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Jahnke 2
Jahnke 2
Functional Dimensions
Author(s): David G. Lloyd and Daniel J. Schoen
Source: International Journal of Plant Sciences, Vol. 153, No. 3, Part 1 (Sep., 1992), pp. 358-
369
Published by: The University of Chicago Press
Stable URL: http://www.jstor.org/stable/2995676 .
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SELF-ANDCROSS-FERTILIZATION
IN PLANTS.
1. FUNCTIONAL
DIMENSIONS
DAVID G. LLOYD AND DANIEL J. SCHOEN
Plant and MicrobialSciences,University of Canterbury,PrivateBag, Christchurch,New Zealand;
and Biology Department,McGill University, Montreal,Quebec H3A IBI, Canada
In this and the following articles we examine erties of cross-fertilizationand the genetic prop-
these major functional dimensions of self- and erties of self-fertilization.The distinctive nature
cross-fertilizationand attempt to integratethem of geitonogamyhas led to its being the only mode
with genetic approachesto the subject. This ar- of chasmogamous selfing that was distinguished
ticle introduces functional aspects of self- and traditionally(Kemer 1895). A certainamount of
cross-fertilizationby describingthe variousmodes geitonogamy is virtually inevitable in self-com-
by which selfing occurs and the ecological, mor- patible plants that produce a number of flowers
phological, and physiological factors that influ- at anthesis at the same time. Geitonogamy is
ence their frequencies.It also reviews published probablythe most widespreadmode of self-pol-
work on spontaneousself-pollinationto examine lination, but it may never achieve the predomi-
functional factors that contributeto variation in nance that the autonomous modes acquirein ha-
the frequency of self-fertilization. The two fol- bitually selfing species. It would be even more
lowing articlespresenta phenotypicmodel of the important but for the fortunate and still largely
selectionof self-fertilization(Lloyd 1992) and de- unexplained habit shared by virtually all flower
scribe and illustrateexperimentalproceduresfor visitors of visiting only a fractionof the available
estimating the selective forces and partitioning flowerson a plant beforemoving to the next plant
the full complement of self-fertilizationinto its (Frankieet al. 1976; Kadmon and Shmida 1992;
component modes (Schoen and Lloyd 1992). Robertson 1992).
Charles Darwin (1859, 1876) recognized the
Modesof self-pollination importanceof geitonogamywhen he arguedthat
trees are likely to be self-pollinated more fre-
CLEISTOGAMY
quently than other plants because they display
In morphologicalterms,the most distinctmode more flowersat one time. Darwin postulatedthat
of selfingis cleistogamy(Kuhn 1867; Lord 1981), this could explain the higherfrequencyof species
which occurs in closed flowers that are structur- with separatesexes among the trees of the United
ally specialized for self-fertilizationand do not Kingdom, New Zealand, and the United States
outcross.Cleistogamydiffersfromall othermodes (but not Australia) than among other plants of
of selfing in several respects. It is the only mode the same regions. A centurylater, Arroyo (1976)
that occurs in morphologicallydistinct flowers. proposedthat the occurrenceof geitonogamymay
Hence, it can be recognizedimmediately and its be an important factor in the selection of self-
frequencycan be measured simply by counting incompatibility as well as separatesexes.
