Table Of ContentFLORAL
BIOLOGY
FLORAL
BIOLOGY
Studies on Floral Evolution
in Animal-Pollinated Plants
David G. Lloyd
EDITED BY
University of Canterbury, New Zealand
Spencer C. H. Barrett
University of Toronto, Canada
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Library of Congress Cataloging-in-Publication Data
Floral biology: studies on floral evolution in animal-pollinated plants / edited by David G. Lloyd, Spencer C. H. Barrett.
p. em.
Includes bibliographical references and index.
ISBN-13: 978-1-4612-8494-9 e-ISBN-13: 978-1-4613-1165-2
DOl: 10.1007/978-1-4613-1165-2
I, Flowers. 2. Pollination by animals. 3. Pollination by insects. 4, Angiosperms--Evolution, I. Lloyd, David G. II. Barrett,
Spencer Charles Hilton.
QK653.F58 1995 94-42927
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Contents
Preface vii
Contributors xiii
Part 1: Historical Perspective
l. Discovery of the Secret of Nature in the Structure and
Fertilization of Flowers
Christian Konrad Sprengel (translated by Peter Haase) 3
2. Christian Konrad Sprengel's Theory of the Flower:
The Cradle of Floral Ecology
Stefan Vogel 44
Part 2: Conceptual Issues
3. Floral Traits and Plant Adaptation to Insect Pollinators:
A Devil's Advocate Approach
Carlos M. Herrera 65
4. How Do Flowers Diverge?
Paul Wilson and James D. Thomson 88
5. Floral Longevity: Fitness Consequences and Resource Costs
Tia-Lynn Ashman and Daniel J. Schoen 112
6. Pollen Dispersal and Mating Patterns in Animal-Pollinated Plants
Laurence D. Harder and Spencer C.H. Barrett 140
7. The Ecology of Geitonogamous Pollination
Allison A. Snow, Timothy P. Spira, Rachel Simpson,
and Robert A. Klips 191
v
vi / Contents
8. Flower Size Dimorphism in Plants with Unisexual Flowers
Lynda F. Delph 217
Part 3: Model Systems
9. Evolution of Floral Morphology and Function: An Integrative
Approach to Adaptation, Constraint, and Compromise in
Dalechampia (Euphorbiaceae)
W. Scott Armbruster 241
10. The Evolution of Floral Form: Insights from an Alpine
Wildflower, Po/,?monium viscosum (Polemoniaceae)
Candace Galen 273
11. Deceit Pollination in the Monoecious, Neotropical Herb
Begonia oaxacana (Begoniaceae)
Douglas W. Schemske, Jon A.gren, and Josiane Le Corff 292
12. Reproductive Success and Gender Variation in
Deceit-Pollinated Orchids
Anna-Lena Fritz and L. Anders Nilsson 319
13. Stylar Polymorphisms and the Evolution of Heterostyly in
Narcissus (Amaryllidaceae)
Spencer C.H. Barrett, David G. Lloyd, and Juan Arroyo 339
14. Evolution of Campanula Flowers in Relation to Insect
Pollinators on Islands
Ken Inoue, Masayuki Maki, and Michiko Masuda 377
Subject Index 401
Taxonomic Index 405
Preface
Studies in floral biology are largely concerned with how flowers function to
promote pollination and mating. The role of pollination in governing mating
patterns in plant populations inextricably links the evolution of pollination and
mating systems. Despite the close functional link between pollination and mating,
research conducted for most of this century on these two fundamental aspects
of plant reproduction has taken quite separate courses. This has resulted in
suprisingly little cross-fertilization between the fields of pollination biology on
the one hand and plant mating-system studies on the other. The separation of
the two areas has largely resulted from the different backgrounds and approaches
adopted by workers in these fields. Most pollination studies have been ecological
in nature with a strong emphasis on field research and until recently few workers
considered how the mechanics of pollen dispersal might influence mating patterns
and individual plant fitness. In contrast, work on plant mating patterns has often
been conducted in an ecological vacuum largely devoid of information on the
environmental and demographic context in which mating occurs. Mating-system
research has been dominated by population genetic and theoretical perspectives
with surprisingly little consideration given to the proximate ecological factors
responsible for causing a particular pattern of mating to occur. Over the past
decade, however, this situation has begun to change as a new generation of floral
biologists are trained with backgrounds in both ecology and genetics, as well as
an appreciation of the natural history tradition of pollination biology and the
need for theoretical approaches to guide problem-solving. This book is an attempt
to highlight this new synthesis that is rejuvenating the 200-year-old discipline
of floral biology and turning it into one of the most challenging and fast-moving
areas of ecology and evolutionary biology.
