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ADAPTIVE RADIATION OF REPRODUCTIVE 4012

CHARACTERISTICS IN ANGIOSPERMS,
I: POLLINATION MECHANISMS
G. LEDYARD STEBBINS
University of California, Davis

INTRODUCTION

The overwhelming majority of biologists who have studied both the origin
of races and species and major trends of evolution in animals have reached the
conclusion, in agreement with Darwin, that these visible evolutionary
changes are based upon shifts in adaptive systems, guided by natural selec-
tion (30, 31, 94, 117, 120). The evidence is convincing for all phyla of ani-
mals that have been carefully studied. In plants, however, the situation is
much less clear, and a wide spectrum of opinions has been expressed during
the past twenty years. With respect to the origin of races and of manyspe-
cies that occupy different habitats from those of their nearest relatives, the
evidence for divergent adaptation guided by natural selection is as convinc-
ing for plants as it is for animals (20, 50, 127). On the other hand, bota-
nists opinions are still divided wtih respect to the role of natural selection
in the origin of genera, families, and other higher categories. Good (42)
has expressed in strong terms his belief that the diversity of floral types
present in angiosperms evolved independently of adaptation and selection,
and Nelson (99) has presented a similar point of view. Neither of these
authors discussed the genetic mechanisms that might be involved. Both
Cronquist (22, 23) and Werth (135) believe that the principal guiding
force has been differential directed mutation. In Cronquists words (23, pp.
120-21): "The influence of differential mutation is often so strong that
group appears to be predisposed to evolve in a certain direction." A note-
worthy feature of both his general interpretation (p. 118) and his refer-
ences to possible adaptive characteristics of individual families that are
scattered throughout his book is that he apparently equates adaptation
largely with the survival value of the adult plant. One of the principal ob-
jectives of this review is to point out the fallacy of this viewpoint, since it is
probably held by the majority of plant taxonomists. In angiosperms, the
adaptive significance of differences between most higher categories, as well
as between a large proportion of related species, is most probably associated
with reproductive efficiency and successful establishment of seedlings
rather than with any of the morphological characteristics of the vegetative
parts.
The latter point of view has been maintained by botanists who have
307
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308 STEBBINS
madecareful studies of pollination mechanisms (8, 12, 17, 47, 52, 107, 108),
seed dispersal mechanisms(8, 13, 38, 109, 119), and the ecology of seedling
establishment (59). These authors have accumulated numerousexamples
showhowmorphological differences between categories at all levels are re-
lated to various kinds of adaptations for reproductive efficiency. The state
of our knowledgein this field is still very rudimentary, since it has becomea
fashionable field of study only recently and then only in a relatively small
numberof botanical laboratories. Nevertheless, enoughis already knownso
that we can predict that research in these fields is going to be the most
fruitful approachto understanding evolutionary trends in higher plants.
One might at this point ask whydifferences between major categories in
higher plants should be recognized chiefly in characteristics that affect re-
productive biology, whereasin animals they maybe equally significant, and
often moresignificant, with respect to characters concernedwith survival?
In motile animals, in which survival dependsto a large extent upon captur-
ing prey, escaping from predators, or both, a high degree of functional and
developmentalintegration is required f6r both survival and reproduction. In
plants, on the other hand, survival depends to a muchlesser degree upon
integrated activities than it does in animals. Consequently, the plant body
can ai~ord to be muchmore plastic, and its size and shape can be governed
to a large extent by environmental factors. This plasticity extends to the
potentialities that can be realized by modifying the same overall adaptive
system to the demandsof very different environments. Consequently, many
of the larger plant genera, such as Pinus, Quercus, Euphorbia, Senecio, and
Care:r, have evolved adaptations to a great variety of climates and edaphic
habitats, while retaining very similar reproductive structures. A further
consequenceis that, in contrast to the correspondingcategories of most ani-
mal phyla, orders and ~amilies of higher plants are not usually characterized
by distinctive vegetative characteristics that fit themfor a particular mode
of survival. There are, of course, manyexceptions to this rule. Someof the
best knownare the succulent Cactaceae and Crassulaceae, the parasitic or
partly parasitic Loranthaceae, the aquatic and floating ]Lemnaceae,and the
Podostemaceae,which are strongly modified for llfe in flowing streams of
tropical regions.
On the other hand, the reproductive functions of higher plants require
levels of integration quite comparableto those found in animals. For adap-
tation to cross-pollination by animals with specialized habits, such as bees,
butterflies, moths, birds, and bats, the flower must becomea highly inte-
grated structure, with all of its parts precisely adjusted to each other. Suc-
cessful development and maturation of seeds requires coordination with
ovary and fruit development, and both of these processes must be adjusted
to the favorable growing season of the plant. In addition, precise mecha-
nisms have often been evolved for seed dispersal by either windor animals.
These mechanismsinclude: adjustment of buoyancyto seed size, attractive-
ness to animal vectors, adherence to animals that serve as involuntary vec-
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 309

tots, or retention of viability after passing through the animals digestive
system. Finally, embryosize and structure, stored food, seed coats, and
other auxiliary structures must be adjusted both morphologicallyand physi-
ologically to insure germination and seedling establishment whenconditions
are favorable and to prevent their occurrence under unfavorable conditions.
This need for integration often confers the greatest adaptive value upon
systems which involve various kinds of compromises. For instance, in-
creased seed size often confers an advantage because it makespossible ei-
ther more vigorous growth of seedlings or the continuation of seedling
growth for longer periods of time before photosynthesis begins in the
leaves. Large seeds, however,are less easily dispersed than small ones, and
they usually require a longer period of developmentafter the end of flower-
ing. Betweenthese conflicting demands,therefore, each species must estab-
lish a compromise that adapts it to a particular ecological niche.
Becauseof the overriding importance of reproductive ecology for an un-
derstanding of trends of evolution, the remainder of the present review will
be devoted to surveying one series of factors that contribute to reproductive
success. The space allotted to this article permits considerationonly of polli-
nation mechanisms.

