- Email: [email protected]
When Earth started blooming: insights from the fossil record
When Earth started blooming: insights from the fossil record Else Marie Friis1, Kaj Raunsgaard Pedersen2 and Peter R Crane3 Recent palaeobotanical studies have greatly increased the quantity and quality of information available about the structure and relationships of Cretaceous angiosperms. Discoveries of extremely well preserved Cretaceous flowers have been especially informative and, combined with results from phylogenetic analyses of extant angiosperms (based mainly on molecular sequence data), have greatly clarified important aspects of early angiosperm diversification. Nevertheless, many questions still persist. The phylogenetic origin of the group itself remains as enigmatic as ever and, in some cases, newly introduced techniques from molecular biology have given confusing results. In particular, relationships between the five groups of extant seed plants remain uncertain, and it has sometimes proved difficult to reconcile estimates of the time of divergence between extant lineages made using a ‘molecular clock’ with the fossil record. One result, however, is becoming increasingly clear: a great deal of angiosperm diversity is extinct. Some groups of angiosperms were evidently more diverse in the past than they are today. In other cases, fossils defy assignment to extant groups at the family level or below. This raises the possibility that evolutionary conclusions based solely upon extant taxa that are merely relics of groups that were once much more diverse might be misled by the effects of extinction. It also introduces the possibility that some early enigmatic fossils might represent lineages that diverged from the main line of angiosperm evolution below the most recent common ancestor of all extant taxa. These, and other questions, are among those that need to be addressed by future palaeobotanical research. Addresses 1 Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden 2 Department of Geology, University of Aarhus, Universitetsparken, DK-8000 A˚rhus C, Denmark 3 Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK Corresponding author: Friis, Else Marie ([email protected])
Current Opinion in Plant Biology 2005, 8:5–12 This review comes from a themed issue on Growth and development Edited by Liam Dolan and Michael Freeling
his widely cited letter to Joseph Hooker in 1879, remains as one of the most persistent puzzles in modern evolutionary biology. Although much has been written on this topic, a convincing understanding of how angiosperms originated remains to be developed. One impediment to progress is the apparent evolutionary distance that separates angiosperms from other living seed plants, and that obscures morphological homologies. Another difficulty is our poor knowledge of the enormous diversity of extinct plants from the Mesozoic, some of which might be relevant to our understanding of how specific angiosperm features, such as the flower, carpel and stamen, might have evolved from the reproductive structures of fossil gymnosperms. However, although the enigma of angiosperm origin remains intractable, recent advances in biology and palaeontology have contributed to a much clearer picture of angiosperm diversification, including some of the earliest known phases that occurred during the Early Cretaceous. Large-scale molecular analyses have resulted in increasingly well-supported models of angiosperm phylogeny, including patterns of relationships among those extant orders and families that appear to have differentiated early in the evolution of the group [1–3]. Studies of plant morphology have also provided new insights into the distribution of critical reproductive characters among these extant taxa [4,5]. At the same time, palaeobotanical and palynological studies of Cretaceous angiosperms [6–15,16,17] have generated a wealth of new data that are pertinent to understanding the timing of major evolutionary events in angiosperm history. Most recently, studies integrating results from molecular sequence data with those from the fossil record have begun to offer new insights into diversification rates and the age of different angiosperm clades [18,19,20,21,22,23,24]. In this review, we focus on the recent accumulation of palaeobotanical data on angiosperm floral structures from the Cretaceous, and the implications of these discoveries for our current understanding of angiosperm diversification in time and space.
Available online 25th November 2004
First major radiation of angiosperms
1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved.
The fossil record provides unequivocal evidence for the presence of diverse angiosperm assemblages in the Early Cretaceous, and indicates that many major lineages of extant angiosperms were already differentiated by the early Late Cretaceous. It has also become clear that there was a distinctive and regular expansion in the diversity and complexity of angiosperms over a relatively short interval through the mid- to late-Early Cretaceous (Hauterivian–Barremian–Aptian–Albian), and that this
DOI 10.1016/j.pbi.2004.11.006
Introduction The sudden appearance of angiosperms in the Cretaceous, highlighted by Darwin as an abominable mystery in www.sciencedirect.com
Current Opinion in Plant Biology 2005, 8:5–12
6 Growth and development
is paralleled by a marked increase in angiosperm abundance during the same period. This general pattern of angiosperm diversification was first elaborated on the basis of morphological evidence from pollen and leaves [6,7], but a similar stratigraphic increase in diversity and structural complexity is also seen among Cretaceous flowers that have been discovered over the past 25 years.
and age estimates of the same divergence obtained using different approaches can vary by tens of or even hundreds of millions of years. In addition, because most analyses use fossil taxa as calibration points, they face the same challenges and uncertainties as traditional palaeobotanical studies regarding the reliability of these points [23,55].
Following the first major discovery of fossil flowers from the Late Cretaceous in Sweden [25], many new sites with angiosperm flowers have also been discovered. In the past few years, much new information about Cretaceous flowers has been accumulated from fossils from Europe [12,26–30,31,32,33], North America [34–38], Asia [15,39,40,41,42,43], South America [44,45], New Zealand [46] and Antarctica [47], covering most of the stratigraphic column from the mid-Early Cretaceous (Barremian–Aptian) to the end of the Cretaceous (Maastrichtian). The fossil flowers are often preserved as charcoalifications, which were formed as a result of fire in Cretaceous vegetation, and typically retain their original three-dimensional shape. Many flowers also have pollen grains in situ, thereby providing an invaluable link to the dispersed pollen record. This link is of great importance for phylogenetic biogeography and for understanding the tempo and mode of angiosperm diversification.
An important motivation behind attempts to understand the time of divergence of different angiosperm lineages is to clarify the changing pattern of angiosperm diversity through time. This will help us to better understand how the extraordinarily high current levels of angiosperm diversity have arisen. Early studies approached this issue by quantifying the changing composition of the palaeobotanical record through time [56]. More recently, an alternative approach has been to compare the estimated time of origin of different angiosperm clades with their present day diversity. This approach indicates that, typically, species-rich clades are relatively young and are nested among the more derived lineages of monocots or eudicots [18,57]. Clades that have extremely low levels of species diversity are typically more ancient and diverged close to the root of either angiosperms or of major angiosperm subgroups [18]. Magallo´ n and Sanderson [18] suggested that ancient species-poor clades are probably relicts of groups that experienced early diversification followed by extinction. Although these kinds of studies, which integrate palaeobotanical data with insights from molecular biology, offer considerable potential for future research, there are also many difficulties that remain to be overcome. This is illustrated below by two examples from the fossil record.
Relationships of angiosperms Resolving the relationships of angiosperms to other seed plants is crucial to understanding the origin of the group. In the mid-1990s, a consensus developed that Gnetales were the closest living relatives to angiosperms, and that the extinct Bennettitales and certain Mesozoic ‘seed ferns’ were also important for understanding the origin of the group. More recently, however, attempts to resolve relationships among extant seed plants using molecular sequence data do not support a close relationship between angiosperms and Gnetales, and instead have suggested a range of alternative phylogenetic patterns [48,49]. As a result, the relationships of angiosperms remain uncertain and the prospects for understanding the origin of characteristic angiosperm features, such as the carpel and stamen, are as remote as ever.
