Early Evolution of Flowers

230 Pages·1994·9.84 MB·English

by  Peter K. Endress

Plant
Systematics
and
Evolution . Supplement 8
P. K. Endress and E. M. Friis (eds.)
Early Evolution of Flowers
Springer-Verlag Wien New York
Prof. Dr. PETER K. ENDRESS
Institut fur Systematische Botanik der Universitat,
Zurich, Schweiz
Prof. Dr. ELSE MARIE FRIIS
Naturhistorika Riksmuseet
Sektionen for Paleobotanik, Stockholm, Sweden
This work is subject to copyright.
All rights are reserved, whether the whole or part of the material is concerned, specifically those of
translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machines
or similar means, and storage in data banks.
© 1994 Springer-Verlag/Wien
Softcover reprint ofthe hardcover 1st edition 1994
Typesetting: Thomson Press (India) Ltd., New Delhi, 110001
Printed on acid-free and chlorine-free bleached paper
With 130 Figures
Library of Congress Cataloging-in-Publication Data
Early evolution of flowers/Po K. Endress, E. M. Friis (eds.).
p. cm. - (Plant systematics and evolution. Supplement; 8)
ISBN-13: 978-3-7091-7432-6 e-ISBN-13: 978-3-7091-6910-0
DOl: 10.1007/978-3-7091-6910-0
1. Flowers. 2. Angiosperms - Evolution. 3. Flowers - Morphology.
I. Endress, Peter K. II. Friis, Else Marie. III. Series: Plant systematics and evolution. Supplementum; 8.
QK653.E2 1994
582.13'04463 - dc20
ISSN 0172-6668
Contents
ENDRESS, P. K., FRIIS, E. M.: Introduction-Major trends in the study of early
flower evolution
DOYLE, J. A.: Origin of the angiosperm flower: a phylogenetic perspective 7
FRIIS, E. M., PEDERSEN, K. RAUNSGAARD, CRANE, P. R.: Angiosperm floral
structures from the Early Cretaceous of Portugal 31
CRANE, P. R., FRIIS, E. M., PEDERSEN, K. RAUNSGAARD. Palaeobotanical
evidence on the early radiation of magnoliid angiosperms 51
CREPET, W. L., NIXON, K. c.: Flowers of Turonian Magnoliidae and their
implications 73
DRINNAN, A. N., CRANE, P. R., HOOT, S. B.: Patterns of floral evolution in the
early diversification of non-magnoliid dicotyledons (eudicots) 93
NISHIDA, H.: Elsemaria, a Late Cretaceous angiosperm fructification from
Hokkaido, Japan 123
TUCKER, S. c., BOURLAND, J. A.: Ontogeny of staminate and carpellate flowers of
Schisandra glabra (Schisandraceae) 137
WILLIAMSON, P. S., SCHNEIDER, E. L.: Floral aspects of Barclaya (Nymphaeaceae):
pollination, ontogeny and structure 159
ENDRESS, P. K.: Evolutionary aspects of the floral structure in Ceratophyllum 175
KOSUGE, K.: Petal evolution in Ranunculaceae 185
ERBAR, c., LEINS, P.: Flowers in M agnoliidae and the origin of flowers in
other subclasses of the angiosperms. I. The relationships between flowers of
Magnoliidae and Alismatidae 193
LEINS, P., ERBAR, c.: Flowers in M agnoliidae and the origin of flowers in
other subclasses of the angiosperms. II. The relationships between flowers
of Magnoliidae, Dilleniidae, and Caryophyllidae . 209
Taxonomic Index 219
Subject Index 225
Listed in Current Contents
Pl. Syst. Evol. [Suppl.] 8: 1-6 (1994)
Introduction - Major trends in the study of early
flower evolution
Our knowledge of early angiosperm phylogeny and of flower evolution is rapidly
expanding. New evidence comes from different directions, and it seems important
to constantly synthesize new results from these fields. (1) Palaeobotany brought two
major developments, first comparative structural and stratigraphic pollen studies
(since BRENNER 1963 and DOYLE 1969), followed by the discovery of excellently
preserved Cretaceous flowers (since FRIIS & SKARBY 1981). (2) Development and
biology of extant flowers and structure of modern pollen was studied in many
living conservative groups during the same period. Application of the SEM for
comparative floral development was especially helpful (since ENDRESS 1972). The
comparative study of pollen with combined SEM and TEM techniques provided
a powerful approach to link extant and fossil material (since WALKER 1976).
Comparative pollination biology of primitive flowers in relation to floral structure
brought another new dimension (since GOTTSBERGER 1974). (3) The application of
cladistic techniques facilitated the rigorous discussion on the origin of the angio
sperms from other seed plants and on early angiosperm diversification (since CRANE
1985, DOYLE & DONOGHUE 1986). (4) More recently comparative molecular studies
with DNA and RNA became possible due to new techniques, applied for macro
systematics of angiosperms (since JANSEN & PALMER 1987). (5) The latest develop
ment is the direct analysis of floral development with molecular genetic techniques,
which, however, as yet has been done only for few model species of evolutionarily
more advanced angiosperm groups (COEN & MEYEROWITZ 1991).
