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Patterns of Floral Variation between Dimorphic and Monomorphic Populations in Distylous Luculia pinceana (Rubiaceae)

二型花柱植物滇丁香二态和单态种群间花部形态变异模式



全 文 :二型花柱植物滇丁香二态和单态种群间花部形态变异模式∗
周  伟1ꎬ2ꎬ 李德铢1ꎬ2ꎬ 王  红1∗∗
(1 中国科学院昆明植物研究所东亚植物多样性与生物地理学重点实验室ꎬ 昆明  650201ꎻ
2 中国科学院昆明植物研究所中国西南野生生物种质资源库ꎬ 昆明  650201)
摘要: 花部形态特征在植物交配系统的演化与维持过程中起关键作用ꎬ 交配方式的转变将可能伴随着相应
花部形态的调整ꎮ 为探寻交配系统与花形态变异之间的联系ꎬ 本研究对二型花柱植物滇丁香 (Luculia pin ̄
ceana) 的二态和单态种群的花部形态特征进行比较分析ꎮ 结果表明花部形态在两种不同花型构造的种群
间分化程度显著大于花型构造相同的种群间变异ꎮ 相对于二态种群而言ꎬ 长花柱的单态种群中雌雄异位距
离缩小ꎬ 且个体间雌雄生殖器官在空间上的非法重叠程度增高ꎬ 花部形态的调整能够同时促进自交和同型
异交ꎮ 在异型花柱物种内ꎬ 异交为主的二型花柱种群向单态种群转变过程中自交比率预期上升ꎬ 本研究表
明花部形态的变异模式与交配系统转变相一致ꎮ
关键词: 滇丁香ꎻ 花部形态变异ꎻ 二型花柱ꎻ 二态ꎻ 单态
中图分类号: Q 944              文献标志码: A              文章编号: 2095-0845(2015)05-513-09
Patterns of Floral Variation between Dimorphic and Monomorphic
Populations in Distylous Luculia pinceana (Rubiaceae)∗
ZHOU Wei1ꎬ2ꎬ LI De ̄zhu1ꎬ2ꎬ WANG Hong1∗∗
(1 Key Laboratory for Plant Biodiversity and Biogeography of East Asiaꎬ Kunming Institute of Botanyꎬ Chinese
Academy of Sciencesꎬ Kunming 650201ꎬ Chinaꎻ 2 Germplasm Bank of Wild Species in Southwest Chinaꎬ
Kunming Institute of Botanyꎬ Chinese Academy of Sciencesꎬ Kunming 650201ꎬ China)
Abstract: Flower morphology plays an important role in the evolution and maintenance of plant mating systemsꎬ in ̄
cluding disassortative mating of heterostylous species. The transition of mating patterns may be associated with the re ̄
modification of intraspecific flower morphology. To determine the functional relationship between floral variation and
transition of mating patternsꎬ we conducted a series of morphometric analyses in a distylous species Luculia pin ̄
ceanaꎬ which possesses dimorphic and monomorphic populations. Our results indicate that floral variation was higher
between different types of populations than between populations of the same type. Compared to dimorphic popula ̄
tionsꎬ some floral charactersꎬ reduced stigma ̄anther separation within flowers and increased overlap of stigmas and
anthers (illegitimate spatial matching of sexual organs) among individuals in populations containing only the long ̄
styled morph may have been modified to increase both selfing and intra ̄morph crossing. The observed patterns of flo ̄
ral variation between dimorphic and monomorphic populations coincide with the transition of mating patterns from
disassortative mating to selfing and / or intra ̄morph crossing.