METHODS OF ~OLLINATION

Since the time of Darwin(27, 28), botanists have marveledat the vari-
ety of devices that have evolved in plants to insure cross-pollination. Even
more remarkable is the fact that none of these devices are necessary for
survival, or even for the successful perpetuation of a species over thousands
or even millions of years. The existence of manyspecies that are largely or
entirely self-fertilizing has long been recognized(40, 129). Moreover,such
species can maintain stores of genetic variability that are nearly or quite as
great as those found in related species whichare obligate outcrossers (1, 2,
66). Nevertheless, self-fertilizing species are usually the end of evolution-
ary lines and rarely if ever contribute to major evolutionary trends. Appar-
ently the genetic structure that is most characteristic of obligate outcross-
ers, particularly the presence of heterozygosity at a large proportion of
gene loci, is a sine qua non for the continuance of major evolutionary
trends.
Nevertheless, we cannot regard, increased potentiality for evolutionary
changeas the chief basis for the persistence of obligate outcrossing in most
species. Natural selection has no foresight; only immediate advantages or
disadvantagesare significant. If, however,a species has for a long time ex-
isted as an obligate outcrosser, its populations usually harbor so manyreces-
sive alleles that great reduction in vigor results froma suddenshift to self-
fertilization. This phenomenonof inbreeding depression has long been
knownand has been reaffirmed by recent authors (Mfintzing 97). It is prob-
ably responsible for the fact that in manyinstances evolutionary lines re-
spond to newhabitats by evolving newmechanismsfor cross-fertilization.
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310 STEBBINS

EVOLUTIONOF SELF-FERTILIZING SPECIES FROM OBLIGATE OUTCROSSERS

The evolutionary pathwayfrom obligate outcrossing based upon self-in-
compatibility to predominantself-fertilization has probably been followed
by moredifferent liues of evolution in flowering plants than has any other.
As I mentioned in an earlier publication (129), numerousexamplesof this
trend can be found in families of herbs, such as Cruciferae, Leguminosae,
Onagraceae, Compositae, and Graminae. More recently described examples
are those of Grant (51) in Gilia, Lewis & Szweykowski(82) in Gayophy-
turn, Raven (114) in Camissonia, Khoshoo& Sachdeva (68) in Convolvu-
lus arvensis, Martin (92) in Melochia (Sterculiaceae), and Ornduff (101,
102) in the Limnanthaceae.In all of these examples, self-compatibility has
probably been acquired through loss mutations of genes at the self-incom-
patibility locus (81). The origin of self-fertilization from cross-fertilizing
heterostylous groups, through persistence of one of the monomorphic types
that can arise from "illegitimate" fertilizations, is well knownthrough the
research of Crosby (24, 25) on Prinvula, of Baker (3, 4, 5, 14) on the
Plumbaginaceae, and of Mulcahy(96) on Oxalis.
In most of these examples, the morphological alterations of the flower
that are associated with this shi{t are minimal. In most genera of Grami-
neae, for instance, cleistogamous flowers evolve from chasmogamousones
merely by the reduction in size of anthers and lodicules (57). The self-fer-
tilizing Eupatoriummicrosternon is morphologically almost indistinguisha-
ble from its cross-fertilizing relative, E. Sinclairii (15). In Lycopersicurn,
the self-fertilizing species related to L. esculenturn and L. pimpinellifoliurn
differ chiefly with respect to minoradjustments in the structure and position
of anthers and stigma (118). The homostylous descendents of heterostylous
species contain a favorable combinationof characteristics found in the two
different flower types present in their ancestors: usually long styles com-
bined with anthers situated high on the corolla tube. This condition can
originate through rare crossing over between closely linked genes (33).
all self-fertilizers, flower size diminishes belowthat found in their cross-
fertilizing ancestors.
1V~oreprofound changes have accompaniedthe shift from cross- to self-
fertilization in the small North Americanfamily Limnanthaceae(102).
most species of the GenusLimnanthes, whichare cross-fertilizing, the flow-
ers are large and consistently 5-merouswith respect to all of their parts. A
few species, however,are self-fertilizing and have flowers of reduced size,
though without reduction in the number of parts. Finally, the monotypic
genus Floerkea resembles Limnanthesin all respects except that its flowers
are still smaller and are trimerous. Floerkea apparently evolved from Lirn-
nanthes by reduction following the acquisition of self-fertilization. In the
grass species Bothriochloadeciplens, self-fertilization via cleistogamy has
been aided by the acquisition of a distinctive morphologicalcharacteristic, a
pit on the glumes(63).
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 311

