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Botanical Journal of the Linnean Society, 2014, 174, 326–333. With 4 figures
VIEWPOINT
Proto-South-East Asia as a trigger of early
angiosperm diversification
SVEN BUERKI1*, FÉLIX FOREST1 and NADIR ALVAREZ2
1
Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond TW9 3DS, UK
Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015 Lausanne,
Switzerland
2
Received 11 July 2013; revised 3 October 2013; accepted for publication 21 October 2013
Darwin described as an ‘abominable mystery’ the abrupt origin of angiosperms in the mid-Cretaceous and the high
diversification rates in their early history. The father of evolutionary theory could not fathom this rapid
diversification and rather invoked that ‘there was during long ages a small isolated continent in the S. hemisphere,
which served as the birthplace of the higher plants’. In this essay, we comment on the spatial origin of angiosperms,
but focus primarily on understanding the abiotic factors that promoted the early diversification of angiosperms by
reviewing palaeobotanical, palaeogeographical, phylogenetics and biogeographical evidence. We argue that islands
located in the region today occupied by South-East Asia played a major role in angiosperm diversification during
the Late Jurassic and Early Cretaceous. © 2013 The Linnean Society of London, Botanical Journal of the Linnean
Society, 2014, 174, 326–333.
ADDITIONAL KEYWORDS: Darwin – islands – South-East Asia – Wallace.
INTRODUCTION
Angiosperms represent one of the greatest terrestrial
radiations in recent geological times (Davies et al.,
2004). Nowadays, approximately 250 000 extant
species of flowering plants growing in all types of
ecosystems across the globe have been described
(Soltis et al., 2005), this number representing only a
fraction of the current overall diversity of this group
(e.g. Bramwell, 2002). Although we have made significant progress in describing this diversity and
inferring phylogenetic relationships among the major
lineages of angiosperms (e.g. APG III, 2009), the
origin and early rapid diversification of angiosperms
remains one of the most enduring unsolved mysteries
in evolutionary biology. Darwin referred to this
unsolved question as an ‘abominable mystery’ in his
famous letter to Joseph Hooker on 22 July 1879
(Darwin & Seward, 1903; but see Friedman, 2009 for
a review of the context of this letter). The father of
evolutionary theory could not fathom this rapid diver-
*Corresponding author. E-mail: [email protected]
326
sification and rather invoked that ‘there was during
long ages a small isolated continent in the S. hemisphere, which served as the birthplace of the higher
plants’ (Darwin & Seward, 1903). Support for this
hypothesis was, however, weak and Darwin admitted
that ‘this is a wretchedly poor conjecture’ (Darwin &
Seward, 1903). In this essay, we comment on the
spatial origin of angiosperms, but focus primarily on
understanding the abiotic factors that promoted the
early diversification of angiosperms by reviewing palaeobotanical, palaeogeographical, phylogenetics and
biogeographical evidence. More precisely, we discuss
the idea that islands located in the region today
occupied by South-East Asia (Fig. 1) played a major
role in angiosperm diversification during the Late
Jurassic and Early Cretaceous.
PALAEOBOTANICAL EVIDENCE
The earliest fossils with distinctive angiosperm features are pollen grains from the Early Cretaceous
(Hauterivian, 136–130 million years ago; hereafter
Mya) found in deposits in China, Israel and England
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333
DIVERSIFICATION IN PROTO-SOUTH-EAST ASIA
327
20°N
Philippines
Late Devonian–
Early Carboniferous
10°N
La
te
rly
Ea
Cr
et
Cr
ac
eo
us
eo
New
us
c
eta
0°
Guin
Wallacea
ea
(Oligocene/Miocene)
10°S
Australia
20°S
90°E
100°E
110°E
120°E
130°E
140°E
150°E
Figure 1. Map of South-East Asia showing the age of the different regions that were accreted from Gondwanan terranes
from the Late Devonian to Late Cretaceous. Most islands in the Wallacea region resulted from the collision of the
Australian and Eurasian plates that started at the Eocene–Oligocene boundary, but was particularly intense during the
Oligocene–Miocene (see Hall, 2009 for more details).
