Journal of Systematics

JSE and Evolution doi: 10.1111/jse.12182

Research Article

Phylogenetic tree of vascular plants reveals the origins of

aquatic angiosperms
Zhi-Yuan Du, Qing-Feng Wang*, and China Phylogeny Consortium†
Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China
†
Members of the China Phylogeny Consortium are listed in the Appendix.
*Author for correspondence. E-mail: [email protected]. Tel./Fax: 86-27-87510526.
Received 5 July 2015; Accepted 5 September 2015; Article first published online 26 October 2015

Abstract Although aquatic plants are discussed as a unified biological group, they are phylogenetically well
dispersed across the angiosperms. In this study, we annotated the aquatic taxa on the tree of vascular plants, and
extracted the topology of these aquatic lineages to construct the tree of aquatic angiosperms. We also
reconstructed the ancestral areas of aquatic families. We found that aquatic angiosperms could be divided into two
different categories: the four aquatic orders and the aquatic taxa in terrestrial orders. Aquatic lineages evolved early
in the radiation of angiosperms, both in the orders Nymphaeales and Ceratophyllales and among basal monocots
(Acorales and Alismatales). These aquatic orders do not have any extant terrestrial relatives. They originated from
aquatic habitats during the Early Cretaceous. Asia would have been one of the centers for early diversification of
aquatic angiosperms. The aquatic families within terrestrial orders may originate from other areas besides Asia, such
as America or Australia. The lineages leading to extant angiosperms diversified early in underexploited freshwater
habitats. The four extant aquatic orders were relicts of an early radiation of angiosperm in aquatic environments.
Their extinct ancestors might be aquatic early angiosperms.
Key words: ancestral area, aquatic plant, early angiosperm, fossil age, origin.

Amborella, Nymphaeales, and Austrobaileyales represent the Aquatic plants are plants that have adapted to live in
three earliest splits in angiosperm phylogeny (ANA grade aquatic environments (freshwater or saltwater). These plants
angiosperms), followed by the five lineages of mesangio- require special adaptations for living submerged in water, or
sperms, Magnoliids, Chloranthales, monocots, Ceratophyl- at the water’s surface (Sculthorpe, 1967; Cook, 1990).
lales, and eudicots (Cantino et al., 2007; Soltis et al., 2008). The Although aquatic plants are discussed as a unified biological
rapid diversification of angiosperms in the Early Cretaceous is group, the ways that species have evolved to live in the
well documented in the fossil record (Feild & Arens, 2005). aquatic environment are diverse (Sculthorpe, 1967; Philbrick &
Due to the diversity of fossils, it is impossible to draw Les, 1996). Aquatic plants are phylogenetically well dispersed
unequivocal conclusions on the life form of early angiosperms across the angiosperms, with at least 50 independent origins,
(L€ohne, 2006). There are two divergent views on the general although they comprise less than 2% of the angiosperm
habit of the earliest angiosperms: woody and terrestrial or species (Cook, 1990; Les et al., 1997).
herbaceous and aquatic (Soltis et al., 2005). The hypothesis Traditional systematic studies proposed that all aquatic
that the earliest angiosperms were woody is supported by the plants evolved from terrestrial relatives (Sculthorpe, 1967;
evidence that most basal angiosperms are woody and all Cook, 1990). However, some recent phylogenetic and
gymnosperms are woody (Soltis et al., 2008). paleobotanical studies suggested the aquatic origin of
An aquatic origin of angiosperms is supported by the angiosperms. Therefore, it is necessary for researchers of
evidence that several of the earliest known fossil angiosperms aquatic plants to examine the phylogenetic tree of vascular
were aquatic. Archaefructus represents one of the oldest, plants to find whether all the aquatic angiosperms were
most complete angiosperm fossils (Sun et al., 2002). It is evolved from terrestrial relatives, and to explore the
estimated to be approximately 125 million years old, and on possibility of an aquatic origin of angiosperms. In this study,
the basis of morphology, it clearly was aquatic. The we annotated the aquatic taxa on the tree of vascular plants,
phylogenetic placement of Archaefructus as sister to all and extracted the topology of these aquatic lineages to
extant angiosperms (Sun et al., 2002), and the near-basal construct the tree of aquatic angiosperms. We also recon-
phylogenetic position of Nymphaeales, support the hypothe- structed the ancestral areas of aquatic families. Our aim is to
sis that the aquatic habit arose early in angiosperms and the study the origins of aquatic angiosperms and find whether
earliest angiosperms might be aquatic (Coiffard et al., 2007; there is any possibility that some aquatic lineages might
Soltis et al., 2008). originate from aquatic ancestors.