the numbers of cleistogamously and chasmoga- A few recent studies have examined the rela-
mously producedseeds. Morever, cleistogamy is tionship between the frequency of geitonogamy
uniqueamongmodes of selfing(Schoenand Lloyd and flower number that Darwin implied (Craw-
1984; Lively and Lloyd 1990) in possessing an ford 1984; Geber 1985; Handel 1985; Hessing
advantage over outcrossing (the "cost of out- 1988; Robertson 1992). The amount of geito-
crossing")that is derivedfroma cost of producing nogamy is influencednot only by the flower dis-
males, as modeled by Maynard Smith (1971), play but also by factors that affect the extent of
rather than a cost of meiosis, as described by pollen carryover(Robertson 1992). Otheraspects
Williams (1971). Cleistogamousflowerscost less of geitonogamy, such as its distribution among
to producebecause the cost of pollen and attrac- the flowers on a plant, variation with pollinator
tants is very low. Cleistogamy is also distinct in abundanceand type, changes throughouta flow-
that in many species the cleistogamously and ering season, and the relative degree to which it
chasmogamouslyderivedseeds differin their size, displaces cross-fertilizationand the autogamous
dispersal, germination, and survival character- modes of selfing, remain unexplored. All these
istics (Campbellet al. 1983; Schmitt and Gamble factorsinfluencethe measurementor selection of
1990). Altogether,the operationand selection of geitonogamy.
cleistogamy differ widely from those of other
FACILITATED SELF-POLLINATION
modes of selfing(Schoenand Lloyd 1984). In this
series of articles we confine our attention to the In the course of foraging for rewards, flower
chasmogamous modes of selfing that occur in visitors may cause some autogamyas well as gei-
flowers that can also engage in self-pollination. tonogamy (Knuth 1906-1909; Estes and Brown
1973; Hinton 1976; Schneider and Buchanan
1980; Pazy 1984). Like geitonogamy and com-
GEITONOGAMY
peting selfing (see below), such facilitated selfing
Geitonogamy is the most distinct of the chas- (so named by Schneiderand Buchanan 1980) oc-
mogamous modes of selfing because it involves curs at the same time as outcrossing.Facilitated
transferof pollen between flowers and requires selfing is primarily a by-product of adaptations
the same pollination mechanism as cross-polli- for outcrossing, again resembling geitonogamy
nation. Consequently,it has the ecological prop- (Lloyd 1992). In flowers that present pollen and
stigmas duringthe same visits, facilitatedselfing (Lloyd 1992). The original definition of compet-
is almost impossible to eliminate completely un- ing selfing (Lloyd 1979) did not distinguish it
less thereis a mechanismthat ensuresthat stigma from facilitatedselfingand was thereforebroader
contacts in a flower strictly precede pollen con- than the present definition. The two modes can
tacts, as in Cypripediumspecies (van der Pijl and be separatedexperimentallyin animal-pollinated
Dodson 1966) or species with sensitive stigmas species(Schoenand Lloyd 1992). Competingself-
(Newcombe 1922). ing is probably relatively unimportant in abiot-
The amounts of facilitated selfing that animal ically pollinatedplants,which are often unisexual
visitors cause in the course of their foragingac- or completely dichogamous.
tivities are likely to vary enormously, depending Competingselfingoccursby a variety of mech-
on the way visitors move, the time they spend anisms. In some species, such as many self-com-
on each flower, and the positions of the anthers patible Brassicaceaein which the paired anthers
and stigmas. There are no data available, but, surround the stigma, competing selfing results
following Heine (1937), we expect that less spe- simply from the close proximity of pollen and
cialized visitors that forage on promiscuously stigmas duringanthesis. In other species, the ex-
pollinated flowers are likely to cause more facil- act temporal relationships between selfing and
itated selfingthan specializedvisitors with more crossing events, and thus the degree to which
precise movements. competingselfingpreemptsoutcrossing,are more
complex. They depend in part on the pattern of
THE THREE MODES OF AUTONOMOUS
dichogamy.In incompletelyprotogynousspecies,
SELF-POLLINATION the stigmas have an opportunity to receive out-
Prior, competing, and delayed self-pollination crossingpollen first.In incompletelyprotandrous
are similarin being autonomous modes of selfing species, competing selfingthat occurs when stig-
that occurwithoutthe participationof an external mas become receptivetakesplaceduringthe same
agent. The three modes differ in their timing interval as outcrossingand is thereforelikely to
(Lloyd 1979). They occur before, during,and af- have a greatereffect on the amount of cross-fer-
ter opportunitiesfor outcrossingin a flower, re- tilization. An intermediate situation occurs in
spectively. As a result of their different timing, flowersthat open and close daily for several days
they also differ in the degree to which they dis- if they undergo competing selfing only when the
place cross-fertilization(Ockendon and Currah petals are moving or when they are closed (Mee-
1978) and in the conditions required for their han 1876).
