Measured on a capitulum of an early branch
10.
No. of outer involucral bracts
11.
Capitulum length (mm)
12.
Capitulum width (mm)
13.
Capitulum length : width ratio
14.
Ligule length (mm)
15.
No. of disc florets
16.
No. of florets
NOIB
LCAP
WCAP
SCAP
LRAY
NDISC
NFLORET
Scored on an isolated capitulum of an early branch
17.
No. of achenes
18.
Percentage seed set
NACH
SET
the parental and F2 progenies are reported
here.
A total of 18 quantitative characters
were measured for each plant in all progenies. These characters are listed in detail
in Table 1. Attention was principally focused on vegetative, floral, and reproductive characters that contribute conspicuously to intraspecific differences in certain
annual and winter annual species of sect.
Senecio (Comes 1995a). No attempt was
made to include all characters that are
taxonomically important to distinguish
the parental taxa. Measurements of leaf
area were made using a HAFF Planimeter
No. 315 E. Floral measurements and
counts were made on a single capitulum
of an early flowering branch, stored in 70%
ethanol until usage. Most measurements
were made using caliper rules or calipers
and are accurate to 0.2 mm. Ray floret
length was measured from the apex of the
ligule to the distal part of the floral tube
using either an ocular micrometer to within 0.04 mm, or millimeter paper to within
0.2 mm (only subsp. denticulatus).
Statistical Analysis
The two F2 populations segregated for the
ray floret marker. Goodness-of-fit to a codominant ratio of 1:2:1, expected for an F2,
was tested by chi-square analysis. Associations between alleles at the ray floret
locus and all scored quantitative traits
were detected by comparing variation between allelic classes with variation within
classes, using single-factor ANOVA F statistics. As the number of comparisons
made between allelic classes increases in
the ANOVA, so too does the probability
that a type I statistical error will occur. In
order to eliminate this bias, sequential
Bonferroni tests (Rice 1989) were conducted to determine table-wide statistical
significance (a 5 0.05) for the 17 hypothesis tests for each character within each
of the two F2 populations. Nonparametric
statistics ( Kruskal–Wallis test, Wilcoxon’s
two-sample test), which do not depend on
the assumption of homogeneous variances (Sokal and Rohlf 1981) were also
computed, but were consistent with the
results of the ANOVAs given here.
To determine the magnitude of the phenotypic effect of QTLs that are putatively
linked to the ray floret marker, the proportion of phenotypic variance explained
by the marker locus genotype classes was
computed by using the general linear
model (GLM) procedure of SAS ( VMS version of SAS release 6.07; SAS Institute Inc.
1988). This fraction is indicated by the r2
value of the variance-analytical regression
model. Comparisons between the parental
taxa, as well as the mean F2 phenotypic
values of the three genotype classes were
made using Tukey’s test (Steel and Torrie
1980), evaluated at a significance level of
1%. From the means of homozygous and
heterozygous F2 genotype classes, the ratio of dominant (d) to additive (a) gene
effects at a putative QTL was estimated
with a statistic modified after Stuber
(1989):
A/B 2 [(A/A 1 B/B)/2]
5 (1 2 2r) d/a
(B/B 2 A/A)/2
where A and B are the alleles at the ray
floret locus and r is the recombination frequency between the latter and the QTL.
Estimates of this ratio, which describe the
degree to which the heterozygous genotype class (A/B) resembles either the
greater ( B/B) or lesser (A/A) homozygote
class (d/a . 0 or d/a , 0), can be regarded
as only approximate, because information
on r is generally lacking. Though an increase in r (maximum 0.5) would certainly
cause a downward bias of estimates, it is
assumed that significant differences between genotype classes are indicative of
small r values (e.g., Edwards et al. 1987).
The recombination frequency between
the ray floret marker and the previously
identified gene controlling speed of development was calculated using an F2 maximum likelihood algorithm published by Allard (1956), and their map distance, presented in centiMorgans (cM), was derived
employing the Kosambi function ( Kosambi 1944). All computations were accomplished using the computer package Linkage-1 version 3.50, by Suiter et al. (1983).
Results
Segregation of the Morphological
Marker Locus
The observed bimodal phenotypic F2 distribution for ray floret length clearly reflected segregation at the ray floret locus
( Figure 2). Based on variation among contemporaneous subsp. denticulatus plants,
radiate F2 individuals with a ray floret
length shorter than 2 mm were classified
as short rayed, while those having a
length of 2 mm or longer were considered
long rayed. The data of 80 discoid [TnTn]
individuals, together with 171 short-rayed
[TrTn] and 79 long-rayed [TrTr] individuals
adequately fitted their expected codominant ratio of 1:2:1 (for F2A, x2[2] 5 1.02, .75
. P . .5; for F2B, x2[2] 5 0.01, P 5 .995;
pooled data, x2[2] 5 0.44, .9 . P . .75).