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Origins of aquatic angiosperms 343

Material and Methods The diversification of the Nymphaeales crown group

started in Asia and Australia (Fig. 1). The ancestors of core
We annotated the aquatic taxa on the tree of vascular plants
Nymphaeales distributed in Asia and North America. There
(Fig. S1), and extracted the topology of these aquatic
were two distinct radiation events in core Nymphaeales, a
lineages to construct the tree of aquatic angiosperms. These
rapid first differentiation into two major lineages (Cabomba-
40 families used in this study represent the majority of
ceae and Nymphaeaceae) and the radiation of Nymphaeaceae
aquatic angiosperms that are obligately living in water
(Nuphar, Barclaya, Nymphaea, Ondined, Victoria, and Euryale).
(Cook, 1990). Amphibious plants are distinct from aquatic
Cabombaceae were ancestrally distributed in the American
species that live constantly in water, and most amphibious
continents (Fig. 1). After the two genera diverged, Cabomba
plants were not included in this study. The known fossil ages
diversified on the American continents. Brasenia occurred on
of aquatic families and orders were annotated on the tree
all continents except Europe and Antarctica. The fossil record
(Lumbert et al., 1984; Crabtree, 1987; Friis et al., 2001, 2004;
supported that Brasenia was distributed in Europe and extinct
Gandolfo et al., 2004; Riley & Stockey, 2004; Sille et al., 2006;
during glaciations (Yoo et al., 2005). The second radiation
Taylor et al., 2008). A fossil species Sinocarpus decussatus
probably started in the Northern Hemisphere. Nuphar
Leng & Friis of the Late Barremian–Early Aptian age (125 Ma)
retained its ancestral distribution in the Northern Hemisphere.
was chosen as the oldest eudicot fossil (Leng & Friis, 2003).
Four of the remaining five genera in Nymphaeaceae were
We used the statistical dispersal–vicariance analysis (S-DIVA)
distributed in small geographic areas. Barclaya and Euryale
option in RASP (Yu et al., 2011) to construct the ancestral
were found only in Southeast Asia. Ondinea occurred only in
areas of aquatic families and orders. The distributions were
Western Australia, and Victoria was native to South America.
categorized into the following areas: Asia (A), Africa (B),
Nymphaea had a cosmopolitan distribution, due to its ability to
North America (C), South America (D), Australia (E), and
adapt to a wider range of temperatures than other genera of
Europe (F).
Nymphaeaceae (Yoo et al., 2005).

