Summary
The following figure is a summarized phylogenetic tree for the flowering plants, or angiosperms, showing which branches of the tree are associated with transitional fossils. The remarkable thing is that there are so few. As will be seen in the following sections, the full tree has many more branches than shown here, and none of those additional branches is associated with transitional fossils.
Introduction
The angiosperms, or flowering plants, formally known as the Magnoliopsida (Thorne and Reveal, 2007), are vascular plants in which the seeds develop from fertilization of the ovule, or egg, within an enclosed hollow ovary. The ovary itself is usually enclosed in a flower, that part of the angiospermous plant that contains the male or female reproductive organs or both. This is in contrast to the reproductive system of the gymnosperms, in which the seeds are generally borne exposed on the surfaces of reproductive structures such as cones (Encyclopædia Britannica).
Angiosperms dominate the plant world. Their approximately 300,000 species represent about 80% of all extant green plants (Encyclopædia Britannica).
A recent phylogenetic tree of the extant angiosperms is shown below:
Angiosperms dominate the plant world. Their approximately 300,000 species represent about 80% of all extant green plants (Encyclopædia Britannica).
A recent phylogenetic tree of the extant angiosperms is shown below:
As usual, the black dot represents a crown node. Note that the Gnetales are not associated with a crown node because they belong to the paraphyletic gymnosperms; in contrast the angiosperms are monophyletic and have their own crown node.
The full phylogenetic tree from which the above figure is summarized is shown below down to the level of the order:
The full phylogenetic tree from which the above figure is summarized is shown below down to the level of the order:
The evolutionary origin of the angiosperms has been subject to debate from the time of Darwin up to the present day. Darwin’s statement in 1879 that “The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery” (quoted in Friedman, 2009) remains largely unresolved even today. Even though Darwin’s “abominable mystery” applied not to the origin of the angiosperms but to their rapid diversification during the Early Cretaceous (Friedman, 2009), the phrase has commonly been used to express the continuing difficulty of tracing the origin of the flowering plants in the fossil record (Bateman, 2020). This difficulty is represented by a gap in the fossil record between the earliest angiosperm fossils in the Early Cretaceous and the molecular clock estimates based on DNA sequencing of an origin in the Triassic (Bateman, 2020).
We will now document the nature of this apparent lack of transitional fossils. This gap in the fossil record is expressed as following:
Thus it appears to be the case that neither the origin of the angiosperm clade (as would be represented by stem-group angiosperms) nor that of the great majority of angiosperm orders can be documented in the fossil record.
The fossil data that are available will now be summarized.
We will now document the nature of this apparent lack of transitional fossils. This gap in the fossil record is expressed as following:
- There is no consensus in the literature on the existence of stem-group angiosperms, monocots or pentamerous flowers (Pentapetalae);
- Stem-group eudicots have been recognized in the form of tricolpate pollen grains (see below);
- Stem-group representatives have been recognized for only four orders (Nymphaeales, Trochodendrales, Buxales and Fagales) out of the 64 known angiosperm orders.
Thus it appears to be the case that neither the origin of the angiosperm clade (as would be represented by stem-group angiosperms) nor that of the great majority of angiosperm orders can be documented in the fossil record.
The fossil data that are available will now be summarized.
Angiosperm origin
As mentioned above, no fossil has been accepted with consensus in the literature as a stem-group angiosperm. The oldest known crown-group fossil is represented by pollen grains with columellar and perforate to reticulate wall structure in Early Cretaceous (late Valanginian to Hauterivian) sediments in Israel and England (Magallón et al, 2015). No images of these pollen grains are available in the public domain, but the images below, of extant pollen, illustrate the meaning of the terminology of pollen morphology (click on image for larger view):
Some pollens from the Triassic have been suggested to be more closely related to the angiosperms than the gymnosperms (e.g. Hochuli and Feist-Burkhardt, 2013), but these have not been demonstrated to have the wall structure characteristic of angiosperms (Coiro et al, 2019).
As demonstrated by Coiro et al (2019), no pollen with definite angiosperm affinities have been described from the time interval between these Triassic examples and the Late Valanginian crown-angiosperm pollen mentioned above. Given that gymnosperm pollen are well known throughout the Jurassic and pre-Valanginian, this absence of angiosperm pollen almost certainly indicates that the crown-group did not appear before the Valanginian (Donoghue, 2019).