Although there still remains an unknown
amount of inaccuracy in identifying the genotype of radiate F2 individuals, these results provide evidence for the utility of ray
floret length as a codominant morphological marker.
Associations Between the Ray Floret
Locus and Quantitative Traits
The parental values for the traits listed in
Table 1 are shown in Table 2, and the corresponding F2A and F2B values of the three
genotype classes [TnTn, TrTn, and TrTr], together with the essential results of the
cosegregational analysis, are summarized
in Table 3A and B, respectively.
Figure 2. Frequency distributions for ray floret length in S. vulgaris subsp. denticulatus and F1 and F2 progenies
derived from a cross with the rayless var. vulgaris ( F2 data from two progenies pooled).
Of those 17 traits examined in both F2
progenies, 8 traits within F2A (47.1%) and
15 within F2B (88.2%) showed statistically
significant associations with the marker
locus as indicated by the sequential Bonferroni procedure. All associations significant in the F2A progeny were also present
in the larger F2B population. These included associations of the marker with leaf
number, pedicel length, leaf length, and all
floral characters except capitulum width.
The proportion of the phenotypic variation explained by the marker locus (r2)
was generally lower in the F2A than in the
F2B progeny. It is likely, however, that lower predictability of marker genotypes in
the F2A population was more influenced
by statistical chance effects due to small
sample size rather than by an unknown biological effect peculiar to that progeny. In
the following, therefore, all results reported will refer to the F2B population, if not
stated otherwise.
With respect to leaf length, leaf area,
pedicel length, and number of outer involucral bracts, the proportion of phenotyp-
Comes • Cosegregation in Senecio vulgaris 57
Table 2. Number of observations (N), mean
values (X), and standard errors (SE) analyzed in
S. vulgaris subsp. denticulatus and S. vulgaris
var. vulgaris grown together with their F 2; means
sharing the same superscript are not significantly
different (P , .01, Tukey’s test)
Subsp. denticulatus
Var. vulgaris
Trait
N
Vegetative
STH
NL
PL
NB
LIN
LL
WL
SL
AL
131 9.7b
130 18.9b
124 4.6a
130 11.7b
130 22.3b
122 5.8b
122 2.1b
122 2.8b
121 4.8b
Floral
NOIB
LCAP
WCAP
SCAP
NDISC
NFLORET
Reproductive
NACH
SET
X
99 14.9b
98 7.95a
99 4.32a
98 1.84a
99 58.3a
99 58.3a
127 28.3a
127 46.1b
SE
N
X
SE
0.24
0.17
0.21
0.39
0.44
0.07
0.04
0.03
0.12
68
68
67
55
56
44
44
44
44
23.9a
30.3a
4.1a
15.5a
27.9a
8.7a
2.6a
3.5a
6.6a
0.76
0.43
0.19
0.45
0.92
0.19
0.06
0.10
0.25
0.25
0.048
0.030
0.015
0.76
0.76
62 21.0a
61 7.71a
62 4.43a
61 1.74b
62 52.2b
61 62.3a
0.64
0.074
0.038
0.019
0.91
1.01
1.03
1.59
46 30.7a
46 50.8a
1.92
3.12
ic variance explained by the morphological marker ranged from 17–37%. For all
other vegetative traits analyzed, variation
in marker locus genotypes accounted for
much less of the phenotypic variation
present. Although significant differences
between F2B genotype classes were observed for stem length, number of branches, internode length, and leaf width, only
2–7% of the total phenotypic F2B variation
could be traced back to variation at the
ray floret locus. The cosegregation of the
marker with capitulum dimensions and
(disc-) floret number still explained 7–20%
of the corresponding variances. Marker
prediction in absolute seed set (only significant in F2B) was poor, with an r2 value
of 5%.
With the exception of branch number,
variation in the discoid class [TnTn] was
generally in the direction of var. vulgaris.
