Evolution of Vascular Plants a Kaleidoscope, Not a Tree

 

Kaleidoscope of Design Combinations:
Vascular Plant Form and Function

By Margaret Helder, PhD

All things considered, it must be discouraging to be a specialist in land plant phylogeny. The evolutionary botanist beholds a wild scattering of traits across numerous taxa; how can it be organized into a tree of ancestry? Nevertheless, some authors try to convey a positive interpretation of their data. For example, in a recently published study,¹  the authors declared that what they observed “may have been an important intermediate step in the evolution of more advanced plant reproductive strategies.”²  So let us see what the situation is, relevant to their claims.

Perhaps the best place to start the discussion is with a basic/stripped down land plant. You can imagine a basic car model, for example, with chassis, wheels, engine, gears, brakes, steering wheel, windshield and nothing else. There actually is a plant which is similarly basic. Psilotum or whisk fern grows in some southern American states and tropical Asia. It is often considered to be a living fossil although no fossils have been found. (There are however similar fossil plants like Psilophyton.)

Typically this living plant is 6-10 inches (15-25 cm) tall. It consists of an underground stem with no roots, vertical stems which are evenly (dichotomously) branched, and very short branches which bear small capsules called sporangia, inside of which spores are produced. The process of spore production results in cells with one set of chromosomes each, whereas the parent plant has two sets of chromosomes each per cell. The stems of this plant contain conductive tissue so that the more remote parts of the plant have access to water and nutrients. The plant is naked; there are no leaves. It is the stem that photosynthesizes. Once released, the spores germinate into tiny plants which grow underground and produce eggs and sperm. After fertilization, the embryo grows into the dominant diploid (two sets of chromosomes per cell) plant again.

If we want fancier plants, we have to add other features to the basic design. These features include roots with a root cap and root hairs for better absorbing of water and minerals, leaves, variations on spore production, and thicker stronger stems with secondary vascular tissue called wood. There is no pattern of gradual acquisition of these features among land plants such as would support evolutionary interpretations. Instead what we see is a phenomenon called parallel or convergent evolution that cannot be linked to descent with modification from a common ancestor, but is nevertheless assumed to have come about by evolutionary processes.  Thus Dr. Wilson Steward defined these processes: “Parallel or convergent evolution occurs when similar characteristics evolve in two or more distantly or unrelated groups.” ³

So what are some of the features in vascular land plants which cannot be linked as having common origins? Many qualify for this description. Leaves provide one excellent example. For a start, most plant specialists consider that club moss relatives constitute a dead end in evolution. The club mosses exhibit roots and leaves, and spore bearing capsules closely connected with special leaves. Today most of these plants are small, only a few inches high, but there were some designs in the past that grew into very large trees such as Lepidodendron (famous for its fossilized trunks with conspicuous leaf scar markings on the trunk).

The interpretation today is to separate vascular (trachophyte) land plants into two major groupings, the lycophytes (club moss types) and the euphyllophytes (everything else). Thus one expert confided:

[P]rogress in paleobotany led to the realization that vascular plant phylogeny was itself divided by a major dichotomy, dating back ~415 million years to the Late Silurian-Early Devonian, that paralleled, to some extent, the taxonomic distribution of the two leaf types. The two major lineages of that phylogenetic divide originated from among two distinct grades of early vascular plants the zosterophylls and the trimerophytes [known only as fossils]. The descendants of those two lineages form the two clades that comprise most vascular plant phylogeny, the lycophytes and the euphyllophytes.⁴

Origin of Leaves

An evolutionist might insist that two types of leaf origins within the vascular plants are not too bad. But that is only the start. Among the rest of the vascular plants however, specialists detect as many as nine separate origins of leaves. Thus the same expert declared: “[E]uphyllophyte leaves are neither homologous at the level of their precursor structures nor at the level of the genetic pathways that control their development.”⁵ Not homologous means that they are not connected by common descent. Other specialists similarly declared: “The evidence demonstrates that vascular plant leaves have evolved multiple times from branching shoot systems, and that branching forms diversified extensively in lycophyte,  monilophyte [euphyllophytes] and seed plant lineages…” ⁶

Reproductive Structures

The criterion of most concern in looking for lines of descent in plants is, of course, reproductive structures. In our basic plant example, Psilotum or whisk fern, the spores, produced by the adult plant, all look the same. We call them homospores. Botanists declare that this is the “primitive” condition. So, if a plant produces spores of different sizes, these are considered to be “derived” or evolutionarily advanced.⁷ If the larger spores are greatly reduced in number, this condition is considered to be further derived. The great interest in spores is that they develop into the haploid (single set of chromosomes) sexually reproducing plants. The expectation is that large spores develop into female sexual plants (producing an egg) and the small spores develop into male sexual plants that produce swimming sperm.

