The Alternation of Generations in Earth’s Earliest Land Plants


Featured image by: Richard Bizley

In 1912, Dr. William Mackie, a British medical practitioner, as well as a member of the Geological Society of Edinburgh, was undertaking a geology survey in the small village of Rhynie. After coming across a stone fence marking the boundary between adjacent fields, he became intrigued by the rocks that had been used to make it, which were comprised of siliceous chert. So he did what any good geologist would do and made a few sections of the rock, the contents of which would radically change our perceptions of early life on our planet. Within the rocks was an ancient landscape that had been almost perfectly preserved for 400 million years. Mackie made his discovery known to local paleontologists, and within the year excavations were underway in a nearby field, from which the original stones had been taken. For the next century, scientists would study these rocks, slowly piecing together the tattered history of life in the early Devonian.




500 million years ago, the Earth’s oceans were teeming with a diverse array of fish, coral, invertebrates, and several types of algae. Very few organisms, however, had yet to make their way onto land, a seemingly inhospitable environment with fluctuating temperatures, high amounts of solar radiation (compared to the dappled light that permeated Earth’s young oceans), and dangerously dry air, which could easily dehydrate the aquatic organisms that for the past 3 billion years had evolved with and relied on the ocean’s sustaining water to survive. But around this time, an otherwise unremarkable group of algae began to colonize terrestrial environments. In order to survive on land, however, they would have to undergo several radical transformations that would change almost everything but their underlying cell structure. Even their lifecycle had to be amended to make life on land a possibility.


Green algae, which are today the closest living relatives of land plants, have a haplodiplontic lifecycle. They have multicellular gametophytes which produce sperm and eggs; once the eggs are fertilized, however, the resulting unicellular zygote doesn’t undergo any subsequent divisions, which would allow for a multicellular embryo. Instead, the zygote immediately undergoes meiosis to produce haploid zoospores that grow into gametophytes. Most green algae, therefore, do not have an alternation of generations, one of the unifying traits that unites all land plants. Because while a freely spawned zygote is a great way to reproduce in the ocean, it would be an inefficient strategy to enact on land, where an unprotected zygote would quickly dry out. So the first land plants, the bryophytes, retained their zygotes. This meant, however, that, lacking a means of dispersal, the subsequent zoospores would grow directly on top of the parent plant tissue. Zygotes thus proliferated into embryos, which developed into sporophytes that were dependent on their respective gametophyte counterparts for nutrition. Thus these plants had a true alternation of generations, a diploid portion (the sporophyte) and a haploid (the gametophyte). This had several important evolutionary implications for the plants that would evolve millions of years later, the most obvious being the eventual rise and dominance of the sporophyte generation that we observe in most living plants today.


But for several million years (from 470 to 440 mya), bryophytes ruled the world (Willis and McElwain, 2014). At the end of the Silurian, other groups of plants, collectively known as the protracheophytes, began to diversify as well, and the relationship between the haploid and diploid stages of the plant lifecycle changed yet again. The earliest land plant for which we have identifiable fossils is Cooksonia, the oldest remains of which are approximately 425 million years old, discovered in Ireland (Edwards and Feehan, 1980). These plants lacked a cuticle, a feature also lacking in hornworts and liverworts. Because of this, as well as a lack of defining internal stem features that might otherwise suggest the presence of water-conducting cells, Cooksonia is currently hypothesized to have been nutritionally dependent on its gametophyte, which, unfortunately, has never been discovered.


When paleobotanists began to analyze rocks from the Rhynie chert, it became clear that it contained a very different group of plants, of a type never seen before. The sporophytes of these plants had cuticles, primitive and sometimes remarkably sophisticated water conducting cells, and were photosynthetic, all of which indicated that these sporophytes were no longer dependent on their gametophytes. But just like the missing Cooksonia gametophytes, the haploid generation for these plants were elusive and remained so for several decades.




If we leave behind the world of bryophytes and step forward in time some 40 million years, we will have made it to the beginning of the Devonian, a time of rapid diversification for both plants and animals alike. The Earth had just recently recovered from a short ice age that had resulted in a mass extinction of life in the oceans. It’s no small coincidence that this ice age occurred during the height of bryophyte dominance either; it’s currently hypothesized to have been directly caused by the weathering of bare rock by these first plants, which would have locked up a significant amount of atmospheric carbon in the form of calcium and magnesium carbonate in the world’s oceans (Lenton et al., 2012). The sky was also noticeably darker than our own, the sun emitting only a pallid glow due to what is known as the faint young sun hypothesis, first proposed by Carl Sagan and George Mullen (1972).