Diversification rates and ages of angiosperm lineages In terms of understanding angiosperm diversification, an interesting recent development attempts to use rates of molecular divergence to estimate the timing of deep splits between angiosperm lineages. This research requires converting genetic distances into absolute ages using different kinds of ‘molecular clock’ assumptions [19,20,22,23,24,50–53]. Currently, much attention continues to be directed towards developing and testing methods that can help mitigate the difficulties posed by the strikingly different rates of molecular evolution in different angiosperm lineages [54]. Results are confusing Current Opinion in Plant Biology 2005, 8:5–12
Chloranthaceae Dispersed pollen assigned to the fossil genus Asteropollis is among the first evidence of angiosperms to appear in the Cretaceous and shows an almost worldwide distribution during the Early and mid-Cretaceous [58,59]. Close morphological and ultrastructural resemblance between the pollen of Asteropollis and that of extant Hedyosmum (Chloranthaceae) has long been documented [60], and this link has been confirmed by the discovery of pollen grains of the Asteropollis type inside Cretaceous flowers that possess all of the critical floral features of extant Hedyosmum [58,61]. On the basis of molecular data, a midCainozoic age (45 million years ago) was suggested for the initial divergence of extant Hedyosmum species [20]. However, Eklund et al. [59] showed that the Cretaceous fossils fit equally well below, within or above the three basal species of extant Hedyosmum (Figure 1). Taking into account the proposed late divergence of the crown group Hedyosmum, which include all extant and extinct species that diverged after the origin of the most recent common ancestor, they argued that a stem-group position for the fossils is more likely, implying that not all defining features (synapomorphies) of the genus were present in www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 7
Figure 1
Age Mya
Crown group
Crown group
∗
Fossil pollen and flowers with distinctive Hedyosmum features
Paleogene
Origin of crown group Origin of some defining features of Hedyosmum Origin of all defining features of Hedyosmum
65
Lineage divergence Stem representatives Sister group lineage
Early Cretaceous
Mesozoic
Late Cretaceous
Cainozoic
Neogene
0
∗
∗ First unequivocal angiosperm pollen
Jurassic
144.2 (a)
(b)
Two alternative scenarios for the age of crown-group Hedyosmum (Chloranthaceae). (a) Plants with all the defining features of modern Hedyosmum (crown-group Hedyosmum) are old and originated soon after the lineage divergence between Hedyosmum and its sister group. According to this scenario, modern Hedyosmum developed soon after the first appearance of angiosperms in the fossil record and has retained its defining features for more than 120 million years; this scenario is supported by the finding of fossil pollen (Asteropollis) and flowers indistinguishable from those of modern Hedyosmum [58,59]. (b) Crown-group Hedyosmum is young and originated in the Cenozoic more than 100 million years after the lineage divergence between Hedyosmum and its sister group and almost as long after the appearance of plants with distinctive Hedyosmum reproductive features. According to this scenario, some of the defining features of extant Hedyosmum originated some time during the Late Cretaceous or Cenozoic. This scenario is suggested by molecular dating [20]; fossil data according to Eklund et al. [59] are equivocal.
the fossils. However, this indicates that Hedyosmum experienced two major phases of diversification: first, an Early Cretaceous radiation resulting in a worldwide expansion followed by Late Cretaceous extinctions; and a second, mid-Cainozoic radiation that generated the extant diversity of the genus. There are no apparent morphological innovations associated with the second radiation and an alternative explanation is that the age calculated for the crown group is erroneous. More research is needed to establish which of these contrasting hypotheses is more likely to be correct. A comparable apparent conflict between molecular ages and the fossil record has recently been demonstrated for the genus Ephedra of the Gnetales [62].
Fagales Dispersed triaperturate pollen grains with distinctive protruding and elaborate apertures (Figure 2a–d) are very www.sciencedirect.com
conspicuous and diverse elements in Late Cretaceous floras in Europe and eastern North America. They are collectively referred to as the Normapolles complex. Members of this complex diversified initially in the early Late Cretaceous, expanded dramatically during the Late Cretaceous and underwent significant extinction during the latest Cretaceous and Palaeogene (see references in [31]). Fossil flowers containing pollen grains of the Normapolles type show that these plants represent a complex of extinct lineages nested within Fagales [28,31,63,64]. Endressianthus and Normanthus plants recently (Figure 2e–h) described from the Late Cretaceous of Portugal [28,31] are the most completely understood Normapolles flowers. They constitute extinct lineages close to the root of the Betulaceae lineage [31]. Other Normapolles lineages are more closely related to Rhoipteleaceae, Myricaceae and Juglandaceae [31]. Based on this emerging fossil record there is little Current Opinion in Plant Biology 2005, 8:5–12
8 Growth and development
Figure 2
(a)
(b)
(g)
(c)
(h)
(e)
(f) (d)
Cretaceous pollen and flowers assigned to the extinct Normapolles complex. (a) Dispersed pollen grain of Interporopollenites type (scale = 10 mm). (b) Dispersed pollen of the Pseudopapillopollis type (scale = 10 mm). (c–d) Schematic sections through an Interporopollenites-type pollen showing complex aperture regions (taken with permission from [31]). Fragments of (e) pistillate (scale = 1 mm) and (f) staminate (scale = 0.3 mm) flowerbearing axes of Endressianthus, a new Normapolles genus described from the Late Cretaceous of Portugal [31]; pollen grains produced by Endressianthus are similar to dispersed Interporopollenites. (g) Complete flower of Normanthus described from the Late Cretaceous of Portugal [28] and (h) the same flower with part of perianth removed showing bisexual structure of flower (scale bar = 1 mm). The Normapolles genera constitute a large complex of extinct lineages within Fagales. Endressianthus/Interporopollenites and Normanthus/Pseudopapillopollis are closely related to Betulaceae.
doubt that Fagales were diverse during the Late Cretaceous, but that this was followed by considerable extinction before the radiations of diverse modern genera.
Pre-Cretaceous prelude and stem-group angiosperms? Although the fossil record unequivocally demonstrates a first major radiation of angiosperms in the Early Cretaceous, the high diversity of these early angiosperms raises questions about their possible pre-Cretaceous evolutionary precursors. Also, most analyses of divergence time for angiosperms using molecular techniques have concluded that their ages are considerably older than those inferred directly from the fossil record [19]. However, there is no definite evidence of pre-Cretaceous angiosperms. Reticulate pollen from the Triassic [65,66] are from intriguing plant taxa that are potential angiosperm relatives, but unfortunately there are no macrofossil remains that can help to clarify the phylogenetic significance of these Triassic forms. Evidence from the history of other major clades of land plants suggests that the characteristic features of angioCurrent Opinion in Plant Biology 2005, 8:5–12
sperms were probably acquired sequentially through time. The recent ‘transitional-combinational theory’ of angiosperm origin [67] suggests an evolution of angiosperms from Jurassic seed ferns that occurred through three fundamental transitions: the evolution of the carpel, the emergence of double fertilisation and last the origin of the flower in the Early Cretaceous. However, no phylogenetic framework has been used to test this sequence of character evolution and improved palaeobotanical data are needed to pursue these ideas more rigorously. One genus that has received particular attention in discussions of angiosperm origin is the Mesozoic seed fern Caytonia [68,69]. The early assignment of Caytonia to angiosperms [70] made it an obvious object for further study. Palaeobotanically, however, Caytonia is among a multitude of extinct plants, most of which have not yet been studied in comparable detail. Some of the extraordinary diversity of extinct Mesozoic seed plants has recently been exposed in a comprehensive atlas of Late Triassic fructifications from the Molteno Formation of South Africa [71]. Some of these fossils are assignable to www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 9
previously known groups such as peltasperms, corystosperms and Bennettitales. However, the systematic position of many of these fossils is unknown and a more detailed study of this, and other material, is imperative for a better understanding of extinct seed plant diversity and relationships. The genus Archaefructus, with three species described from the Yixian Formation of north eastern China [15,72,73], has also been suggested as a possible angiosperm precursor or angiosperm stem group [15,67]. The age of the fossils has been disputed, but there is now strong support for a mid-Early Cretaceous age for the oldest horizons that contain Archaefructus [74,75]. Archaefructus fossils are exceptional in that they include specimens preserved as whole plants with roots, stems, leaves, flowers and fruits [73]. Archaefructus is an herbaceous plant with a habit that suggests an aquatic life-style. Carpels and stamens are borne either singly or in clusters of two or three on short common stalks along an elongated axis. Stamens are proximal whereas carpels are in a distal position. There are no traces of bracts or perianth parts and Sun et al. [15] interpreted the reproductive axis as a primitively naked, multiparted and bisexual flower. This interpretation is controversial and, alternatively, it has been suggested that Archaefructus is a crown-group angiosperm that has advanced, rather than primitive, floral features [16]. According to this interpretation Archaefructus was totally submerged and its reproductive axes were inflorescences with many small, simple and unisexual flowers that had lost perianth and bracts as an adaptation to underwater flowering. Recent observations of Archaefructus eoflora show a small bisexual flower comprising two carpels and one stamen between the staminate and pistillate zone [73]. This supports the inflorescence interpretation. However, although the Yixian fossils beautifully show features of general morphology, the preservation of details is typically obscured by pyrite infiltrations [42,76]. More information is clearly needed to provide a full understanding of the phylogenetic significance of Archaefructus.