As demonstrated by Coiro et al (2019), no pollen with definite angiosperm affinities have been described from the time interval between these Triassic examples and the Late Valanginian crown-angiosperm pollen mentioned above. Given that gymnosperm pollen are well known throughout the Jurassic and pre-Valanginian, this absence of angiosperm pollen almost certainly indicates that the crown-group did not appear before the Valanginian (Donoghue, 2019).
Monocots
Wheat - a modern monocot
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The monocots, or monocotyledons, are one of the two major groups of angiosperms, the other being the eudicotelydons. They are distinguished from the latter by having only a single seed leaf, or cotyledon, in the embryo contained in the seed (Encyclopædia Britannica). As for the angiosperm lineage, monocots have no known stem-group representatives. The earliest known crown-group monocot is represented by pollen grains assigned to Mayoa portugallica, described from a locality at Torres Vedras in Portugal, considered to be of late Barremian to early Aptian age (Foster et al, 2017; Magallón et al, 2015). Again, no public-domain image is available.
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Eudicots
Blue jacaranda seedling - a modern eudicot
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The eudicots, or eudicotyledons, have a pair of leaves, or cotyledons, in the embryo of the seed (Encyclopædia Britannica). Several stem-group representatives have been proposed:
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No images of the above fossils are available in the public domain, but some examples of tricolpate extant pollen are illustrated below:
The oldest known crown-group eudicot is Leefructus mirus, described from the Early Cretaceous (Barremian to Aptian) Daxinfangzi Bed of the Yixian Formation at the Dawangzhangzi locality in Lingyuan, Liaoning Province, China (Sun et al, 2011; Janssens et al, 2020). No public-domain image of this fossil is available.
Pentapetalae
Rose (Rosa uchiyamane) - a modern member of Pentapetalae
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No stem-group fossils of this clade are known. The oldest known member of the crown group was originally described as an unnamed pentamerous fossil flower from the Early Cretaceous (latest Albian) Dakota Formation at the Rose Creek locality in Nebraska, USA (Basinger and Dilcher, 1984; Magallón et al, 2015) but has been recently named as Dakotanthus cordiformis (Manchester et al, 2018). Some images are shown below:
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Nympheales
Water lily (Nymphaea alba) - a modern member of Nympheales
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The Nympheales (water lilies and related plants) are an order in the basal angiosperms (see phylogenetic tree above). The only fossil accepted as a member of the stem-Nympheales is Carpestella lacunata, described from the Early Cretaceous (Early Albian) Patapsco Formation at the Puddledock locality, Virginia, USA (von Balthazar et al, 2008; Hertweck et al, 2015). No image is available in the public domain.
In terms of the crown group, the oldest known fossil is Monetianthus mirus, described from the Early Cretaceous (Late Aptian to Early Albian) basal part (Famalicão Member) of the Figueira da Foz Formation near the village of Vale de Agua in western Portugal (Friis et al, 2009; Magallón et al, 2015). Again, no public-domain image is available. |
Trochodendrales
Trochodendron aralioides - a modern member of Trochodendrales
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The Trochodendrales (the wheel tree and related trees) are an order in the basal eudicots (see phylogenetic tree above). The only fossil recognized as a member of the stem group is Nordenskioldia borealis, described from many localities of Late Cretaceous and Paleogene of Asia, the Arctic and Western North America (Magallón et al, 2015). However, the specimens collected by Edouard von Toll in 1886 from Late Cretaceous sediments on the southern coast of New Siberia Island in Arctic Russia are now thought to be of Turonian – Coniacian age (Herman and Domogatskaya, 2020). No image is available in the public domain.
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The age of the oldest member of the crown-Trochodendrales is unknown because none of the fossils described to date have been assigned to the crown group.
Buxales
Buxus microphylla var. sinica - a modern member of Buxales
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The Buxales (boxwoods and related trees and shrubs) are another order in the basal eudicots (see phylogenetic tree above). The only stem-group member is Spanomera marylandensis, described from the Late Cretaceous (Late Albian) Patapsco Formation of the Potomac Group at the West Brothers Pit in Maryland near Washington DC, USA (Drinnan et al, 1991; Magallón et al, 2015). Again, no public-domain image is available.
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As for the Trochodendrales, the age of the earliest member of crown-Buxales is unknown owing to lack of published assignment to the crown group.