What is now the Rhynie Chert in northern Scotland was a large sinter terrace, formed by the expulsion of silica-rich waters from nearby hot springs and geysers. The closest analogue today would be hot springs of Yellowstone National Park and the Rotorua in New Zealand. While this provided great habitat for early plants, the springs would also periodically flood the surrounding area with boiling, silica-laden water. As the water cooled and receded, the silica precipitated out, adding additional layers to the terrace and preserving the plants that grew there.


There are currently seven known plant species from the Rhynie Chert, the last of which, Ventarura lyonii, was described in 1999 (Powell, Edwards, and Trewin). These plants (which included one of the earliest lycophytes, Asteroxylon mackiei) were small, with prostrate rhizomes bundled closely together, likely to support the protruding stems in an upright posture. Most only rose a few centimeters from the ground, sporting terminal sporangia at their tips to allow for effective wind dispersal. Nor were they alone. Paleontologists have found the remains of small microarthropods and crustaceans, mostly detrivores, that lived among the dense stands of Aglaophyton, Asteroxylon, and Nothia.


But still paleobotanists were unable to find specimens of plant gametophytes embedded in the rock. Suggestions floated about for several decades. What if the horizontal strands of Rhynia gwynne-vaughanii weren’t actually rhizomes but gametophytes (Merker, 1958)? Or more controversial still, what if the entire plant itself was a gametophyte (Pant, 1962)? After all, detailed sporangia from this species weren’t formally described until 1980 (Edwards). But none of these hypotheses stood the test of time or scrutiny. But in 1977, a German husband and wife team of paleobotanists collected samples from the chert and described seeing “two fractured bowl-shaped structures, which bore blackish, globular bodies” (Remy and Remy, 1980). The structure they had discovered, which looks nondescript until close examination, was an intricately complex gametophyte, unlike anything alive today. A central axis, with a prominent conducting strand, supported a cup-shaped thallus with crenellated margins that bore multiple male (antheridia) and female (archegonia) sex organs. Later, fossils collected of the same species were so pristine that coiled sperm can be observed locked away in the permineralized remains of its antheridia.


This particular species was given the name Lyonophyton rhyniensis. However, paleobotanical nomenclatures is different from modern taxonomy in one very important aspect. When separate fossils are found of the different organs or life stages of a particular plant, even if they are thought to be from the same species, they are given different scientific names. Thus the species L. rhyniensis is actually hypothesized to be the gametophyte of Aglaophyton major, also found in the Rhynie Chert. Other discoveries quickly found their way into the scientific literature. Kidstonophyton discoides is thought to be the gametophyte of Nothia aphylla (Remy and Hass, 1991a), Langiophyton makie the gametophyte of Horneophyton lignieri (Remy and Hass, 1991b), and the latest addition, published in 2004 (Kerp, Trewin, and Hass), Remyophyton delicatum is the presumed gametophyte of Rhynia gwynne-vaughanii, which was the very first sporophyte to be described from the Rhynie Chert back in 1917 (Kidston and Lang).

Sporophytes of the Rhynie Chert on top, and their respective gametophytes below. Top: A. Rhynia gwynne-vaughanii B. Aglaophyton major C. Ventarura lyonii D. Asteroxylon mackiei E. Horneophyton lignieri F. Nothia aphylla Bottom: A. Remiophyton delicatum B. Lyonophyton rhyniensis E. Langiophyton mackei F. Kidstonophyton discoides Credits: Falconaumanni: Remiophyton delicatum (Kerp, Trewin, and Hass, 2004) Lyonophyton Rhyniensis and Langiophyton mackei (Remy, Gensel, and Hass, 1993)
Sporophytes of the Rhynie Chert on top and their respective gametophytes below.
Top: A. Rhynia gwynne-vaughanii B. Aglaophyton major C. Ventarura lyonii D. Asteroxylon mackiei E. Horneophyton lignieri F. Nothia aphylla
Bottom: A. Remiophyton delicatum B. Lyonophyton rhyniensis E. Langiophyton mackei F. Kidstonophyton discoides
Credits: Falconaumanni:
Remiophyton delicatum (Kerp, Trewin, and Hass, 2004)
Lyonophyton Rhyniensis and Langiophyton mackei (Remy, Gensel, and Hass, 1993)