For example, discoid F2B plants possessed
on average 20.0 leaves, while the homozygous radiate individuals showed on average 27.5 leaves—a difference which
equaled 65.8% of the difference in the parental controls. Similarly the mean difference in leaf length associated with the two
homozygous classes was 2.4 cm in both F2
progenies, corresponding to 82.8% of the
parental difference. For a large number of
characters in each F2 progeny, the heterozygous radiate [TrTn] marker class did not
differ significantly (P , .01) from the discoid one [TnTn]. These included: leaf num-
58 The Journal of Heredity 1998:89(1)
ber, pedicel length, bract number, capitulum length and shape, and floret number.
Dominance Relationships at QTLs
For those traits found to be significantly
associated with alleles at the marker locus, a wide range of gene effects were observed in both F2 progenies ( Table 3). Approximately 25% ( F2A) and 40% ( F2B) of
these characters had ratios of dominance
to additive effects of 0.55 or less, indicating additive or only partially dominant
gene action ( Edwards et al. 1987). A comparatively large proportion of traits, 62%
in F2A and 47% in F2B, were partially dominant or dominant, with values ranging between 0.55 and 1.25. Only a small fraction
of traits, 13% in both F2A and F2B, exhibited ratios exceeding 1.25, implying overdominance/underdominance (i.e., heterosis) for chromosomal regions associated
with the ray floret locus.
In each F2 progeny, (partial) dominance
or heterosis was generally in the direction
of the discoid individuals, that is, in the
direction of var. vulgaris ( Tables 2 and 3).
Of those traits significantly associated
with the marker locus, only branch number in F2B showed overdominance in the
direction of subsp. denticulatus. Pronounced additivity (ø d/a ø 0) was found
for leaf length, width, and area ( both latter
traits only significant in F2B). For all traits
consistently associated with the ray floret
locus, gene action did not vary markedly
among progenies.
Linkage Relationship Between the Ray
Floret Locus and the Major Gene for
Speed of Development
A previous genetic study (Comes and Kadereit 1996) involving the present cross indicated that speed of development in S.
vulgaris is controlled by a major gene
( here arbitrarily called [G/g]) with the
trait expressions ‘‘early’’ and ‘‘late,’’ and
with homozygous recessive plants exhibiting late development. A total of 329 F2
individuals were classified for ray floret
length, based on the criteria given above,
and for the time to bud formation, given a
discrimination point of 42 days between
early and late developing plants and assuming a 1.5% probability of early/late
misclassification ( Figure 1). With parental
genotypes of var. vulgaris and subsp. denticulatus designated as [GGTnTn] and [ggTrTr], respectively, and assuming independent assortment of the speed of development locus and the ray floret locus, the F2
was expected to provide six phenotypic
classes in a Mendelian ratio of 3:6:3:1:2:1.
A chi-square contingency test revealed a
highly significant deviation from the Mendelian expectation (pooled data F2A and
F2B, x2[2] 5 137.2, P , .001). However, the
recombination frequency between the pair
of loci remained rather high, r 5 0.15 6
0.02 (15.37 cM 6 2.10), suggesting only
‘‘loose’’ linkage and the possibility of recombination events between the ray floret
locus and the major gene controlling
speed of development.
Discussion
Association of Alleles at the Ray Floret
Locus With Quantitative Characters
Determining the genetic basis of phenotypic changes during plant speciation is
critical both to understanding how and at
what rate species respond evolutionarily
to changing environmental conditions and
to evaluating alternative genetic models of
speciation. To do this requires the availability of adequate model systems of comparatively young geologic age, allowing direct insights into the genetic changes involved. Taxa that have recently evolved
into weeds and their nearest nonweedy
relatives provide such excellent experimental material.