Fossil ages and ancestral areas of Alismatales

Results The order Alismatales includes core Alismatales and two other
Annotation of aquatic taxa on the tree of vascular plants families, Araceae and Tofieldiaceae. Core Alismatales consists
The overall phylogeny of angiosperms (see Fig. S1) was of 12 families and 56 genera. Species of Alismatales are
congruent with other angiosperm phylogenetic studies wetland or aquatic herbs, most of which have a completely
(Jansen et al., 2007; Moore et al., 2007; Graham & Iles, submerged seedling phase. All marine angiosperms and most
2009). Nymphaeales diverged from the near basal node of the water-pollinated angiosperms are confined to this order.
angiosperm tree. Monocots and eudicots were well sup- Previous studies proposed that Alismatales originated in the
ported as monophyletic. Acorales and Alismatales were Early Cretaceous (Janssen & Bremer, 2004; Magallon &
successive sister groups of the remaining monocots. Cerato- Castillo, 2008), with all the families presented in the Late
phyllum was placed sister to eudicots. From the annotated Cretaceous and Early Tertiary periods (Les et al., 2003; Janssen
tree (see Fig. S1), we could find that aquatic plants evolved & Bremer, 2004; Chen et al., 2012a, b). A fossil species Mayoa
from different ecological backgrounds at different times. portugallica Friis, Pedersen & Crane of Late Barremian–Early
Some old ones are aquatic at the level of order or family, while Aptian age (125 Ma) was the oldest fossil found in Alismatales
other recent ones are isolated genera or species in the (Friis et al., 2004).
terrestrial family. When studying the origins of aquatic plants, The RASP results suggested that the ancestor of core
the aquatic orders and the aquatic taxa in terrestrial orders Alismatales probably occurred in Asia in the Early Cretaceous
should be treated differently. The fossil ages suggested that (Fig. 1). The core Alismatales split into two lineages. The
the aquatic orders (Nymphaeales, Alismatales, and Cerato- lineage comprising Butomaceae, Alismataceae, and Hydro-
phyllales) dated from the Early Cretaceous (Fig. 1). charitaceae originated in Asia. Its first clade (Butomaceae and
Alismataceae) dispersed from Asia to South America.
Fossil ages and ancestral areas of Nymphaeales Alismataceae originated in Asia and South America, and
The order Nymphaeales was considered to be among the dispersed to Europe and Africa. The oldest fossil in
oldest independent lineages of angiosperms. Recent molecu- Alismataceae was a fossil similar to Limnocharis from the
lar study placed the family Hydatellaceae (Trithuria) in Late Cretaceous (Riley & Stockey, 2004). The second clade
Nymphaeales, as sister to traditional Nymphaeales (Saarela (Hydrocharitaceae) dispersed from Asia to Africa. In Hydro-
et al., 2007). The stem lineage to Nymphaeales is old, based on charitaceae, the seagrasses diversified in Asia and dispersed to
a fossil attributed to Nymphaeales from the Early Cretaceous other regions by ocean currents. The oldest fossil in Hydro-
(Friis et al., 2001). Pluricarpellatia peltata B. Mohr, Bernardes- charitaceae was a fossil of Stratiotes, which was 0.1 Ma
de-Oliveira & David W. Taylor is another nymphaealean fossil younger than the Paleocene–Eocene boundary (55.9 Ma; Sille
from the Early Cretaceous (late Aptian to earliest Albian). It et al., 2006).
was an extinct member of Nymphaeales and branched off Another lineage comprising the remaining families dis-
early in this lineage (Mohr et al., 2008). The Cretaceous age of persed from Asia to Australia (Fig. 1). Australia played an
the Cabombaceous fossils was supported by Scutifolium important role in the diversification of this lineage. Several
jordanicum Taylor, Brenner & Basha, a fossil species of seagrass families (Posidoniaceae, Cymodoceaceae, and Zos-
Cabombaceae from the Albian (100 Ma; Taylor et al., 2008). teraceae) originated from Australia. Previous studies pro-
The oldest fossil in Nymphaeaceae was some fossil flowers posed that seagrasses had independently arisen from their
from the Turonian (90 Ma; Gandolfo et al., 2004). freshwater relatives in the course of habitat alteration from

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344 Du et al.

Fig. 1. Fossil ages and ancestral areas of aquatic families and orders. The known fossil ages of aquatic families and orders are
below their names. Because the fossil records of some aquatic families are problematic, they are not used in this study. The
timescale is in million years ago. Ancestral areas of aquatic families are below the nodes. We categorized the distributions into
the following areas: Asia (A), Africa (B), North America (C), South America (D), Australia (E), and Europe (F). The ancestral areas
of terrestrial families that have aquatic taxa were not reconstructed.

fresh water to salty water (Les et al., 1997; Kato et al., 2003). disjunct distribution in Asia and North America. The fossil
The fossil records of these families were problematic, except a record of Nelumbonaceae can date back to the Albain
Thalassodendron fossil of Cymodoceaceae from the Middle (100 Ma; Crabtree, 1987). The ancestral areas of two aquatic
Eocene (Lumbert et al., 1984). families Pontederiaceae and Menyanthaceae were recon-
structed. Pontederiaceae originated and diversified in Ameri-
Ancestral areas of aquatic families in terrestrial orders can continents (Fig. 1). The five genera of Menyanthaceae split
In monocots and eudicots, there are some families in into two clades. One clade originated in North America and
terrestrial orders composed entirely of aquatic plants, e.g., another clade in Australia (Fig. 1). These aquatic families within
Pontederiaceae (Commelinales), Nelumbonaceae (Proteales), terrestrial orders might originate from other areas besides
and Menyanthaceae (Asterales) (see Fig. S1). Their geographi- Asia. Some terrestrial families also contained aquatic genera,
cal distributions are annotated in Fig. 1. Nelumbonaceae had a e.g., Hygroryza (Poaceae), Batrachium (Ranunculaceae),