Fagales
Birches - a modern member of Fagales
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The Fagales (beeches, birches, walnuts and some other well-known trees) are an order in the Fabids, a clade within the core eudicots (see phylogenetic tree above). Two fossils have been identified as stem-Fagales: Archaefagaceae futabensis (Magallón et al, 2015) and Protofagacea allonensis (Foster et al, 2017). They are both of Late Cretaceous age, but A. futabensis is slightly older (Early Coniacian) than P. allonensis (Early Santonian). A. futabensis is described from the Asamigawa Member of the Ashizawa Formation of the Futaba Group along a tributary of the Kitaba River in Kamikitaba, northeastern Honshu, Japan (Takahashi et al, 2008). No public-domain images are available either for Archaefagaceae futabensis or Protofagacea allonensis.
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The oldest known member of the crown-Fagales is Caryanthus triasseris, described from the Late Cretaceous (Middle Cenomanian) Peruc Member of the Peruc-Korycany Formation at Vyšehořovice in the Czech Republic (Kvaček, 2017; Beaulieu et al, 2015). Again, no image is available in the public domain.
Note that the oldest crown-group Fagales is older than the oldest stem-group member. This means that the stem-group fossil tells us nothing about the duration of the stem-to-crown transition.
Note that the oldest crown-group Fagales is older than the oldest stem-group member. This means that the stem-group fossil tells us nothing about the duration of the stem-to-crown transition.
Synthesis
The manner in which the fossil data outlined above constrain the evolutionary history of the angiosperms is expressed in a phylogenetic time tree, broken into two parts, in the figure below:
Owing to the extreme scarcity of stem-group fossils, the above tree is very poorly constrained. However, it does indicate that the crown angiosperms and the crown groups of many of the orders basal to the core eudicots (i.e. more basal than the Gunnerales) appeared before the end of the Early Cretaceous. Furthermore, even though some of the core-eudicot orders might not have appeared before the Cenozoic, the crown-group ages do imply very rapid branching within the Superrosids (Saxifragales to Malvales) during the latest Early Cretaceous and earliest Late Cretaceous.
In conclusion, the fact that almost all of the angiosperm orders, as well as the angiosperms themselves, appear first as crown-group but not stem-group fossils indicates that Darwin’s “abominable mystery” remains largely unresolved even to this day.
In conclusion, the fact that almost all of the angiosperm orders, as well as the angiosperms themselves, appear first as crown-group but not stem-group fossils indicates that Darwin’s “abominable mystery” remains largely unresolved even to this day.
References
Basinger, J. F., & Dilcher, D. L. (1984). Ancient bisexual flowers. Science, 224(4648), 511-513.
Bateman, R. M. (2020). Hunting the Snark: the flawed search for mythical Jurassic angiosperms. Journal of Experimental Botany, 71(1), 22-35.
Beaulieu, J. M., O'Meara, B. C., Crane, P., & Donoghue, M. J. (2015). Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Systematic biology, 64(5), 869-878.
Chase, M. W., Christenhusz, M. J. M., Fay, M. F., Byng, J. W., Judd, W. S., Soltis, D. E., ... & Stevens, P. F. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181(1), 1-20.
Coiro, M., Doyle, J. A., & Hilton, J. (2019). How deep is the conflict between molecular and fossil evidence on the age of angiosperms?. New Phytologist, 223(1), 83-99.
Donoghue, P. (2019). Evolution: the flowering of land plant evolution. Current Biology, 29(15), R753-R756.
Drinnan, A. N., Crane, P. R., Friis, E. M., & Pedersen, K. R. (1991). Angiosperm flowers and tricolpate pollen of buxaceous affinity from the Potomac Group (mid‐Cretaceous) of eastern North America. American Journal of Botany, 78(2), 153-176.
Foster, C. S., Sauquet, H., Van der Merwe, M., McPherson, H., Rossetto, M., & Ho, S. Y. (2017). Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Systematic Biology, 66(3), 338-351.
Friis, E. M., Pedersen, K. R., von Balthazar, M., Grimm, G. W., & Crane, P. R. (2009). Monetianthus mirus gen. et sp. nov., a nymphaealean flower from the Early Cretaceous of Portugal. International Journal of Plant Sciences, 170 (8), 1086-1101.
Friedman, W. E. (2009). The meaning of Darwin's “abominable mystery”. American Journal of Botany, 96(1), 5-21.
Herman, A. B., & Domogatskaya, K. V. (2020). The Late Cretaceous flora of the New Siberia Island (Arctic Russia): E. von Toll's and JT Schmalhausen's palaeobotanical heritage revisited. Cretaceous Research, 108, 104346.