Eudicots
Ceratophyllales
Monocots
Laurales
Magnoliales
Piperales
Magnollids
Canellales
Chloranthales
Austrobaileyales
ANA grade
Nymphaeales
Amborellales
Figure 2. Simplified angiosperm phylogenetic tree adapted from APG III (2009).
(Friis, Crane & Pedersen, 2011). Micro- and macrofossils of groups such as magnoliids, monocots and
eudicots (e.g. Ranunculales; Fig. 2) are globally relatively common during the Hauterivian–Aptian interval (c. 130–112 Mya). These findings provide evidence
for a first major event of spread and diversification in
angiosperm history closely following their appearance
in the fossil record (Friis et al., 2011, and references
therein). There is especially good knowledge of the
stratigraphic succession of these fossils in eastern
North America (Cretaceous deposits of the Potomac
Group sequence), Portugal (Cretaceous sediments in
the northern part of the Lusitanian Basin) and China
(Yixian formation; Friis et al., 2011). The rapid diversification and spread of angiosperms during the
Hauterivian–Aptian period and the absence of
‘archaic’ fossil lineages are compatible with a location
of the cradle of this group anywhere across the planet
and not necessarily close to these known areas of high
fossil accumulation, as stated by Takhtajan (1987). In
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333
328
S. BUERKI ET AL.
this context, although significant progress in the
description and understanding of the phylogenetic
placement of early angiosperm fossils has been made
since Darwin’s time (e.g. phylogenetic position of
Archaefructus Sun, Dilcher, Zheng & Zhou in the
angiosperm crown group, perhaps related to Nymphaeales; Sun et al., 1998), it is becoming clear that
palaeobotanical data alone are not sufficient to
unravel the origin and, more importantly, the conditions enabling the early diversification of this group.
Can we use other lines of evidence to provide insights
into the conditions that promoted this pattern?
Wallace (1869), who has been recognized as the
father of biogeography (Fay & Forest, 2013, and references therein), strongly insisted on the use of an
approach combining current distributions with palaeogeographical knowledge to unravel the evolution
of organisms. Wallace hypothesized that ocean depth
combined with information on the geological origin of
areas (i.e. terrane vs. volcanic origin) were good
indicators of the dynamics and evolution of biological connections between geographical areas. For
instance, this multidisciplinary approach enabled him
to propose the concept of a clear biogeographical
boundary in the Malay Archipelago (here referred to
as South-East Asia; Fig. 1), today known as the
Wallace line, primarily developed based on the distribution of morphological features in animals (but see
van Welzen, Parnell & Slik, 2011 for information on
plants; Fig. 1). However, for a more objective glimpse
into the past, Wallace would have needed an access to
palaeogeographical information, such as a more
precise timing of the succession of islands in SouthEast Asia, the effect of climate change on sea levels
and patterns of phylogenetic relationships. Modern
data from these fields might enable the application of
Wallace’s vision to unravel Darwin’s abominable
mystery.
PHYLOGENETIC RELATIONSHIPS, DATING
AND BIOGEOGRAPHY OF
EARLY-DIVERGING LINEAGES
OF ANGIOSPERMS
Recent advances in DNA technologies have opened
new avenues, allowing the investigation of phylogenetic relationships and the inference of temporal and
spatial evolution of angiosperms. We provide here an
overview of the type of information offered by these
new approaches that is relevant to the understanding
of early angiosperm evolution.
Phylogenetic studies based on plastid and nuclear
data supported the definition of a grade at the base of
angiosperms, formerly known as the ANITA grade (Qiu
et al., 1999), which we here refer to as the ANA grade
composed of Amborellales (Amborellaceae), Nymphaeales (Hydatellaceae, Nymphaeaceae, Cabombaceae)
and Austrobaileyales (Austrobaileyaceae, Trimeniaceae, Schisandraceae; Fig. 2; APG III, 2009). These
studies also support the endemic and monotypic New
Caledonian genus Amborella Baill. (Amborellaceae) as
the earliest-diverging lineage of angiosperms (Fig. 2;
APG III, 2009).
