G. L. Stebbins and the process of adaptive modification

The convergence of modern phylogenetics, genetics and evolutionary development (EVO-DEVO) has allowed us to make better and better hypotheses about the evolutionary history of plants, for which the fossil record still leaves many gaps.  There is another dimension to this fascinating pursuit, an older one that isn't talked about as much: the analysis of adaptive or evolutionary trends.  This was the core logic of evolutionary biology through much of the twentieth century, before cladistic analysis came to dominate.  The publication of "Flowering Plants: Evolution above the Species Level" by G. L. Stebbins in 1974 represented the finest of this approach.  Far from being obsolete, the thought processes of  Stebbins and other 20th century evolutionary biologists are still applicable to the various, sometimes controversial theories that are appearing currently.  In my opinion, Stebbins' book should be required reading for all graduate students of evolution.

Adaptive modification along the lines of least resistance

  One of the general principles of evolutionary biology is that evolutionary change, under the force of natural selection, will tend to proceed along the lines of least resistance - i.e. the simplest route. For example, a leafless cactus adapts to epiphytic life in the rain forest, not by reconstructing the leaves abandoned by its ancestors, but by flattening its stem segments into leaf-like units (e.g. genus Schlumbergia - the Christmas cactus).  This is one aspect of the bigger picture of evolutionary canalization, which essentially states that the possible adaptations of a plant species or individual organs are limited by what they already are.  A coconut has little prospect of evolving into an orchid-like capsule with millions of tiny, wind-pollinated seeds, just as an elephant has little prospect of evolving wings (or flying with its ears!).

Let me expand upon one of Stebbins' most lucid examples.  Suppose there is selective pressure for an increase in seed production.  This could occur for a variety of reasons: improved growing conditions, adaptation to a sunnier environment where smaller seeds can be created in greater numbers, and/or an increase in the numbers of seed-eating animals present.  All could all favor a species that increases its output.  How a species would respond to such a challenge would depend on its starting equipment.

A legume is a modified follicle containing a variable
number of seeds. Ovules are created in a
meristematic zone in the young carpel
 that can be increased or decreased. Photo by
by Renee Comet - NCI, posted on Wikipedia.

A species that has a fixed number of carpels in its flowers, but a variable number of ovules in each carpel, might respond by producing more ovules within each carpel.  The capsules of lilies, irises, and orchids, along with simpler follicles of columbines, delphiniums, etc. produce ovules in sequence from meristematic (embryonic) tissues within the carpel.  Simply continuing that activity for a longer period of time would result in more ovules.  To some extent, this flexibility is important on a day-to-day basis.  When conditions are poor, fewer ovules may be produced, and when better, more may be produced.  Extended onto an evolutionary scale, adaptations for more and more seed production can result.  Orchids represent one culmination of this trend, producing millions of tiny airborne seeds in each capsule. By the same token, reduction to a single seed is also possible from an ancestor in which the number is variable.

In the flower of a strawberry, the numerous carpels are
produced by the apical meristem in the embryonic bud.
Each will become a seed-like achene on the outside of
the swollen, Fruit-like receptacle (central stalk). Photo by
Papas2010, posted on Wikipedia.

In species that have a fixed number of ovules in each carpel, but a variable number of carpels in each flower, the number of carpels can be increased.  This is what happens in something like a strawberry (see "Why are the seeds of a strawberry on the outside?").   The tiny fruits of the strawberry (the seed-like structures on the outside of the swollen receptacle) are adapted as achenes. The number of seeds in each tiny carpel is rigidly fixed at one.  It would take an extraordinary amount of genetic and developmental reorganization to increase the number of seeds within each achene, which in the process would have to adapt to a different dispersal strategy.  The meristem in the center of the flower, which produces the carpels sequentially, however, can continue to operate a little longer and easily produce many more single-seeded carpels.
the number of carpels might be increased.

