Dichogamy - a term coined by Sprengel as “Dichogamie” refers to a temporal separation of sexual functions
Individual bisexual flowers begin anthesis with a functionally male or female phase and continue anthesis with both sexes or only the other sex functional
In the case of unisexual flowers, flowering begins with one sex, and the other sex comes later
In flowers of an individual or a population, the functionally male and female phases are often synchronized
As complete synchronization without overlapping male and female phases in a population would not only exclude cross-pollination, but all pollination, such synchronization needs to be combined with further elaborations that circumvent this disadvantage.
The simplest pattern is slightly overlapping male and female phases, as reported, e.g. for Anaxagorea dolichocarpa
2. INTRODUCTION
Different kinds of heteromorphy in angiosperm flowers with two
reciprocal morphs promote cross pollination.
The most studied is heterostyly, in which anthers and stigmas are
reciprocally positioned, and many aspects of heterostyly have
been studied since Darwin (1877)
Another kind of heteromorphy is resupinate dimorphy, found
only recently in a genus of the Lamiaceae, in which
monosymmetric flowers are resupinate in half of the individuals
of a population and non-resupinate in the other half (Harley et al.,
2017)
Heterodichogamy, like heterostyly and resupinate dimorphy, is
based on a dimorphism, in which two reciprocal genetic morphs
occur in a population in the same frequency, but in a temporal
sequence, suggesting a simple genetic mechanism (Renner,
2001).
3. Cont...
Synchronization of flowering is also important.
This synchrony is either at the level of an individual or also population.
Many heterodichogamous species are selfcompatible as heterodichogamy is an
alternative means to prevent or reduce self-pollination
Other heterodichogamous species have been reported to be self-incompatible
Study flowers
of Kingdonia uniflora, an
isolated endemic of China, that
it posesses heterodichogamous
flowers with protandrous and
protogynous morphs that have
a 1 : 1 ratio.
Flower of Alpinia bracteata
showing an upword curved style.
At around noon, this style will
begin to curve downwards,
bringing the stgma into a
position where it will contact
incoming bees and receives
pollen.
4. DICHOGAMY AND
HETERODICHOGAMY
Dichogamy - a term coined by Sprengel as “Dichogamie” refers to a temporal separation of
sexual functions
Individual bisexual flowers begin anthesis with a functionally male or female phase and
continue anthesis with both sexes or only the other sex functional
In the case of unisexual flowers, flowering begins with one sex, and the other sex comes later
In flowers of an individual or a population, the functionally male and female phases are often
synchronized
As complete synchronization without overlapping male and female phases in a population
would not only exclude cross-pollination, but all pollination, such synchronization needs to
be combined with further elaborations that circumvent this disadvantage.
The simplest pattern is slightly overlapping male and female phases, as reported, e.g. for
Anaxagorea dolichocarpa
5. DIFFERENT STRUCTURAL AND TEMPORAL KINDS OF
HETERODICHOGAMY AND RELATED PATTERNS
(DUODICHOGAMY, PSEUDOHETERODICHOGAMY)
Heterodichogamy was first reported by Delpino for
Juglans regia L.
The term was apparently coined by Errera & Gevaert as
“hétérodichogamie”
In heterodichogamy, male and female functional stages
behave in a way that cross-pollination between the same
morphs is excluded throughout the flowering season or
part of it.
At the transition between the different flowering phases
there can be a short overlap of the two functions (during
which cross-pollination is possible) or
a neutral, functionless phase (during which, as in the more
common case of a smooth transition between the two
phases, cross-pollination is prevented)
Juglans regia L. (Walnut)
6. Classification of Heterodichigamy
(1) Temporally, the change in the sex function occurs only once per vegetation
period.
(1a) Structurally, the flowers are bisexual (e.g. Trochodendron Siebold & Zucc.).
(1b) Structurally, the flowers are unisexual (e.g. Juglans L.).
(2) Temporally, the change in the sex function occurs in a regular pattern many
times per flowering period.
(2a) Structurally, the flowers are bisexual (e.g. Alpinia Roxb.).
(2b) Structurally, the flowers are unisexual (e.g. Hernandia L.).
In addition to heterodichogamy, there are cases in which the synchronization
mechanism is not based on genetic dimorphism.
Similar patterns of synchrony can also come about without the presence of two
reciprocal genetic morphs, but by a specific temporal behaviour of a single morph.
7. (II)Duodichogamy
Term coined by Stout
the two phases come about without two genetic morphs by alternating periods of
several days of the same phase three or more times during a flowering season, but
they are of irregular length.