The record of Cretaceous reproductive structures makes it clear that there has been considerable extinction within certain angiosperm lineages, and that the extant taxa constitute only a small proportion of the total diversity of the group. This raises questions about the extent to which phylogenetic analyses based on extant taxa that include these groups might have been distorted by uneven sampling introduced as a result of differential extinction. In terms of the earliest phases of angiosperm diversification, the presence of diverse angiosperm species that are difficult to link definitively with extant taxa raises the possibility that some of these groups might have diverged from the main line of angiosperm evolution at a level below the common ancestor of all extant taxa. Investigation of these taxa, as well as studies of extinct groups of gymnosperms from throughout the Mesozoic, will be important to identify potential stem-group angiosperms. Perhaps such investigation will also develop a clearer understanding of the sequence in which the defining characteristics of extant angiosperms were acquired.
Acknowledgements We acknowledge Pollyanna von Knorring for line drawings of fossil pollen and flowers and research grants from the Swedish Research Council (to EM Friis) and from the Carlsberg Foundation (to KR Pedersen).
References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1.
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Conclusions and future perspectives Information concerning fossil flowers that has been accumulated over the past two decades has provided a wealth of new data about the systematic diversity of Cretaceous angiosperms. Especially interesting are insights into the diversity of the group soon after its first appearance during the mid-Early Cretaceous. Even at this relatively early stage, angiosperms were diverse at the species level. However, most early angiosperm species cannot be attributed reliably to extant angiosperm clades. Instead, they appear to represent extinct lineages. According to analyses of molecular data from extant taxa, the few extant groups that can be recognized definitively at the family level or below are mainly taxa that belong to basal branches of the angiosperm phylogenetic tree. www.sciencedirect.com
10. Crepet WL: Timing in the evolution of derived floral characters: upper Cretaceous (Turonian) taxa with tricolpate and Current Opinion in Plant Biology 2005, 8:5–12
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26. Friis EM, Pedersen KR, Crane PR: Reproductive structure and organization of basal angiosperms from the Early Cretaceous (Barremian or Aptian) of Western Portugal. Int J Plant Sci 2000, 161(6 Suppl.):S169-S182. 27. Friis EM, Pedersen KR, Crane PR: Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 2001, 410:357-360. 28. Scho¨ nenberger J, Pedersen KR, Friis EM: Normapolles flowers of fagalean affinity from the Late Cretaceous of Portugal. Pl Syst Evol 2001, 226:205-230. 29. Scho¨ nenberger J, Friis EM, Matthews ML, Endress PK: Cunoniaceae in the Cretaceous of Europe: evidence from fossil flowers. Ann Bot (Lond) 2001, 88:423-437. 30. Scho¨ nenberger J, Friis EM: Fossil flowers of ericalean affinity from the Late Cretaceous of Southern Sweden. Am J Bot 2001, 88:467-480. 31. Friis EM, Pedersen KR, Scho¨ nenberger J: Endressianthus, a new Normapolles producing plant genus of fagalean affinity from the Late Cretaceous of Portugal. Int J Plant Sci 2003, 164(5 Suppl.):S201-S223. Endressianthus is the most completely known Normapolles flower. It is excellently preserved and provides information on inflorescence structure, staminate and pistillate flowers, and pollen that give a better understanding of the Cretaceous diversification of Fagales. 32. Kvacˇ ek J, Eklund H: A report on newly recovered reproductive structures from the Cenomanian of Bohemia (Central Europe). Int J Plant Sci 2003, 194:1021-1039. Rich Cretaceous floras containing angiosperm leaves have long been known from the mid-Cretaceous of the Bohemian Massif. Recently, several angiosperm floral structures have also been reported from this classic area. The present work describes several new intriguing fossils pertinent to our understanding of Cretaceous angiosperm diversification. 33. Friis EM, Pedersen KR, Crane PR: Araceae from the Early Cretaceous of Portugal: evidence on the emergence of monocotyledons. Proc Natl Acad Sci USA 2004, 101:16565-16570. This study describes a unique polyplicate pollen from Portugal with distinctive features of the tribe Spathiphyllum (Araceae). It is significant in providing the first unequivocal evidence of monocots in the Early Cretaceous. 34. Herendeen PS, Magallo´ n-Puebla S, Lupia R, Crane PR, Kobylinska J: A preliminary conspectus of the Allon flora from the Late Cretaceous (late Santonian) of central Georgia, USA. Ann Mo Bot Gard 1999, 86:407-471. 35. Eklund H: Lauraceous flowers from the Late Cretaceous of North Carolina, USA. Bot J Linn Soc 2000, 132:397-428. 36. Gandolfo MA, Nixon KC, Crepet WL: Triuridaceae fossil flowers from the Upper Cretaceous of New Jersey. Am J Bot 2002, 89:1940-1957. 37. Hermsen EJ, Gandolfo MA, Nixon KC, Crepet WL: Divisestylus gen. nov. (aff. Iteaceae), a fossil saxifrage from the Late Cretaceous of New Jersey, USA. Am J Bot 2003, 90:1373-1388.
22. Renner SS, Zhang L-B, Murata J: A chloroplast phylogeny of Arisaema (Araceae) illustrates Tertiary floristic links between Asia, North America, and East Africa. Am J Bot 2004, 91:881-888.
38. Gandolfo MA, Nixon KC, Crepet WL: Cretaceous flowers of Nymphaeaceae and implications for complex insect entrapment pollination mechanisms in early angiosperms. Proc Natl Acad Sci USA 2004, 101:8056-8060.
23. Bremer K, Friis EM, Bremer B: Molecular phylogenetic dating of asterid flowering plants shows Early Cretaceous diversification. Syst Biol 2004, 53:496-505. This study presents a phylogenetic dating of the asterid clade using an 111-taxon asterid tree that represents all major clades of the group and six fossils as calibration points. Importantly, this study shows that the use of more reference fossils reduces variation in age estimates.
39. Frumin S, Friis EM: Magnoliid reproductive organs from the Cenomanian-Turonian of north-western Kazakhstan: Magnoliaceae and Illiciaceae. Pl Syst Evol 1999, 216:265-288.
24. Magallo´ n SA: Dating lineages: molecular and paleontological approaches to the temporal framework of clades. Int J Plant Sci 2004, 165:S7-S21. This work provides an excellent overview with up to date references of molecular and paleontological methods used in age estimates of clades. 25. Friis EM, Skarby A: Structurally preserved angiosperm flowers from the Upper Cretaceous of southern Sweden. Nature 1981, 291:485-486. Current Opinion in Plant Biology 2005, 8:5–12
40. Frumin S, Eklund H, Friis EM: Mauldinia hirsuta sp. nov., a new member of the extinct genus Mauldinia (Lauraceae) from the Late Cretaceous (Cenomanian-Turonian) of Kazakhstan. Int J Plant Sci 2004, in press. This work describes a new species of the extinct genus Mauldinia of the family Lauraceae from the mid-Cretaceous of Kazakhstan. The Sarbay flora is important as the oldest mesofossil flora from Asia and is crucial for understanding early angiosperm radition. 41. Takahashi M, Crane PR, Manchester SR: Hironoia fusiformis gen. et sp. nov.: a cornalean fruit from the Kamikitaba locality (Upper Cretecous, Lower Coniacian) in northeastern Japan. J Plant Res 2002, 115:463-473. www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 11
42. Leng Q, Friis EM: Sinocarpus decussatus gen. et sp. nov, a new angiosperm with syncarpous fruits from the Yixian Formation of Northeast China. Pl Syst Evol 2003, 241:77-88. The extinct genus Sinocarpus described in this work from the Early Cretaceous of north western China is significant in being the earliest fossil flower with a syncarpous gynoecium. Its distinct morphology indicates affinity with eudicots and shows that angiosperms in the Jehol Biota were diversified to some extent.
The authors provide a thorough analysis of morphological character evolution in both fossil and extant Chloranthaceae. There are many useful illustrations, mostly of reproductive features, and a comprehensive literature survey of fossil and living members of the group.
43. Maslova NP, Kodrul TM: New platanaceous inflorescence Archaranthus gen. nov. from the Maastrichtian-Paleocene of the Amur Region. Paleontological J 2003, 37:89-98.
61. Friis EM, Pedersen KR, Crane PR: Early angiosperm diversification: the diversity of pollen associated with angiosperm reproductive structures in Early Cretaceous floras from Portugal. Ann Mo Bot Gard 1999, 86:259-296.