selection (Lloyd 1979, 1992). Delayed selfingoccurswhen the movements of
Numerous but brief anecdotal accounts con- flowerparts at the end of anthesis lead to pollen-
cerningwhen and how autonomousselfingoccurs stigmacontactsand the fertilizationof ovules that
in various species are scattered through the lit- have not been previously cross-fertilized.In spe-
erature. Earlier observations were collected by cies that areherkogamousduringthe periodwhen
the Germanencyclopedists(Muller 1883; Kerner cross-pollinationoccurs, flowermovements dur-
1895; Knuth 1906-1909). A notable modem ex- ing senescencemay cause self-pollination.In cer-
ample is the work on the self-pollination of or- tain Campanulaceaeand Asteraceae,e.g., the style
chids by Catling (1990), who made careful ob- armscurlaroundand touch the style wherepollen
servationsof floralbehavior that showed exactly has been presented secondarily (Faegriand van
when and how, though not precisely how much, der Pijl 1979). In some species with epipetalous
autonomous self-pollination occurs in various stamens, the fall of senescent corollas may cause
species. We know of no experimental attempts a portion of any remainingpollen to be brushed
to determinethe relative importanceof the three against the stigmas (Hagerup 1957; Dole 1990,
modes of autonomous selfing in any species. but compare Dudash and Ritland 1991).
Prior selfing occurs when anthers dehisce and
stigmasare receptivebeforeanthesis and the two Factorsthat influencethe frequency
pollinating surfacesare positioned and oriented of self-pollination
so there is contact between them in unopened The amount of self-fertilizationin a plant is
buds. Some self-fertilizingspecies regularlyen- affectedby a number of factorsthat provide fur-
gage in bud pollinations (Hagerup 1952). Many ther functional dimensions of self- vs. cross-fer-
species may undergo an increase in prior selfing tilization.
when floweropeningis postponedin poor weath-
er and herkogamyis less fully developed (again CONSTRAINTSON THE MODES
there are no firm data). OF SELF-POLLINATION
Competingselfingresembles facilitated selfing The morphologicaland phenological features
in that it occursduringthe same intervalas cross- of flowers impose distinct constraints on each
pollination, but it differs in being achieved au- mode of self-pollination. Species that have any
tonomously and, hence, it is more easily selected degree of dichogamy, either protandry or protog-
yny, cannot engage in prior selfing. Conversely, observationsof the prepotencyof cross-pollenin
delayed selfing cannot take place in species in competition experiments with nominally self-
which the pollen is no longer viable, or stigmas compatible species-those in which the success
are no longer receptive, when the opportunities of separate self- and cross-pollinations is ap-
for cross-pollinationin a flower are over. If the proximatelythe same (Bateman 1956; Ockendon
structureof flowersallows pollen to be picked up and Currah1978; Wellerand Omduff 1989; Cru-
during a pollinator visit only after the stigmas zan and Barrett1992).The phenomenonis known
have been contacted,facilitatedselfingcannot oc- as cryptic self-incompatibility. A weak self-in-
cur.In many herkogamousspecies,the pollen and compatibilityreaction can also lead to a reduced
stigmasare too distantly separatedduringanthe- probabilityof fruit set from self-pollinatedflow-
sis for competing selfing to be possible. The de- ers that compete with outcrossedflowers(Becerra
gree of anther-stigmaseparation affects the fre- and Lloyd 1992). Not all self-compatibleplants
quency of self-pollinationin some species (Rick have competitively inferior self-pollen, however
and Dempsey 1969; Schoen 1982; Barrett and (Snow and Spira 1991).
