Annals of Botany 108: 65 –71, 2011
doi:10.1093/aob/mcr105, available online at www.aob.oxfordjournals.org
Function and evolution of sterile sex organs in cryptically dioecious
Petasites tricholobus (Asteraceae)
Qian Yu, Deng-Xiu Li, Wei Luo and You-Hao Guo*
College of Life Sciences, Wuhan University, Wuhan, 430072, P.R. China
* For correspondence. E-mail [email protected]
Received: 9 January 2011 Returned for revision: 14 February 2011 Accepted: 18 March 2011 Published electronically: 5 May 2011
† Background and Aims Why are sterile anthers and carpels retained in some flowering plants, given their likely
costs? To address this question, a cryptically dioecious species, Petasites tricholobus, in which male and female
plants each have two floret types that appear pistillate and hermaphroditic, was studied. The aim was to understand the function of sterile hermaphroditic florets in females. In addition, the first examination of functions of
sterile female structures in male plants was conducted in the hermaphroditic florets on males of this species.
These female structures are exceptionally large in this species despite being sterile.
† Methods Differences in floret morphology between the sex morphs were documented and the possible functions
of sterile sex organs investigated using manipulative experiments. Tests were carried out to find out if sterile
female structures in male florets attract pollinators and if they aid in pollen dispersal, also to find out if the presence and quantity of sterile hermaphroditic florets in females increase pollinator attraction and reproductive
success. To investigate what floret types provide nectar, all types of florets were examined under a scanning electron microscope to search for nectaries.
† Key Results The sterile female structures in male florets did not increase pollinator visits but were essential to
secondary pollen presentation, which significantly enhanced pollen dispersal. Sterile pistillate florets on male
plants did not contribute to floral display and disappeared in nearly half of the male plants. The sterile hermaphroditic florets on female plants attracted pollinators by producing nectar and enhanced seed production.
† Conclusions The presence of female structures in male florets and hermaphroditic florets on female plants is
adaptive despite being sterile, and may be evolutionarily stable. However, the pistillate florets on male plants
appear non-adaptive and are presumably in decline. Differential fates of the sterile sex organs in the species
are determined by both the historical constraints and the ecological functions.
Key words: Cryptic dioecy, sterile sex organ, secondary pollen presentation, pollinator attraction, breeding
system evolution, ecological function, Petasites tricholobus.
IN T RO DU C T IO N
In living organisms, appearances can be deceptive with regard
to function, and the degree of deception varies. For example,
pseudoanthers in plants, which resemble real anthers but are
infertile, can be fairly easy to detect by checking pollen production or viability (Dafni and Calder, 1987). In contrast,
pseudogamy in animals and plants, which is essentially
asexual reproduction, is less apparent, especially when male
gametes are required to provide stimuli for parthenogenesis
(Bicknell et al., 2003; Engelstädter, 2008). Examining the
non-apparent functional dimensions of traits could yield interesting insight about the adaptation and evolution of organisms.
For example, orchids often display signs for pollinator reward,
like nectar guides or sex-deceptive odours, but the signs can be
completely misleading with no real reward for the animals at
all. Studies in the orchid family revealed that the richness of
floral deception is a significant evolutionary driving force in
this large group, which is unrivalled in plant – animal interactions (Cozzolino and Widmer, 2005; Waterman and
Bidartondo, 2008).
Breeding systems of plants can also be less than obvious. One
common example is cryptic dioecy, a dioecious breeding system
in which one or both of the functionally unisexual morphs
appear to have large opposite-sex structures. At least 78
species from 18 families have been recognized as cryptically
dioecious (Mayer and Charlesworth, 1991). However, given
that the sterile organs may be similar in size and appearance to
the functional organs, cryptic dioecy can be difficult to discern
(Mayer and Charlesworth, 1991; Strittmatter et al., 2002).
Two reasons have been suggested for the retention of sterile
sex organs in flowers: the genetic correlations between androecium and gynoecium that cause the suppression of one to
impact on the other (Davis, 1997), or the importance of such
organs in pollinator attraction (Mayer and Charlesworth,
1991).