The shift from obligate crossing to self-fertilization occurs chiefly, and
perhaps exclusively, in species that occupytemporary, pioneer habitats. Such
species can persist only through the repeated colonization of new hab-
itats, usually by one or a few individuals. Underthese conditions, self-fertil-
ization maybe the only way in which the new colonizers can produce off-
spring. Often, these pioneer habitats are on the margins of the area of dis-
tribution for the species and its genus and maybe subject to adverse condi~
tions for cross-pollination, such as excessive moisture in northern and
oceanic regions (55, 56) or drought and absence of suitable pollen vectors
in the deserts. Baker (5, 6, 9) has documentedwell the association of the
shift fromcross-fertilization to selfing with the transoceanic migration of a
species. In order to be successful, the changemust be gradual, via an inter-
mediate stage of facultative selfing. In this waythe adverse effects are min-
imized, and in a favorable new location, free from competition against vig-
orous outcrossing ancestors, the new colonist mayadjust its genetic system
to facultative selfing. Althoughmanygenera exist in which the self-incom-
patible species are predominantlyperennials and the self-fertilizers are an-
nuals, the shift from cross- to self-fertilization does not usually accompany
the acquisition of the annual habit of growth. In manygenera of grasses,
such as Bromus(58), Elymus (121), Festuca, and Poa (personal observa-
tions), self-fertilizing perennials are common, and the shift to selfing has
apparently occurred at the perennial level. In Lolium, on the other hand
(67), both outcrossing and self-fertilizing annuals exist, and the shift
selfing has apparently occurred at the annual level. The sameis true of pre-
viously mentionedexamples, such as Clarkia, Camissoa,Gayophytum,Gilia,
and Limnanthes, as well as ,4msinckla (115, 116) and manyother genera.
The frequent correlation in a genus of the perennial habit with outcrossing
and the annual habit with selfing is probably due to the fact that annuals,
because of their general adaptation for frequent colonization of new habi-
tats, are morelikely to succeedand spread as sellers than are perennials.
The shift from one mechanismthat favors outcrossing to another kind
of adaptation having the same effect is best documentedwith respect to the
origin of heterstyly and of dioecism (134). Dioecism can arise directly
from heterostyly, as in Nymphoides(100), but it more often evolves
other ways, particularly from facultative selvers having bisexual, mono-
morphic flowers, as in Silene (Melandrium)dioica and other Caryophylla-
ceae (8). The same is probably true of the origin of heterostyly, as sug-
gested by Vuilleumier (134) after reviewing a large numberof examples.

SHIFTS BETWEEN INSECT AND WIND POLLINATION

The three principal ways in which pollen can be borne from one plant to
another are by insects, wind, and--amongaquatic plants--water. The latter
methodhas been little studied, and no good examplesof adaptive radiation
to it are kn6wnto this author. Adaptive shifts from insect to wind pollina-
tion and vice versa are, however, well known. They are accompanied by
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312 STEBBINS
characteristic alterations of floral morphology(39). Wind-pollinated flow-
ers differ from those of related insect-pollinated species in: 1. their ten-
deneyto be clustered in denseinflorescences, 2. their small size, 3. their re-
duced, inconspicuousperianth, 4. their lack of nectar, 5. their anthers, which
have abundant pollen and open with explosive dehiscence, 6. the expanded
surface of their stigma, and 7. usually in the separation of the sexes, either
on different inflorescences (monoecism)or different plants (dioecism).
though the majority of wind-pollinated flowering plants occur in distinctive
families or genera, whoserelationships are often in doubt, several examples
exist in which the direction of evolution can be postulated with reasonable
assurance. The following are representative:

Ranunculaceae.--Thalictrum is the only genus of this family that con-

tains wind-pollinated species (69). All of the species of this large genus are
apetalous and have flowers in dense panicles or racemes. Somehave bisex-
ual flowers, others are dioecious, and still other species are of various inter-
mediate conditions. The nearest relative of Thalictrum is the small genus
Anemonella, which consists of low-growing perennials having" solitary,
more conscpicuous white flowers that are probably pollinated by small in-
sects, although gooddocumentationis lacking.

Rosaceae.--The only exceptions to insect pollination in this family are

genera belonging to the tribe Poterieae, such as Poterium, Sanguisorba, and
Acaena. These genera--found chiefly in the Mediterranean region and
South America, although there are several species of Acaena in NewZea-
land and one in California--possess the syndromeof characteristics men-
tioned above: apetalous, inconspicuous, unisexual flowers in dense inflores-
cences. Most of them are vigorous, thick-stemmed herbs or small shrubs
adapted to rocky, semiarid sites. In Sanguisorba, one group of species (S.
oficinalis, S. canadensis, S. microcephala, S. tenuifolia) consists of tall
herbs that inhabit swampsin northern Eurasia and North America. In spite
of having apetalous flowers, they produce nectar and are pollinated by in-
sects. They mayrepresent a secondary reversion from wind to insect polli-
nation.

Compositae.--In this, the largest family of flowering plants, two groups

of genera have diverged from the entomophily that is characteristic of the
family and have acquired wind pollination. One of them is the subtribe Am-
brosiinae, or ragweeds, of the tribe Heliantheae. Its largest genus, Ambro-
s/a (including Franseria), consists of shrubs, herbs, and weedyannuals,
whosecenter of distribution is the arid southwestern portion of the United
States and adjacent Mexico (103). The genus Ira, found in the same re-
gion, forms a partial link betweenthis subtribe and the subtribe Melampodi-
inae, particularly the genus Parthenlum. Other small genera of Ambrosii-
nae, Oxytaenia, Dicoria, Hymenoctea,and Xanthium, are radiants from this
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 313

complexthat have retained wind pollination and have acquired various spe-
cializations in their fruits. Of these, only Xanthlumhas spread beyondthe
dispersal center of the subtribe; it has becomeworld-wide, exceeding the
geographical area even of ~tmbrosiaitself.
Windpollination in the Compositaeoriginated independently in the ge-
nus ~trtemisia of the tribe Anthemidae.This large genus, possessing "over
100" (98) or "more than four hundred" (111) species, has its main center
of distribution in Central Asia, where 174 species are recognized. This is
also a region of great diversity for other genera of the tribe, there being 18
genera endemicto this area. Most of these genera are insect-pollinated.
The origin of z4rtemisia, therefore, was probably in the cold, arid steppes of
Central Asia, where it acquired all of the morphologicalcharacteristics of
wind-pollinated groups. Its present distribution is in temperate regions
throughout the world, including those having moist, equable climates.

Cyperaceae.--This family consists almost entirely of wind-pollinated

species. Alongwith the related .luncaceae, it has a long evolutionary history
of wind pollination, whose origin is obscure. Nevertheless, the genus Di-
chromena, which is widespread in moist tropical regions, has reverted to
insect pollination (76). In association with this shift, it has evolved a con-
spicuous group of white leaves surroundingits inflorescence.