44. Mohr B, Friis EM: Early angiosperms from the Aptian Crato Formation (Brazil), a preliminary report. Int J Plant Sci 2000, 161(6 Suppl.):S155-S167. 45. Mohr B, Eklund H: Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Rev Palaeobot Palynol 2003, 126:279-292. This paper provides the first formal description of an early angiosperm plant from the Crato Formation, Brazil. The material from this formation is significant in comprising whole-plant preservation. Araripia is a magnoliid plant with leaves and flowers attached to the same branching system. 46. Kennedy EM, Lovis JD, Daniel JL: Discovery of a Cretaceous angiosperm reproductive structure from New Zealand. New Zeal J Geol Geop 2003, 46:519-522. 47. Eklund H: First Cretaceous flowers from Antarctica. Rev Palaeobot Palynol 2003, 127:187-217. Most of the fossil flowers discovered in Cretaceous strata are from the Northern Hemisphere. This study is important in providing the first evidence from Antarctica of flowers that have an organization and structure comparable to contemporary flowers from other areas. 48. Bowe LG, Coat G, DePamphilis CW: Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci USA 2000, 97:4092-4097. 49. Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer JD: Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales and conifers. Proc Natl Acad Sci USA 2000, 97:4086-4091. 50. Bremer K: Early Cretaceous lineages of monocot flowering plants. Proc Natl Acad Sci USA 2000, 97:4707-4711. 51. Renner SS, Foreman DB, Murray D: Timing transacrtic disjunctions in the Atherospermataceae (Laurales): evidence from coding and noncoding chloroplast sequences. Syst Bot 2000, 49:579-591. 52. Wikstro¨ m N, Savolainen V, Chase MW: Evolution of the angiosperms. Calibrating the tree. Proc R Soc Lond B Biol Sci 2001, 268:2211-2220. 53. Chaw SM, Chang CC, Chen HL, Li WH: Dating the monocot– dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 2004, 58:424-441. 54. Sanderson MJ: Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 2002, 19:101-109. 55. Crane PR, Herendeen P, Friis EM: Fossils and plant phylogeny. Am J Bot 2004, 91:1684-1699. 56. Crane PR, Lidgard S: Angiosperm diversification and palaeolatitudinal gradients in Cretaceous floristic diversity. Science 1989, 246:675-678. 57. Magallo´ n S, Crane PR, Herendeen PS: Phylogenetic pattern, diversity and diversification of eudicots. Ann Mo Bot Gard 1999, 86:297-372. 58. Friis EM, Crane PR, Pedersen KR: Fossil history of magnoliid angiosperms. In Evolution and Diversification of Land Plants. Edited by Iwatsuki K, Raven PH. New York: Springer Verlag; 1997:121-156. 59. Eklund H, Doyle JA, Herendeen PS: Morphological phylogenetic analysis of living and fossil Chloranthaceae. Int J Plant Sci 2003, 165:107-151. www.sciencedirect.com
60. Walker JW, Walker AG: Ultrastructure of Lower Cretaceous angiosperm pollen and the origin and early evolution of flowering plants. Ann Mo Bot Gard 1984, 71:464-521.
62. Rydin C, Pedersen KR, Friis EM: On the evolutionary history of Ephedra; Cretaceous fossils and extant molecules. Proc Natl Acad Sci USA 2004, 101:16571-16576. This study describes exceptionally well-preserved seeds with distinctive characters of Ephedra from the Early Cretaceous of Portugal and discusses the finding based on a molecular phylogeny. The finding demonstrates that modern species of Ephedra have retained unique reproductive features, including the peculiar naked male gametophyte, for more than 110 million years. It also highlights the apparent conflict between molecular dating of crown-group Ephedra and the fossil record. 63. Friis EM: Upper Cretaceous (Senonian) floral structures of juglandalean affinity containing Normapolles pollen. Rev Palaeobot Palynol 1983, 39:161-188. 64. Sims HJ, Herendeen PS, Lupia R, Christopher RA, Crane PR: Fossil flowers with Normapolles pollen from the Late Cretaceous of southeastern North America. Rev Palaeobot Palynol 1999, 106:131-151. 65. Hochuli PA, Colin JP, Vigran JO: Triassic biostratigraphy of the Barents Sea area. In Correlation in Hydrocarbon Exploration. Edited by Collinson JD. London: Norwegian Petroleum Society (Graham & Trotman); 1989:131-153. 66. Cornet B: Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia, U.S.A. Palaeontogr B 1989, 213:37-87. 67. Stuessy TF: A transitional-combinational theory for the origin of angiosperms. Taxon 2004, 53:3-16. 68. Gaussen H: Les Gymnospermes, actuelles et fossiles. Trav Lab for Toulouse T II 1946, 1:1-130. 69. Doyle JA: Origin of the angiosperm flower: a phylogenetic perspective. Plant Syst Evol 1994, 8:7-29. 70. Thomas HH: The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philos Trans R Soc Lond B Biol Sci 1925, 213:299-363. 71. Anderson JM, Anderson HM: Heyday of the gymnosperms: systematics and biodiversity of the Late Triassic Molteno fructifications Pretoria: National Botanical Institute; 2003:1-398. This article is the result of more than 35 years field work and study of plant fossils from the Molteno Formation. It describes one of the most extensive collections of Mesozoic seed plant fructifications and describes an unexpected and extraordinary diversity in reproductive structures of extinct seed plants. 72. Sun G, Dilcher DL, Zheng S, Zhou Z: In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 1998, 282:1692-1695. 73. Ji Q, Li H, Bowe LM, Liu Y, Taylor DW: Early Cretaceous Archaefructus eoflora sp. nov., with bisexual flowers from Beipiao, Western Liaoning, China. Acta Geologica Sinica 2004, 78:883-896. The paper provides a description of a new Early Cretaceous species of Archaefructus preserved as a whole plant with roots, stems, leaves, flowers and fruits. Although anatomical and fine morphological details are poorly preserved, this fossil shows excellent gross morphological features and is significant in our understanding of the early angiosperm habit. 74. Zhou Z, Barrett PM, Hilton J: An exceptionally preserved Lower Cretaceous ecosystem. Nature 2003, 421:807-814. This review paper provides a critical overview of the Jehol Biota with particular focus on the stratigraphy and palaeoenvironmental setting. The fossil plants are also discussed briefly and the authors suggest a possible pteridospermous nature of the Archaefructus plant. Current Opinion in Plant Biology 2005, 8:5–12
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75. Chang M-m, Chen P-j, Wang Y-q, Wang Y, Mioa D-s (Eds): The Jehol Biota. Series. Shanghai: Shanghai Scientific and Technical Publishers; 2003. This book includes a collection of articles summarizing current knowledge of the Jehol Biota, from insects to angiosperms. It includes high-quality illustrations of the fossils as well as many excellent reconstructions. It also provides a broad overview of geology and stratigraphy of this important
Current Opinion in Plant Biology 2005, 8:5–12
Mesozoic ecosystem. The book is written for non-specialists but is based on strict scientific criteria. 76. Leng Q, Yang H: Pyrite framboids associated with the Mesozoic Jehol Biota in northeastern China: implications for microenvironment during early fossilization. Prog Nat Sci 2003, 13:206-212.
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Current Opinion in Plant Biology 2005, 8:5–12 This review comes from a themed issue on Growth and development Edited by Liam Dolan and Michael Freeling
his widely cited letter to Joseph Hooker in 1879, remains as one of the most persistent puzzles in modern evolutionary biology. Although much has been written on this topic, a convincing understanding of how angiosperms originated remains to be developed. One impediment to progress is the apparent evolutionary distance that separates angiosperms from other living seed plants, and that obscures morphological homologies. Another difficulty is our poor knowledge of the enormous diversity of extinct plants from the Mesozoic, some of which might be relevant to our understanding of how specific angiosperm features, such as the flower, carpel and stamen, might have evolved from the reproductive structures of fossil gymnosperms. However, although the enigma of angiosperm origin remains intractable, recent advances in biology and palaeontology have contributed to a much clearer picture of angiosperm diversification, including some of the earliest known phases that occurred during the Early Cretaceous. Large-scale molecular analyses have resulted in increasingly well-supported models of angiosperm phylogeny, including patterns of relationships among those extant orders and families that appear to have differentiated early in the evolution of the group [1–3]. Studies of plant morphology have also provided new insights into the distribution of critical reproductive characters among these extant taxa [4,5]. At the same time, palaeobotanical and palynological studies of Cretaceous angiosperms [6–15,16,17] have generated a wealth of new data that are pertinent to understanding the timing of major evolutionary events in angiosperm history. Most recently, studies integrating results from molecular sequence data with those from the fossil record have begun to offer new insights into diversification rates and the age of different angiosperm clades [18,19,20,21,22,23,24]. In this review, we focus on the recent accumulation of palaeobotanical data on angiosperm floral structures from the Cretaceous, and the implications of these discoveries for our current understanding of angiosperm diversification in time and space.