The pollinator-attraction hypothesis has been tested in
several cases. In Thalictrum pubescens, Davis (1997) documented that sterile stamens are not an essential attractant for
pollinators, while in Actinidia polygama investigations
strongly supported the hypothesis that stamens functioned as
pollinator attractants in cryptic females (Kawagoe and
Suzuki, 2004). In females of Petasites japonicus, the wholly
sterile hermaphrodite florets were proven to enhance female
success by prolonging the stay of pollinators on female inflorescences (Sakai et al., 2008).
# The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
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66
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
In addition, a major question concerning cryptic dioecy is
whether it can be an evolutionary stable system. Cryptically
dioecious species are often regarded as being in transition to
morphological dioecy and, in this view, it is thought that the
production of the sterile sex organs could be suppressed,
given enough evolutionary time (Mayer and Charlesworth,
1991 and references therein). However, few studies have
addressed the evolutionary stability of this breeding system.
Petasites tricholobus Franch is a cryptic dioecious herb that
bears extensive and conspicuous sterile sex organs in its inflorescences. It belongs to the species-rich sunflower family, the
success of which lies in its principal innovation of the
common flower type variation within the composite flower
heads (Broholm et al., 2008). While cryptic dioecy documented in species other than Petasites spans morphological androdioecy, hermaphroditism or gynodioecy, Petasites plants
a
basically appear gynomonoecious with most plants containing
morphologically hermaphroditic and pistillate florets on the
same plant, and few plants containing only hermaphroditic
florets. Petasites tricholobus male plants bear male florets
that appear hermaphroditic and sterile florets that appear pistillate, while the female plants produce sterile hermaphroditic
florets and female pistillate florets (Fig. 1). Notably, more
than half of the sex organs produced by males are sterile,
and the sterile pistils in male florets are the largest among
all sex organs in the species. Similarly, the sterile hermaphroditic florets on females are also a substantial part of the floral
display. Although the morphology is perplexing, the functional
breeding system is unambiguous dioecy for the species. In this
study, potential functions of the sterile sex organs were experimentally investigated to determine whether or in what way
they contribute to reproductive success. There is also a
b
A
BC
B
C
D
AD
F I G . 1. Appearance and functional gender of P. tricholobus flowers. Top: one male (a) and one female (b) inflorescence of P. tricholobus. A, B, C and D indentify the locations of different floret types in a flower head. The dashed line indicates that the presence of the type-A floret is not constant. Scale bar ¼ 1cm. At the
bottom, on the left, are schematic drawings of floret morphology: (BC) disc floret (the variation in sizes of floral parts between disc floret on males and disc floret
on females is shown in Table 1); (AD) laciniate floret (the variation in sizes of floral parts between laciniate floret on males and laciniate floret on females is
shown in Table 1). At the bottom, on the right, are schematic drawings of floret morphological and functional gender corresponding to the types of florets: (A)
morphologically pistillate but sterile floret (laciniate floret on males); (B) morphologically hermaphroditic but functional male floret (disc floret on males); (C)
morphologically hermaphroditic but sterile floret (disc floret on females); (D) morphologically pistillate and functional female floret (laciniate floret on females).
The dashed line indicates sterility.
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
discussion on the evolutionary lability of the species with
references from related groups.
M AT E R I A L S A N D M E T H O D S
Study species and population
Petasites tricholobus is in the Asteraceae family, subfamily
Asteroideae, tribe Senecioneae. The species is an herbaceous
perennial occurring in mountainous areas of East Asia. It
flowers in March and April. Pollen and ovules are produced
in separate plants, and both types of plants bear inflorescences
composed of multiple flower heads. Heads in male plants
contain central disc florets (referred to as disc floret on
males) with or without a few surrounding laciniate florets
(laciniate floret on males; Fig. 1). Florets in male heads
flower centripetally. Heads in female plants contain several
inner disc florets (disc floret on females) surrounded by abundant outer laciniate florets (laciniate floret on females; Fig. 1).
Florets in male heads flower simultaneously. Disc florets on
both plant types each have one pistil and five stamens, appearing hermaphroditic. Laciniate florets on male and female
plants each have one pistil and no stamen, appearing pistillate.