Results from the fossil record
The fossil record of pollen and leaves has provided a rough framework for under
standing patterns in early angiosperm evolution (BRENNER 1963, 1976; DOYLE &
HICKEY 1976; HUGHES 1976). Based on these organs DOYLE & HICKEY (1976)
demonstrated a progressive complexity and diversity in angiosperm morphology
in the Early to mid-Cretaceous Potomac group sequence from eastern North
America. Recent discoveries of well-preserved angiosperm floral structures from
Cretaceous strata in Europe and North America indicate that a parallel increase
in complexity in floral organs took place during the same time interval (e.g., FRIIS
& CREPET 1987, FRIIS & ENDRESS 1990). Although the fossil floral structures are
much more rare in the Cretaceous strata than are leaves and pollen, they provide
a broader and more profound basis for comparison with modern angiosperms and
the establishment of systematic affinities of early angiosperms. Results obtained
2 P. K. Endress & E. M. Friis:
so far from the study of Cretaceous flowers support the generally accepted view
that the magnoliids contain the most primitive angiosperms, and that the hamame
lidids diversified from the magnoliids early in the history of angiosperms. Early
Cretaceous flowers are typically minute, unisexual or bisexual with few floral parts,
undifferentiated perianth, massive stamens typically with valvate dehiscence, and
uniovulate carpels, indicating that flowers of generallauralean or piperalean organi
zation were well-established in the Early Cretaceous (e.g., FRIIS & ENDRESS 1990,
CRANE & al., contribution 3 in this volume).
Larger floral structures related to the woody M agnoliales are rare in the
Cretaceous fossil record (DILCHER & CRANE 1985) and appeared later than the
smaller flowers. The abundance of small simple flowers early in the history of
angiosperms may reflect a particular rapid diversification of lauralean taxa rather
than reflecting the basal floral organization in angiosperms, and rooting of the
angiosperms is still much debated (contribution by DOYLE in this volume). Based
on leaf architecture and sedimentological data DOYLE & HICKEY (1976) suggested
that early angiosperms were riparian weeds of magnoliid and monocot affinity
(paleoherbs). A herbaceous growth form was also suggested by TAYLOR & HICKEY
(1990) based on the leaf architecture of a small compression/impression fossil from
the Aptian of Australia. Little is known about growth form in early angiosperms,
but the scarcity of larger pieces of angiosperm wood in the Cretaceous, particularly
in the Early and mid-Cretaceous, could be an indication for the absence of larger
angiosperm trees in the early phases of angiosperm diversification (UPCHURCH &
WOLFE 1987, HERENDEEN 1991).
While the fossil record clearly indicates that the first major radiation of
angiosperms took place in the Early Cretaceous (e.g., DOYLE & HICKEY 1976,
CRANE & LrDGARD 1989) phylogenetic analysis indicates that angiosperms may
have originated much earlier, possibly in the Triassic (DOYLE & DONOGHUE 1993,
CRANE 1993). An early radiation of angiosperms has also been claimed by CORNET
(e.g., 1989a, b) based on dispersed pollen and the enigmatic Sanmiguelia plant.
However, the nature of these fossils is still poorly understood and their angiosperm
affinity remains to be established. Although several of the dispersed pollen grains
show angiospermous features such as reticulate and tectate exine (e.g., CORNET
1989b), details in wall ultrastructure and aperture configuration indicate that they
are more related to non-angiospermous anthophytes (see discussion in FRIIS &
PEDERSEN 1995).
Results from the study of the structure and biology of extant flowers
The extant M agnoliidae contain many families with a single or only few species.
In the classification of CRONQUIST (1988) of the 39 families 14 contain a single
genus. Some of the families with more than one genus have a pronouncedly scattered
relictual distribution (such as Chloranthaceae, Winteraceae, Lardizabalaceae), and
some are known to have occurred in a much wider area in the Cretaceous or early
Tertiary {e.g., Chloranthaceae, Winteraceae) and have been more diverse than today
(KRUTZSCH 1989).