Shore 1987;Holtsfordand Ellstrand1992).More- Self-incompatibilityis often incomplete, lead-
over, the amount of selfingmay dependon wheth- ing to varying degrees of seed set after artificial
er the stigmas or anthersare higher(approachor self-pollination (pseudocompatibility). In par-
reverseherkogamy)(Sobrevilaand Arroyo 1982; tially self-incompatible species (those in which
Kohn and Barrett 1992). the seed set is lower in selfed flowers than in
Geitonogamyis the most constrainedmode of separatelycrossed flowers), self-pollen performs
chasmogamous self-pollination. A considerable poorly even in the absence of competition from
amount of geitonogamy is often unavoidable as cross-pollen.We thereforeexpect the prepotency
a consequence of the movement of pollinators of outcrossed pollen to be more pronounced in
between flowers of the same plant. The amount competition experimentswith these species than
of geitonogamy may be varied by altering the in crypticallyself-incompatiblespecies. A num-
number or disposition of flowers or their indi- ber of studies of species with both gametophytic
vidual attractiveness,which altersthe numberof and sporophyticself-incompatibilitysystemshave
successive visits that a pollinator makes to the confirmed that compatible pollen is prepotent
flowersof a plant, or by changingfloral structure over partiallyincompatiblepollen (Eenink 1982;
so that the amount of pollen carryoveris altered Visser and Marcucci 1984; Bertin 1990). In pol-
(Robertson 1992). All these changes, however, len competition experimentson tristylousspecies
alternot only the amountof geitonogamybut also of Pontederiaceae, Barrett and colleagues have
that of cross-pollination. found that legitimate pollen is prepotentover il-
The operation of these structuraland behav- legitimate pollen in both self-incompatible and
ioral constraintsmeans that a particularspecies self-compatiblepopulations (Barrettand Ander-
of plants may be able to employ, or prevent, only son 1985; Cruzanand Barrett 1992).
a limited fractionof the modes of self-pollination. We recommendthat Darwin's term, prepoten-
cy, be revived to cover all the above phenomena
that cause cross-pollen to succeed in fertilizing
THE RELATIVE COMPETITIVE ABILITIES
ovules more often than by chance when it com-
OF SELF- AND CROSS-POLLEN
petes with self-pollen. This definition applies to
The competitive abilities of self- and cross- partially self-incompatible plants as well as to
pollen influence the amount of self-fertilization, those that exhibitcrypticself-incompatibility,but
particularlywhen selfing occurs over the same it excludes postzygotic expressionsof inbreeding
period as crossing (the geitonogamous, compet- depression. When prepotency occurs, the pro-
ing, and facilitatedmodes). Darwin (1876) dem- portions of self- and cross-fertilizationneed not
onstrated that a number of species are highly match those of self- and cross-pollination,even
self-fertile when isolated and yet produce pre- in nominally self-compatiblespecies. Prepotency
dominantly outcrossed progeny when they are is probablyan importantdeterminantof the mat-
surroundedby differentvarietiesof the same spe- ing system in many species that have incomplete
cies or differentindividuals of the same variety. self-incompatibilitybarriers,althoughit may not
The observations were made by growing plants have the ubiquity that Darwin postulated (Jones
in close proximity and identifying outcrossed 1928).
plants by their characters(when from different Despite Darwin's lead, there has been no
varieties) or vigor (when from individuals of the attempt to determine the degree to which pre-
same variety). Darwin postulated that the "pre- potency limits natural frequencies of self-fertil-
potency" of outcrossingpollen was the most im- ization in self-compatibleor partiallyself-incom-
portant factor in limiting the natural frequency patible species. This would require experiments
of self-fertilization. on the timing of self-pollinationas well as others
In modem times there have been a number of on the prepotencyof outcrossedpollen deposited
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16 %Fruit (seed) set following artificial self-pollination
114 B Fig.2 The relationshipbetweenthe frequenciesof fruitor
6 12 seed set after self-pollinationand in isolated flowersamong
10 the samples of self-compatibleand self-incompatiblespecies
in tables 1 and 2.
