Introduction
The “bryophytes” are non-vascular seedless plants that have an alternation of generations between the independent gametophyte generation, which produces the sex organs and the sperm and eggs, and the dependent sporophyte generation, which produces the spores (Encyclopaedia Britannica). They comprise the mosses, liverworts and hornworts.
There has been much debate about phylogenetic relationships within the bryophytes (see discussion in Morris et al, 2018). The main issue is whether the mosses, liverworts and hornworts form a monophyletic group. This debate has led to confusion in nomenclature; the term “Bryophyta” has been used as a synonym for mosses as well as a name for the mosses, liverworts and hornworts taken together. Here we follow recent research (e.g. de Sousa et al, 2019) that presents evidence for bryophyte monophyly, as shown in the following phylogenetic tree:
There has been much debate about phylogenetic relationships within the bryophytes (see discussion in Morris et al, 2018). The main issue is whether the mosses, liverworts and hornworts form a monophyletic group. This debate has led to confusion in nomenclature; the term “Bryophyta” has been used as a synonym for mosses as well as a name for the mosses, liverworts and hornworts taken together. Here we follow recent research (e.g. de Sousa et al, 2019) that presents evidence for bryophyte monophyly, as shown in the following phylogenetic tree:
As usual, the node of the crown group is represented by a black dot.
Given that the term Bryophyta is established as a phylum name for the mosses (Ruggiero et al, 2015), we will use the informal term “bryophytes” here. The bryophytes comprise a sister group to the vascular plants, or Tracheophyta, as shown in the following phylogenetic tree:
Given that the term Bryophyta is established as a phylum name for the mosses (Ruggiero et al, 2015), we will use the informal term “bryophytes” here. The bryophytes comprise a sister group to the vascular plants, or Tracheophyta, as shown in the following phylogenetic tree:
The above tree is constrained by the ages of the few pre-Cenozoic fossils that represent the taxa shown. The oldest known stem-bryophyte is Tetrahedraletes cf. medinensis, a spore described from the Middle Ordovician (Dapingian) Zanjón Formation at the Rio Capillas outcrop, southern part of the Sierra de Zapla of the Subandean Ranges in north‐western Argentina (Rubinstein et al, 2010; Edwards et al, 2020). No image is available in the public domain. The earliest known crown-group bryophyte is the Early Devonian crown liverwort Riccardiothallus devonicus, which will be discussed below in the section on liverworts.
These data indicate that the crown group of the bryophytes appeared some time between the middle of the Ordovician and the early Devonian (an uncertainty range of 63 million years), and that the vascular plants have a ghost lineage resulting in the difference in times of first appearance of the stem-Bryophyta and the stem-group vascular plants (39 million years). Another interesting point about the above tree is that the oldest known crown-hornwort (Early Cretaceous) is much younger than the oldest known members of the liverwort and moss crown groups, even though the hornworts were apparently the first of the three bryophyte groups to split off.
These data indicate that the crown group of the bryophytes appeared some time between the middle of the Ordovician and the early Devonian (an uncertainty range of 63 million years), and that the vascular plants have a ghost lineage resulting in the difference in times of first appearance of the stem-Bryophyta and the stem-group vascular plants (39 million years). Another interesting point about the above tree is that the oldest known crown-hornwort (Early Cretaceous) is much younger than the oldest known members of the liverwort and moss crown groups, even though the hornworts were apparently the first of the three bryophyte groups to split off.
Evolution of the mosses
Mosses (Division Musci in superphylum Embryophyta) are small non-vascular land plants that are commonly found in damp and shady locations. More than 12,000 species exist (Shaw et al, 2005). Their anatomy comprises three structures: a root-like rhizoid which anchors the plant; a leafy stem representing the gametophyte stage, in which sexual reproduction occurs; and a stalk and sporangium representing the asexual reproduction stage that generates spores which can germinate to form a new plant. Sporangia can be seen in the header photograph above.
A recent phylogenetic tree of the extant mosses is summarized below:
A recent phylogenetic tree of the extant mosses is summarized below:
The fossil record of the mosses is quite sparse (Shelton et al, 2015), and many of the terminal clades shown above are not known as fossils. Furthermore, no stem-group mosses have been identified (Kenrick, 2000); the only constraint we have on the age of the earliest stem-group moss is that it cannot have been greater than that of the first appearance of the stem-Bryophyta around the middle of the Ordovician.