Moraceae. The mulberry family probably represents the best example

in flowering plants of extensive reversion from wind to insect pollination,
even thoughinformation on its floral biology is very scanty. It belongs to an
order, Urticales, in which all of the other families (Ulmaceae, Cannaba-
ceae, Urticaceae) are wind-pollinated; Within the Moraceae,wind pollina-
tion is recorded for Morusand Broussonetia (69). Nevertheless, the largest
genus of the family, Ficus, whichcontains about 600 species, is one of the
most remarkable examples of entomophily in the plant kingdom. Almost all
of the species investigated are pollinated by one or a few species of chalcid
wasp, distinctive for that species of Ficus (11, 107, 108, 136). Since Ficus
has manyspecies in tropical regions of both hemispheres, this condition
must be very old.
The Moraceaeapparently are an exampleof a family that evolved from
wind-pollinated ancestors adapted to a relatively dry tropical climate. After
invading the moist tropics, they evolved at least one secondary adaptation
for insect pollination.
The facts summarizedabove lead to the conclusion that the shift from
insect to windpollination is most likely to occur in open, often arid habitats,
which may be cold (Thalictrum, Artemisia), warmtemperate (Poterieae,
Ambrosiinae), or tropical Urticales). Since the groups involved may
herbaceous, shrubby, or aboreal, this shift is not favored by any particu-
lar growth habit. If derivatives of wind-pollinated groups reinvade regions
having a moist climate, they usually either retain wind pollination and oc-
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314 STEBBINS
cupy only relatively open habitats that have free circulation of air (~m-
brosia, Xanth~m,,4rtemisia) or revert to ~acultative self-pollination, which
enables them to enter closed, forest habitats. Muchmore rarely, they may
evolve secondary adaptations for insect pollination (Dichromena,Ficus).

ADAPTATIVE I{ADIATION FOIADIFFERENT POLLEN VECTOR~

This subject has been extensively studied ever since the time of Charles
Darwin, Until recently, however, most of the observations were made by
naturalists workingin a relatively restricted region whodid not, as a rule,
apply their observations to the evolutionary relationships between the
groups under study. A paper by Grant (47) to someextent marks a turning
point in our understanding of comparative floral morphologyin relation to
evolution. He pointed out that in plant genera adapted to pollination by spe-
cialized animal vectors, a high proportion of the morphological characters
that distinguish species concerns those parts of the flower that adapt it
for e~cient pollination by these vectors. On the other hand, in genera
adapted to unspecialized vectors or to windor water pollination, the distinc-
tive characteristics of the species affect other parts of the plants reproduc-
tive or vegetative system.
Using this foundation, Grant madea careful comparative study of adap-
tations to pollen vectors in all geaera of the family Polemoniaceae.His re-
sults will form the central focus of the present section (52). Adaptive radi-
ation for different pollinators was found at all levels of the taxonomichier-
archy, from subspecies of the samespecies (Gilia splendens) to related spe-
cies of the same genus (Polemonium,Gilia, Linanthus, Ipomopsis, Cobaea,
Loeselia) and finally to the origin of a genus in association with adaptation
to a particular pollinator (Lepidopteran pollination in Phlox).
As a result of their investigations, the Grants were able to construct a
probable phylogenyof adaptive radiation in the family. In addition to fre-
quent reversions toward autogamy,six different lines of radiation could be
detected. Most of these were independently paralleled by several dii~erent
lines. Thus the shift from bee to hummingbirdpollination has occurred
seven times; that from bees to long-tongued flies ten times; from bees to
butterflies (day flying Lepidoptera) three times, to noctuid moths four
times, to beetles twice, and to scavengerflies once.
The second important monographon adaptive radiation with respect to
floral biology is that of van der Pijl & Dodson(110) on Orchidaceae.
These authors have presented a systematic and analytical review of the
complexrelationships that have long been recognized to exist between these
remarkable flowers and their pollinators, and they have added manyobser-
vations and illustrations of their own,particularly fromthe flora of tropical
America. As in the Polemoniaceae,the most primitive condition in Orchida-
ceae is adaptation to Hymenopteranvectors. Adaptive radiations to hum-
mingbird, scavenger fly, beefly (Bombylidae),butterfly, moth, and possibly
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 315