Available online 25th November 2004
First major radiation of angiosperms
1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved.
The fossil record provides unequivocal evidence for the presence of diverse angiosperm assemblages in the Early Cretaceous, and indicates that many major lineages of extant angiosperms were already differentiated by the early Late Cretaceous. It has also become clear that there was a distinctive and regular expansion in the diversity and complexity of angiosperms over a relatively short interval through the mid- to late-Early Cretaceous (Hauterivian–Barremian–Aptian–Albian), and that this
DOI 10.1016/j.pbi.2004.11.006
Introduction The sudden appearance of angiosperms in the Cretaceous, highlighted by Darwin as an abominable mystery in www.sciencedirect.com
Current Opinion in Plant Biology 2005, 8:5–12
6 Growth and development
is paralleled by a marked increase in angiosperm abundance during the same period. This general pattern of angiosperm diversification was first elaborated on the basis of morphological evidence from pollen and leaves [6,7], but a similar stratigraphic increase in diversity and structural complexity is also seen among Cretaceous flowers that have been discovered over the past 25 years.
and age estimates of the same divergence obtained using different approaches can vary by tens of or even hundreds of millions of years. In addition, because most analyses use fossil taxa as calibration points, they face the same challenges and uncertainties as traditional palaeobotanical studies regarding the reliability of these points [23,55].
Following the first major discovery of fossil flowers from the Late Cretaceous in Sweden [25], many new sites with angiosperm flowers have also been discovered. In the past few years, much new information about Cretaceous flowers has been accumulated from fossils from Europe [12,26–30,31,32,33], North America [34–38], Asia [15,39,40,41,42,43], South America [44,45], New Zealand [46] and Antarctica [47], covering most of the stratigraphic column from the mid-Early Cretaceous (Barremian–Aptian) to the end of the Cretaceous (Maastrichtian). The fossil flowers are often preserved as charcoalifications, which were formed as a result of fire in Cretaceous vegetation, and typically retain their original three-dimensional shape. Many flowers also have pollen grains in situ, thereby providing an invaluable link to the dispersed pollen record. This link is of great importance for phylogenetic biogeography and for understanding the tempo and mode of angiosperm diversification.
An important motivation behind attempts to understand the time of divergence of different angiosperm lineages is to clarify the changing pattern of angiosperm diversity through time. This will help us to better understand how the extraordinarily high current levels of angiosperm diversity have arisen. Early studies approached this issue by quantifying the changing composition of the palaeobotanical record through time [56]. More recently, an alternative approach has been to compare the estimated time of origin of different angiosperm clades with their present day diversity. This approach indicates that, typically, species-rich clades are relatively young and are nested among the more derived lineages of monocots or eudicots [18,57]. Clades that have extremely low levels of species diversity are typically more ancient and diverged close to the root of either angiosperms or of major angiosperm subgroups [18]. Magallo´ n and Sanderson [18] suggested that ancient species-poor clades are probably relicts of groups that experienced early diversification followed by extinction. Although these kinds of studies, which integrate palaeobotanical data with insights from molecular biology, offer considerable potential for future research, there are also many difficulties that remain to be overcome. This is illustrated below by two examples from the fossil record.
Relationships of angiosperms Resolving the relationships of angiosperms to other seed plants is crucial to understanding the origin of the group. In the mid-1990s, a consensus developed that Gnetales were the closest living relatives to angiosperms, and that the extinct Bennettitales and certain Mesozoic ‘seed ferns’ were also important for understanding the origin of the group. More recently, however, attempts to resolve relationships among extant seed plants using molecular sequence data do not support a close relationship between angiosperms and Gnetales, and instead have suggested a range of alternative phylogenetic patterns [48,49]. As a result, the relationships of angiosperms remain uncertain and the prospects for understanding the origin of characteristic angiosperm features, such as the carpel and stamen, are as remote as ever.
Diversification rates and ages of angiosperm lineages In terms of understanding angiosperm diversification, an interesting recent development attempts to use rates of molecular divergence to estimate the timing of deep splits between angiosperm lineages. This research requires converting genetic distances into absolute ages using different kinds of ‘molecular clock’ assumptions [19,20,22,23,24,50–53]. Currently, much attention continues to be directed towards developing and testing methods that can help mitigate the difficulties posed by the strikingly different rates of molecular evolution in different angiosperm lineages [54]. Results are confusing Current Opinion in Plant Biology 2005, 8:5–12
Chloranthaceae Dispersed pollen assigned to the fossil genus Asteropollis is among the first evidence of angiosperms to appear in the Cretaceous and shows an almost worldwide distribution during the Early and mid-Cretaceous [58,59]. Close morphological and ultrastructural resemblance between the pollen of Asteropollis and that of extant Hedyosmum (Chloranthaceae) has long been documented [60], and this link has been confirmed by the discovery of pollen grains of the Asteropollis type inside Cretaceous flowers that possess all of the critical floral features of extant Hedyosmum [58,61]. On the basis of molecular data, a midCainozoic age (45 million years ago) was suggested for the initial divergence of extant Hedyosmum species [20]. However, Eklund et al. [59] showed that the Cretaceous fossils fit equally well below, within or above the three basal species of extant Hedyosmum (Figure 1). Taking into account the proposed late divergence of the crown group Hedyosmum, which include all extant and extinct species that diverged after the origin of the most recent common ancestor, they argued that a stem-group position for the fossils is more likely, implying that not all defining features (synapomorphies) of the genus were present in www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 7
Figure 1
Age Mya
Crown group
Crown group
∗
Fossil pollen and flowers with distinctive Hedyosmum features
Paleogene
Origin of crown group Origin of some defining features of Hedyosmum Origin of all defining features of Hedyosmum
65
Lineage divergence Stem representatives Sister group lineage
Early Cretaceous
Mesozoic
Late Cretaceous
Cainozoic
Neogene
0
∗
∗ First unequivocal angiosperm pollen
Jurassic
144.2 (a)
(b)
Two alternative scenarios for the age of crown-group Hedyosmum (Chloranthaceae). (a) Plants with all the defining features of modern Hedyosmum (crown-group Hedyosmum) are old and originated soon after the lineage divergence between Hedyosmum and its sister group. According to this scenario, modern Hedyosmum developed soon after the first appearance of angiosperms in the fossil record and has retained its defining features for more than 120 million years; this scenario is supported by the finding of fossil pollen (Asteropollis) and flowers indistinguishable from those of modern Hedyosmum [58,59]. (b) Crown-group Hedyosmum is young and originated in the Cenozoic more than 100 million years after the lineage divergence between Hedyosmum and its sister group and almost as long after the appearance of plants with distinctive Hedyosmum reproductive features. According to this scenario, some of the defining features of extant Hedyosmum originated some time during the Late Cretaceous or Cenozoic. This scenario is suggested by molecular dating [20]; fossil data according to Eklund et al. [59] are equivocal.
the fossils. However, this indicates that Hedyosmum experienced two major phases of diversification: first, an Early Cretaceous radiation resulting in a worldwide expansion followed by Late Cretaceous extinctions; and a second, mid-Cainozoic radiation that generated the extant diversity of the genus. There are no apparent morphological innovations associated with the second radiation and an alternative explanation is that the age calculated for the crown group is erroneous. More research is needed to establish which of these contrasting hypotheses is more likely to be correct. A comparable apparent conflict between molecular ages and the fossil record has recently been demonstrated for the genus Ephedra of the Gnetales [62].