Key words: Luculia pinceanaꎻ Distylyꎻ Floral morphological variationꎻ Dimorphicꎻ Monomorphic
植 物 分 类 与 资 源 学 报  2015ꎬ 37 (5): 513~521
Plant Diversity and Resources                                    DOI: 10.7677 / ynzwyj201515011

∗∗
Funding: The National Key Basic Research Program of China (2014CB954100)ꎬ the Key Research Program of the Chinese Academic of
Sciences (KJZD ̄EW ̄L07)ꎬ the National Natural Science Foundation of China (31200289ꎬ 31570384ꎬ 31320103919)ꎬ and the
Natural Science Foundation of Yunnan Province (2012FB182)
Author for correspondenceꎻ E ̄mail: wanghong@mail􀆰 kib􀆰 ac􀆰 cn
Received date: 2015-01-22ꎬ Accepted date: 2015-03-25
作者简介: 周伟 (1980-) 男ꎬ 博士ꎬ 主要从事植物繁殖生态学研究ꎮ E ̄mail: zhouwei@mail􀆰 kib􀆰 ac􀆰 cn
  Flowers may be morphologically constant within
species because pollinator mediated stabilizing selec ̄
tion may reduce the variation in floral traits (Steb ̄
binsꎬ 1970ꎻ Feinsingerꎬ 1983ꎻ Gong and Huangꎬ
2009). Intraspecific variation in floral morphology
may constitute an obstacle for sexual reproductionꎬ
especially for animal ̄pollinated plants ( Cresswellꎬ
2000ꎻ Herreraꎬ 2001). Neverthelessꎬ floral morpho ̄
logical variation among conspecifics has been repor ̄
ted at different hierarchical levelsꎬ including among
flowers within individualsꎬ among individualsꎬ and
among populations (Cresswellꎬ 1998ꎻ Galenꎬ 1999ꎻ
Williams and Connerꎬ 2001ꎻ Herreraꎬ 2005). Theo ̄
reticallyꎬ variation in floral traits may correlate with
the proportion of mixed mating types ( i􀆰 e. disassor ̄
tative matingꎬ assortative matingꎬ selfingꎬ and cross ̄
ing) (Barrettꎬ 2003). Howeverꎬ it is difficult to in ̄
vestigate the evolutionary relationship between floral
variation patterns and changes in mating patterns di ̄
rectlyꎬ since the differentiation of floral parameters
is hard to quantify and its effect on mating compo ̄
nents could be too weak to detect.
Heterostylous species are an ideal system to in ̄
vestigate the functional relationship between floral
variation and mating patterns (Hodgins and Barrettꎬ
2006ꎬ 2008). In these speciesꎬ the reciprocal ar ̄
rangement of sex organs is recognized as a floral syn ̄
drome that increases the precision of pollen transfer
between the corresponding morphsꎬ resulting in dis ̄
assortative mating in floral polymorphic populations
(Lloyd and Webbꎬ 1992). Previous studies of het ̄
erostylous species with morph ̄biased populations in ̄
dicate that the components of mating patterns showed
variegated variation across the geographical distribu ̄
tion and were strongly associated with floral morpho ̄
logy variation (Barrett and Hodginsꎬ 2006ꎻ Hodgins
and Barrettꎬ 2006ꎬ 2008ꎻ Brys et al.ꎬ 2007ꎻ Valle ̄
jo ̄Marin and Barrettꎬ 2009). Recentlyꎬ monomor ̄
phic populations have been reported in some hetero ̄
stylous species (Naiki and Nagamasuꎬ 2004ꎻ Hod ̄
gins and Barrettꎬ 2008ꎻ Zhou et al.ꎬ 2012). In such
monomorphic populationsꎬ disassortative mating is
impossibleꎬ and therefore the sexual reproductive
mating strategy is predicted to consist of selfing and /
or intra ̄morph crossing. A comparative study between
polymorphic and monomorphic populations can thus
provide an opportunity to shed light on the evolutio ̄
nary paradigm of mating strategy transition and floral
morphological differentiation.
Luculia pinceana Hook. (Rubiaceae) is a geo ̄
graphically restricted shrubꎬ pollinated by both long ̄
and short ̄tongued animals (Ma et al.ꎬ 2009). The
populations of the species are either distylousꎬ con ̄
taining long ̄ and short ̄styled morphs ( hereafter L ̄
and S ̄morphsꎬ pin and thrum flower)ꎬ or are mono ̄
morphicꎬ containing only the L ̄morph (i􀆰 e. L ̄mon ̄
omorphic population)ꎬ which possess a particular
geographic distribution (Zhou et al.ꎬ 2012). In this
studyꎬ morphometric data are used to analyze the
floral differentiation between dimorphic and mono ̄
morphic populations of L􀆰 pinceana. Specificallyꎬ we
address the following two questions: (1) What pat ̄
terns of floral trait variation are existing between
monomorphic and dimorphic populations? ( 2 ) Is
variation in floral morphology correlated with the
transition of mating patterns from disassortative mat ̄
ing to selfing and / or intra ̄morph crossing between
the two types of populations?