This volume was initially conceived as a way of celebrating the bicentenary
of the publication of Christian Konrad Sprengel' s book Das entdeckte Geheimnifs
der Natur im Bau in der Befruchtung der Blumen (The Secret of Nature in the
vii
viii I Preface
Form and Fertilization of Flowers Discovered) in 1793. Sprengel's volume
stands out as one of the most significant works in plant reproductive biology
because it effectively began the systematic study of the relations between flowers
and insects. In his book, Sprengel described in fine detail structural adaptations
of hundreds of species and provided for the first time functional interpretations
of many floral mechanisms that are now the focus of much contemporary research
in floral biology. It has been said that the study of pollination before and after
the appearance of Sprengel's work were two different things.
To commemorate the publication of Sprengel's book, we organized the
Sprengel Bicentenary Symposium on Floral Biology that was held at the XVth
International Botanical Congress on August 29,1993 in Yokohama, Japan. Using
the eight presentations made at Yokohama as the nucleus of this work, we invited
additional authors to write chapters on other areas of floral biology. The main
goal in producing this volume was to provide an account of current issues
and research opportunities in floral biology. Because of the enormous scope of
contemporary research in plant reproduction, we have made no attempt to be
comprehensive in our coverage of topics represented in the book. Instead, the
chapters in this volume focus almost exclusively on research conducted on the
floral biology of animal-pollinated plants, with a primary emphasis on understand
ing the evolution and functional significance of the spectacular range of floral
variation displayed by flowering plants. The authors, all of whom are internation
ally recognized leaders in their field, were encouraged to present new research
results and ideas. This they have done, giving the volume an up-to-date flavor
that enables the reader to judge how far floral biology has come since its birth
200 years ago. This book should be of interest to a wide audience including
advanced undergraduate and graduate students and research workers in the fields
of plant reproductive biology, plant ecology and evolution, plant systematics,
plant genetics and entomology. We also hope that because of the strong natural
history tradition found in floral biology, this book may be of value to anyone
fascinated by plants and their pollinators and who wishes to know more about
how scientists investigate floral evolution.
This volume is divided into three parts. The first, "Historical Perspective,"
commences with an English translation by Peter Haase of the introduction of
Sprengel's book on structural adaptations found in flowering plants that encourage
cross-pollination. This is of considerable historical importance since it is the first
time that Sprengel' s writings have been translated from the original German into
English. The translation will enable biologists to appreciate the full significance
of the many novel discoveries concerning the functional significance of floral
adaptations that were made by Sprengel following his careful observations of
flowers and their pollinators. This is followed by Stefan Vogel's account of the
historical importance of Sprengel's work and some of the reasons why his ideas
were not fully appreciated by naturalists of the time. For it was not until Charles
Darwin and other nineteenth century biologists began to interpret the living world
Preface I ix
in a radically different way that the true significance of Sprengel's work became
evident.