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Origins of aquatic angiosperms 345

Myriophyllum (Haloragidaceae), Utricularia (Lentibulariaceae), distributed in freshwater habitats around the world. A fossil
and Trapella (Pedaliaceae). These aquatic genera evolved species of Ceratophyllaceae, Donlesia dakotensis Dilcher &
from their terrestrial ancestors that adapted to the aquatic Wang was described from the Albian (100 Ma; Dilcher & Wang,
environments. 2009). Paleobotanical evidence supports the hypothesis that
Ceratophyllaceae are relicts of early angiosperms (Les, 1988;
Dilcher & Wang, 2009). Phylogenetic studies indicate that
Ceratophyllales are one of the five lineages of mesangio-
Discussion sperms (Soltis et al., 2008).
Origins of extant aquatic orders
The aquatic angiosperms split into three lineages, and the Ancestral areas and dispersal of aquatic angiosperms
aquatic orders are at the basal node of each lineage with Early The plants in aquatic orders do not have any extant terrestrial
Cretaceous origins. Nymphaeales diverged from the near- relatives. They originated from aquatic habitats during the Early
basal node of the extant angiosperm phylogenetic tree. Cretaceous. Asia would have been one of the centers for early
Considering the diversity and the nearly global distribution of diversification of aquatic angiosperms, which is in accordance
its members, Nymphaeales stands out as the first globally with the geographic origin of angiosperms. In terrestrial
diverse clade in the tree of extant angiosperms (L€ ohne et al., orders, aquatic families and genera evolved from terrestrial
2008). Other basal angiosperm lineages, such as Amborellales ancestors that adapted to aquatic habitats. They may originate
or Austrobaileyales, are restricted to much narrower relict from other areas besides Asia, such as America or Australia.
ranges (L€ ohne et al., 2008). The placement of Trithuria Although aquatic plants comprise less than 2% of the
(Hydatellaceae) in the Nymphaeales indicates that water lilies angiosperm species, they represent a disproportionately
are part of a larger lineage than previously recognized large number of taxa with global distributions including all
(Saarela et al., 2007). It greatly expands the morphological sorts of intercontinental disjunctions (Les et al., 2003). The origin
diversity encompassed by the Nymphaeales. The adaptation times of most aquatic species are far too recent to implicate
of Nymphaeales to seasonal drying pools triggered the continental drift as the major determinant of their discontinuous
evolution of rapid growth via herbaceousness and condensa- distributions. The modern continents (Africa, Eurasia, Australia,
tion of the reproductive axes, which underlay the ecological South America, and North America) have been separated by
success of angiosperms (Feild & Arens, 2007). oceans since at least 105 Ma (Davis et al., 2002). Therefore, the
Beyond the all-aquatic Nymphaeales, basal monocots transoceanic distribution of most aquatic species might have
(Acorus and Alismatales), Ceratophyllum and basal eudicot resulted from dispersals through land bridges, island chains, or
lineages (Nelumbo and some Ranunculus species) are other long-distance dispersal (Les et al., 2003).
examples of near-basal aquatic angiosperms (Les &
Schneider, 1995; Soltis et al., 2005). Monocots may be Early radiation of aquatic angiosperms
relicts of an early radiation of herbaceous angiosperms Molecular phylogeny indicates that angiosperms are not
(Doyle, 1973). Acorales and Alismatales are successive sister closely related to any other extant seed plant group.
groups of the remaining monocots. Acorales distributed Therefore, the information from fossils might provide the
widely in north temperate wetlands. Alismatales globally basis for reconstructing the origins of angiosperms (Friis et al.,
distributed in the aquatic environments. These two lineages 2003). Prior to the angiosperms, the ferns and gymnosperms
differentiated early in the monocots. Therefore, monocots had been widely distributed on land. The fossil records
are likely to be of aquatic origin, followed by gradual indicate that stoneworts and green algae were already
evolution to adapt to the terrestrial environment (Les & present in the Early Palaeozoic, but plant evolution in water
Schneider, 1995). This hypothesis is consistent with the fossil bypassed two of the main steps in terrestrial plant evolution:
records of monocots (Doyle, 1973). the dominance of the ferns during the Palaeozoic, and
In another study, we used Mesquite to reconstruct the the dominance of the gymnosperms during the Mesozoic
ancestral character state of life form in aquatic plants (Du & (Martın-Closas, 2003). The late arrival of aquatic ferns, and
Wang, 2014). The submerged life form was suggested as the complete failure to develop aquatic species in gymnosperms,
progenitorial state of Nymphaeales and Alismatales, which differentiated the evolution of aquatic plants from terrestrial
gave rise to floating-leaved, free-floating, and emergent life plants (Martın-Closas, 2003).
forms. This is in accordance with their aquatic origins. Most of Angiosperms colonized freshwater until the Late Mesozoic.
the aquatic families in terrestrial orders evolved from Angiosperm ancestors may have adopted the aquatic lifestyle
emergent life forms, which is consistent with their terrestrial to escape competition on land (Aquatic hypothesis; Feild &
origins. For example, the ancestral state of Menyanthaceae Arens, 2005), or early angiosperms may have escaped
was emergent, which gave rise to the floating-leaved life form. crowded habitats on land by adaptation to water (Terrestrial
In the past, the genera Ceratophyllum and Nelumbo were hypothesis; Feild & Arens, 2007) (Fig. 2). The early appearance
assumed to be closely related to water lilies and were included of aquatic angiosperms supports the view that early
in the Nymphaeales. However, similarities among these taxa angiosperms had a growth habit of rhizomatous herbs, which
were due to parallel adaptations to aquatic environments. could be easily transformed into aquatic habit (Doyle, 2012).
Ceratophyllum, the only extant genus in the Ceratophyllaceae, Taylor & Hickey (1992) also suggested that early angiosperms
possesses unique morphological characters, which suggests were perennial rhizomatous herbs that competed with ferns
that it has an isolated position and an early divergence from in stream margins. Because of their rhizomatous growth habit
other angiosperms (Les, 1988; Dilcher & Wang, 2009). and efficient seedlings, these herbaceous species invaded the
Ceratophyllum species are submerged aquatic plants widely aquatic habitats in the Early Cretaceous.