beetle pollination occur, and there are manyinstances of reversion to autog-
amy.
Animportant feature of adaptive radiation in orchids, which is poorly
developed in Polemoniaceae, is adaptation to pollination by distinctive
groups of Hymenoptera.The more primitive terrestrial genera, including
Cypripedium,are pollinated chiefly by solitary bees, as are the more primi-
tive Polemoniaceae. A few temperate genera (Listera, Coeloglossum) are
pollinated by Ichneumoidwasps. Amongtropical epiphytic orchids, several
genera (Vanda, Pha]us, Oncidium, Barkeria) have large flowers of firm
texture that are adapted to pollination by large carpenter bees (Xylocopa
spp.). On the other hand, social bees, which are the most commonpollina-
tors of specialized flowers belonging to other families, have only rarely be-
come regularly associated with species of orchids. The most remarkable
adaptive radiations in orchids are to bees of the genera Euglossa and Eu-
laema in tropical America and to males of various groups of Hymenoptera
in the Mediterraneangenus Ophrys, as well as to male wasps in the Austra-
lian genera Cryptostylis and Calochilus. In the latter examples,pollination is
effected by the well-knownbehavior o5 pseudocopulation. The relationship
between male euglossine bees and species of orchids is muchmore complex.
The orchids producea variety of fragrance substances similar to 1,8 cineole
which attract the male bees (32, 34). The bees then gather the substances
and store themin their hind tibia, wherethey serve either as sex attractants
or to attract other males of their species into clusters about whichthe fe-
males gather. Becauseof the specificity of the relationship betweenbee and
flower, it has brought about extensive speciation of both the bees and the
orchids.
Less complete data from other genera support these conclusions about
adaptive radiation at the species level in response to different pollinators.
The elaborate corollas in species of Pedicularis are mostly pollinated by
bumblebees(Bombus)(89, 90), but at least one species, P. densiflora of Cali-
fornia, is adapted to hummingbirds(126). Asiatic species of Pedicularis
have evolved very long corolla tubes, similar to those that in other genera
are associated with pollination by Lepidoptera or long tongued Diptera
(83). This shift has occurred independently .in several different species
complexes. Adaptation of the flowers of Lantana (Verbenaceae) to particu-
lar species of Lepidoptera has been noted by Dronramju(35, 36, 37) and
maybe one basis of speciation in this complexgenus. In the genus Pents-
temon, different species groups are adapted to various genera and families o5
Hymenoptera,as well as to hummingbirds(26, 131, 132). A similar situa-
tion exists in Salvia (44, 46). In the California flora, at least 45 separate
adaptations to hummingbirdpollination, in 18 different families, are con-
firmed by direct observation(46, 49, 53). Specificity of visits (oligolecty)
probably responsible at least in part for the diversity of species of Oenoth-
era and its relatives in western North America(85, 86), as well as for the
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316 STEBBINS
similar diversity of Myrtaceaein Australia (95). In tropical floras, several
genera of various families have evolved large, thick-textured flowers that
are pollinated principally by carpenter bees [J(ylocopa (105)].
Twokinds of adaptations to pollinators have not been discussed in the
review presented above: primitive beetle pollination and bat pollination.
The opinion, originally expressed by Diels (29), that the earliest angio-
sperms were pollinated by beetles (Coleoptera) has been madeincreasingly
plausible by morerecent observations on beetle pollination of various primi-
tive genera, such as Calycanthus (48), Eupomatia (65), Magnolia (62),
and the Annonaceae (104, 107). Manyspecies of Ranunculaceae attract
beetles along with other pollinators (180), but few if any membersof this
family are predominantlyor exclusively pollinated by these insects. Leppik
(79) has madethe interesting suggestion that beetles and other primitive
insects first becamepollen gatherers in association with the Jurassic Ben-
nettitales and later transferred their adaptations to the evolving angio-
sperms.
Although the most primitive flowers may well have been pollinated by
beetles, one cannot concludefromthis fact that beetle-pollinated plants in the
modernflora are primitive. Secondaryadaptation to coleopteran pollination
has been well documentedby Grant & Grant (52) in Linanthus and Ipomop-
sis. The pollination by Coleoptera of the white flowered Japanese species of
Trillium (41) is probably also secondary, since this genus is a relatively
specialized memberof the Liliales. In view of this fact, the suggestion by
van der Pijl (108) that the Compositae, the most advanced of flowering
plants, have retained primitive coleopteran pollination must be regarded
with someskepticism.
Adaptations to pollination by bats (Chiroptera) were the last to be rec-
ognized by naturalists. This is not surprising, since this kind of adaptation
exists only in the tropics and observations on it must be madeat night. The
earlier observations on these pollinators by Porsch (112, 113) have been
verified and amplified by van der Pijl (106), Baker &Harris (7, 9, 16,
61), and others (39). 7ihe plant genera involved belong to various tropical
families; the best documented of them are Parkia (Mimosaceae), Ceiba
(Bombacaceae), and KigeIia (Bignoniaceae). The bat pollination of Co-
baea (Polemoniaceae) has been reviewed by Grant & Grant (52).
Bat pollination is one of the most specialized and probably recent adap-
tations of flowers for pollen vectors. As Baker(9, 10) has pointed out, bat-
pollinated flowers must be large, and they are producedon robust flower stalks
that extend well outward from the foliage. Their parts must also be thick
and tough to survive the bitings and scratchings to whichtheir rude pollina-
tors subject them. Furthermore, they must have powerful odors and excrete
large quantities of nectar. In all probability, therefore, bat pollination has in
every case evolved secondarily from adaptation to other large pollen vec-
tors, such as birds, sphingid moths, and carp.enter bees. Unfortunately, no
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 317

line of adaptive radiation leading to this kind of pollination has yet been
documented.