Fagales Dispersed triaperturate pollen grains with distinctive protruding and elaborate apertures (Figure 2a–d) are very www.sciencedirect.com
conspicuous and diverse elements in Late Cretaceous floras in Europe and eastern North America. They are collectively referred to as the Normapolles complex. Members of this complex diversified initially in the early Late Cretaceous, expanded dramatically during the Late Cretaceous and underwent significant extinction during the latest Cretaceous and Palaeogene (see references in [31]). Fossil flowers containing pollen grains of the Normapolles type show that these plants represent a complex of extinct lineages nested within Fagales [28,31,63,64]. Endressianthus and Normanthus plants recently (Figure 2e–h) described from the Late Cretaceous of Portugal [28,31] are the most completely understood Normapolles flowers. They constitute extinct lineages close to the root of the Betulaceae lineage [31]. Other Normapolles lineages are more closely related to Rhoipteleaceae, Myricaceae and Juglandaceae [31]. Based on this emerging fossil record there is little Current Opinion in Plant Biology 2005, 8:5–12
8 Growth and development
Figure 2
(a)
(b)
(g)
(c)
(h)
(e)
(f) (d)
Cretaceous pollen and flowers assigned to the extinct Normapolles complex. (a) Dispersed pollen grain of Interporopollenites type (scale = 10 mm). (b) Dispersed pollen of the Pseudopapillopollis type (scale = 10 mm). (c–d) Schematic sections through an Interporopollenites-type pollen showing complex aperture regions (taken with permission from [31]). Fragments of (e) pistillate (scale = 1 mm) and (f) staminate (scale = 0.3 mm) flowerbearing axes of Endressianthus, a new Normapolles genus described from the Late Cretaceous of Portugal [31]; pollen grains produced by Endressianthus are similar to dispersed Interporopollenites. (g) Complete flower of Normanthus described from the Late Cretaceous of Portugal [28] and (h) the same flower with part of perianth removed showing bisexual structure of flower (scale bar = 1 mm). The Normapolles genera constitute a large complex of extinct lineages within Fagales. Endressianthus/Interporopollenites and Normanthus/Pseudopapillopollis are closely related to Betulaceae.
doubt that Fagales were diverse during the Late Cretaceous, but that this was followed by considerable extinction before the radiations of diverse modern genera.
Pre-Cretaceous prelude and stem-group angiosperms? Although the fossil record unequivocally demonstrates a first major radiation of angiosperms in the Early Cretaceous, the high diversity of these early angiosperms raises questions about their possible pre-Cretaceous evolutionary precursors. Also, most analyses of divergence time for angiosperms using molecular techniques have concluded that their ages are considerably older than those inferred directly from the fossil record [19]. However, there is no definite evidence of pre-Cretaceous angiosperms. Reticulate pollen from the Triassic [65,66] are from intriguing plant taxa that are potential angiosperm relatives, but unfortunately there are no macrofossil remains that can help to clarify the phylogenetic significance of these Triassic forms. Evidence from the history of other major clades of land plants suggests that the characteristic features of angioCurrent Opinion in Plant Biology 2005, 8:5–12
sperms were probably acquired sequentially through time. The recent ‘transitional-combinational theory’ of angiosperm origin [67] suggests an evolution of angiosperms from Jurassic seed ferns that occurred through three fundamental transitions: the evolution of the carpel, the emergence of double fertilisation and last the origin of the flower in the Early Cretaceous. However, no phylogenetic framework has been used to test this sequence of character evolution and improved palaeobotanical data are needed to pursue these ideas more rigorously. One genus that has received particular attention in discussions of angiosperm origin is the Mesozoic seed fern Caytonia [68,69]. The early assignment of Caytonia to angiosperms [70] made it an obvious object for further study. Palaeobotanically, however, Caytonia is among a multitude of extinct plants, most of which have not yet been studied in comparable detail. Some of the extraordinary diversity of extinct Mesozoic seed plants has recently been exposed in a comprehensive atlas of Late Triassic fructifications from the Molteno Formation of South Africa [71]. Some of these fossils are assignable to www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 9
previously known groups such as peltasperms, corystosperms and Bennettitales. However, the systematic position of many of these fossils is unknown and a more detailed study of this, and other material, is imperative for a better understanding of extinct seed plant diversity and relationships. The genus Archaefructus, with three species described from the Yixian Formation of north eastern China [15,72,73], has also been suggested as a possible angiosperm precursor or angiosperm stem group [15,67]. The age of the fossils has been disputed, but there is now strong support for a mid-Early Cretaceous age for the oldest horizons that contain Archaefructus [74,75]. Archaefructus fossils are exceptional in that they include specimens preserved as whole plants with roots, stems, leaves, flowers and fruits [73]. Archaefructus is an herbaceous plant with a habit that suggests an aquatic life-style. Carpels and stamens are borne either singly or in clusters of two or three on short common stalks along an elongated axis. Stamens are proximal whereas carpels are in a distal position. There are no traces of bracts or perianth parts and Sun et al. [15] interpreted the reproductive axis as a primitively naked, multiparted and bisexual flower. This interpretation is controversial and, alternatively, it has been suggested that Archaefructus is a crown-group angiosperm that has advanced, rather than primitive, floral features [16]. According to this interpretation Archaefructus was totally submerged and its reproductive axes were inflorescences with many small, simple and unisexual flowers that had lost perianth and bracts as an adaptation to underwater flowering. Recent observations of Archaefructus eoflora show a small bisexual flower comprising two carpels and one stamen between the staminate and pistillate zone [73]. This supports the inflorescence interpretation. However, although the Yixian fossils beautifully show features of general morphology, the preservation of details is typically obscured by pyrite infiltrations [42,76]. More information is clearly needed to provide a full understanding of the phylogenetic significance of Archaefructus.
The record of Cretaceous reproductive structures makes it clear that there has been considerable extinction within certain angiosperm lineages, and that the extant taxa constitute only a small proportion of the total diversity of the group. This raises questions about the extent to which phylogenetic analyses based on extant taxa that include these groups might have been distorted by uneven sampling introduced as a result of differential extinction. In terms of the earliest phases of angiosperm diversification, the presence of diverse angiosperm species that are difficult to link definitively with extant taxa raises the possibility that some of these groups might have diverged from the main line of angiosperm evolution at a level below the common ancestor of all extant taxa. Investigation of these taxa, as well as studies of extinct groups of gymnosperms from throughout the Mesozoic, will be important to identify potential stem-group angiosperms. Perhaps such investigation will also develop a clearer understanding of the sequence in which the defining characteristics of extant angiosperms were acquired.
Acknowledgements We acknowledge Pollyanna von Knorring for line drawings of fossil pollen and flowers and research grants from the Swedish Research Council (to EM Friis) and from the Carlsberg Foundation (to KR Pedersen).
References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1.
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Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V: Darwin’s abominable mystery: a supertree of the angiosperms. Proc Natl Acad Sci USA 2004, 101:1904-1909.
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Angiosperm Phylogeny Group: An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 2003, 141:399-436.
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Endress PK, Igersheim A: Gynoecium structure and evolution in basal angiosperms. Int J Plant Sci 2000, 161(6 Suppl.): S211-S223.
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Endress PK: The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci 2001, 162:1111-1140.
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Brenner GJ: The spores and pollen of the Potomac Group of Maryland. Md Dept Geol Mines Water Resour Bull 1963, 27:1-215.
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Doyle JA, Hickey LJ: Pollen and leaves from the midCretaceous Potomac Group and their bearing on early angiosperm evolution. In Origin and Early Evolution of Angiosperms. Edited by Beck CB. New York: Columbia University Press; 1976:139-206.
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Crane PR, Friis EM, Pedersen KR: The origin and early diversification of angiosperms. Nature 1995, 374:27-33.