1  Materials and methods
1􀆰 1  Study species and populations
Luculia pinceana is a perennial shrubꎬ restrict ̄
ed to southwest China and northern Vietnam and
Myanmar at altitudes between 350 and 1 800 m (Luo
et al.ꎬ 1999ꎻ Zhou et al.ꎬ 2012). The species begin
flowering mid ̄July at its southern range margin of
Sapa ( Lào Caiꎬ Vietnam) and continue flowering
until December at higher elevations in northwest
Yunnan (China). Each corymb has five to 12 flow ̄
ers (mean flower per inflorescence = 7􀆰 8ꎬ N = 48ꎬ
SD= 2􀆰 4) that vary in color from white to pale red
among individuals or populations. Each flower lasts
five to eight days and is fragrant. The corolla is sym ̄
petalous with five lobesꎬ and five epipetalous sta ̄
415                                  植 物 分 类 与 资 源 学 报                            第 37卷
mens attach to the corolla ̄tube. Pollinators of L􀆰 pin ̄
ceana are mainly long ̄tongued nectar feeding insects
(bumblebeesꎬ moths and butterflies) and pollen ̄
collecting bees (Apis florae). In this studyꎬ we sam ̄
pled six populations of L􀆰 pinceana in Yunnan. Of
these populationsꎬ three were dimorphic (JCW: 24°
47􀆰 40′ Nꎬ 104°30􀆰 75′ Eꎬ 1 798 m above sea levelꎻ
MN: 22°57􀆰 16′ Nꎬ 104°19􀆰 26′ Eꎬ 1 418 mꎻ LP:
25°58􀆰 92′ Nꎬ 098°48􀆰 39′ Eꎬ 1 763 m) and three
were long ̄styled monomorphic ( WLL: 23° 15􀆰 76′
Nꎬ 103° 58􀆰 06′ Eꎬ 1 780 mꎻ PD: 22° 57􀆰 39′ Nꎬ
103°42􀆰 10′ Eꎬ 1 614 mꎻ JP: 22°53􀆰 52′ Nꎬ 103°
13􀆰 20′ Eꎬ 1 475 m). Each population was separated
from all others by at least 50 kmꎬ with the greatest
amount of separation of nearly 400 km.
1􀆰 2  Floral measurements
In each populationꎬ we obtained a random sam ̄
ple of flowering stems and classified them according
to style morph. Only fresh flowers with mature sex
organs in which styles were fully mature were sam ̄
pled and preserved in FAA (10% formalinꎬ glacial
acetic acidꎬ and 70% ethanol) for subsequent meas ̄
urements. For each flowerꎬ we measured stigma hei ̄
ght (SH) and anther height (AH) from the base of
the ovary to the midpoints of the stigma and antherꎬ
respectively ( Fig􀆰 1). For stigma length ( SL) and
anther length (AL)ꎬ we measured from one end of
the stigma lobe or anther to their other endpoints.
Stigma ̄anther separation (SAS) was measured from
the tip of the anther to the base of the stigma for L ̄
morph flower and reverse for S ̄morph flower (Fig􀆰 1).
All measurements were made using a dissecting mi ̄
croscope or digital calipers.
1􀆰 3  Statistical analysis
To quantify floral morph ratios in dimorphic
populationsꎬ we assessed whether floral morphs oc ̄
curred at equal frequencyꎬ as is typical of many di ̄
stylous speciesꎬ by using goodness ̄of ̄fit G ̄tests. Poo ̄
led G ̄tests were calculated to determine whether
pooled morph ratios differed significantly from 1 ∶ 1.
We also calculated Gheterogeneity statistics to test for het ̄
erogeneous morph ratios among populations. Varia ̄
tion in floral morphological parameters between the
three types of flowersꎬ one type from monomorphic
population and two types from dimorphic populationꎬ
were analyzed in a one ̄way ANOVA followed by a
Tukey ̄Kramer test. Each type exceeded 120 flowersꎬ
which came from three populations at the same pro ̄
portion and more than 30 individuals were sampled
for each population. The stigma ̄anther separation
between monomorphic and dimorphic populations was
compared using the same method.