Molecular dating inferences provided estimates
placing the origin of angiosperms between the Early
Cretaceous (c. 130 Mya; Magallon & Castillo, 2009)
and Late Jurassic (c. 160 Mya; Bell, Soltis & Soltis,
2010); there is, however, a wide range of published
estimates based on molecular data, often less credible
and irreconcilable with fossil evidence.
Five of the seven families in the ANA grade are
restricted to East and South-East Asia, Australia and
the Pacific islands, whereas Cabombaceae and Nymphaeaceae are cosmopolitan, but with most of their
species found in the first region (Fig. 3). The earliestdiverging lineage of angiosperms (i.e. Amborella) is
endemic to New Caledonia, an archipelago located in
the south-western Pacific on the eastern margin of
the Australian plate (c. 1200 km east of Queensland
and c. 1700 km north of New Zealand). The main
island, Grande Terre, is mostly comprised of a continental fragment that separated from Australia during
the Late Cretaceous (c. 83 Mya; Grandcolas et al.,
2008), but was subsequently submerged, especially
during the Palaeocene, when the characteristic ultramafic substrates were laid down deep under the ocean
(Pelletier, 2006), emerging only during the Oligocene
(see Grandcolas et al., 2008 and literature herein).
Because of its relative young emergence, the New
Caledonian Archipelago could only have been a secondary centre of dispersal for the Amborella lineage.
Similar conclusions also apply to the rest of the
ANA lineages occurring in South-East Asia (Fig. 3), as
most of the islands in this region (with the exception
of Borneo, Sumatra and Java that were accreted
between the Early and Late Cretaceous; Fig. 1) are
the product of the collision between the Australian
and Eurasian plates, which started to take place
at the Eocene–Oligocene boundary (c. 33.9 Mya;
Metcalfe, 1998); several islands of the Wallacea region
were formed in the 15- to 5-Mya interval (Fig. 1; Hall,
2009). Whereas the fate of modern lineages in those
early-diverging groups seems to be associated with
long-term refugia in South-East Asia since the Eocene
(e.g. as observed in Sapindaceae; Buerki et al.,
2013a), we argue that this region of the globe played
a major role in angiosperm diversification during
much earlier times. In this context, the geological
conformation of continents at the Late Jurassic–Early
Cretaceous boundary would provide insight into the
identity of a region (more likely an archipelago) that
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333
Figure 3. Distribution of families in the ANA grade (see Fig. 2). Cabombaceae and Nymphaeaceae are cosmopolitan and not displayed on this map (see text for
more details).
Austrobaileyaceae
Hydatellaceae
Schisandraceae
Trimeniaceae
Legend
Amborellaceae
DIVERSIFICATION IN PROTO-SOUTH-EAST ASIA
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S. BUERKI ET AL.
would have played the role of Darwin’s ‘small isolated
continent’. Here, we propose that the archipelago
located between Australia and Eurasia in the Jurassic
(referred to as proto-South-East Asia by Buerki et al.,
2011) and formed by terranes that derived from the
Gondwana continent (Metcalfe, 1998; see below for
more details) promoted the early diversification of
angiosperms (Fig. 4).
PALAEOGEOGRAPHY OF SOUTH-EAST ASIA
The South-East Asian region has one of the most
complex palaeogeographical histories on the planet
(Figs 1, 4). It involves numerous small terranes that
rifted away from Gondwana during the Palaeozoic–
Mesozoic and were progressively accreted to the
southern part of the Eurasian Plate (northern China)
at different times during the Mesozoic and Cenozoic
(Metcalfe, 1998; Figs 1, 4). In addition, more recent
volcanic activity resulting from the collision of the
Eurasian and Australian plates at the Eocene–
Oligocene boundary onwards resulted in the creation
of additional islands (the Wallacea region) connecting
Borneo and Sumatra to New Guinea and Australia
(Hall, 2009; Fig. 1). The origin of proto-South-East
Asia was initiated by the accretion of Gondwana
terranes to Eurasia (corresponding to southern China
and Indochina today) in the Late Devonian–Early
Carboniferous and followed by the Quiantang and
Sibumasu blocks (the eastern half of the Malay Peninsula) in the Permian–Triassic (Fig. 4A). Although it
might have influenced the evolution of other lineages
of plants such as ferns and gymnosperms, this geological event occurred prior to the origin of angiosperms (160–130 Mya) and is therefore of limited
interest here. However, the following geological
events taking place from the Late Jurassic onwards
are of prime interest to our line of reasoning (Fig. 4).