DIFFERENTIAL ADAPTATIONS TO THE SAME POLLINATORS

In addition to adaptive radiation for pollination by different vectors,

many genera have evolved distinct species adapted in different ways to pol-
lination by the same vector. Two species of Pedicularis, P. attoIlens and P.
groenlandica, in the Sierra Nevada of California are clear-cut examples.
These two species occur sympatrically over a wide area, are very similar in
growth habit, but have different ecological preferences. They resemble each
other in flower color and structure. The chief difference between their flow-
ers is in the length of the beak of the corolla, which encloses the style and
stigma. Sprague (126) has observed pollination of both species by the same
species of Bombus. Nevertheless, the stigma and anthers of P. attollens are
so situated that the bee receives pollen on its head and transfers this pollen
to the stigma of another flower. The longer beak of P. groenlandica causes
the pollen to be transferred on the bees renter. The pollination of P. groen-
landica has also been observed by Macior (89) in the Rocky Mountains,
where P. attollens does not occur. Although Maciors observations disagree
with those of Sprague with respect to the behavior pattern of the bee, both
agree that the pollen is deposited on the bees venter.
Muchmore extensive differentiation of species in adaptation to different
methods of pollination by the same vectors has taken place in the Orchida-
ceae and is well documented by van der Piil& Dodson (110). Another fam-
ily in which this kind of differentiation may have been responsible for the
principal morphological differences between species is the Asclepiadaceae
(milkweed). Unfortunately, no recent studies of this family are available,
the latest known to me being Woodsons (137) monograph of North Ameri-
can species of ~tsclepias. There, he reviews the observations of earlier natu-
ralists, who showed that all of the species may be visited by a large number
of different kinds of insects belonging to various families and orders and
that the same species of insect may visit on the same day several different
species of milkweeds. Nevertheless, hybridization between species is excep-
tionally rare. The cause of this is partly the inviability of hybrid embryos,
but also the peculiar and specific morphology of their pollen sacs, or pol-
linia. These are borne in pairs that are connected by clips, in such a way
that an insect visiting the flower for nectar picks up pollen clips on its hind
legs. On a visit to another flower, it may deposit a clip with its pollinia in
the stigmatic sac and so effect pollination, but only if the pollinium belongs
to the species on which the insect has landed. The fit between pollinium and
stigmatic chamber is so precise that only pollination between different indi-
viduals of the same species can be carried out, even though the vector may
be carrying on its legs pollinia derived from several species of .4sclepias.
This condition almost certainly is the climax of a long course of adaptive
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318 STEBBINS
radiation for specificity of pollination. Perhaps noteworthyin this connec-
tion are the observations of Holm(64) on the related genus Sarcostemma
of Mexico.The species of this genus are apparently visited by oligolectic
insects, whichconfine their visits to a single species of flower. In all proba-
bility, this kind of spec!ficity precededthe present situation in /tsclepias,
since otherwise it is difficult to see howthe morphologicaldifferentiation
was brought about.
Twoother examplesof adaptive radiation for different methodsof polli-
nation by the same vectors are in the families Aristolochiaceae and Ara-
ceae. In both instances, the flowers act as "flytraps" that capture small flies
and imprison themuntil pollination is effected. The Europeangenera of Ara-
ceae are described by Knuth (69), Kugler (70), and Werth (135).
same volumesalso have accounts of the Aristolochiaceae, including the Eu-
ropean species of both Asarumand ,~ristolochia. Information on the flytrap
mechanismof pollination in other species of ,tristolochia is given by Cam-
merloher (19) and Lindner (84). Myownand others observations Aris-
tolochia californica are the only more receut ones knownto me. This lat-
ter species, along with several others, differs from A. clematitis of Europe
mwhichis often figured in textbooks--in not possessing the stiff, downward
pointing hairs whichprevent the flies from climbingout of the trap until pol-
lination has been effected, whenthe hairs shrivel up. Instead, the traps of A.
californlca, A. sipho, and other species have light "windows"arranged in
such a way that the flies, because of their phototropism, beat against the
walls of the perianth rather than flying out though its opening. Escape be-
comespossible after pollination, due to the expansion of the perianth. The
approximately 180 species of Aristolochia, plus the 20 of Asarumand a few
that belong to other, smaller genera (54), present a good exampleof a fam-
ily in which differentiation of both species and genera has been based
largely upon diversification of adaptations for pollination by one kind of
vector. Moreobservations of its species are badly needed.

PRINCIPLES INVOLVED IN ADAPTIVE RADIATION FORPOLLINATION

If adaptive radiation for characters of floral biology is to be understood
as a series of examplesof the action of natural selection, observations and
interpretations must be madewith this factor definitely in mind. The fol-
lowingprinciples are essential for understanding the process. -

1. The mosteffective pollinator principle.--Since selection is a quantita-

tive process, the characteristics of the flower will be moldedby those polli-
nators that visit it most frequently and effectively in the region whereit is
evolving. Hence when an evolutionist speaks of a "bee flower" or a "hum-
mingbird flower," he refers to its relationship with the predominant and
most effective vector. He does riot meanthat the flower is pollinated exclu-
sively by this vector. Secondaryvectors, such as Bombuson Aquilegia cana-
densis (88), mayretard the process of evolutionary modification, but they
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 319

are not likely either to stop it or to destroy the genetic integration of a
floral type once it has evolved. Failure to recognize this principle has re-
sulted in someunwarrantedskepticism as to the action of selection by polli-
nators in the origin of particular forms of flowers.