Spiral phyllotaxis, which is mostly considered to be the basal pattern of
arrangement of floral organs, is less generally common in the extant M agnoliidae
Introduction - Major trends in the study of early flower evolution 3
than was earlier believed (TUCKER 1984, ENDRESS 1986). Irregular and whorled
patterns are equally common. All these patterns may co-occur at low systematic
levels, even within single species. Variability in floral organ number may be equally
extensive (ENDRESS 1986). There are many families with predominantly unicarpellate
flowers and many with uniovulate carpels. There are several families without a
distinct perianth, and many with a simple perianth that is not differentiated into
calyx and corolla. The delimitation of a flower towards the bract region outside
the flower is not always clear-cut. Valvate dehiscence of anthers is widespread
(ENDRESS & HUFFORD 1989). In some groups, especially in Ceratophyllales, Piperales
and in some Laurales, the flowers are small, sometimes exceedingly so. Large,
beetle-pollinated flowers show peculiar specializations. Their organization does
seem less primitive than that of some smaller, less functionally differentiated flowers
(GOTTSBERGER 1974, 1988; GOTTSBERGER & al. 1980). Flies or small moths may
contain pollinators as primitive as beetles (THIEN & al. 1985, PELLMYR 1992, KATO
& INOUE 1994). Floral secretions, such as nectar and stigmatic fluid, in addition
to pollen, may constitute important rewards for pollinators in magnoliid flowers.
Protogyny is the dominant kind of dichogamy in bisexual flowers (ENDRESS 1990),
which could also indicate that secretions, and not pollen, were a primitive reward.
Optical and olfactorial attraction of pollinators is by stamens and carpels in many
groups, and not by the perianth. The advent of anatropous ovules may have
preceded that of closed carpels (TOMLINSON 1991, LLOYD & WELLS 1992). However,
some paleo herbs, such as Ceratophyllaceae and Piperales, and also Chloranthaceae,
have orthotropous ovules, which may be viewed as apomorphies due to particular
ovary architectures.
A consequence of these various new developments is that classification of major
angiosperm groups is under extensive revision. The application of some informal
names for the most problematical groups, such as, e.g., "paleo herbs", seems wise
before a new classification can be worked out on a relatively consolidated new
basis. As a working basis we here still use the classification by CRONQUIST (1988)
in addition to the informal names.
As its appears now, earlier assumptions on primitive angiosperms were not
completely wrong. What remains valid in particular is that the M agnoliidae are
the most basal group. However, it has become uncertain whether the woody
M agnoliales are at the base. There are equally good arguments to place herbaceous
groups (paleoherbs) at the base of the Magnoliidae (e.g., DOYLE & HICKEY 1976,
ZIMMER & al. 1989, LES & al. 1991, TAYLOR & HICKEY 1992, CHASE & al. 1993,
DOYLE & DONOGHUE 1993, QIU & al. 1993, and discussion in the contribution by
DOYLE in this volume).
This volume includes new advances in our understanding of early angiosperm
and flower evolution and brings together contributions from palaeobotanical as
well as neobotanical studies. The contributions were presented at two symposia
held at the XV International Botanical Congress in Yokohama on September 1,
1993, and organized by PETER K. ENDRESS, ELSE MARIE FRIIS, HARUFUMI NISHIDA,
and MICHIO TAMURA.
The first contribution discusses various hypotheses on the evolution of flowers
and floral organs based on recent phylogenetic-cladistic analyses (DOYLE). The
4 P. K. Endress & E. M. Friis:
following three contributions give a survey of the vast diversity of Cretaceous
magnoliid floral organs discovered during the past few years, and two chapters
deal with higher dicots. Early Cretaceous assemblages from Portugal (FRIIS & aI.,
contribution 2) and from eastern North America (CRANE & aI., contribution 3)
exhibit a wide range of magnoliid fossils, and particularly taxa related to the
Laurales appear to be well differentiated, but it is characteristic that none of the
fossils can be assigned with certainty to a modern family. Magnoliid fossils continue
to be important also in Late Cretaceous (Turonian) floras of eastern North America
and include several taxa that are comparable to extant taxa at the family level
(CREPET & NIXON, contribution 4). The earliest diversification of the Hamamelididae
started in the Early Cretaceous; and a large variety of taxa are present by the Late
Cretaceous (DRINNAN & aI., contribution 5). By that time most higher dicotyledon
subclasses were established, and the new genus Elsemaria described from the rich
Coniacian to Santonian flora of Hokkaido, Japan, exemplifies a permineralized
capsular fruit of possible dilleniid affinity (NISHIDA, contribution 6). For age and
sequence of stratigraphic names used in the palaeobotanical contributions readers
may consult Fig. 4 in contribution 5 (DRINNAN & aI.). The neobotanical papers
deal with floral development and biological aspects of previously poorly known
magnoliids: Schisandra of Schisandraceae (TUCKER & BOURLAND, contribution 7),
Barclaya of Nymphaeaceae (WILLIAMSON & SCHNEIDER, contribution 8), Cera to"
phyllum of Ceratophyllaceae (ENDRESS, contribution 9, not read at the Symposium).
Among ranunculids petal evolution is traced in Ranunculaceae (KOSUGE, contribu
tion 10). Potential relationships of magnoliid flowers concerning outstanding
features to those of other groups are discussed for monocots (ERBAR & LEINS,
contribution 11) and for dilleniids and caryophyllids (LEINS & ERBAR, contribu
tion 12).
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