In a third "starting point," we have sunflowers and their relatives (family Asteraceae), in which flowers are highly canalized.  The actual flowers are tiny and crowded onto a dense head.  Each contains a single seed in a highly specialized ovary. It is inconceivable that a pressure for higher seed output would result in more seeds or more carpels being produced in each flower.  It is vastly simpler to increase the number of flowers within the composite head.  This is what we see in the massive cultivated sunflowers, which have evolved under human selection, compared with their wild relatives.

The massive sunflower is actually a composite head of several hundred tiny flowers that each bear a single seed.  The
size of the head depends on how long the central apical meristem actively produces new flowers (oldest flowers
around the outside are open, newer ones toward the inside are still in bud).  Photo by Amada44, posted in Wikipedia.

The imperative of evolutionary canalization, and modification along the lines of least resistance can be stronger than the imperative of parsimony in phylogenetic analysis.  It is the basis for my conclusion that the single-seeded drupes of Amborella represented a specialization from a more flexible common ancestor (see "What's so primitive about Amborella.")  I will also invoke these principles in some upcoming posts.

References cited

Stebbins, G. L. 1974.  Flowering Plants: Evolution above the Species Level.  Belknap Press of Harvard University.

What's so primitive about Amborella?

The male flowers of Amborella are crowded with stamens.
Photo by Scott Zona, posted on Wikipedia

The discovery that the lonely species Amborella trichopoda occupies the tip of the most ancient known clade of flowering plants has caused quite a sensation in the botanical community.  Here was the closest living relative of the common ancestor of all known flowering plants - a glimpse of what that ancestor might have been like! (Bailey & Swamy 1948).

Amborella is in the same position relative to angiosperms in genera, as Acorus is to other monocots.  I argued in a recent post (What's so primitive about Acorus?), however, that being at the tip of a very long evolutionary branch does not necessarily mean being exactly the same as the very first members of that branch.  It is likely in fact that some changes have been made as conditions and competition changed over the tens of millions of years since that ancient phylogenetic split.  I identified several ways in which Acorus was probably more advanced than some other archaic monocots that branched off slightly later.

The female flower of Amborella
contains several carpels and a few
sterile stamens.  The carpels are
ascidiate and unsealed. An opening
just below the stigma is blocked
only by a drop of fluid.
 Photo by Sangtae Kim

So we must consider that possibility with Amborella.  If Amborella is the sister group to all other known angiosperms, it must have split off somewhere between 120 and 140 million years ago, certainly time for a few changes to have occurred.  There may have been a whole family of amborellids early on, perhaps adapted for different light levels, soil types, pollinators, fruit dispersers, etc. Some may have even been flirting with the aquatic habitat, for the very next branch on the angiosperm tree consists of the waterlilies and their relatives.  We have no idea - because at present at least, we have no fossil record of this lineage.  All we have is the one species that survived to the present day.

To be sure, Amborella trichopoda,  has retained a number of truly archaic features. For one thing, it has the most primitive wood (consisting only of tracheids), of any living angiosperm (Carlquist & Schneider 2001). It also has very basic flowers, as we'll see below.

Amborella occurs in the rain forests of New Caledonian, a gentle environment isolated from both climate change and the hotbeds of aggressive evolution on the continents.  Other relics of past ages survive in similar habitats, including the nearly-as-ancient order Austrobaileyales.

If we include the Austrobaileyales and the Nymphaeales with Amborella in our analysis, we can create a more general picture of the ancestral angiosperm.  Together these three clades are referred to as the ANITA grade, and contrast with the higher angiosperms of the magnolids, eudiots, and monocots. Each can be assumed to have a different mix of ancestral and specialized characteristics.  The likely characteristics of the ancestral flower have been in fact derived from a study of this group (Endress 2001).