2. The significance of character syndromes.--The more specialized vec-

tors are attracted to flowers by a variety of stimuli, of which scent maybe
even moreimportant than either shape or color (18, 32, 70, 72, 73, 74, 91).
With respect to color, we must recognize that both the visual sense and re-
action to color on the part of the vector maybe very different from our
own.For instance, the greater sensitivity of bees to ultraviolet light renders
highly significant the muchgreater contrast of pattern that can be seen in
photographs of flowers taken with an ultraviolet sensitive camera, as com-
pared to the perceptions of the naked eye (71, 87). Grant (43) has shown
that hummingbirdsin a back yard do not prefer red-colored feeders to those
of other colors, provided that the food is the same. Nevertheless, the great
sensitivity of the birds eye to red colors must meanthat a red flower is
moreeasily detected from a long distance than one of another color, and in
view of the rapidity of flight, this factor is probablyof considerable impor-
tance. Leppik (75, 77) has emphasizedthe ability of bees and other special-
ized insects to recognizepatterns based on definite numbersof parts, e.g. 4-
or 5-merousflowers, as the basis of the constancyof these patterns. This hy-
pothesis needs experimental confirmation.
Leppik (78, 80) has attempted to classify and place in an evolutionary
sequencethe different forms of flowers that are related to specific modesof
pollination. This attempt has met with only partial success, since the types
are very difficult to classify and sometimesa particular form is not associ-
ated with the expected pollinator. For instance, the cup-like flower of Trol-
lius has a form resembling that of most coleopteran-pollinated flowers, but
is actually pollinated by a fly (80). A somewhat moresatisfactory classifica-
tion is presented by Faegri & van der Pijl (39). These attempts suggest
that, at least in our present state of knowledge,we shall learn more from
makingdirect studies of the functional relationships of particular kinds of
flowers to clearly identify pollinators than from attempting new classifica-
tions or evolutionary generalizations. The important facts, which have al-
ready been reviewed, are the numerouscorrelations that exist in most flow-
ers between scent, color, form, texture, and the recognized behavior pat-
terns of the predominantpollinators.
Perhaps the most important feature of character syndromesis that they
favor correlations betweencharacters. Oneof the most conspicuous of these
is betweenzygomorphic,or bilaterally symmetrical, flowers and racemoseor
spicate inflorescences (128). Pollination by insects that land on a flower,
such as bees, is most efficient if the flower possesses a "landing platform"
upon which the insect can alight before entering it to seek nectar. If the
inflorescence is a flat-topped or roundedcymeor corymb,as in Ranunculus,
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320 STEBBINS
Gentiana, or the Compositae, the flower is borne on an erect stalk, and its
horizontally spreading petals or rays can provide the platform. If, however,
the inflorescence is a raceme or spike, the flower stalk projects horizontally,
so that the petals or rays of a radially symmetrical flower would be vertically
oriented and would provide a poor platform. Under these conditions, genetic
changes that would modify the flower into a zygomorphic shape, providing
the platform by modifying the lower petals or corolla lobes so that they
assume a horizontal position, would have a high adaptive value. On the
other hand, in flo~vers pollinated chiefly by vectors that hover rather than
]and on the flower, such as Lepidoptera and hummingbirds, radial symmetry
would be compatible with a racemose or spicate inflorescence. This condition
is found in Ipomopsis aggregata (Polemoniaceae), the genus Nicotiana, and
others.
In my opinion, failure to recognize the significance of character syn-
dromes as the principal basis of character correlations has led to many mis-
taken conclusions--particularly those of K. Sporne (122, 123, 124, 125)-
about trends of evolution in flowering plants.

3. Selection along the lines of least resistance.--The flower structure-pol-

len vector relationship can develop along many different evolutionary path-
ways involving both adaptation to different vectors and different ways of
adaptation to the same vector. The particular pathway that a given line will
take depends upon the principle of selection along the lines of least resistance
(127, p. 497; 130). The significant factors in the flower-vector relationship
are : 1. frequency of a particular vector, 2. limitations imposed by the existing
structure of the flower, and 3. ]imitations imposed by the external environ-
ment. The evolutionary shift from one vector to another is probably trig-
gered by the entrance of the plant into a habitat where the original vector is
scarce and the new vector is abundant. For instance, many of the humming-
bird-pollinated flowers of western North America, which for the most part
are derived from bee-pollinated .flowers, occur most abundantly and proba-
bly arose in forests, where bees are uncommon,or flower at times when bees
are less than normally active (45, 46). The shift to pseudocopulation on the
part of Ophrys species in the Mediterranean region is associated with their
adaptation to relatively dry sites, in which early seed maturation is essential
so that dormancy can begin when the dry season comes. Since male hyme-
uoptera usually emerge earlier than worker females (74), adaptation to these
vectors may have originated in response to selection pressure for early flower-
ing.
Limitations imposed by the existing structure of the flower are responsi-
ble for many of the radiating pathways shown by Grant & Grant (52). The
long corolla tube characteristic of most bird-, long-tongued fly-, and Lepidop-
reran-pollinated flowers can evolve only from corollas that are already
somewhat tubular, as adaptations to hymenopteran pollination. On the other
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ADAPTIVE RADIATION IN ANGIOSPERMS, I 321

hand, the relatively broad chamberscharacteristic of flytrap flowers are
more likely to evolve from coleopteran-pollinated flowers, which have a sim-
ilar shape.
The environment can be limiting chiefly because of its influence on the
time available for flower developmentand the conditions that prevail at the
time of pollination. Primitive beetle-pollinated, as well as bat-pollinated,
flowers are most common in the tropics because their massive structure can
develop best in climates in which the favorable period for flower and seed
development is very long. Adaptation to moth-pollination, involving the
shift from diurnal to vespertine or nocturnal flowering, is most likely to
take place in dry, hot climates, where the high temperature and dry atmo-
sphere that prevail during the day are conditions unfavorable for flowering
and successful pollination. At the other end of the climatic spectrum, adap-
tation to indiscriminate pollination by nonspecific flies and other small in-
sects is most likely to evolve in cool, shady regions, such as temperate for-
ests. Finally, the shift from insect to windpollination is most likely to take
place in regions where, either because of drought or cold, insects are scarce
and the openness of the plant community promotes exposure to strong
winds.

4. Transfer of function via an intermediate stage of double function.-

Flowers shift of adaptation from Onespecialized pollinator to another must
be based upon the same kind of change in selection pressures as that which
accompaniesthe change of function in a particular organ of an animal. This
shift is generally recognized by zoologists to require an intermediate stage
in which either the same organ performs two functions or the same func-
tion is performed by two different organs (21, 93). Since in animals and
plants the function of reproduction is carried out by only one set of organs,
only the intermediate stage of double function is possible for these organs.
In terms of flower pollination, this meansthat the shift from one specialized
pollinator to another can be carried out only via an intermediate stage dur-
ing which both vectors are capable of pollinating the .flower. Situations of
this sort are described in manyof the references already given. They em-
phasize even more the need for avoiding a classification of flowers into
sharply delimited types and the implication that flowers belonging to one
particular type are pollinated exclusively by one particular vector.