Fig􀆰 1  The floral diagrams of (A) S ̄morph (thrum) and (B)
L ̄morph (pin) flowers in Luculia pinceana. SH: stigma heightꎻ
AH: anther heightꎻ AL: anther lengthꎻ SL: stigma lengthꎻ
SAS: stigma ̄anther separation
    To examine potential differentiation in floral
morphology between the two types of populationsꎬ we
used the reciprocity index (R) proposed by Sanchez
et al. ( 2008). Eighteen R values were calculated
(three from natural dimorphic populationsꎬ six from
dimorphic populations constructed using two floral
morphs from different natural dimorphic populationsꎬ
and the remaining nine from populations constructed
with floral morphs from both the monomorphic and
dimorphic populations) and compared. To determine
if the morphological variation between population
types was associated with the functional change and
the transition of mating patternsꎬ the degree of recip ̄
rocal herkogamy was evaluated by calculating the
spatial matching of organ i (stigma or anther) to or ̄
5155期        ZHOU Wei et al.: Patterns of Floral Variation between Dimorphic and Monomorphic Populations 􀆺       
gan j (stigma or anther) as follows (Lau and Bos ̄
queꎬ 2003ꎻ Kalman et al.ꎬ 2007): spatial matching
(ij)= (Aij / Ai)×100ꎬ where Aij is the area of over ̄
lap between the distribution of organ i and organ jꎬ
and Ai is the area of the distribution of organ i. The
length of divided part is 0􀆰 5 mm. All analyses were
performed in R version 2􀆰 51 (R Development Core
Teamꎬ 2010).
2  Results
Analysis of floral morphs showed that individu ̄
als of L􀆰 pinceana exhibited either short ̄styled or
long ̄styled flowers. The co ̄existence of both morphs
in the same individual was not observed in any of the
populations. Field observations revealed there were
two types of populations in L􀆰 pinceanaꎬ monomor ̄
phic and dimorphic. In dimorphic populationsꎬ stig ̄
mas and anthers were reciprocally placed in each flo ̄
ral morph. Distribution of anther height was bimod ̄
alꎬ and the average distance between the S ̄ and L ̄
morph exceeded 5 mm (Fig􀆰 2A-C). Alternativelyꎬ
stigma height showed a continuous distribution in
population JCW and LPꎬ but the degree of overlap
between floral morphs within the same population
was not significantꎬ especially in population MN
(Fig􀆰 2A-C). In monomorphic populationsꎬ the stig ̄
mas were located above the anthers in all flowers
(Fig􀆰 2D-F)ꎬ suggesting these populations are mo ̄
nomorphic only for the L ̄morph. The floral morph
ratio was 1∶1􀆰 11 (N=80) in population MNꎬ 1∶0􀆰 52
(N= 70) in population JCW and 1 ∶ 1􀆰 54 (N = 56)
in population LP. The G ̄tests indicated that the flo ̄
ral morph ratios of all dimorphic populations do not
deviate from 1 ∶ 1 ( MN: G = 0􀆰 200ꎻ P = 0􀆰 655ꎻ
JCW: G= 3􀆰 457ꎻ P = 0􀆰 063ꎻ LP: G = 1􀆰 286ꎻ P =
0􀆰 257). There was also no significant deviation from
a 1 ∶ 1 ratio when the data were pooled across three
populations (Gpooled = 1􀆰 53ꎬ P>>0􀆰 05). No signifi ̄
cant heterogeneity was detected among population
morph ratios (Gheterogeneity = 3􀆰 62ꎬ P>>0􀆰 05).
In dimorphic populationsꎬ significant differ ̄
ences were found between morphs for anther heightꎬ
stigma heightꎬ and stigma length (Fig􀆰 3). Howeverꎬ
there was no significant difference between morphs
Fig􀆰 2  Flowers of Luculia pinceana ranked by style length to illustrate the reciprocal correspondence of stigma and anther positions
in L ̄ and S ̄morphs. The flowers are sampled from two extreme of stigma height. Positions of stigma are indicated by crosses
and those of anthers by rectangles. Aꎬ B and C represent dimorphic populations JCWꎬ LP and MNꎻ Dꎬ E
and F represent L ̄monomorphic populations PDꎬ JP and WLL
615                                  植 物 分 类 与 资 源 学 报                            第 37卷
Fig􀆰 3  Mean value of floral traits of three types of flowers in Luculia
pinceana. PFM represent L ̄morph flowers of L ̄monomorphic popula ̄
tions (WLLꎬ PD and JP)ꎻ PFD and TFD represent L ̄ and S ̄morph
flowers of dimorphic population (MNꎬ JCW and LP)ꎬ respectively.