In this model, the ancestor of all known angiosperms had bisexual flowers consisting of simple, separate organs: tepals, stamens and carpels, which were spirally arranged and indefinite in number. Advancements from this model, such as carpels fused into a compound pistil, stamens in whorls of definite numbers, and tepals in two distinct whorls of sepals and petals, show up in various higher groups at different times.

Three other aspects of the carpels are also part of the model:

1. carpels are unsealed. They are open just below the stigmatic region, and entry of dirt, pathogens and small animals is blocked only by a drop of fluid. This contrasts with most modern carpels, which are completely  sealed by a tight suture.

2. carpels are ascidiate, i.e. urn-shaped. The wall of the carpel is smooth and seamless,  like a sock pulled up around its contents. This contrasts both with earlier accepted models of the first angiosperm carpels, and those of most modern angiosperms, which are plicate (folded).  In the plicate model, a row of ovules along each margin of an ancient, leaf-like structure were brought inside as the margins joined together in a tight suture.

3. carpels contain just a few ovules placed opposite the backbone of the carpel, though there is some variation. Amborella has just one ovule, some waterlilies have many.

The carpel of Amborella is ascidate and unsealed at the top,
though the stigma region shows a folded structure
consistent with the plicate model  of the carpel.
Drawing from Bailey & Swamy (1948)

In the plicate, or folded-leaf
model, the first carpels folded
or rolled together, bringing rows
of marginal ovules inside. The
two edges eventually became
tightly sealed by an interlocking
suture.
Drawing from the 1879
textbook by Asa Gray

Assuming that this correctly describes the flower of the common ancestor, Amborella is likely specialized in several ways.  First the flowers are relatively small compared to others like most waterlilies, Austrobaileya, and Illicium, and massed together in an apparent group display. Masses of small, whitish flowers are common among eudicots, magnolids and monocots. Examples include viburnum, most palms, and carrots/Queen Anne's lace. Such displays are adaptation for a particular pollination strategy involving a variety of insects and possibly wind (Thien, et al. 2003).

 The flowers are also unisexual, with pollen-producing flowers on separate plants from those that bear ovule-producing flowers.  Such an arrangement is likely  a means of avoiding self-pollination (Ferrandiz et al. 2010).  Similar patterns can be seen in a variety of other plants, such as date palms.  The fact that the female flowers contain  sterile stamens between the tepals and the carpels is compelling evidence that the ancestors of Amborella did indeed have bisexual flowers. This has recently been confirmed by Sauchet et al. (2017).

The fruits of Amborella are described as small drupes.  These are fleshy fruits with large seeds filled with food reserves, typically adapted for germination in shady forests.  Drupes are found among many different families of flowering plants, but to my knowledge are always the endpoints of evolution from more generalized ancestors with flexible ovule production.  In the Rose family, for example, drupes are found in the genus Prunus (plums, cherries, etc.), a specialized genus in a family that includes a wide variety of fruit types.

The bisexual flowers of Austrobaileya have a
number of carpels, each containing two rows of
 ovules, as well as flattened, blade-like stamens.
Source: http://www.naturalist.if.ua/?p=3585

Drupes are constrained developmentally to produce only one ovule, which becomes surrounded by a pit, a hard layer the develops from the inner fruit wall.  Reorganization of the development process to begin producing more ovules, and in two rows at that, would require numerous genetic changes.  It would conceivably happen if there were selective pressure to produce more, smaller seeds, but this could be  much more easily accomplished by increasing the number of carpels in the flower, or by increasing the number of flowers produced.  Such a rigidly one-seeded carpel is therefore not likely the ancestor of the variety of carpels and fruit types we find among angiosperms today, or even what we find in the ANITA grade. Something like the multi-seeded fruit of Austrobaileya is a much more likely starting point for all kinds of fruits, including drupes, berries, and capsules that open to release their seeds.