5. Reversals of evolutionary trends.--If we view phyletic evolution as

the outcomeof a succession of adaptive radiations, we must recognize the
probability that reversals of general trends can occur whenevera reversal
of environmentalconditions elicits them. This principle is widely recognized
by zoologists and is well documentedby the fossil record. Whenthese re-
versals occur, however,they do not retrace the original evolutionary path-
way with respect to details of structure, but only with respect to general
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STEBBIN$
adaptation. In termsof pollinating mechanisms, thismeansthatwe canex-
pectreversals offlowers adaptations toparticular vectors,butthese rever-
salswillnotrestore theprimitive adaptation totheoriginal vector. Shifts
from wind to insect pollination and vice versa provide numerousexamples
of this principle. Mostsystematists whohave studied the origin of the flow-
ering plants believe that the original ancestors of the angiosperms were
wind-pollinated, but that the shift from windto insect pollination originated
along with the angiospermsthemselves (23, 133). Accordingto this theory,
all of the numerous groups of wind-pollinated angiosperms must be re-
garded as the products of secondary reversal. Such secondary reversal is
well documentedin some instances, such as the genera Thalictrum and Ar-
ternisia, as well as the subtribe Ambrosiinaeof the Compositae, mentioned
above. Becauseof their great age, documentationfor the woodyfamilies of
the temperate regions, such as the Betulaceae, bagaceae, and other families
formerly grouped together as "Amentiferae," is less clear but nevertheless
indicates that most if not all of themare the products of secondary reversal
to windpollination.
If this is so, then Ficus, mentioned above, as well as Salix and other
examples,represents a tertiary reversal, i.e. : primitive ancestors (wind) --~
earliest angiosperms (insects) --~ primitive Moraceae(wind) ~Ficus
sects). In the case of the last reversal, the structural readaptations to insect
pollination are entirely different from those that existed in the primitive
insect-pollinated ancestors. In manyinstances, readaptation o~ wind-polll-
nated angiosperms to secondary insect pollination involves the appearance
of conspicuous colors inthe stamen filaments, as in Salix and probably the
insect-pollinated species of Thalictrum. Here, the principle of selection
along the lines of least resistance is operating, since the acquisition of col-
ored pigments in stamen filaments involves less reorganization of the devel-
opmentalpattern than the restoration of petals that have been lost.
Similar reversals from one vector to-another and back to the same kind
of vector have undoubtedly been frequent, but are muchmore difficult to
recognize. Possible examples are the two shifts from hymenopteranto co-
leopteran pollination in the Polemoniaeeae,already mentioned(52). If,
seems probable, the earliest angiospermswere pollinated by Coleoptera, the
shift from eoleopteran to hymenopteranpollinations must have taken place
at some point along the line of evolution that led from primitive angio-
sperms to the relatively advanced Polemoniaceae. Linanthus parryae and
Ipomopsiscongesta, the twospecies that havereverted with respect to the pol-
len vector, bear hardly even a superficial resemblance to primitive angio-
sperms in their floral structure. Wecan conclude therefore, that the shift
from one vector to another, including reversals to the original vector, in-
volves very generalized alterations of selective pressure that can elicit any
one of a numberof structural modifications of the flower. Underthese con-
ditions, the principle of adaptive modificationsalong the lines of least resis-
tance can be expected to appear in its most extreme form.
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ADAPTIVE RADIATION iN ANGIOSPERMS, i 323

Co~re~.vsIo~r ,~NDStrvtM,~nY
The principal conclusions that emerge from this review are the follow-
ing: The diverse floral structures and pollination mechanismsfound in an-
giospermsrepresent a series of adaptive radiations to different pollen vec-
tors and different ways of becomingadapted to the same vector. Although
most of themowe their adaptive success to their promotionof cross-fertil-
ization, with consequent genetic diversity and heterozygosity, mechanisms
that promote self-fertilization have arisen repeatedly. They have an
adaptive advantage in association with the colonization of new habitats,
particularly those that are remotefrom the mainarea of a species distribu-
tion and that have unfavorable conditions for pollination. Althoughthe ear-
liest angiosperms were probably insect-pollinated, wind pollination arose
several times in relatively primitive groups, as well as in advancedones
such as the Compositae.Adaptive radiation toward wind pollination was fa-
vored in groups inhabiting dry or cold climates, where pollinators were
scarce, the plant formations were relatively open, and winds were strong.
Secondaryreversion to insect pollination probably took place in somederiv-
atives of wind-pollinated angiosperms that became readapted to moister,
more equable climates (e.g. Ficus).
Adaptive radiation for pollination by animal vectors has been recognized
in two families that have been intensively studied, the Polemoniaceaeand
Orchidaceae. In these families, adaptation to solitary aculeate Hymenoptera
and other relatively unspecialized insects is the primitive condition. Several
lines of radiation have led to pollination by more specialized Hymenoptera
(Bombus,Xylocopa), as well as by long-tongued flies (Bombylidae,Syrphi-
dae), day- and night-flying Lepidoptera, Coleoptera, and hummingbirds
(Trochilidae). Each of these adaptations involves characteristic modifica-
tions of the color, form, and odor of the flower. In the orchids, two adapta-
tions for attracting male Hymenopteraas pollen vectors have evolved: re-
semblanceto females, which induces pseudocopulation, and chemical sex at-
tractants. Someflowers of moreprimitive families are adapted to pollination
by Coleoptera, and this mayhave been the earliest form of insect pollination.
Pollination by carrion flies, involving the modification of flowers into fly-
traps, probably represents secondaryderivation from coleopteran pollination.
Diversification of species in somegenera (~tsclepias, Pedicularis) is as-
sociated with the evolution of different structural adaptations for pollina-
tion by the samevector.
Adaptiveradiation for pollen vectors involves the following evolutionary
principles: predominantinfluence of the most effective pollinator, adaptive
syndromesof characters, selection along the lines of least resistance, transfer
of function via an intermediate stage of double function, and reversals of
adaptive trends. Each of these phenomenacontributes to the complexity of
adaptive radiation in higher plants.
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324 STEBBINS
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I 325
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