Conclusions and future perspectives Information concerning fossil flowers that has been accumulated over the past two decades has provided a wealth of new data about the systematic diversity of Cretaceous angiosperms. Especially interesting are insights into the diversity of the group soon after its first appearance during the mid-Early Cretaceous. Even at this relatively early stage, angiosperms were diverse at the species level. However, most early angiosperm species cannot be attributed reliably to extant angiosperm clades. Instead, they appear to represent extinct lineages. According to analyses of molecular data from extant taxa, the few extant groups that can be recognized definitively at the family level or below are mainly taxa that belong to basal branches of the angiosperm phylogenetic tree. www.sciencedirect.com
10. Crepet WL: Timing in the evolution of derived floral characters: upper Cretaceous (Turonian) taxa with tricolpate and Current Opinion in Plant Biology 2005, 8:5–12
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tricolpate derived pollen. Rev Palaeobot Palynol 1996, 90:339-359. 11. Crepet WL: Progress in understanding angiosperm history, success, and relationships: Darwin’s abominably ‘‘perplexing phenomenon’’. Proc Natl Acad Sci USA 2000, 97:12939-12941. 12. Friis EM, Pedersen KR, Crane PR: Fossil floral structures of a basal angiosperm with monocolpate, reticulate-acolumellate pollen from the Early Cretaceous of Portugal. Grana 2000, 39:226-245. 13. Friis EM, Pedersen KR, Crane PR: Origin and radiation of angiosperms. In Palaeobiology II. Edited by Briggs DEG, Crowther PR. Oxford: Blackwell Science; 2001:97-102. 14. Dilcher DL: Palaeobotany: some aspects of non-flowering and flowering plant evolution. Taxon 2001, 50:697-711. 15. Sun G, Ji Q, Dilcher DL, Zheng S, Nixon KC, Wang X: Archaefructaceae, a new basal angiosperm family. Science 2002, 296:899-904. 16. Friis EM, Doyle JA, Endress PK, Leng Q: Archaefructus — angiosperm precursor or specialized early angiosperm? Trends Plant Sci 2003, 8:369-373. This work challenges the original interpretation of the Early Cretaceous Archaefructus as being a stem-group angiosperm with bisexual, multiparted flowers and suggests that Archaefructus is a crown-group angiosperm with advanced floral features that are adapted to a totally submerged life form rather than a stem-group angiosperm with primitive floral features. 17. Raynolds RG, Johnson KR: Synopsis of the stratigraphy and paleontology of the uppermost Cretaceous and lower Tertiary strata in the Denver Basin, Colorado. Rocky Mountain Geology 2003, 38:171-181. 18. Magallo´ n S, Sanderson MJ: Absolute diversification rates in angiosperm clades. Evolution 2001, 55:1762-1780. 19. Sanderson MJ, Doyle JA: Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Am J Bot 2001, 88:1499-1516. 20. Zhang L-B, Renner SS: The deepest splits in Chloranthaceae as resolved by chloroplast sequences. Int J Plant Sci 2003, 164:S383-S392. The authors analyse intra-Chloranthaceae relationships and phylogenetic biogeography based on a comprehensive DNA-sequence dataset. From the resulting phylogenetic tree and using two reference fossils as alternative calibration points, the authors infer mid- to late-Cainozoic divergence of extant species in this geologically old family. 21. Renner SS, Zhang L-B: Biogeography of the Pistia clade (Araceae): based on chloroplast and mitochondrial DNA sequences and Bayesian divergence time inference. Syst Biol 2004, 53:422-432. The phylogeny and age of the Pistia clade are investigated using molecular sequence data as well as multiple fossils and geological calibration points. The study provides an interesting discussion of temporal and spatial differentiation in the group and concludes that the clade extends far back into the Cretaceous.
26. Friis EM, Pedersen KR, Crane PR: Reproductive structure and organization of basal angiosperms from the Early Cretaceous (Barremian or Aptian) of Western Portugal. Int J Plant Sci 2000, 161(6 Suppl.):S169-S182. 27. Friis EM, Pedersen KR, Crane PR: Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous. Nature 2001, 410:357-360. 28. Scho¨ nenberger J, Pedersen KR, Friis EM: Normapolles flowers of fagalean affinity from the Late Cretaceous of Portugal. Pl Syst Evol 2001, 226:205-230. 29. Scho¨ nenberger J, Friis EM, Matthews ML, Endress PK: Cunoniaceae in the Cretaceous of Europe: evidence from fossil flowers. Ann Bot (Lond) 2001, 88:423-437. 30. Scho¨ nenberger J, Friis EM: Fossil flowers of ericalean affinity from the Late Cretaceous of Southern Sweden. Am J Bot 2001, 88:467-480. 31. Friis EM, Pedersen KR, Scho¨ nenberger J: Endressianthus, a new Normapolles producing plant genus of fagalean affinity from the Late Cretaceous of Portugal. Int J Plant Sci 2003, 164(5 Suppl.):S201-S223. Endressianthus is the most completely known Normapolles flower. It is excellently preserved and provides information on inflorescence structure, staminate and pistillate flowers, and pollen that give a better understanding of the Cretaceous diversification of Fagales. 32. Kvacˇ ek J, Eklund H: A report on newly recovered reproductive structures from the Cenomanian of Bohemia (Central Europe). Int J Plant Sci 2003, 194:1021-1039. Rich Cretaceous floras containing angiosperm leaves have long been known from the mid-Cretaceous of the Bohemian Massif. Recently, several angiosperm floral structures have also been reported from this classic area. The present work describes several new intriguing fossils pertinent to our understanding of Cretaceous angiosperm diversification. 33. Friis EM, Pedersen KR, Crane PR: Araceae from the Early Cretaceous of Portugal: evidence on the emergence of monocotyledons. Proc Natl Acad Sci USA 2004, 101:16565-16570. This study describes a unique polyplicate pollen from Portugal with distinctive features of the tribe Spathiphyllum (Araceae). It is significant in providing the first unequivocal evidence of monocots in the Early Cretaceous. 34. Herendeen PS, Magallo´ n-Puebla S, Lupia R, Crane PR, Kobylinska J: A preliminary conspectus of the Allon flora from the Late Cretaceous (late Santonian) of central Georgia, USA. Ann Mo Bot Gard 1999, 86:407-471. 35. Eklund H: Lauraceous flowers from the Late Cretaceous of North Carolina, USA. Bot J Linn Soc 2000, 132:397-428. 36. Gandolfo MA, Nixon KC, Crepet WL: Triuridaceae fossil flowers from the Upper Cretaceous of New Jersey. Am J Bot 2002, 89:1940-1957. 37. Hermsen EJ, Gandolfo MA, Nixon KC, Crepet WL: Divisestylus gen. nov. (aff. Iteaceae), a fossil saxifrage from the Late Cretaceous of New Jersey, USA. Am J Bot 2003, 90:1373-1388.
22. Renner SS, Zhang L-B, Murata J: A chloroplast phylogeny of Arisaema (Araceae) illustrates Tertiary floristic links between Asia, North America, and East Africa. Am J Bot 2004, 91:881-888.
38. Gandolfo MA, Nixon KC, Crepet WL: Cretaceous flowers of Nymphaeaceae and implications for complex insect entrapment pollination mechanisms in early angiosperms. Proc Natl Acad Sci USA 2004, 101:8056-8060.
23. Bremer K, Friis EM, Bremer B: Molecular phylogenetic dating of asterid flowering plants shows Early Cretaceous diversification. Syst Biol 2004, 53:496-505. This study presents a phylogenetic dating of the asterid clade using an 111-taxon asterid tree that represents all major clades of the group and six fossils as calibration points. Importantly, this study shows that the use of more reference fossils reduces variation in age estimates.
39. Frumin S, Friis EM: Magnoliid reproductive organs from the Cenomanian-Turonian of north-western Kazakhstan: Magnoliaceae and Illiciaceae. Pl Syst Evol 1999, 216:265-288.
24. Magallo´ n SA: Dating lineages: molecular and paleontological approaches to the temporal framework of clades. Int J Plant Sci 2004, 165:S7-S21. This work provides an excellent overview with up to date references of molecular and paleontological methods used in age estimates of clades. 25. Friis EM, Skarby A: Structurally preserved angiosperm flowers from the Upper Cretaceous of southern Sweden. Nature 1981, 291:485-486. Current Opinion in Plant Biology 2005, 8:5–12
40. Frumin S, Eklund H, Friis EM: Mauldinia hirsuta sp. nov., a new member of the extinct genus Mauldinia (Lauraceae) from the Late Cretaceous (Cenomanian-Turonian) of Kazakhstan. Int J Plant Sci 2004, in press. This work describes a new species of the extinct genus Mauldinia of the family Lauraceae from the mid-Cretaceous of Kazakhstan. The Sarbay flora is important as the oldest mesofossil flora from Asia and is crucial for understanding early angiosperm radition. 41. Takahashi M, Crane PR, Manchester SR: Hironoia fusiformis gen. et sp. nov.: a cornalean fruit from the Kamikitaba locality (Upper Cretecous, Lower Coniacian) in northeastern Japan. J Plant Res 2002, 115:463-473. www.sciencedirect.com
Floral evolution Friis, Pedersen and Crane 11
42. Leng Q, Friis EM: Sinocarpus decussatus gen. et sp. nov, a new angiosperm with syncarpous fruits from the Yixian Formation of Northeast China. Pl Syst Evol 2003, 241:77-88. The extinct genus Sinocarpus described in this work from the Early Cretaceous of north western China is significant in being the earliest fossil flower with a syncarpous gynoecium. Its distinct morphology indicates affinity with eudicots and shows that angiosperms in the Jehol Biota were diversified to some extent.