There are some large spores that retain the developing female plant (gametophyte) inside the split open wall of the spore. This is observed in some taxonomically unpromising groups for evolution like Selaginella and arborescent lycopods such as Lepidodendron (all considered “dead ends” for evolution). Thus Dr. Steward declared: “Obviously heterospory and the resulting ovulelike structures of the arborescent lycopods have evolved quite independently of the evolution of the ovule of seed plants.”⁸  It is nevertheless the position of most specialists that heterospory was an important stage preceeding the appearance of seeds⁹  and that a seed is  a megasporangium [for “mega” read pertaining to larger size] containing a megaspore containing a megagametophyte which produces several eggs. The situation can be likened to Russian stacking dolls where the megaspore is the largest doll and each next stage is a smaller doll inside the previous one. The resulting seed inside them all, contains a fertilized egg which begins to develop into the embryonic stage of the adult plant.

Assuming What Needs to Be Proved

This is the theoretical significance of heterospory. It is all assumed. Thus other authors declare: [H]eterospory was an innovation that occurred repeatedly in the history of land plants … [but] the adaptive value of heterospory has never been well established.” In fact we don’t know much about heterospory: “Its role as a precursor to the evolution of seeds has received much attention but this is an evolutionary consequence of heterospory that cannot explain the transition from homospory to heterospory.”¹⁰  it is interesting to see the distribution of this phenomenon among land plants. Dr. Stewart reflected on the topic:

There is a general tendency among heterosporous plants to reduce the number of megaspores from several to one functional megaspore. We have seen good examples of this tendency in the Lycopsida [club mosses], Sphenopsida [horsetails] , and the Filicopsida [ferns]. This provides us with an excellent example of the independent and parallel evolution of heterospory in divergent groups of vascular plants.¹¹

How straightforward is it then to trace lines of descent among vascular plants based on the phenomenon of heterospory? Bateman and DiMichelle, in an article on this very topic, declared that the appearance of heterospory among vascular plant taxa was “highly iterative” [i.e., it appeared again and again]. Thus they declared that “current evidence suggests a minimum [sic] of eleven origins of heterospory.” In addition, they made clear that: “Heterospory reflects the convergent attainment of similar modes of reproduction in phylogenetically disparate lineages.”  And they also remarked that: “No origin of heterospory coincides with the origin of (and thus delimits) any taxonomic class of tracheophytes [vascular plants].” ¹² This is pretty clear that possession of heterospory does not affect what other features a plant group might display. These authors therefore concluded tentatively that all the plant lineages exhibit “similar sequences of characters.”¹³

Asking the Right Question

The question therefore arises as to why both homospory and heterospory would be found within most of the plant groups (Table 1). Bateman and DiMichelle suggest that ecological specialization is why some taxa exhibit one or the other trait. In this context they shared that “[S]imilar patterns of character acquisition in different lineages together suggest that its evolution [heterospory] was largely adaptively driven.” ¹⁴  In other words, both heterospory and homospory conveyed particular ecological benefits.

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Table I

Major non-seed-bearing vascular plants with spore type:

Lycopsida  (club mosses) – many are homosporous, but Selaginella and arborescept types are heterosporous

Psilopsida  (whisk ferns) – homosporous

Sphenopsida (horsetails) – homosporous but large fossils Calamites – heterosporous  [These plants are all characterized by branches and leaves arranged in whorls at widely separated nodes along the stem.]

Filicopsida (ferns) – almost all ferns are homosporous except for a few aquatic genera which are heterosporous. [Ferns have unusually large numbers of chromosomes. The number of chromosomes coming from one parent could be 50 while the flowering plant average is about 16. One fern has a count as high as 700+ chromosomes from each parent. Michael S. Barker and Paul G. Wolf. 2010. Unfurling fern biology in the genomics age. BioScience 60 (3): 177-185. See pp. 179 and 184.]