In this study, the genetic analysis of the
nonweedy S. vulgaris subsp. denticulatus
and its weedy derivative var. vulgaris revealed that a significant portion of the vegetative and floral differences between the
two taxa can be explained by the segregation of the ray floret locus. With respect
to the larger F2B progeny and using the
sequential Bonferroni procedure for declaring a marker effect significant, this major gene, that is, the chromosomal region
associated with it, controlled more than
10% of the phenotypic variation of 9 of the
17 characters analyzed ( Table 3B). However, an important caveat must be introduced at this point. Throughout this article, significant associations are interpreted as indicating linkage between the ray
floret marker and individual QTLs affecting the trait, but given the linkage relationship between the ray floret marker and the
major gene controlling speed of development (15.37 cM 6 2.10), pleiotropic or developmental (epistatic) effects of each of
the two major genes on all quantitative
traits measured may not be excluded a
priori. However, in a preceding study
(Comes 1994) it was found that variation
in none of these traits is controlled by a
single gene locus, so pleiotropic effects of
the major genes would be highly unlikely
to create the association patterns ob-
Table 3. Number of observations (N), mean values (X), and standard errors (SE), F values, results of Tukey’s test, and fraction of phenotypic variation
explained by the ray floret locus (r2) for characters analyzed in discoid [TnTn], heterozygous radiate [TrTn], and homozygous radiate [TrTr] individuals of two F2
Senecio progenies F 2A (Panel A) and F 2B (Panel B)
Discoid [TnTn]
Short-rayed [TrTn]
N
X
SE
Vegetative
STH
NL
PL
NB
LIN
LL
WL
SL
AL
28
28
27
27
27
25
25
25
25
17.1a
20.0b
6.7a
13.9a
28.9a
7.2b
2.2a
3.4a
5.9a
0.89
0.60
0.49
0.47
1.11
0.25
0.13
0.18
0.49
Floral
NOIB
LCAP
WCAP
SCAP
NDISC
NFLORET
27
26
26
26
27
27
14.7b
8.52a
4.63a
1.85a
66.9a
66.9b
Reproductive
NACH
SET
21
21
Vegetative
STH
NL
PL
NB
LIN
LL
WL
SL
AL
N
Long-rayed [TrTr]
ø d/a
X
SE
N
X
SE
F value
P value
r2
66
66
61
63
63
56
56
56
53
18.2a
20.7b
6.4a
13.5a
28.5a
7.7ab
2.3a
3.3a
6.5a
0.69
0.46
0.30
0.36
0.89
0.16
0.06
0.06
0.30
27
27
27
23
23
19
19
19
19
20.6a
26.9a
3.3b
12.5a
27.2a
8.4a
2.4a
3.5a
6.6a
1.25
0.89
0.35
0.51
1.50
0.25
0.08
0.12
0.31
2.79
29.70
20.49
1.89
0.41
5.78
0.73
0.79
0.72
0.0637
,0.0001*
,0.0001*
0.1537
0.6701
0.0044*
0.4888
0.4604
0.4937
0.05
0.33
0.28
0.03
0.01
0.11
0.02
0.02
0.02
20.37
20.80
0.82
0.43
0.53
20.17
0.00
23.00
0.71
v
v
v
d
v
v
—
v
d
0.65
0.110
0.078
0.035
2.39
2.39
66
66
66
66
66
66
15.2b
8.36a
4.72a
1.78a
58.4b
68.9b
0.48
0.077
0.049
0.022
3.79
1.20
27
27
27
27
27
27
20.4a
7.70b
4.79a
1.62b
67.1a
79.0a
1.21
0.118
0.090
0.034
2.52
2.74
14.93
14.43
0.96
12.13
9.10
9.25
,0.0001*
,0.0001*
0.3879
,0.0001*
0.0003*
0.0002*
0.20
0.20
0.02
0.17
0.13
0.14
20.83
0.61
0.13
0.40
286.00
20.67
v
v
d
v
v
v
18.7a
28.0a
3.57
5.11
55
55
27.1a
39.4a
2.54
3.46
18
18
31.4a
38.8a
4.89
5.53
2.45
1.69
0.0899
0.1883
0.05
0.04
0.32
1.11
d
d
51
51
46
52
52
47
47
47
47
19.9b
20.0b
7.6a
13.8ab
32.0a
7.3c
2.4b
3.3a
6.1c
0.82
0.52
0.41
0.46
0.92
0.19
0.08
0.15
0.29
103
103
101
103
102
93
93
93
93
21.4ab
21.5b
7.0a
14.5a
32.4a
8.5b
2.6ab
3.3a
7.5b
0.55
0.35
0.25
0.25
0.70
0.15
0.05
0.06
0.22
52
52
49
48
48
32
32
32
32
23.7a
27.5a
3.6b
12.6b
27.8b
9.7a
2.8a
3.6a
8.9a
0.78
0.58
0.33
0.41
0.96
0.22
0.08
0.11
0.41
5.87
60.65
37.33
7.45
7.73
28.44
6.74
1.88
16.78
0.0035*
,0.0001*
,0.0001*
0.0009*
0.0007*
,0.0001*
0.0069*
0.1534
,0.0001*
0.05
0.37
0.28
0.07
0.07
0.25
0.07
0.02
0.17
20.21
20.60
0.70
2.17
1.19
0.00
0.00
21.00
0.00
v
v
v
d
v
—
—
v
—
Floral
NOIB
LCAP
WCAP
SCAP
NDISC
NFLORET
52
51
51
51
51
51
14.4b
8.50a
4.54b
1.88a
66.7a
66.7b
0.47
0.093
0.062
0.026
1.38
1.38
105
105
105
105
105
105
14.6b
8.45a
4.64ab
1.84a
57.2b
67.3b
0.36
0.056
0.040
0.017
0.92
1.03
52
52
52
52
52
52
20.8a
8.00b
4.84a
1.66b
67.6a
79.3a
0.73
0.093
0.051
0.023
1.57
1.70
45.26
11.70
7.38
25.47
25.44
24.69
,0.0001*
,0.0001*
0.0009*
,0.0001*
,0.0001*
,0.0001*
0.31
0.10
0.07
0.20
0.20
0.19
20.94
0.80
20.33
0.64
222.11
0.91
v
v
v
v
v
v
Reproductive
NACH
SET
50
50
21.7b
31.0a
2.63
3.62
88
88
26.2ab
38.3a
2.01
2.78
41
41
34.2a
44.6a
3.28
3.86
4.83
3.24
0.0091*
0.0405
0.05
0.04
20.28
0.07
v
d
Trait
Da
Panel A
Panel B
a
Direction of the dominant effect, that is, if the heterozygote marker class resembles var. vulgaris (v) or subsp. denticulatus (d).