Only the disc floret on males produces pollen for the species,
and only the laciniate floret on females bears ovules. The
laciniate floret on males and the disc floret on females are
completely sterile.
The study population was on the mountain slope at Muyu,
Shennongjia, Hubei Province, P.R. China (31828′ N,
110823′ E, 1275 m a.s.l.), where P. tricholobus is the dominant
wild flower in March. The most common insect visitor was
Apis cerana Fabr, which collected both nectar and pollen.
Experiments were conducted during the years 2008 – 2010.
Survey of inflorescence composition and floral-organ size
The number of flower heads and different types of florets in
one plant were recorded for 40 randomly chosen male plants.
For female plants, flower head production was recorded for 38
randomly chosen plants, and 21 of them were examined for
floret production. Lengths of the corolla, stamen and carpel
were measured with vernier calipers for 30 mature disc
florets on males and 30 disc florets on females, with each
floret from one male or female plant. Carpel length and
corolla length were measured for 30 mature laciniate florets
from 30 male plants and 30 mature laciniate florets from 30
female plants. The choice of plant or floret was random.
Corolla length was measured from the corolla-tube base to
the end of longest petal. Student’s t-test (a ¼ 0.05, two-tailed)
including Levene’s test for equality of variances was conducted on each morphological trait to determine whether
dimensions differed between plant sexes. SPSS 16.0 was
used for all data analysis.
Male plant studies
Pollinator attraction. To test whether the protruding sterile
stigmas in disc florets on males help to attract pollinators, 30
pairs of adjacent male plants similar in size and both in full
flower were selected. To make the floral display size the
67
same, extra flower heads were cut off one plant when necessary. All the stigmas on one plant were removed, while those on
the other plant remained intact. Pollinator approaches to each
plant and the number of heads visited were recorded for a
15-min period. The number of visits and visitation duration
per visit were counted. Paired t-tests (a ¼ 0.05, two-tailed)
were conducted to compare the number of visits and visitation
duration per visit between plants without stigmas and controls.
Secondary pollen presentation in disc floret on males. At
anthesis, stigmas of disc florets on males carry large pollen
loads, which is a form of secondary pollen presentation.
Pollen grains are brushed out by stigmas while styles elongate
during anthesis, and they are presented on the stigmatic surfaces. To quantify the distribution of pollen on stigmas and
anthers, 30 florets from 30 plants were examined. The
stigma was cut off above the anthers and stored in a small
tube. The rest of the floret was harvested and placed in
another tube. Floral parts were crushed using forceps to
release pollen into the 0.5 mL FAA solution in the tubes.
Pollen grains on the two parts were counted under a light
microscope. The tube was shaken for 30 s to suspend pollen
grains evenly in the solution, and a drop of 20 mL solution
was transferred onto a glass slide by pipette to be examined
under the microscope. Five drops were examined for each
sample. The fraction of pollen presented on the stigma was
determined.
Assessment of functional importance of secondary pollen
presentation. A united anther tube is an important precondition
for the secondary pollen presentation mechanism in
Asteraceae, because it builds the proper pressure for pollen
to be brushed out by a stigma (Leins and Erbar, 2006). A
method was developed to separate the anther tube to prevent
secondary pollen presentation. In a pilot experiment, the five
anthers were separated along their longitudinal seams using
a dissecting needle after opening the corolla of a mature
disc-floret bud along the petal seam. Treated florets opened
as usual, typically the next day. Separation of the anthers
resulted in the stigma growing above the anthers without carrying an obvious pollen load and pollen remaining primarily on
the anthers. No other conspicuous difference was observed
between treated florets and controls.