Progymnospermopsidea – These exhibit secondary wood (as in trees) but spores rather than seeds.  Of these the Aneurophytales are homosporous and the Archaeopteridales are heterosporous. These are all fossil plants.

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The Latest Fossil Snap Chat

Knowing what we do about heterospory and its lack of implications for evolutionary relationships,  we now turn our attention to the recent study already mentioned. On May 4, 2020 Science Daily highlighted a newly published study. Their headline said it all: “New ancient plant captures snapshot of evolution.¹⁵ The less dramatic actual title was “A novel reproductive strategy in an early Devonian plant.”¹  One of the authors had collected small chips of rock from a site across the Restigouche River from Miguasha, Quebec, Canada which boasts a catastrophic deposit of extinct fish.¹⁶  The Campbellton Formation (in northern New Brunswick) from which the rock chips came, is at most 35 miles (55 km) from the Quebec fossils (Escuminac Formation). The New Brunswick site lies lower down in the strata than the Quebec fossils and so is considered to be older. Both sites have been dated by the plant spores contained in the sediments.¹⁷

The rock chips had been collected some time ago and were deposited at the Smithsonian Museum of National History. These weren’t just any rock chips however. The multiple authors, connected with this study, observed dense arrangements of sporangia in cones (strobili) along short pieces of plant stem.  Some of the sporangia were split open, revealing some spores all of the same size (either large or small) and other sporangia exhibited a mixed collection of spore sizes. They noted that a mixed collection of spore sizes in one sporangium is extremely rare among vascular plants.

Since the rock chips had been collected from a Campbellton Formation site in northern New Brunswick, they were naturally interested to compare their find with other plant material from the same sediments. The cones (strobili) preserved in the rock are similar to an obscure fossil taxon called Barinophyton.¹⁸ All that has ever been found of this plant are the cones, and that is the case in the present study as well. The present authors understand that the previously studied Barinophyton cones may come from a plant of lycophyte affinities (not helpful for evolutionary speculation). In any case, Brauer suggests that the possession of microspores and megaspores in one sporangium of Barinophyton is reasonably considered to represent an adaptation [design feature] for an aquatic habitat such as we see in the aquatic fern Marislea.¹⁹

They Must Have Evolved

The authors of the present study however are not so easily dissuaded from evolutionary speculation. Based on the assigned age of the deposit, the authors claim that the production of two sizes of spore in one sporangium marked the start of a long process of evolution in land plants that ended with seed plants. They therefore declared of this phenomenon: “The evolution of contrasting spore size classes is therefore one of the most fundamental innovations in land plant history.” ²⁰

Other plants identified in Campbellton Formation deposits include Chaleuria (with a mixture of spore sizes like the present unknown taxon),²¹  Psilophyton (homosporous) ²²  and Oocampsa, which is homosporous. ²³  The book on the Miguasha fossils ²⁴  cites Sir J. W. Dawson as reporting barinophytes from Lower Deposits in the Campbellton Formation. Barinophytes were also reported from the Escuminac Formation at Miguasha along with the progymnosperm Archaeopteris.

Anecdote on Archaeopteris: There are a lot of Archaeopteris (means “ancient fern”) fragments in the Miguasha sediments. Sir William Dawson apparently first described these fronds from Miguasha in the mid 19th century. But in similar sediments in other places there was also lots of wood known by the form genus Callixylon. According to a 1972 botany text book by Harold C. Bold, trunks of Callixylon 5 ft in diameter have been found in Oklahoma, and trunks 3 ft in diameter and 28 feet long have been found in Indiana and Texas. Then in 1960 it was discovered that the Archaeopteris fronds were attached to the Callixylon wood! So now they had giant trees with fern leaves and no seeds (as one would expect for gymnosperm trees). The “fern fronds” were reevaluated and now they are considered highly branched with small leaves. And “ancient fern” became a progymnosperm. Not surprisingly, Archaeopteris is quite a celebrated plant fossil, but the mere listing of a name does not convey its celebrated history!   —M.H.

Summary

So, is the possession of two spore sizes in one sporangium highly significant for evolution, as the present authors claim? The phenomenon had already been reported for another taxon Chaleuria from the same deposits.²⁵  And barinophytes have been reported there and elsewhere to exhibit two spore sizes.²⁶  Still it seems fair to ask, “Does the production of two spore sizes in one sporangium represent a fundamental innovation in land plant evolution?” Obviously not. Rather, the expression of heterospory seems more closely connected to the ecological needs of various plant designs.