The authors provide a thorough analysis of morphological character evolution in both fossil and extant Chloranthaceae. There are many useful illustrations, mostly of reproductive features, and a comprehensive literature survey of fossil and living members of the group.
43. Maslova NP, Kodrul TM: New platanaceous inflorescence Archaranthus gen. nov. from the Maastrichtian-Paleocene of the Amur Region. Paleontological J 2003, 37:89-98.
61. Friis EM, Pedersen KR, Crane PR: Early angiosperm diversification: the diversity of pollen associated with angiosperm reproductive structures in Early Cretaceous floras from Portugal. Ann Mo Bot Gard 1999, 86:259-296.
44. Mohr B, Friis EM: Early angiosperms from the Aptian Crato Formation (Brazil), a preliminary report. Int J Plant Sci 2000, 161(6 Suppl.):S155-S167. 45. Mohr B, Eklund H: Araripia florifera, a magnoliid angiosperm from the Lower Cretaceous Crato Formation (Brazil). Rev Palaeobot Palynol 2003, 126:279-292. This paper provides the first formal description of an early angiosperm plant from the Crato Formation, Brazil. The material from this formation is significant in comprising whole-plant preservation. Araripia is a magnoliid plant with leaves and flowers attached to the same branching system. 46. Kennedy EM, Lovis JD, Daniel JL: Discovery of a Cretaceous angiosperm reproductive structure from New Zealand. New Zeal J Geol Geop 2003, 46:519-522. 47. Eklund H: First Cretaceous flowers from Antarctica. Rev Palaeobot Palynol 2003, 127:187-217. Most of the fossil flowers discovered in Cretaceous strata are from the Northern Hemisphere. This study is important in providing the first evidence from Antarctica of flowers that have an organization and structure comparable to contemporary flowers from other areas. 48. Bowe LG, Coat G, DePamphilis CW: Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci USA 2000, 97:4092-4097. 49. Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer JD: Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales and conifers. Proc Natl Acad Sci USA 2000, 97:4086-4091. 50. Bremer K: Early Cretaceous lineages of monocot flowering plants. Proc Natl Acad Sci USA 2000, 97:4707-4711. 51. Renner SS, Foreman DB, Murray D: Timing transacrtic disjunctions in the Atherospermataceae (Laurales): evidence from coding and noncoding chloroplast sequences. Syst Bot 2000, 49:579-591. 52. Wikstro¨ m N, Savolainen V, Chase MW: Evolution of the angiosperms. Calibrating the tree. Proc R Soc Lond B Biol Sci 2001, 268:2211-2220. 53. Chaw SM, Chang CC, Chen HL, Li WH: Dating the monocot– dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 2004, 58:424-441. 54. Sanderson MJ: Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 2002, 19:101-109. 55. Crane PR, Herendeen P, Friis EM: Fossils and plant phylogeny. Am J Bot 2004, 91:1684-1699. 56. Crane PR, Lidgard S: Angiosperm diversification and palaeolatitudinal gradients in Cretaceous floristic diversity. Science 1989, 246:675-678. 57. Magallo´ n S, Crane PR, Herendeen PS: Phylogenetic pattern, diversity and diversification of eudicots. Ann Mo Bot Gard 1999, 86:297-372. 58. Friis EM, Crane PR, Pedersen KR: Fossil history of magnoliid angiosperms. In Evolution and Diversification of Land Plants. Edited by Iwatsuki K, Raven PH. New York: Springer Verlag; 1997:121-156. 59. Eklund H, Doyle JA, Herendeen PS: Morphological phylogenetic analysis of living and fossil Chloranthaceae. Int J Plant Sci 2003, 165:107-151. www.sciencedirect.com
60. Walker JW, Walker AG: Ultrastructure of Lower Cretaceous angiosperm pollen and the origin and early evolution of flowering plants. Ann Mo Bot Gard 1984, 71:464-521.
62. Rydin C, Pedersen KR, Friis EM: On the evolutionary history of Ephedra; Cretaceous fossils and extant molecules. Proc Natl Acad Sci USA 2004, 101:16571-16576. This study describes exceptionally well-preserved seeds with distinctive characters of Ephedra from the Early Cretaceous of Portugal and discusses the finding based on a molecular phylogeny. The finding demonstrates that modern species of Ephedra have retained unique reproductive features, including the peculiar naked male gametophyte, for more than 110 million years. It also highlights the apparent conflict between molecular dating of crown-group Ephedra and the fossil record. 63. Friis EM: Upper Cretaceous (Senonian) floral structures of juglandalean affinity containing Normapolles pollen. Rev Palaeobot Palynol 1983, 39:161-188. 64. Sims HJ, Herendeen PS, Lupia R, Christopher RA, Crane PR: Fossil flowers with Normapolles pollen from the Late Cretaceous of southeastern North America. Rev Palaeobot Palynol 1999, 106:131-151. 65. Hochuli PA, Colin JP, Vigran JO: Triassic biostratigraphy of the Barents Sea area. In Correlation in Hydrocarbon Exploration. Edited by Collinson JD. London: Norwegian Petroleum Society (Graham & Trotman); 1989:131-153. 66. Cornet B: Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia, U.S.A. Palaeontogr B 1989, 213:37-87. 67. Stuessy TF: A transitional-combinational theory for the origin of angiosperms. Taxon 2004, 53:3-16. 68. Gaussen H: Les Gymnospermes, actuelles et fossiles. Trav Lab for Toulouse T II 1946, 1:1-130. 69. Doyle JA: Origin of the angiosperm flower: a phylogenetic perspective. Plant Syst Evol 1994, 8:7-29. 70. Thomas HH: The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philos Trans R Soc Lond B Biol Sci 1925, 213:299-363. 71. Anderson JM, Anderson HM: Heyday of the gymnosperms: systematics and biodiversity of the Late Triassic Molteno fructifications Pretoria: National Botanical Institute; 2003:1-398. This article is the result of more than 35 years field work and study of plant fossils from the Molteno Formation. It describes one of the most extensive collections of Mesozoic seed plant fructifications and describes an unexpected and extraordinary diversity in reproductive structures of extinct seed plants. 72. Sun G, Dilcher DL, Zheng S, Zhou Z: In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science 1998, 282:1692-1695. 73. Ji Q, Li H, Bowe LM, Liu Y, Taylor DW: Early Cretaceous Archaefructus eoflora sp. nov., with bisexual flowers from Beipiao, Western Liaoning, China. Acta Geologica Sinica 2004, 78:883-896. The paper provides a description of a new Early Cretaceous species of Archaefructus preserved as a whole plant with roots, stems, leaves, flowers and fruits. Although anatomical and fine morphological details are poorly preserved, this fossil shows excellent gross morphological features and is significant in our understanding of the early angiosperm habit. 74. Zhou Z, Barrett PM, Hilton J: An exceptionally preserved Lower Cretaceous ecosystem. Nature 2003, 421:807-814. This review paper provides a critical overview of the Jehol Biota with particular focus on the stratigraphy and palaeoenvironmental setting. The fossil plants are also discussed briefly and the authors suggest a possible pteridospermous nature of the Archaefructus plant. Current Opinion in Plant Biology 2005, 8:5–12
12 Growth and development
75. Chang M-m, Chen P-j, Wang Y-q, Wang Y, Mioa D-s (Eds): The Jehol Biota. Series. Shanghai: Shanghai Scientific and Technical Publishers; 2003. This book includes a collection of articles summarizing current knowledge of the Jehol Biota, from insects to angiosperms. It includes high-quality illustrations of the fossils as well as many excellent reconstructions. It also provides a broad overview of geology and stratigraphy of this important
Current Opinion in Plant Biology 2005, 8:5–12
Mesozoic ecosystem. The book is written for non-specialists but is based on strict scientific criteria. 76. Leng Q, Yang H: Pyrite framboids associated with the Mesozoic Jehol Biota in northeastern China: implications for microenvironment during early fossilization. Prog Nat Sci 2003, 13:206-212.
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