In the simplest case there are 1½ cycles, mostly with a sequence of male—
female— male or, more rarely, female—male—female phases of flowering of
functionally unisexual or bisexual flowers in an inflorescence
Duodichogamy was first found in the Apiaceae, in which the dichogamous bisexual
flowers in an umbel are synchronized and the phase changes occur when umbels of
the next higher branching order begin to bloom (Müller, 1873).
Apiaceae or Umbelliferae is a family of mostly
aromatic flowering plants. Economically
important plants such as carrot, celery,
cariander, cumin etc.
8. Mostly, duodichogamy occurs in small-flowered, richly-branched inflorescences with
unisexual or bisexual flowers.
It is especially frequent in the Sapindales, such as the Sapindaceae
Synchronization cycles with several or numerous phase changes are quite common (in
the Sapindales and the Apiales), such patterns with multiple phase changes
were called multi-cycle dichogamy by Lloyd & Webb (1986)
(III). Pseudoheterodichogamy
It resembles heterodichogamy but most probably has only one genetic morph.
The two phases come about without two morphs by repeated flushes of flowering
within individuals with always one or two flowerless days in between.
In contrast to duodichogamy, the male and female phases alternate in a daily
rhythm coordinated with the day-night rhythm.
Pseudoheterodichogamy is known from Eupomatia laurina R.Br. (Eupomatiaceae)
(Endress, 1984) and from a few Annonaceae
9.
10. TEMPORAL AND STRUCTURAL FRAMEWORK FOR
THE EVOLUTION OF HETERODICHOGAMY AND
RELATED PATTERNS OF FLOWERING
Annual rhythm
The temporal framework is provided by the annual rhythm of the climate and by the
daily rhythm between day and night.
The annual rhythm is used in heterodichogamous Fagales (prominently in the
Juglandaceae), which have unisexual flowers, flower in spring and are wind pollinated.
In individuals of one morph the male flowers start blooming earlier than the female
flowers, and in the second morph they behave the other way around,
Daily rhythm
The daily (day-night) rhythm (combined with the annual rhythm) provides the framework for
the majority of groups with heterodichogamy and related patterns.
A daily rhythm allows a daily alternation of functional sexes in the flowers, which is realized
in the majority of cases with a daily rhythm of flowering.
A prominent clade of this category are magnoliids, in which this behaviour is known from
five families out of three orders (Magnoliales, Laurales, Canellales).
11.
12.
13.
14. Presence of two flower morphs that exhibit male and female functions at different times among individuals within a
population, and is regarded as an adaptation to promote outbreeding through enhanced intermorph pollination.
In highly fragmented populations in which the morph frequency is biased, heterodichogamy may hamper population
growth by reducing seed sets of the more numerous morph, and enhancing seed sets of the less numerous morph.
Individual plants experience greater seed sets if the opposite sexual morphs are nearby
Individuals of a less numerous sexual morph have greater seed sets.
Observations confirmed that M. thunbergiiis heterodichogamous, consisting of two types of protogynous and
bisexual flowers:
• a morning female (MF)–afternoon male morph
• a morning male (MM)–afternoon female morph at the individual level
Sexual expression of the two morphs was highly synchronized and reciprocal.
Investigation of seed-set rates revealed greater rates of both morphs if the opposite morph was nearby.
The less numerous sexual morph (MF) showed a greater seed-set rate than the more numerous sexual morph (MM).
15. CONCLUSIONS
AND
PROSPECTS
Heterodichogamy has at present been reported in
angiosperms from 12 orders and 13 families (15
families if pseudoheterodichogamy is also included)
It is expected that both patterns, and especially
duodichogamy, will be found in a greater number of
additional families in due course.
Heterodichogamy and related patterns known to date
are concentrated in certain larger clades of
angiosperms (Magnoliidae, Zingiberaceae, Fagales,
Sapindales, Apiales)
Across angiosperms they are, in addition, scattered
across different groups and most probably originated a
number of times.
It is expected that there are still many undiscovered
cases, as they are commonly only detected after
extensive studies of populations over a longer period of
time.
16. Reference
Susannae S. Renner. Trends in Ecology and Evolution Vol.16 No.11 November
2001
Risa D. Sargent* and Sarah P. Otto. A phylogenetic analysis of pollination mode
and the evolution of dichogamy in angiosperms. Evolutionary Ecology
Research, 2004, 6: 1183–1199
PETER K. ENDRESS. Structural and temporal modes of heterodichogamy and
similar patterns across angiosperms. Botanical Journal of the Linnean Society,
2020, 193, 5–18.
SHUNTARO WATANABE, NAOHIKO NOMA and TAKAYOSHI NISHIDA