These early gametophytes can tell us a lot about the evolution of plant life on land. Very quickly after plants left the oceans, they evolved a diplobiontic lifecycle that better enabled them to reproduce on land, as seen in the bryophytes. This first attempt at alternating generations produced a lifecycle in which the multicellular sporophyte was dependent on the gametophyte for nutrition. The gametophytes of the Rhynie Chert, however, show that early on, before even the evolution of vascular tissue, the lifecycle of many plants had evolved to allow for the independence of both the gametophyte and sporophyte, a pattern seen today in only the ferns and lycophytes.


This transition to independent sporophytes is part of a larger trend of increasing sporophyte size and complexity along with gametophyte reduction. Angiosperms, today the most diverse group of land plants on Earth, have taken this trend to the opposite extreme of the bryophytes. Their gametophytes are small, having been reduced to just a few cells, and are produced by the flowers of the much larger and more dominant sporophyte. But why the switch? What advantages were conferred by having dominant sporophytes? Possibly the biggest benefit was size. Gymnosperms and angiosperms are today the largest plants in the world, a stature that gametophytes would never have been able to attain, not because of an inability to produce vascular tissue or the lack of a cuticle. Both of these features could have easily evolved in a haploid organism; mosses, in fact, already have cuticles and a very primitive form of conducting tissue. Rather it is the reliance on water of free-living gametophytes that inhibits their size. Bryophytes, Lycophytes, and Ferns have flagellate sperm that require water in order to swim short distances to nearby eggs. If such plants increased in size, it would make outcrossing impossible. Gymnosperms and angiosperms, on the other hand, produce pollen, which in turn grow pollen tubes that carry sperm directly to the egg, thus eliminating the need for water-mediated dispersal and allowing for the evolution of fruits.



Edwards, D., & Feehan, J. (1980). Records of Cooksonia-type sporangia from late Wenlock strata in Ireland. Nature 287: 41-42.

Kerp, H., Trewin, N. H., & Hass, H. (2004). New gametophytes from the Early Devonian Rhynie chert. Transactions: Earth Sciences 94: 411-428.

Kidston, R. & Lang, W. H. (1917). On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part 1: Rhynia gwynne-vaughanii Kidston and Lang. Transactions of the Royal Society of Edinburgh 51: 761–84.

Lenton, T. M., Crouch, M., Johnson, M., Pires, N., & Dolan, L. (2012). First plants cooled the Ordovician. Nature Geoscience 5: 86-89.

Merker, H. (1958). Zum fehlenden Gliede der Rhynienflora. Botaniske Notiser 111: 608–18.

Pant, D. D. (1962). The gametophyte of the Psilophytales. In Mahesh- wari, P., Johri, B. M. & Vasil, I. K. (eds) Proceedings of the Summer School of Botany, Darjeeling, June 2–15, 1960: 276–301.

Powell, C. L., Edwards, D., & Trewin, N. H. (1999). A new vascular plant from the Lower Devonian Windyfield chert, Rhynie, NE Scotland. Earth and Environmental Science Transactions of The Royal Society of Edinburgh 90: 331-349.

Remy, W., & Remy, R. (1980). Lyonophyton rhyniensis nov. gen. et nov. spec., ein Gametophyt aus dem Chert von Rhynie (Unterdevon, Schottland). Argumenta Palaeobotanica 6: 37-72.

Remy, W. & Hass, H. (1991a). Kidstonophyton discoides nov. gen. nov. spec., ein Gametophyt aus dem Chert von Rhynie (Unterdevon, Schottland). Argumenta Palaeobotanica 8: 29–45.

Remy, W. & Hass, H. (1991b). Langiophyton mackiei nov. gen., nov. spec., ein Gametophyt mit Archegoniophoren aus dem Chert von Rhynie (Unterdevon Schottland). Argumenta Palaeobotanica 8: 69–117.

Remy, W., Gensel, P. G., & Hass, H. (1993). The gametophyte generation of some early Devonian land plants. International Journal of Plant Sciences 154: 35-58.

Sagan, C., & Mullen, G. (1972). Earth and Mars: Evolution of atmospheres and surface temperatures. Science 177: 52-56.

Willis, K. J., & McElwain, J. C. (2014). The evolution of plants. New York: Oxford University Press.

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