Columns with the same letters do not differ significantly (Turkey testꎬ
P < 0􀆰 01) . Vertical lines show standard deviations
for anther length or between the stigma height of L ̄
morph and anther height of S ̄morph. The stigma
length in S ̄morph (6􀆰 54 ± 0􀆰 73 mm) was nearly 1􀆰 3
times greater than that of L ̄morph (4􀆰 88 ± 0􀆰 71 mm).
Stigma and anther lengths of the L ̄monomorphic
populations were statistically similar to those of the
dimorphic populationsꎬ but stigma and anther posi ̄
tions were all higher in the L ̄monomorphic popula ̄
tions compared to the pin flowers in the dimorphic
populations.
The indices of reciprocity ( R) for dimorphic
populations were all less than 0􀆰 025 (MN: 0􀆰 007ꎻ
LP: 0􀆰 017ꎻ JCW: 0􀆰 021) (Fig􀆰 4). When pin flowers
from L ̄monomorphic populations matched to thrum
flowers from dimorphic populationsꎬ nine putative
dimorphic populations were createdꎬ and their resul ̄
ting R values were all greater than 0􀆰 1 (MN ̄WLL:
0􀆰 105ꎻ MN ̄PD: 0􀆰 112ꎻ MN ̄JP: 0􀆰 100ꎻ LP ̄WLL:
Fig􀆰 4  Reciprocity index (R) in populations of Luculia pinceana. The values were calculated from three natural dimorphic
populations and fifteen constructed populations using two floral morphs from different populations of
monomorphic or dimorphic (see Materials and Methods for details)
7155期        ZHOU Wei et al.: Patterns of Floral Variation between Dimorphic and Monomorphic Populations 􀆺       
0􀆰 107ꎻ LP ̄PD: 0􀆰 115ꎻ LP ̄JP: 0􀆰 105ꎻ JCW ̄WLL:
0􀆰 121ꎻ JCW ̄PD: 0􀆰 128ꎻ JCW ̄JP: 0􀆰 116) (Fig􀆰 4).
Alternativelyꎬ the R values of another six putative
dimorphic populationsꎬ which were composed of L ̄
morph from one dimorphic population and S ̄morph
flowers from another two dimorphic populationsꎬ were
all less than 0􀆰 025 ( MN ̄JCW: 0􀆰 010ꎻ MN ̄LP:
0􀆰 024ꎻ LP ̄JCW: 0􀆰 015ꎻ LP ̄MN: 0􀆰 023ꎻ JCW ̄LP:
0􀆰 012ꎻ JCW ̄MN: 0􀆰 013). These results indicate that
L ̄morph flowers in the monomorphic populations
were significantly differentiated from those of the di ̄
morphic populationsꎬ but there was no significant di ̄
fferentiation between the dimorphic populations.
In dimorphic populationsꎬ there was higher spa ̄
tial matching between corresponding legitimate sexual
organs than between illegitimate ones (Fig􀆰 5A-D).
Overlap between S ̄morph stigmas and their corre ̄
sponding legitimate organsꎬ i􀆰 e. L ̄morph anthersꎬ was
nearly five times greater than their overlap with their
illegitimate organsꎬ i􀆰 e. S ̄morph anthers (55􀆰 22%
and 11􀆰 38%ꎬ respectively). Overlap between L ̄mor ̄
ph stigmas and their corresponding legitimate organsꎬ
i􀆰 e. S ̄morph anthersꎬ was nearly seven times greater
than their overlap with L ̄morph anthers ( 73􀆰 25%
and 11􀆰 99%ꎬ respectively). Similarlyꎬ pin anthers
matching to S ̄morph stigmas ( 100%) was almost
eight times greater than their matching to L ̄morph
stigmas (12􀆰 02%)ꎬ and the matching of S ̄morph
anthers to legitimate L ̄morph stigmas ( 71􀆰 28%)
was over three times their matching to illegitimate
S ̄morph stigmas (20􀆰 32%). In monomorphic popu ̄
lationsꎬ illegitimate spatial matching of sexual organs
(Fig􀆰 5E - F) was greater than that in dimorphic
populations. The matching of stigmas to anthers was
Fig􀆰 5  Special matching of the sexual organs of Luculia pinceana flowers. Abscissas show the distance from the distal margin of the ovary taken
as arbitrary reference point. The ordinates indicate the percentage of flowers in which at least part of their reproductive organs were present in
each of 0􀆰 5 mm segments along the abscissa. Unfilled triangles pin stigmasꎻ filled triangles pin anthersꎻ unfilled circles thrum stigmasꎻ filled
circles thrum anthers. A-D represents dimorphic population JCWꎻ E and F represent pin ̄monomorphic population JP and PDꎬ respectively
815                                  植 物 分 类 与 资 源 学 报                            第 37卷
22􀆰 96% and 31􀆰 13% in populations JP and PDꎬ re ̄
spectivelyꎬ which was two to three times greater than
population JCW. In contrastꎬ the matching of anthers
to stigmas in the same monomorphic populations was
31􀆰 19% and 33􀆰 66%ꎬ which were three times grea ̄
ter than that of the dimorphic population JCW. The
distribution of stigmas and anthers of the dimorphic
population type was more concentrated compared to
that of the monomorphic population type.