One needs to be determined indeed to see evolutionary significance in a phenomenon that does not demonstrate any trends. Each plant taxon instead displays a different collection of unique features. There are no lines of descent for any feature. Instead the totality of these plant groups represents a beautiful kaleidoscope of design.  

References

1. Nikole K. Bonacorsi, Patricia G. Gensel, Francis M. Hueber, Charles H. Wellman, and Andrew B. Leslie. 2020. A novel reproductive strategy in an Early Devonian plant. Current Biology 30: R388-389.
2. R389.
3. Wilson N. Stewart. 1983. Paleobotany and the evolution of plants. Cambridge University Press. pp. 405. See p. 129.
4. Alexandru M. F. Tomescu. 2009. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14 (1): 5-12. See p. 5.
5. Tomescu p. 11.
6. Jill Harrison and Jennifer L. Morris. 2017. The origin and early evolution of vascular plant shoots and leaves. Phil. Trans. R. Soc. B 373: 1-14. See p. 10. http://dx.doi.org/10.1098/rstb.2016.0496
7. Stewart p. 232.
8. Stewart p. 118.
9. Stewart p. 232.
10. B. Petersen and M. Burd. 2017. Why did heterospory evolve? Biol. Rev. Camb. Philos. Soc. 92 (3): 1739-1754. See p. 1739.
11. Stewart p. 232.
12. Richard M. Bateman and William A. DiMichelle. 1994. Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Rev. Camb. Philos. Soc.  https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1469-85X.1994.tb01276.x          Summary. Point 5.
13. Bateman and DiMichelle. Point 6.
14. Bateman and DiMichelle Summary. Point 7.
15. sciencedaily.com/releases/2020/05/200504114033.htm
16. CEH Latest Tetrapod Ancestor Can’t Stand Up. May 11, 2020 crev.info.2020/05/latest-tetrapod-cant-stand-up/
17. P. Schultze and R. Cloutier (editors). 1996. Devonian Fishes and Plants of Miguasha, Quebec, Canada. Verlag Dr. Friedrich Pfeil. Munchen. See p. 31 and Bonacorsi p. R388.
18. David F. Brauer. 1980. Barinophyton citruliforme (Barinophytales Incertae Sedis, Barinophytaceae) from the Upper Devonian of Pennsylvania. American Journal of Botany 67: 1186-1206. See p. 1186 and Stewart p. 233.
19. Brauer p. 1186.
20. Bonacorsi p. R388.
21. Henry N. Andrews, Patricia G. Gensel, and William H. Forbes. 1974. An apparently heterosporous plant from the Middle Devonian of New Brunswick. Palaeontology 17 (2) 387-408. See p. 394.
22. Andrews et al. See p. 388.  Also Jeffrey B. Doran. 1980. A new species of Psilophyton from the Lower Devonian of northern New Brunswick, Canada. Canadian Journal of Botany. 58: 2241-2262. (similar species, similar deposits)
23. Henry N. Andrews and Patricia G. Gensel and Andrew E. Kasper. 1975. A new fossil plant of probable intermediate affinities (Trimerophyte-Progymnosperm). Canadian Journal of Botany. 53: 1719-1728.
24. Schultz p. 80.
25. Andrews, Gensel and Forbes. 1974.
26. Brauer p. 1186.

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Margaret Helder completed her education with a Ph.D. in Botany from Western University in London, Ontario (Canada). She was hired as Assistant Professor in Biosciences at Brock University in St. Catharines, Ontario. Coming to Alberta in 1977, Dr Helder was an expert witness for the State of Arkansas, December 1981, during the creation/evolution ‘balanced treatment’ trial. She served as member of the editorial board of Occasional Papers of the Baraminology Study Group in 2001. She also lectured once or twice a year (upon invitation) in scheduled classes at University of Alberta (St. Joseph’s College) from 1998-2012. Her technical publications include articles in the Canadian Journal of Botany, chapter 19 in Recent Advances in Aquatic Mycology (E. B. Gareth Jones. Editor. 1976), and most recently she authored No Christian Silence on Science (2016) which promotes critical evaluation of scientific claims. She is married to John Helder and they have six adult children.