To test whether secondary pollen presentation in disc florets,
conferred by the presence of sterile pistils, contributes to more
efficient pollen dispersal, the florets were manipulated and the
pollen-removal rate of different treatments examined. A pair of
flower heads on the same plant with mature disc-floret buds
was chosen. The ten biggest buds in one head were treated
to prevent secondary pollen presentation, leaving the other
head intact. Both heads were caged to exclude floral visitors
for 1 d. The cage was then removed and the plant was monitored for an insect visitor. After one insect visit, three visited
florets were harvested from the treated head and the intact
head. Another set of three randomly chosen mature disc-floret
buds from the same plant was also harvested. Replicates in 21
male plants were conducted. Pollen grains on the florets and in
the buds were counted. The average pollen count from three
treated florets (Rt) was used to estimate the pollen remaining
after one visit to a floret without secondary pollen presentation,
while that from three intact florets (Rc) was used to estimate
68
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
the remaining pollen after one visit to a floret with secondary
pollen presentation. The average pollen quantity of three buds
(T ) was used to represent the pollen quantity before pollen
removal. (T – Ri)/T was used to calculate the pollen-removal
rate for the first visit. A similar experiment was done in the
same population to examine pollen-removal rate for one full
day of exposure to visitors under natural conditions. For the
full-day trials, 30 replicates were performed. Paired t-tests
(a ¼ 0.05, two-tailed) were used to compare pollen-removal
rates between treated florets and controls.
Female plant studies
Disc floret removal. To test whether the presence of sterile disc
florets in female plants influences pollinator behaviour, two
adjacent female plants similar in plant size and flowering
phase were chosen for observation. The numbers of heads in
the plants were recorded. The disc florets in one plant were
all removed while the other plant remained intact. Floret
removal was conducted gently by forceps. Pollinator
approaches to each plant and the number of heads visited
were recorded for a 15-min period. Visitor approach rate
plant21 min21 and visitation rate head21 min21 were
counted. Thirty replicates of different pairs of plants were performed. GLMs (general linear models) were conducted to
compare visitor approach rate per plant m21 and visitation
rate per head m21 in the presence or absence of disc florets
on females with the number of heads included as a covariate.
In the same population, 21 female plants at anthesis were
marked to test whether the quantity of sterile disc florets in
female plants affects reproductive success. Random numbers
of disc florets were kept in each flower head. Plants were left
open to pollinators, and fruits were harvested after maturation
for 1 month. The number of disc florets, laciniate florets in the
head and seed set (number of full achenes/number of all
achenes of a head) were recorded. GLM was conducted to
analyse the effect of disc floret number on seed set with the
laciniate floret number included as a covariate. Correlation
was analysed between disc floret number and seed set.
Nectary observation. To check which floret types bear
nectaries, floral parts of the four floret types were observed
under a Hitachi S-800 scanning electron mocroscope.
Sample preparation followed Yu et al. (2005).
RES ULT S
Survey of inflorescence composition and floral organ size
Male plants of P. tricholobus produced 36.8 + 1.9 (mean +
s.e.) flower heads, bearing 12.4 + 5.7 (mean + s.e.) laciniate
florets and 779.2 + 42.2 (mean+ s.e.) disc florets (n ¼ 40).
Laciniate florets on male were present on 22 of the 40 plants
surveyed. They were sandwiched between the bracts and disc
florets and noticeable only upon dissection of the flower
head. Female plants produced 73.3 + 3.6 (mean + s.e., n ¼
38) flower heads, which contained 5.8 + 1.0 (mean + s.e.,
n ¼ 21) disc and 80.9 + 3.4 (mean + s.e., n ¼ 21) laciniate
florets. Male and female plants both had the same types of
floral organs, but the size of all of the organs was significantly
different between the counterparts in opposite sexes, with male
plants having bigger disc floral parts and female plants having
bigger laciniate floral parts (Table 1).
Male plant studies
Pollinator attraction. The number of visits and visitation duration per visit were 1.8 + 0.2 (mean + s.e., n ¼ 30) and
17.8 + 3.6 s (mean + s.e., n ¼ 30) for plants without
stigmas, and 1.8 + 0.2 (mean + s.e., n ¼ 30) and 26.0 + 5.6
s (mean + s.e., n ¼ 30) for the control. The absence of
stigmas in disc florets on males did not significantly reduce
the number of pollinator visits (t29 ¼ 0.199, P ¼ 0.844) or
the average visit duration (t29 ¼ 1.777, P ¼ 0.086).