In L ̄monomorphic populations WLLꎬ PDꎬ and
JPꎬ the means of stigma ̄anther separation were 2􀆰 53
± 0􀆰 98 mm (N=56)ꎬ 2􀆰 76 ± 0􀆰 77 mm (N=60)ꎬ and
2􀆰 88 ± 0􀆰 72 mm (N=63)ꎬ respectively. For pin flow ̄
ers of dimorphic populations MNꎬ JCWꎬ and LPꎬ the
means of stigma ̄anther separation were 3􀆰 85 ± 1􀆰 13
mm (N=60)ꎬ 4􀆰 03 ± 1􀆰 01 mm (N=60)ꎬ and 4􀆰 13 ±
1􀆰 18 mm (N=60)ꎬ respectively. There were no sig ̄
nificant difference within each type of population in
anther ̄stigma separationꎬ but anther ̄stigma separa ̄
tion was significantly different between the two types
of populations.
3  Discussion
In heterostylous speciesꎬ sex ̄organ reciprocity
serves to promote cross ̄pollen transfer between floral
morphs and the floral polymorphism maintained by
negative frequency ̄dependent selection ( Charles ̄
worth and Charlesworthꎬ 1979ꎻ Lloyd and Webbꎬ
1992). In L􀆰 pinceanaꎬ the stigma and anthers never
occupied the same position within a given flower and
the homostyly individual was not present in this and
previous survey (Zhou et al.ꎬ 2012)ꎬ thus the spe ̄
cies was convinced to be a true distylous species.
Quantified reciprocal herkogamy described by legiti ̄
mate and illegitimate matching of sexual organs fur ̄
ther confirmed the functional syndrome of distyly in
this species.
Sanchez et al. (2008) proposed the reciprocity
index (R value) to evaluate the matching fidelity of
stigma and anther between morphsꎬ which can re ̄
flect the role of floral traits on promoting disassorta ̄
tive mating. The reciprocity indices in three natural
dimorphic populations were all less than 0􀆰 025
(0􀆰 007~ 0􀆰 021)ꎬ which were similar to the values
resulting from matching L ̄ and S ̄morph flowers from
different dimorphic populations ( 0􀆰 010 ~ 0􀆰 024).
These results indicate that these floral morphological
characters are very efficient in promoting inter ̄morph
pollination and that there was no significant differen ̄
tiation in floral morphology between dimorphic popu ̄
lations. Howeverꎬ the R values generated from the
two types of populations all exceed 0􀆰 1 (0􀆰 100 ~
0􀆰 128) (Fig􀆰 4)ꎬ and the variability was similar to
the R values generated by matching different dimor ̄
phic populations. As suggested by Sanchez et al.
(2008)ꎬ an R value of 0􀆰 1 or greater represents no
functional significance considering with heterostyly.
Thusꎬ we suggest that floral morphology has experi ̄
enced significant differentiation between dimorphic
and monomorphic populationsꎬ but that it is stable
within the same type of population.