South-western Borneo and the Semitau terranes
derived from the margin of Cathaysialand (southern
China and Indochina) following the opening of a marginal basin in the Cretaceous–Tertiary (Metcalfe,
1998) (Fig. 4A). The current Kurosegawa terrane of
Japan, derived from terranes that rifted from the
Australian Gondwana and accreted to Japanese
Eurasia in the Late Jurassic (Metcalfe, 1998). The
Lhasa, West Burma and Woyla terranes also rifted
from Australian Gondwana in the Late Triassic to the
Late Jurassic and were accreted to proto-South-East
Asia during the Cretaceous (Metcalfe, 1998; Fig. 4).
Finally, the rest of the region currently known as
Wallacea was formed as a result of the collision of the
Australian and Eurasian plates that was initiated at
the Eocene–Oligocene boundary, but most of the
islands were in place between the Oligocene and
Miocene (Hall, 2009; Buerki et al., 2013a; Figs 1, 4C).
EVOLUTIONARY MECHANISMS
PROMOTING THE EARLY DIVERSIFICATION
OF ANGIOSPERMS ACROSS THE
SOUTH-EAST ASIAN ARCHIPELAGO
Whereas the spatial origin of angiosperms has been
largely challenged with numerous hypotheses spanning the Northern and Southern Hemispheres (e.g.
Seward, 1931; Axelrod, 1952, 1970), we here propose
that the wide range of ecological niches (e.g. contrasting humid and dry climates along latitudinal
and longitudinal gradients) in association with the
island biogeography features experienced by protoSouth-East Asia between the Late Jurassic and
Early Cretaceous could have triggered the early
diversification of angiosperms (Fig. 4). What the
causal factors responsible for this event are remains
an open question.
Island biogeography predicts a higher probability of
gene flow disruption and therefore an increased
rate of speciation by isolation combined with local
adaptation (Carlquist, 1974) and other evolutionary
mechanisms such as hybridization (e.g. Seehausen,
2004) and polyploidy (e.g. Soltis & Soltis, 1995; Jiao
et al., 2011). The intrinsic properties of an insular
system (see above) could have generated high genetic
variability in a short time span, thus providing the
material for natural selection to take place.
Because of its geographical position, proto-SouthEast Asia might have provided a prime location
facilitating the rapid spread of angiosperms along
the archipelago in a stepping-stone manner and enabling the subsequent colonization of the remainder of
the planet (Fig. 4). As a consequence, there might
have been continuous adaptation and speciation
events across this Gondwana–Laurasia stepping
stone archipelago since the Late Jurassic. In addition, these islands might have also provided shelter
for lineages to survive periods of climatic instability,
as for instance at the end of the Cretaceous when
the extent of humid environments suffered a significant decline, especially in the Northern Hemisphere.
This is shown by the extinction of taxa currently
found only in tropical regions, such as the palaeotropical genus Pandanus Parkinson (Pandanaceae),
of which fossils have been found in what is today
Central Europe, suggesting the occurrence of a subtropical climate in this region during the late Cretaceous (Kvacek & Herman, 2004). It is widely
recognized that islands have acted as refugia in
several instances in regions such as Borneo (Buerki
et al., 2013a), Macaronesia (Emerson, 2008), Madagascar (Buerki et al., 2013b) and New Caledonia
(Pillon, 2012).