Secondary pollen presentation in disc floret on males and assessment of its functional importance. At anthesis, 89.3 + 5.3 %
(mean + s.e., n ¼ 30) of the total pollen produced by disc
florets was on the projecting stigma. In the secondary pollenpresentation prevention experiment, the pollen-removal rate
for the first visit was 10.9 + 3.8 % (mean + s.e.) for treated
florets and 59.8 + 4.1 % (mean + s.e.) for controls (n ¼ 21,
t20 ¼ 21.829, P , 0.001). The pollen-removal rate after 1 d
of exposure to pollinators was 34.8 + 26.4 % for treated
florets and 76.8 + 12.4 % for controls (n ¼ 30, t29 ¼ 7.873,
P , 0.001). The pollen-removal rate in both sets was significantly lowered when secondary pollen presentation was prevented (Fig. 2).
Female plant studies
Disc floret removal. Both the approach rate and the visitation
rate were significantly reduced in the absence of disc florets
on females (Fig. 3 and Table 2). The visitor approach rate
was 0.6 + 0.1 plant21 min21 (mean + s.e., n ¼ 30) for
treated florets and 1.0 + 0.1 plant21 min21 (mean + s.e.,
n ¼ 30) for controls. Visitation rate was 0.0 + 0.0
head21 min21 (mean + s.e., n ¼ 30) for treated florets versus
0.2 + 0.0 head21 min21 (mean + s.e., n ¼ 30) for controls.
The number of heads did not significantly affect either rate
(Table 2). The number of both laciniate florets and disc
florets on females had a significant effect on seed set
(Table 3), and seed set was found to positively correlate
with the number of disc florets on females (r ¼ 0.065 P ¼
0.001) (Fig. 4).
TA B L E 1. Length of floral parts for each floret type and
statistical significance (Student’s t-test, two-tailed) of differences
in lengths between male and female plants
Male (mm)
Disc floret
Corolla
10.6 + 0.1
Pistil
17.7 + 0.2
Stamen
5.3 + 0.1
Laciniate floret
Corolla
4.3 + 0.2
Pistil
7.8 + 0.3
Values are means + s.e.
Female (mm)
d.f.
t
P
3.1 + 0.1
7.6 + 0.1
2.8 + 0.1
21
27
18
33.031
3.585
15.362
,0.0001
0.00013
,0.0001
8.0 + 0.1
9.5 + 0.2
26
27
–0.127
–3.585
,0.0001
,0.0001
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
90
80
Control
Treated
***
Pollen-removal rate (%)
70
60
***
50
40
30
20
10
0
First visit
1-d exposure
F I G . 2. Pollen-removal rates of the first visit and 1-d exposure for disc florets
on males with secondary pollen presentation prevention and control florets.
Bars indicate s.e.; ***, P , 0.001.
Approach rate (plant –1 min–1) and
visitation rate (head–1 min–1)
1·2
1·0
Control
Treated
*
0·8
0·6
0·4
***
0·2
0
Approach rate
Visitation rate
F I G . 3. Pollinator approach rate and visitation rate for female heads with disc
florets on females removed and control heads. Bars indicate the standard error;
*, P , 0.05; ***, P , 0.001.
Nectary observation. Nectaries were detected in both types of
disc florets and were absent in both laciniate floret types.
The nectaries were in the shape of round bumps, located alternate to the base of filaments.