Group means sharing the same superscript are not significantly (P , .01) different. P values from one-way ANOVAs found to be significant at a table-wide a 5 0.05 with
sequential Bonferroni adjustments (Rice 1989) are indicated by asterisks, otherwise values are nonsignificant. Also given is the approximate ratio of dominance to additive
effects (ø d/a).
served. Nonetheless, it is feasible that a
significant portion of the variance in several quantitative traits may be influenced
by developmental constraints imposed by
the epistatic interaction of alleles at each
of the two major genes with different
regions of the genome, and this possibility
requires further investigation.
It has to be pointed out that assaying
the ray floret gene as a codominant marker is clearly advantageous compared to its
use as a qualitative, dominant-recessive
one with the character states ‘‘radiate’’
and ‘‘discoid.’’ Subsuming the heterozygote marker class into the dominant class
of ‘‘radiate’’ individuals normally would
have resulted in an underestimate of the
r2 value of the regression model and its
overall significance, with not a single comparison in the F2A, and only 47% rather
than 70% of the comparisons showing P
values of less than .001 in the F2B (Comes
HP, unpublished data). Limited statistical
resolution of dominant marker-based predictability of phenotypic trait expression
is most likely due to the fact that the direction of effects of many QTLs analyzed
here do not match with the a priori assumption that the presence of a single
dominant denticulatus allele [R] at the ray
floret locus is already associated with a
denticulatus-like phenotype. This is in-
ferred from the above comparisons of discoid [TnTn] and heterozygous radiate
[TrTn] marker classes, revealing nonsignificant (P , .01) differences for several vegetative and floral traits ( Table 3).
Since presence versus absence of ray
florets in various Asteraceae has often
been claimed to have a simple genetic basis, the results presented here can be contrasted with other recent investigations
into the suite of characters associated either with capitulum variation within populations or the evolutionary shift from the
radiate to the discoid condition among
closely related taxa. Thus British populations of S. vulgaris often contain two ca-
Comes • Cosegregation in Senecio vulgaris 59
pitulum morphs (radiate and discoid) in
addition to a rare short radiate one, a situation most likely resulting from introgressive hybridization involving S. squalidus L.
(e.g., Abbott 1992). Extensive genecological research has demonstrated that differences between the radiate and discoid
morphs do exist for various life-history
traits, such as germination behavior, flowering time, and reproductive capacity (reviewed by Abbott 1986; Theaker and
Briggs 1992). In a recent article Oxford et
al. (1996) provide cosegregational evidence suggesting that the reasons for
these differences are complex and may
vary across populations. The different degrees of associations found among the
three populations studied appear to reflect various stages in an evolutionary scenario that includes (1) introgression of an
S. squalidus linkage group containing the
radiate allele, among others; (2) its subsequent disruption by chromosomal rearrangements over time; and (3) the persistence of resulting chance associations because of low levels of outcrossing. At this
point it is certainly premature to speculate
on any structural similarities or even evolutionary relationships between the gene
cluster identified by Oxford et al. (1996)
and the hypothesized linkage group described in the present article.