Hertweck, K. L., Kinney, M. S., Stuart, S. A., Maurin, O., Mathews, S., Chase, M. W., ... & Pires, J. C. (2015). Phylogenetics, divergence times and diversification from three genomic partitions in monocots. Botanical Journal of the Linnean Society, 178(3), 375-393.
Hochuli, P. A., & Feist-Burkhardt, S. (2013). Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (northern Switzerland). Frontiers in plant science, 4, 344.
Janssens, S. B., Couvreur, T. L., Mertens, A., Dauby, G., Dagallier, L. P. M., Abeele, S. V., ... & Droissart, V. (2020). A large-scale species level dated angiosperm phylogeny for evolutionary and ecological analyses. Biodiversity data journal, 8.
Kvaček, J. (2017). Late Cretaceous Floras in Central Europe and their palaeoenvironment. Thesis, Charles University, Prague.
Magallón, S., Gómez‐Acevedo, S., Sánchez‐Reyes, L. L., & Hernández‐Hernández, T. (2015). A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, 207 (2), 437-453.
Manchester, S. R., Dilcher, D. L., Judd, W. S., Corder, B., & Basinger, J. F. (2018). Early Eudicot flower and fruit: Dakotanthus gen. nov. from the Cretaceous Dakota Formation of Kansas and Nebraska, USA. Acta Palaeobotanica, 58(1), 27-40.
Sun, G., Dilcher, D. L., Wang, H., & Chen, Z. (2011). A eudicot from the Early Cretaceous of China. Nature, 471(7340), 625-628.
Takahashi, M., Friis, E. M., Herendeen, P. S., & Crane, P. R. (2008). Fossil flowers of Fagales from the Kamikitaba locality (early Coniacian; Late Cretaceous) of northeastern Japan. International Journal of Plant Sciences, 169(7), 899-907.
Thorne, R. F., & Reveal, J. L. (2007). An updated classification of the class Magnoliopsida (“Angiospermae”). The Botanical Review, 73(2), 67.
von Balthazar, M., Pedersen, K. R., Crane, P. R., & Friis, E. M. (2008). Carpestella lacunata gen. et sp. nov., a new basal angiosperm flower from the Early Cretaceous (Early to Middle Albian) of eastern North America. International Journal of Plant Sciences, 169(7), 890-898.
Bateman, R. M. (2020). Hunting the Snark: the flawed search for mythical Jurassic angiosperms. Journal of Experimental Botany, 71(1), 22-35.
Beaulieu, J. M., O'Meara, B. C., Crane, P., & Donoghue, M. J. (2015). Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Systematic biology, 64(5), 869-878.
Chase, M. W., Christenhusz, M. J. M., Fay, M. F., Byng, J. W., Judd, W. S., Soltis, D. E., ... & Stevens, P. F. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181(1), 1-20.
Coiro, M., Doyle, J. A., & Hilton, J. (2019). How deep is the conflict between molecular and fossil evidence on the age of angiosperms?. New Phytologist, 223(1), 83-99.
Donoghue, P. (2019). Evolution: the flowering of land plant evolution. Current Biology, 29(15), R753-R756.
Drinnan, A. N., Crane, P. R., Friis, E. M., & Pedersen, K. R. (1991). Angiosperm flowers and tricolpate pollen of buxaceous affinity from the Potomac Group (mid‐Cretaceous) of eastern North America. American Journal of Botany, 78(2), 153-176.
Foster, C. S., Sauquet, H., Van der Merwe, M., McPherson, H., Rossetto, M., & Ho, S. Y. (2017). Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Systematic Biology, 66(3), 338-351.
Friis, E. M., Pedersen, K. R., von Balthazar, M., Grimm, G. W., & Crane, P. R. (2009). Monetianthus mirus gen. et sp. nov., a nymphaealean flower from the Early Cretaceous of Portugal. International Journal of Plant Sciences, 170 (8), 1086-1101.
Friedman, W. E. (2009). The meaning of Darwin's “abominable mystery”. American Journal of Botany, 96(1), 5-21.
Herman, A. B., & Domogatskaya, K. V. (2020). The Late Cretaceous flora of the New Siberia Island (Arctic Russia): E. von Toll's and JT Schmalhausen's palaeobotanical heritage revisited. Cretaceous Research, 108, 104346.
Hertweck, K. L., Kinney, M. S., Stuart, S. A., Maurin, O., Mathews, S., Chase, M. W., ... & Pires, J. C. (2015). Phylogenetics, divergence times and diversification from three genomic partitions in monocots. Botanical Journal of the Linnean Society, 178(3), 375-393.