0
6
5-
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4 What is surprisingis that this association is not
Z 2 stronger,as is seen in the wide ranges of auto-
0 fertilityin self-incompatibleand self-compatible
00. 2 0.4 0.6 0.8 1.0 1.2 1.4 1.6C species and in the scatterin figure2. In some self-
AUTOFERTILITY
INDEX incompatible species, the evolution of even a re-
Fig.1 The distributionsof AutofertilityIndicesfor (A)self-
stricted ability of self-pollen to succeed in fertil-
compatiblespecies and (B) self-incompatiblespecies. ization is sufficient to allow some autonomous
selfingdespite the partialincompatibilitybarrier.
On the other hand, the range of autofertilityin
self-compatiblespecies shows that complete self-
patibility,we comparedfirstthe AutofertilityIn- compatibility,at least as evident in separateself-
dices for the self-compatibleand self-incompat- and cross-pollinations, does not guarantee that
iblegroups.Amongthe self-incompatiblesamples, much, or even any, autonomous self-pollination
the AutofertilityIndices rangefrom zero (six spe- will be possible. The degreeof self-compatibility
cies) to 0.76 (fig. 1B); the geometricmean of non- apparentlyis not the only factor that influences
zero values is 18%of the potential seed set. The the extent of autonomous pollination.
AutofertilityIndicesfor the self-compatibleplants To identify morphological and phenological
rangeeven more widely, from zero (11 samples) factors that affect the ease of autonomous polli-
to 1.52 (fig. 1A);five samples have values of one nation, we have examined a number of features
or more, and the geometricmean of nonzero val- of the floralbiology of the speciesreviewed(tables
ues is 47%. The results indicate a significant re- 1, 2). The species lacking autofertilityaltogether
lationship between self-compatibility and auto- or having low Autofertility Indices tend to be
fertility, as one would expect. The association concentratedin a few families, particularlythe
between self-compatibility and autofertility is Balsaminaceae, Fabaceae, Lobeliaceae, Orchi-
confirmedwhen the average frequenciesof seed daceae,and Scrophulariaceae. These familieshave
set in isolated flowers and after self-pollination specialized pollination mechanisms and charac-
are graphedagainst each other (fig. 2; r = +.32, teristicallyhave bilaterallysymmetrical flowers,
n = 65, P = .01 when both frequencies are trans- fused petals, and, in most species, relatively few
formed to angles to improve the approximation stamens per flower. In most species there is a
to a bivariate normal distribution). The corre- strongherkogamymechanismseparatingthe pol-
lation between the two indices cannot be tested len and stigmas.The three species with unisexual
directly because both indices include the cross- flowers, Caperoniapalustris, Dieffenbachialon-
pollination success in their computations. Fur- gispatha, and Croton hirtus, also have low Au-
thermore, several detailed studies have shown tofertilityIndices. Moreover,all species reported
that autofertilityis correlatedwith the estimated as dichogamoushave low autofertility,e.g., spe-
selfingrate among populations of a species (Har- cies of Impatiens, Lobelia, and Isopyrum.
ding et al. 1974; Schoen 1982; Lyons and An- At the other extreme, the species with more
tonovics 1991). In these species, at least some of than 50%autofertilityusually have radiallysym-
the self-fertilization appears to result from the metrical flowers, separatepetals, and more than
operation of one or more of the autonomous five stamensperflower(tables 1, 2). These species
modes of selfing. are likely to have less precise placement of floral
The association between the degrees of self- parts, and this may allow less herkogamy and
compatibilityand autofertilityis not unexpected. greaterlevels of autonomous selfing.
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