The second section of this volume, "Conceptual Issues," covers current concep
tual problems in floral biology. Foremost in the minds of most biologists when
they contemplate floral evolution is the question of how pollinators have driven
the diversification of floral form. In Chapters 3 and 4 by Carlos Herrera, and
Paul Wilson and James Thomson, respectively, this issue is addressed from a
critical and somewhat unorthodox perspective. In both chapters the authors ques
tion the common assumption that current selection pressures exerted by pollinators
provide a universal explanation for the maintenance of variation in floral traits
in populations of animal-pollinated plants and provide experimental data to sup
port this view. Although in neither chapter do the authors doubt that floral
syndromes in animal-pollinated flowers arise through pollinator-mediated selec
tion, they challenge students of floral biology to provide more convincing evi
dence of this process and present several novel ways of approaching the problem.
Why do some flowers last for only a few hours, whereas others may be
functional for several weeks? This question has often intrigued floral biologists,
but until now there has been little attempt to address the problem in a rigorous
manner. In Chapter 5, Tia-Lyn Ashman and Daniel Schoen provide a conceptual
framework for approaching the question of the adaptive significance of floral
longevity. The authors develop and test a model that predicts floral longevities
are optimized by natural selection acting on the interaction between fitness returns
through male and female reproductive function and floral construction and mainte
nance costs. Their chapter serves as an excellent illustration of how the develop
ment of phenotypic selection models can be applied to addressing long-standing
issues in floral biology.
The next two chapters by Lawrence Harder and Spencer Barrett (Chapter 6)
and Allison Snow and colleagues (Chapter 7) are both concerned with the general
problem of the functional significance of inflorescence displays and the linkage
between pollination and mating patterns. Harder and Barrett focus on how the
design and display of flowers influence pollen dispersal. Based on theoretical
analysis and empirical work using genetic markers, they propose novel adaptive
explanations involving the promotion of fitness through male reproductive func
tion for a range of traits (e.g., dicliny, dichogamy, and heterostyly) traditionally
interpreted as antiselfing mechanisms. They argue that such floral mechanisms
decouple the benefits of large inflorescences through increased pollinator at
traction, from the costs associated with lost mating opportunities through male
function. Under this view, the inflorescence rather than the individual flower is
the more relevant unit of male function for most animal-pollinated plants. In
Chapter 7, Snow and her collaborators also examine mating costs associated
with large inflorescence displays, but in this case largely from the perspective
of female reproductive function. The authors examine ecological factors that
affect the frequency of self-fertilization as a result of geitonogamous pollinations
x / Preface
in plants that simultaneously expose many flowers to pollinators. Geitonogamy
is one of the least studied aspects of plant mating despite the fact that it is
probably near ubiquitous in mass flowering species. Snow and colleagues argue
for more attention to be paid to the ecology of geitonogamy and review experimen
tal methods that can be used to study the phenomenom.
The last chapter on conceptual issues is by Lynda Delph and deals with the
problem of flower-size dimorphism in species with unisexual flowers. The view
that staminate flowers are generally larger than pistillate flowers has a long
tradition beginning with Darwin's observations on dioecious and gynodioecious
plants. More recently, this pattern has been used as evidence that the evolution
of many floral traits is driven by sexual selection operating on male reproductive
function. Delph reports on the results of a comprehensive survey of flower size
in over 900 species of monoecious and dioecious species. In the survey female
flowers are larger than male flowers in nearly half the species where a dimorphism
exists and strong geographical patterns are evident in the data indicating that a
reexamination of functional explanations for flower-size dimorphism in plants
is in order. Delph proposes several adaptive and nonadaptive hypotheses that
could account for the patterns revealed by her studies.
Many of the conceptual advances in floral biology have come from detailed
work using model systems. These involve plant groups with attributes that make
them suitable for addressing particular questions using observational, experimen
tal, and/or comparative approaches. In the last part of the book, "Model Systems,"
a selection of research projects involving different model systems is presented.