Major gene associations of capitulum
type with quantitative characters have
also been reported in an interspecific
cross of the progenitor-derivative pair Layia glandulosa ( Hook.) Hook. & Arn. and L.
discoidea Keck ( Ford and Gottlieb 1989).
Although radiate and discoid F2 plants
were found to differ significantly in a number of floral traits, they did not differ consistently in vegetative ones. Moreover, in
a series of backcross progenies with L. discoidea as recurrent parent, radiate and
discoid plants only differed slightly in pappus length, but not in other traits. In Layia,
however, complete classification of marker genotypes in hybrid progenies, and
consequently estimates of gene effects at
individual QTLs putatively linked to the
morphological marker, cannot be straightforwardly obtained because variation in
capitulum type is controlled in a complex
manner by two epistatically interacting
genes ( Ford and Gottlieb 1990).
Amount and Direction of Dominance at
QTLs
According to theoretical models ( Broadhurst 1979; Fisher 1958; Mather and Jinks
1982), natural selection is expected to promote dominance of favorable alleles,
60 The Journal of Heredity 1998:89(1)
masking the less fit, supposedly intermediate phenotype of the heterozygote. As
expected, in the case of significant (P ,
.01) differences between the means of discoid [TnTn] and homozygous radiate [TrTr]
F2 plants, all discoid plants varied in the
direction of S. vulgaris var. vulgaris, while
all radiate ones varied in the direction of
subsp. denticulatus ( Table 3). The more interesting finding was that in both F2 progenies the heterozygote marker class had a
large number of characters more similar
to those of the fast developing derivative
var. vulgaris than to those of the slow developing progenitor subsp. denticulatus.
These characters included leaf number,
pedicel length, internode length, bract
number, capitulum length and shape, and
total floret number. All these traits exhibited high dominance:additive ratios (0.61
# d/a # 1.35) at individual QTLs. Accordingly these results may indicate that
rapid development together with the reduction of vegetative and reproductive
structures had been under (strong) directional selection in the past, probably enabling the derivative taxon to utilize alternative, weedy habitats. That directional
selection may not have been acting directly on these structures but on the
pleiotropic effects of the postulated gene
for speed of development seems rather
unlikely, as pointed out above. In an automatically self-fertilizing species like S.
vulgaris, the observation that dominant
gene action is predominant may be somewhat surprising, since fixation probabilities for recessive and dominant mutations
are likely to be similar under inbreeding.
It should be kept in mind, however, that
the populations studied here occur in routinely—naturally or humanly—disturbed
habitats. For this reason, it can be assumed that these populations are permanently confronted with drift, founder
events, etc. Under such a setting, recessive mutations are more likely to be lost
both on a local and a wider scale unless
the effect of strong inbreeding is combined with selection (Caballero et al. 1991;
Caballero and Hill 1992).
Conclusions
The present study does not support the
assumption that ecotypic differentiation
or speciation in the wild often involves selection in quantitative polygenic systems
encompassing the joint effect of a large
number of unlinked loci, each with a relatively small, additive effect on the phenotype (e.g., Charlesworth 1984; Coyne and
Lande 1985). Instead, quantitative characters in S. vulgaris such as leaf number, pedicel length, and bract number were shown
to be controlled by chromosomal regions
with comparatively large, nonadditive effects (i.e., with r2 values of 28–37%; and [ø
d/a] values of between 0.60 and 0.94). In
considering that these regions together
with the major gene for speed of development are presumably linked to the ray
floret gene, a single chromosomal region
within S. vulgaris seems likely to exhibit a
substantial proportion of gene effects that
contribute considerably to the identity of
the weedy var. vulgaris. A similar pattern
is seen with subspecies of Plantago major
L., where in particular the Pgm-1 marker
locus forms a gene complex with a substantial number of loci affecting ecologically important characters (van Dijk
1984). In addition, extensive molecular
QTL studies have provided evidence that
a few chromosomal regions of large and
often dominant effect are responsible for
key morphological differences between
maize and its wild progenitor teosinte
( Doebley and Stec 1993; Doebley et al.
1995). If gene complexes encompassing
genes of large nonadditive effects are an
important feature of the genetic architecture not only of recently evolved domesticated but also natural plant species, then
the practice of ignoring such major genetic coadaptation in quantitative genetic
models of speciation (e.g., Barton and Turelli 1989; Charlesworth 1984; Coyne and
Lande 1985) must be questioned.
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Received September 17, 1996
Accepted May 5, 1997
Corresponding Editor: Jonathan F. Wendel
Comes • Cosegregation in Senecio vulgaris 61