Hochuli, P. A., & Feist-Burkhardt, S. (2013). Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (northern Switzerland). Frontiers in plant science, 4, 344.
Janssens, S. B., Couvreur, T. L., Mertens, A., Dauby, G., Dagallier, L. P. M., Abeele, S. V., ... & Droissart, V. (2020). A large-scale species level dated angiosperm phylogeny for evolutionary and ecological analyses. Biodiversity data journal, 8.
Kvaček, J. (2017). Late Cretaceous Floras in Central Europe and their palaeoenvironment. Thesis, Charles University, Prague.
Magallón, S., Gómez‐Acevedo, S., Sánchez‐Reyes, L. L., & Hernández‐Hernández, T. (2015). A metacalibrated time‐tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist, 207 (2), 437-453.
Manchester, S. R., Dilcher, D. L., Judd, W. S., Corder, B., & Basinger, J. F. (2018). Early Eudicot flower and fruit: Dakotanthus gen. nov. from the Cretaceous Dakota Formation of Kansas and Nebraska, USA. Acta Palaeobotanica, 58(1), 27-40.
Sun, G., Dilcher, D. L., Wang, H., & Chen, Z. (2011). A eudicot from the Early Cretaceous of China. Nature, 471(7340), 625-628.
Takahashi, M., Friis, E. M., Herendeen, P. S., & Crane, P. R. (2008). Fossil flowers of Fagales from the Kamikitaba locality (early Coniacian; Late Cretaceous) of northeastern Japan. International Journal of Plant Sciences, 169(7), 899-907.
Thorne, R. F., & Reveal, J. L. (2007). An updated classification of the class Magnoliopsida (“Angiospermae”). The Botanical Review, 73(2), 67.
von Balthazar, M., Pedersen, K. R., Crane, P. R., & Friis, E. M. (2008). Carpestella lacunata gen. et sp. nov., a new basal angiosperm flower from the Early Cretaceous (Early to Middle Albian) of eastern North America. International Journal of Plant Sciences, 169(7), 890-898.
Image credits - Angiosperms
- Header: Specially sown pasture next to the N276 road in Brunssum, Netherlands. By Maurice van Bruggen / CC BY-SA (https://creativecommons.org/licenses/by-sa/3.0)
- Pollen images 1,2 and 3: From open-access book (Halbritter, H., Ulrich, S., Grímsson, F., Weber, M., Zetter, R., Hesse, M., … & Frosch-Radivo, A. (2018). Illustrated pollen terminology, Second Edition, Springer) licensed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).
- Close-up of wheat: By Bluemoose / CC BY-SA (http://creativecommons.org/licenses/by-sa/3.0/)
- Blue jacaranda seedling: By Martin Bahmann, licensed under the Creative Commons Attribution-Share Alike 3.0 Unported license
- Tricolpate pollen grains (pollen images 4): From open-access book (Halbritter, H., Ulrich, S., Grímsson, F., Weber, M., Zetter, R., Hesse, M., ... & Frosch-Radivo, A. (2018). Illustrated pollen terminology, Second Edition, Springer) licensed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/).
- Rose (Rosa uchiyamane): By Sakurai Midori / CC BY-SA 2.1 JP (https://creativecommons.org/licenses/by-sa/2.1/jp/deed.en)
- Dakotanthus cordiformis: From open-access article (Manchester, S. R., Dilcher, D. L., Judd, W. S., Corder, B., & Basinger, J. F. (2018). Early Eudicot flower and fruit: Dakotanthus gen. nov. from the Cretaceous Dakota Formation of Kansas and Nebraska, USA. Acta Palaeobotanica, 58(1), 27-40) licensed under Attribution-NonCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND 3.0).
- Water lily (Nymphaea alba): By Jacek Halicki / CC BY-SA (https://creativecommons.org/licenses/by-sa/4.0)
- Trochodendron aralioides flowers, Botanical Garden, Århus, Denmark: By Sten / CC BY-SA (https://creativecommons.org/licenses/by-sa/3.0)
- Buxus microphylla var. sinica: By Sten Porse / CC BY-SA (http://creativecommons.org/licenses/by-sa/3.0/)
- Birches, Novosibirsk, Russia, November 2008: By Brian Jeffery Beggerly / CC BY (https://creativecommons.org/licenses/by/2.0)