D IS C US S IO N
Dioecy in P. tricholobus is cryptic, due to the extent of the
sterile sex organs. The most important distinction between
cryptic and non-cryptic dioecy depends on whether the nonfunctional sex organs are substantially developed or are
rather vestigial (Mayer and Charlesworth, 1991). Both the
disc florets on females and the female structures in disc
florets on males are well formed in P. tricholobus and make
a significant part of the floral display, making it difficult to
determine the actual breeding system. So the species is cryptically dioecious. Ever since Darwin, dioecious species with
non-functional sex parts were thought to have originated
69
from the cosexual state (Darwin, 1877; Mayer and
Charlesworth 1991). Surveys of relevant characters of related
groups suggest that the ancestral state of P. tricholobus was
cosexual gynomonoecy. All 19 species of Petasites are polymorphic, with individuals being either male or female
(Bremer, 1994; Cherniawsky and Bayer, 1998). However,
both types of individuals are composed of morphologically
hermaphroditic florets and pistillate florets. Species differ in
the proportion of the two types of floret, but basically all
appear gynomonoecious. The only exception is P. japonicus,
which has no pistillate florets on males (Toman, 1972; Sakai
et al., 2008). The two genera closest to Petasites, namely
Endocellion and Tussilago, also have morphologically gynomonoecious individuals (Toman, 1972; Bremer, 1994). It is
most likely that the functional dioecy in Petasites was
derived from gynomonoecy. So the discrepancy between morphology and function in P. tricholobus is rooted in its historical constraint.
During the evolution of dioecy, floral parts that have lost
their primary sex functions may still be retained because
they function in the reproductive process in other ways. For
example, the present results for P. tricholobus showed that
the sterile disc florets on females significantly increased pollinator attraction and enhanced female reproductive success
(Figs 3 and 4). This result is consistent with the findings of
Sakai et al. (2008) in P. japonicus a sister species
of P. tricholobus. Their study showed that the presence of
sterile hermaphroditic florets in female plants enhanced
female reproductive success by prolonging the duration of
visits. Moreover, nectaries were observed in disc florets on
females in P. tricholobus, and an absence of nectaries recognized in laciniate florets from both male and female plants.
Thus, the retention of disc florets on females is attributable
not only to their resemblance to disc florets on males, but
also to their provision of nectar as direct reward for visitors
to females.
In male plants of P. tricholobus, the large stigmas in disc
florets were not found to serve as an important pollinator
attractant, but had a significant role in secondary pollen presentation, which contributes to male success by enhancing
pollen-removal efficiency (Fig. 3). The united anther tube
and a matching size stigma in P. tricholobus are both important for secondary pollen presentation, as the anther tube
creates pressure for the wide stigma to brush pollen out. In
all the recognized forms of secondary pollen presentation,
stigmas reveal or develop a receptive surface after the presented pollen is shed (Leins and Erbar, 2006, and references
therein). In contrast, the female function was completely lost
in disc florets on males in P. tricholobus. However, the
stigmas of the disc florets on males are very specialized for
presenting pollen through their exceptionally large size compared with other floral parts in both male and female plants
(Table 1). In fact, cases of male flowers bearing non-functional
female parts are rather rare. According to both theory (Willson
and Ågren, 1989) and empirical evidence (Mayer and
Charlesworth, 1991), the phenomenon of female flowers
mimicking hermaphroditism is more likely than the reverse,
presumably because male success is usually less limited by
pollination owing to the attraction of pollen to pollinators.
The present study is the first one to test the function of
70
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
TA B L E 2. ANOVA tables of the effects of the absence of disc florets on females on pollinator approaches per plant and visitation rate
per flower in female plants
Approach rate per plant
Visitation rate per flower
Source
No. of heads
Treatment
Error
d.f.
SS
F
P
d.f.
SS
F
P
1
1
293
1.694
5.632
307.488
1.615
5.367
0.205
0.021
1
1
293
0.082
2.758
16.713
1.438
48.355
0.231
0.000
TA B L E 3. ANOVA table of the effect of the abundance of disc
florets on females on seed set in female plants
d.f.
SS
F
P
No. of laciniate florets on females
No. of disc florets on females
Error
1
5
169
5315.536
4257.937
43491.483
20.655
3.309
,0.001
0.007
sterile female structures in male plants, and the results suggest
that augmenting male pollination success could be an evolutionary force behind retaining female structures in males.
On the other hand, the laciniate florets on males could
hardly play any role in reproductive success. From the
survey, they only occurred in about 55 % of male plants and
had very low representation in those plants. In male flower
heads that did produce them, they were not only sterile, but
also invisible without dissection of the flower head and
made virtually no contribution to floral display. Thus, these
florets may simply be an incompletely reduced residue from
their gynomonoecious ancestors.