The oldest known crown moss (and crown-Sphagnophytina) is represented by Carboniferous fossils assigned to the order Sphagnales by Hübers and Kerp (2012). They were found in the upper part of the Visean (Early Carboniferous) Ortelsdorf Formation in a roadcut of the A4 motorway near Chemnitz-Glösa, Saxony, Germany (Morris et al, 2018). No public-domain images are available, but an example of a modern member of the Sphagnophytina crown group is shown below:
The oldest known crown moss (and crown-Sphagnophytina) is represented by Carboniferous fossils assigned to the order Sphagnales by Hübers and Kerp (2012). They were found in the upper part of the Visean (Early Carboniferous) Ortelsdorf Formation in a roadcut of the A4 motorway near Chemnitz-Glösa, Saxony, Germany (Morris et al, 2018). No public-domain images are available, but an example of a modern member of the Sphagnophytina crown group is shown below:
The time of first appearance of the crown-Sphagnophytina and of other subordinate crown groups within the moss crown group is shown in the following time tree:
The above time tree indicates that the crown group of the mosses appeared no later than the middle of the Carboniferous. However, in the absence of stem-group moss fossils, the timing of appearance of the stem-group is constrained only by the appearance of the stem-Bryophyta (the spore Tetrahedraletes cf. medinensis) in the middle of the Ordovician; this implies an uncertainty of around 139 million years in the timing of appearance of the crown-group mosses.
The evolution of the crown-group mosses cannot be traced further because no stem group representatives have been found for any of the clades shown. One Early Permian fossil, Palaeocampylopus buragoae, has been suggested to be a stem-Polytrichopsida (Laenen et al, 2014) but no reasons were given for this assignment, and it was questioned by Bippus et al (2017). For this reason, that fossil will not be considered here as a stem-Polytrichopsida.
The evolution of the crown-group mosses cannot be traced further because no stem group representatives have been found for any of the clades shown. One Early Permian fossil, Palaeocampylopus buragoae, has been suggested to be a stem-Polytrichopsida (Laenen et al, 2014) but no reasons were given for this assignment, and it was questioned by Bippus et al (2017). For this reason, that fossil will not be considered here as a stem-Polytrichopsida.
Evolution of the liverworts
Liverworts (Division Marchantiophyta in superphylum Embryophyta), like mosses, are small non-vascular plants that have a life cycle comprising gametophyte and sporophyte stages. Around 7,500 species of liverworts are known in the world today (von Konrat et al, 2014). Liverworts fall into two broad categories: the leafy liverworts, in which the gametophyte consists of leaves on stems, and the thallose liverworts whose gametophyte comprises a flattish, possibly wrinkled or lobed, green sheet, or thallus (Australian National Botanic Gardens website). The photographs below depict a leafy liverwort on the left and a thallose liverwort on the right (click on image for a larger view):
A phylogenetic tree of the extant liverworts, somewhat dated but consistent with more recent work, is summarized below:
The leafy liverworts belong to the order Jungermanniales, while all the other liverwort clades have thallose forms.
The fossil record of the liverworts is quite sparse (Wilson et al, 2007), and many of the terminal clades shown above are not known as fossils. Furthermore, no stem-group liverworts have been identified (Kenrick, 2000); the only constraint we have on the age of the earliest stem-group liverwort is that it cannot have been greater than that of the first appearance of the stem-Bryophyta around the middle of the Ordovician.
The oldest known crown liverwort is Riccardiothallus devonicus, found in the Early Devonian (Pragian) Posongchong Formation at Zhichang Village, Gumu Town, Wenshan District, Yunnan Province, China (Guo et al, 2012). According to these authors, the fossil belongs to family Aneuraceae in the order Metzgeriales (in subclass Metzgeriidae), but Morris et al (2018) more conservatively assign it only to the “Jungermanniopsida group”. It is not clear whether they mean stem-, crown- or total-Jungermanniopsida, but given the higher-level assignment of Guo et al, we shall consider it as a representative of the crown-Jungermanniopsida. No image of Riccardiothallus is available in the public domain.
In fact, the only public-domain image available for fossils of the liverwort crown group is from Radula cretacea, a member of the crown-Porellales from mid-Cretaceous amber in Myanmar (Bechteler et al, 2017) (click to enlarge):
The fossil record of the liverworts is quite sparse (Wilson et al, 2007), and many of the terminal clades shown above are not known as fossils. Furthermore, no stem-group liverworts have been identified (Kenrick, 2000); the only constraint we have on the age of the earliest stem-group liverwort is that it cannot have been greater than that of the first appearance of the stem-Bryophyta around the middle of the Ordovician.
The oldest known crown liverwort is Riccardiothallus devonicus, found in the Early Devonian (Pragian) Posongchong Formation at Zhichang Village, Gumu Town, Wenshan District, Yunnan Province, China (Guo et al, 2012). According to these authors, the fossil belongs to family Aneuraceae in the order Metzgeriales (in subclass Metzgeriidae), but Morris et al (2018) more conservatively assign it only to the “Jungermanniopsida group”. It is not clear whether they mean stem-, crown- or total-Jungermanniopsida, but given the higher-level assignment of Guo et al, we shall consider it as a representative of the crown-Jungermanniopsida. No image of Riccardiothallus is available in the public domain.