Previous studies have proposed that reduced
stigma ̄anther separation may increase the degree of
self ̄fertilization ( Barrett and Shoreꎬ 1987ꎻ Motten
and Stoneꎬ 2000) and provide reproductive assur ̄
ance (Mal and Lovett ̄Doustꎬ 2005) in heterostylous
species. In additionꎬ the increased illegitimate spa ̄
tial matching of sexual organs at the population level
suggests that more intra ̄morph crossing could be
possible ( Lau and Bosqueꎬ 2003ꎻ Kalman et al.ꎬ
2007). For L􀆰 pinceanaꎬ the reciprocity values indi ̄
cate that disassortative mating was a reliable mating
system in natural dimorphic populationsꎬ this pattern
was confirmed in a natural population of the species
using microsatellite markers and paternity analysis
(Zhou et al.ꎬ 2015). Howeverꎬ the mating compo ̄
nent characterized by prevailing disassortative mating
in the species may shift to selfing and / or intra ̄mor ̄
ph crossing in L ̄monomorphic populations since the
absence of the inter ̄morph mating pair ( S ̄morph).
Such a mating pattern transition should be accompa ̄
nied with modifications of floral morphology. Our re ̄
sults confirmed this prediction: firstꎬ the stigma ̄an ̄
ther separations were significantly reduced in all
9155期        ZHOU Wei et al.: Patterns of Floral Variation between Dimorphic and Monomorphic Populations 􀆺       
three L ̄monomorphic populations compared to that
in the dimorphic populationsꎬ andꎬ secondꎬ the de ̄
gree of illegitimate spatial matching of sexual organs
in L ̄monomorphic populations was significantly high ̄
er than that in dimorphic populations. These results
indicate that the floral syndrome of disassortative
mating was breakdown and that both selfing and in ̄
tra ̄morph crossing were facilitated by modifications
to floral morphology in pin ̄monomorphic population.
Future studies of the pollen loads deposited by parti ̄
cular pollinator would be required to determine the
mating components of selfing and crossing in L ̄mon ̄
omorphic populations. The shift in mating patterns
from outcrossing to selfing accompanied by a reduc ̄
tion in herkogamy was also reported in the mid ̄
styled morph of Eichhornia paniculata (Vallejo ̄Ma ̄
rin and Barrettꎬ 2009)ꎻ howeverꎬ our results also
indicated that intra ̄morph crossing was increased in
L􀆰 pinaeana. This difference suggests thatꎬ besides
selfingꎬ animal ̄mediated pollination may also have
an important effect on the reproduction of individuals
in monomorphic populations. Sakai and Wright (2008)
have reported that heterostylous and monomorphic
Psychotria species were visited by the same bee spe ̄
ciesꎬ but that visit frequencies were lower in the
monomorphic species. Although we could not dis ̄
criminate the proportion of the two mating types re ̄
spectivelyꎬ the similar pollinator spectrum ( com ̄
prised Apis floraeꎬ moths and butterflies) were ob ̄
served in both the monomorphic and dimorphic po ̄
pulations of L􀆰 pinceana. In L􀆰 pinceanaꎬ the central
monomorphic and the eastern dimorphic area share a
similar latitude compared with the latitude of the
western dimorphic area. Considering the similar cli ̄
matic conditions and the contiguous distribution of
the central and eastern populationsꎬ it is therefore
quite possible that the monomorphic populations
were more likely to be connected with the eastern di ̄
morphic populations than western populations. How ̄
everꎬ this association was not compatible with the
previous molecular phylogeographic analysis which
inferred that the centrally located lineage composed
of long ̄styled morph ̄biased and monomorphic popu ̄
lations were derived from the western dimorphic line ̄
age by founder event after the last glacial maximum
(Zhou et al.ꎬ 2012).
Floral morphology plays an important role in the
evolution and maintenance of many mating systemsꎬ
including the disassortative mating of heterostylous
species. Results from our comparative study of floral
morphology between dimorphic and monomorphic po ̄
pulations of L􀆰 pinceana indicate that patterns of vari ̄
ation in floral morphology coincide with the transition
of mating patterns. These results demonstrate that
different mating patterns could select for different
floral morphologiesꎬ and that reciprocal herkogamy
was not the only means to increase the proficiency of
cross ̄pollination in distylous species ( Lloyd and
Webbꎬ 1992).
Acknowledgements: The authors thank Zong ̄Xin Renꎬ Hai ̄
Dong Liꎬ Yan ̄Hui Zhaoꎬ Ming ̄Ying Zhangꎬ Jie Liuꎬ Li ̄Na
Dongꎬ and Shu Zhang (Kunming Institute of Botanyꎬ Chinese
Academy of Sciences) for help with fieldwork.
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