In addition, recent biogeographical and diversification analyses conducted across angiosperms
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 326–333
Australia
West Burma
Terranes derived
from New Guinea
New Guinea
Woyla
Proto-South-East Asia
SW Borneo
(incl. Semitau)
Antarctica
60
Lhasa
Eurasia
MesoTethys
India
30
0
30
CenoTethys
Australia
West Burma
New
Guinea
Woyla
Proto-South-East Asia
B. Early Cretaceous: 120 million years
Lhasa
Eurasia
30
60
Indian
Ocean
India
CenoTethys
Woyla
Pacific
Ocean
Australia
New Guinea
Proto-South-East Asia
Antarctica
West Burma
Accretion of Lhasa,
0
West Burma
and Woyla
terranes
30
C. Late Cretaceous: 80 million years
Figure 4. Palaeogeographical maps of proto-South-East Asia from the Late Jurassic (A), Early Cretaceous (B) and Late Cretaceous (C). This region is formed
by terranes that rifted from Australia and New Guinea and subsequently accreted into terranes that currently form China and Indochina. We hypothesize here
that the proto-South-East Asian archipelago promoted the diversification of early angiosperms. Present day outlines are for reference only. See text for more
details. The maps were adapted from Metcalfe (1998).
Antarctica
60
India
Northward drift of Lhasa,
30
West Burma
and Woyla
terranes
0
Lhasa
Eurasia
MesoTethys
30
Gondwanan terranes that rifted
during the Late Devonian–
Early Carboniferous
forming the Sundaland
A. Late Jurassic: 165 million years
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S. BUERKI ET AL.
demonstrated that modern South-East Asia has had
several roles in angiosperm evolution. It acted as: (1)
a cradle (Nauheimer, Boyce & Renner, 2012); (2) a
crossroads enabling dispersals between Northern and
Southern Hemispheres (especially during periods of
climate change such as the Eocene–Oligocene boundary; Buerki et al., 2013a); (3) a centre of diversification (e.g. Buerki et al., 2013a); and (4) a refugium for
tropical lineages because of its stable climate (at least
in the last 30 Mya; Lohman et al., 2011; Fig. 1). These
studies have been conducted on a wide array of
groups such as Araceae (Alocasia Neck. ex Raf.,
Nauheimer et al., 2012), Begoniaceae (Begonia L.,
Thomas et al., 2012), Pandanaceae (Pandanus and
Benstonea Callm. & Buerki, Buerki et al., 2012),
Rubiaceae (Margaritopsis C.Wright, Barrabé et al.,
2012) and Sapindaceae (Buerki et al., 2013a).
IS THE MOST RECENT COMMON
ANCESTOR OF ANGIOSPERMS NOW LOST
IN PROTO-SOUTH-EAST ASIA TERRANES
THAT ARE UNDER WATER OR SUBDUCTED?
Historically, Seward (1931) first suggested that angiosperms originated in the Arctic, whereas Axelrod
(1952, 1970) postulated that angiosperms originated
in tropical upland habitats in the Permian or Triassic
and invaded the tropical lowlands and higher latitudes in the Early Cretaceous. These hypotheses
were, however, based on older misidentifications of
Cretaceous angiosperm leaves with diverse and
advanced modern genera and were contradicted by
palynological studies, which revealed no identifiable
angiosperm pollen during the Triassic, Jurassic and
even the earliest Cretaceous, despite a worldwide
sampling (e.g. Friis et al., 2011). As pointed out above,
the earliest fossils with distinctive angiosperm features are pollen grains from the Hauterivian (136–
130 Mya) found in China, Israel and England (Friis
et al., 2011). However, angiosperm dated analyses
indicated an origin of the group during the Late
Jurassic (c. 160 Mya), with current species from the
collection of lineages of the ANA grade mostly
restricted to the Southern Hemisphere (e.g. New Caledonia, Australia, South-East Asia). This apparent
paradox could be solved if we hypothesize that protoSouth-East Asia served both as the cradle and centre
of diversification of early angiosperms. The complex
palaeogeographical history of this region, involving
the rift of terranes mainly from Gondwanan origin
and recent volcanic activities (Hall, 2009), could
explain the lack of fossil evidence for the earliest
angiosperms (i.e. missing link); they might now be
either under water or lost because of the subduction
of terranes/plates.
ACKNOWLEDGEMENTS
We are grateful to the editor, Mike Fay, and associate
editor, Carlos García-Verdugo, for inviting us to
submit this point of view and for their support and
valuable comments on the manuscript. We warmly
thank Jeffrey Doyle for constructive comments made
on an earlier version of this manuscript. We also
would like to thank Mark Chase for help with the
preparation of Figure 2. Finally, we are grateful to
two anonymous reviewers who contributed to improve
this work.
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