The section begins with Chapter 9 by Scott Armbruster who reviews his extensive
research on Dalechampia (Euphorbiaceae), a genus of tropical vines, the flowers
of which produce resins that are collected by bees for nest building. By combining
phylogenetic reconstruction with field studies of the floral biology of populations,
Armbruster has been able to take a truly integrative approach to the study of
floral evolution in the genus. In our view, the research conducted by Armbruster
represents the "way forward" in floral biology since it abandons the largely
ahistorical approach taken by most workers in the field and considers both micro
and macroevolutionary time scales. In his chapter Armbruster focuses on the
role of pollinator-mediated selection, genetic constraints, nonadaptive diver
gence, and adaptive compromise in generating the patterns of floral variation
found within Dalechampia.
Long-term experimental field studies are often necessary to provide convincing
evidence of the evolution of floral traits in response to pollinator-mediated selec
tion. In Chapter 10, Candace Galen reviews her own studies in this regard on
the long-lived alpine herb Polemonium viscosum of the Polemoniaceae. Galen
argues that two basic requirements are necessary for thorough evolutionary analy
sis of floral form: the demonstration of heritable variation in floral morphology
under field conditions and measurements of selection under similar circumstances.
Few workers in thc field of floral biology to date have attempted to satisfy these
Preface / xi
requirements. Galen reviews two sets of field experiments she has conducted on
these topics. The results provide strong evidence for the evolution of elinal
variation in flower size in Polemonium in response to selection exerted by bumble
bees. Experimental field studies also involving bumble bees are employed by
Douglas Schemske, Jon Agren, and Josianne Le Corff in their examination of
deceit pollination in Begonia oaxacana, a neotropical monoecious herb reviewed
in Chapter 11. Borrowing manipulative approaches more commonly employed
by behavioral ecologists, Schemske and colleagues constructed artificial flowers
to investigate whether preferences by foraging bumble bees were evident for
flowers of varying size. Their studies indicate that deceit pollination in B. oaxa
cana is highly effective. Although bumble bees display a striking preference for
male flowers, rewardless female flowers receive sufficient pollen to achieve high
reproductive success.
Deceit-pollinated plants are also used as model systems by Anna-Lena Fritz
and L. Anders Nilsson to investigate the influence of variation in inflorescence
size on male and female reproductive success. In their studies, presented in
Chapter 12, populations of three nectarless orchid species (Anacampsis pyrami
dalis, Orchis palustris, and O. spitzelii) are used. The authors demonstrate that
the gender of plants varies with the size, timing, and duration of the floral display
and this is directly related to changes in pollinator visitation. Plants with small
displays reproduced relatively more as male parents, whereas large-display plants
were more likely to be functionally cosexual. Fritz and Nilsson argue that these
changes in gender with display size are likely to be universal in plant species in
which reproductive success is commonly pollinator-limited.
Despite the fact that the genus Narcissus (Amaryllidaceae) is one of the most
important groups used in ornamental horticulture, the floral biology of wild
species is virtually unknown. In Chapter 13, Spencer Barrett, David Lloyd, and
Juan Arroyo investigate the patterns of sex-organ polymorphism in wild species
from the Iberian peninsula. Their results suggest that this familiar genus may
also have a bright future as a model system for floral biologists. In their chapter
they address functional questions concerning the optimal positioning of sex organs
in flowers experiencing contrasting pollinator regimes. Barrett and colleagues
also settle a long-standing controversy by confirming the occurrence of the genetic
polymorphism heterostyly in Narcissus.
The evolution of self-pollination has fascinated floral biologists for over a
century. Shifts from outcrossing to selfing are particularly likely following island
colonization, and comparisons of the floral biology of mainland and island popula
tions can provide valuable model systems for investigating the selective mecha
nisms responsible for this shift in mating pattern. In the final chapter of the
volume, Ken Inoue, Masayuki Maki, and Michiko Masuda provide evidence that
floral traits and mating patterns in island populations of Campanula microdonta
(Campanulaceae) are differentiated from those of mainland populations. The
authors provide evidence that these changes are the result of adaptation to con-