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346 Du et al.

Fig. 2. Early radiation of aquatic angiosperms.

Fossil records from Asia, Europe, and America all show that their assistance in the laboratory and data analysis. The
angiosperms occurred in aquatic environments (freshwater National Natural Science Foundation of China (Grant No.
lakes, swamps, and floodplains) during the Early Cretaceous 31100175) and the strategic pilot science and technology
(Coiffard et al., 2012). Recently, an early angiosperm fossil projects of the Chinese Academy of Sciences (Grant No.
genus Hyrcantha that lived in Asia 125–122 Ma was discovered XDAO5090305) supported this research.
(Dilcher et al., 2007). The genus appear to be aquatic, living in
shallow water (20–40 cm deep), with the terminal fruiting
axes exposed above the water. The earliest well-documented
fossil records of angiosperms from Asia, such as Archaefructus
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348 Du et al.

Qing-Feng WANG Cheng-Xin FU

Wuhan Botanical Garden, Chinese Academy of Sciences, Zhejiang University, Hangzhou, China
Wuhan, China Qi-Xin LIU
Jian-Hui LI Nanjing Institute of Botany, Jiangsu Province and Chinese
Computer Network Information Center, Chinese Academy of Academy of Sciences, Nanjing, China
Sciences, Beijing, China
De-Zhu LI, Ting-Shuang YI
Kunming Institute of Botany, Chinese Academy of Sciences, Supplementary Material
Kunming, China The following supplementary material is available online for
Hong MA this article at http://onlinelibrary.wiley.com/doi/10.1111/
Fudan University, Shanghai, China jse.12182/suppinfo:
Douglas E. SOLTIS, Pamela S. SOLTIS Fig. S1. Annotation of aquatic taxa on the tree of vascular
University of Florida, Gainesville, USA plants. This tree is edited from Zhi-Duan Chen et al. (pers.
Jian-Hua LI comm.). Aquatic families are in red. Terrestrial families that
Hope College, Holland, USA contain aquatic taxa are in blue.

J. Syst. Evol. 54 (4): 342–348, 2016 www.jse.ac.cn