Whether breeding systems other than hermaphroditism and
dioecy can be evolutionarily stable, or are always transitioning
towards these two ends, is a controversial question. With
respect to the maintenance of gynodioecy, it has been argued
that the stability may be dependent not only on the genetic
basis of sex determination but also on ecological conditions
(Ross, 1978; Delph, 2003; Dunthorn, 2004). Similarly, for
the cryptic dioecy of P. tricholobus, both ecological conditions
and genetic constraint appear to be important for its evolution.
The female structures in male disc florets and female disc
florets existed first because of history, but their retention
could be attributed to their contribution to reproductive
success. So the existence of these structures could be stable,
supported by the consistent presence of such features in all
the species in the genus of Petasites (Toman, 1972; Bremer,
1994; Cherniawsky and Bayer, 1998).
In contrast, the production of laciniate florets on males in
P. tricholobus seems at stake. In the Asteraceae family, peripheral florets often have conspicuous ligulae that collectively
form the petals of flower heads, such as in common sunflowers, dandelions, etc. The two genera closest to Petasites,
namely Endocellion and Tussilago, are both characterized by
outer ray florets with petal-like ligulae. However, the corolla
of pistillate florets is only distinctively petal-like in
Nardosmia, one of the three subgenera of Petasites (Toman,
1972). The ray florets with visible ligulae are likely to
100
Seed set (%)
Source
120
80
60
40
r = 0·065
20
0
P = 0·001
0
1
2
3
4
5
Number of disc florets in a flower head on females
6
F I G . 4. Variation in seed set for female heads with different numbers of disc
florets on females. Curve fit and P-value from correlation analysis.
represent the ancestral form of Petasites, but in species like
P. tricholobus the corolla of pistillate florets was greatly
reduced. Actually, other studies suggest that the necessary
genetic and phenotypic changes are likely to evolve in the sunflower family. The loss of ligulae in peripheral pistillate florets
has happened multiple times in the tribe of Senecioneae (Liu
et al. 2006), and floret-type variation in Asteraceae is under
the control of only a couple of major genes and several modifier genes (Gillies et al., 2002; Berti et al., 2005; Broholm
et al., 2008; Kim et al. 2008). In fact, around half of male
plants no longer exhibit laciniate florets, and variation of
flower head composition has been documented in other
Petasites. Laciniate florets on males are occasionally absent
in species from both the subgenera Petasites and
Capillopetalum (Toman, 1972). While in Petasites palmatus
each male head still has up to 70 pistillate florets with
visible petals in outer rows (Cherniawsky and Bayer, 1998),
P. japonicus male heads have no pistillate florets at all
(Sakai et al., 2008). Since those pistillate florets on males in
P. tricholobus no longer contribute to floral display and pollinator attraction, it seems that genotypes that do not express
them would not be selected against. Hence, we suggest that
mutations to those regulatory genes may have permeated the
populations of P. tricholobus, which resulted in the inconsistent production of laciniate florets on males. This trait may
evolve towards the P. japonicus end of the spectrum.
In conclusion, in P. tricholobus the sterile hermaphroditic
florets on female plants attract pollinators and the sterile
Yu et al. — Function and evolution of sterile sex organs in Asteraceae
pistils in morphologically hermaphroditic florets of male
plants aid secondary pollen presentation and pollen export.
However, the sterile pistillate florets on male plants have no
detectable function. The first two traits are therefore considered adaptive and likely to persist, while the sterile pistillate
florets are vestigial and may disappear over time. Both ecological functions and historical constraints contribute to the evolution of the sterile sex organs in this species.
ACK N OW L E DG E M E N T S
The authors thank Lynda Delph, Benjamin Montgomery,
Leonie Moyle Lab and Yang Chun-feng for providing very
helpful suggestions to experimental design and manuscript
preparation. They also thank Mark Richardson for improving
the language. Yang Xu and Li Xiao-xia helped with the field
work. Two anonymous reviewers are especially thanked for
valuable advice on improving the manuscript. This work was
supported by National Science Foundation of China (grant
number 30670362).
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