In fact, the only public-domain image available for fossils of the liverwort crown group is from Radula cretacea, a member of the crown-Porellales from mid-Cretaceous amber in Myanmar (Bechteler et al, 2017) (click to enlarge):
The time of first appearance of the crown-Jungermanniopsida and of other subordinate crown groups within the liverwort crown group is shown in the following time tree:
The above time tree indicates that the crown group of the liverworts appeared no later than the Early Devonian. However, in the absence of stem-group moss fossils, the timing of appearance of the stem-group is constrained only by the appearance of the stem-Bryophyta (the spore Tetrahedraletes cf. medinensis) in the middle of the Ordovician; this implies an uncertainty of around 63 million years in the timing of appearance of the crown-group liverworts.
The evolution of the crown-group liverworts cannot be traced much further because only one stem-group representative of a higher-level clade has been recognized. This is Metzgeriothallus sharonae, a member of the stem-Pelliidae found in Middle Devonian (Givetian) sediments of eastern New York, USA (Hernick et al, 2008; Laenen et al, 2014). The oldest known representative of the crown-Pelliidae is Pallaviciniites devonicus (Vitt et al, 2014). Again, no public-domain images are available. The existence of these two fossils indicates that the stem-to-crown transition of the Pelliidae took no more than 16 million years.
The evolution of the crown-group liverworts cannot be traced much further because only one stem-group representative of a higher-level clade has been recognized. This is Metzgeriothallus sharonae, a member of the stem-Pelliidae found in Middle Devonian (Givetian) sediments of eastern New York, USA (Hernick et al, 2008; Laenen et al, 2014). The oldest known representative of the crown-Pelliidae is Pallaviciniites devonicus (Vitt et al, 2014). Again, no public-domain images are available. The existence of these two fossils indicates that the stem-to-crown transition of the Pelliidae took no more than 16 million years.
Evolution of the hornworts
The hornworts (Division Anthocerotophyta in superphylum Embryophyta) are flowerless, spore-producing plants whose spores are typically produced in a tapering, horn-like or needle-like capsule which develops from a flattish, green sheet (Australian National Botanic Gardens website). These capsules can be seen in the photograph below:
Hornworts represent the third group of bryophyte plants (the two others are mosses and liverworts) that have a life cycle comprising gametophyte and sporophyte stages. The number of extant hornwort species is estimated to be between 200 and 250 (Villarreal et al, 2014). One of the most recent phylogenetic trees of the extant hornworts is summarized below:
The fossil record of the hornworts is extremely sparse (Villarreal et al, 2014), and many of the terminal clades shown above are not known as fossils. Furthermore, no stem-group hornworts have been identified (Kenrick, 2000); the only constraint we have on the age of the earliest stem-group hornwort is that it cannot have been greater than that of the first appearance of the stem-Bryophyta around the middle of the Ordovician.
The oldest known crown hornwort is the spore Stoverisporites lunaris, found in the Early Cretaceous (Aptian) Baqueró Formation at the Amphitheater of Ticó, Province of Santa Cruz, Argentina (Archangelsky & Villar de Seoane, 1996; Villarreal et al, 2014). No public-domain image is available.
The time of first appearance of the crown-Anthocerotophyta and of other subordinate crown groups within the hornwort crown group is shown in the following time tree:
The oldest known crown hornwort is the spore Stoverisporites lunaris, found in the Early Cretaceous (Aptian) Baqueró Formation at the Amphitheater of Ticó, Province of Santa Cruz, Argentina (Archangelsky & Villar de Seoane, 1996; Villarreal et al, 2014). No public-domain image is available.
The time of first appearance of the crown-Anthocerotophyta and of other subordinate crown groups within the hornwort crown group is shown in the following time tree:
The above time tree indicates that the few fossils that represent the hornwort crown group date from the Cretaceous and Cenozoic. However, in the absence of stem-group hornwort fossils, the timing of appearance of the stem-group is constrained only by the appearance of the stem-Bryophyta (the spore Tetrahedraletes cf. medinensis) in the middle of the Ordovician; this implies an enormous uncertainty (more than 350 million years) in the timing of appearance of the crown-group liverworts.
The evolution of the crown-group hornworts cannot be traced further because no stem-group representatives have been found for any of the clades shown.
The evolution of the crown-group hornworts cannot be traced further because no stem-group representatives have been found for any of the clades shown.
Image credits - Bryophytes
- Header: Barbula spadicea, a member of the subclass Dicranidae By Hermann Schachner / Public domain.
- Sphagnum palustre By Bernd Haynold / CC BY-SA
- Jungermannia leiantha By Hermann Schachner /CC0
- Lunularia cruciate By User:Velela, Public domain
- Radula cretacea From Bechteler, J., Schmidt, A. R., Renner, M. A., Wang, B., Pérez-Escobar, O. A., Schäfer-Verwimp, A., ... & Heinrichs, J. (2017). A Burmese amber fossil of Radula (Porellales, Jungermanniopsida) provides insights into the Cretaceous evolution of epiphytic lineages of leafy liverworts. Fossil Record, 20(2), 201-213, distributed under the terms of Creative Commons license Attribution 3.0 Unported (CC BY 3.0).
- Phaeoceros carolinianus By Hermann Schachner / CC0