In sum, Amborella is likely specialized in its floral display, unisexual flowers, and single-seeded carpels.  In other ways, it does show its age: wood without vessels, simple, separate flower parts of indefinite numbers, and unsealed carpels.  Its present very limited distribution in forests of New Caledonia attest to its archaic status and its proximity to extinction.  The few ways in which it has specialized are probably the keys to it still being with us.

This discussion leads to a deeper question of the nature of the first angiosperm carpels, which evolved well before the common ancestor of living angiosperms.  Were they ascidiate or plicate? The ascidiate carpel itself may be an adaptation for making berries and drupes, maybe nuts and achenes as well, but does not lend itself to carpels that must reopen as capsules, follicles or legumes.  So were the very first carpels fleshy berries?  I'll take that up in a future post.

References:

Bailey I. W. and Swamy B. G. L. 1948 Amborella trichopoda Baill., a new morphological type of vesselless dicotyledon. Journal of the Arnold Arboretum 29: 245–254.

Carlquist, S. J. and E. L. Schneider. 2001. Amborella trichopoda: relationships with the Illiciales and implications for vessel origin. Pacific Science 55 (3): 305-312

Endress, P. K. 2001. The Flowers in Extant Basal Angiosperms and Inferences on Ancestral Flowers
International Journal of Plant Sciences 162 (5): 1111- 1140

Thien, L. B. , T. L. Sage, T. Jaffré, P. Bernhardt, V. Pontieri, P. H. Weston, D. Malloch, H. Azuma, S. W. Graham, M. A. McPherson, H. S. Rai, R. F. Sage and J-L. Dupre. 2003. The Population Structure and Floral Biology of Amborella trichopoda (Amborellaceae) Annals of the Missouri Botanical Garden 90 (3): 466-490.

Sauquet, Hervé, Balthazar, Maria von …Schönenberger,Jürg. 2017  The ancestral flower of angiosperms and its early diversification. Nature Communications volume 8, Article number: 16047  

Mosses of Central Florida 6. Ditrichum pallidum

Ditrichum pallidum plants are like tiny clumps
of grass.

[For other mosses in this series, see the Table of Contents]

Ditrichum pallidum (Hedw.) Hampe (Ditrichaceae) is one of the grass-like mosses. Each shoot consists of
a clump of elongate, grass-like leaves that consist mostly of an elongate midrib (costa). Cells in the upper section are elongate-rectangular, but overlapping and hard to distinguish.   The actual blade of the leaf flares out briefly at the base, where one can see relatively large ovate to rectangular cells.  The capsules rise from elongate, straight stalks, and  and remain more-or-less upright throughout.  At maturity, the capsules are narrow, nearly cylindrical, and with a single row of short teeth around the mouth, attached just below the surface.

Most of the leaf is the thick, prolonged tip of the
midrib, with elongate-rectangular cells.

Near the base, one can find the thin,
flaring blade, with ovate to
rectangular cells.

This species is widespread in both the old and new worlds, having been reported from Europe, Africa, Japan, and eastern North America.  It is common in Florida and found as far west as eastern Texas.  This distribution is consistent with its preference for disturbed soil along roads, fields, lawns, and forest openings.

When dry, the capsules are nearly cylindric, with
blunt tips. Just inside the mouth is a single row
of small teeth.

Medicinal plants in our own backyard

The discovery of plants with medicinal or health-promoting properties began with indigenous cultures around the world thousands of years ago.  The practice of herbal medicine is truly the "oldest profession," and even pre-dates humanity.  Chimpanzees are known to seek out certain plants in their native forests that can relieve illness or discomfort. One such plant comes from a shrub native to the forests of Africa called Aspilia (Asteraceae), which has been shown to kill bacteria, fungi and nematodes in the intestinal tract.  It may also serve as a stimulant - the morning coffee for chimps.  Each culture has discovered useful plants in their own backyards, and modern medicine is now slowly exploring that priceless knowledge and verifying what these people have known for a long time.

The prickly poppy, Argemone mexicana, was introduced into Africa in the
19th century and has been used as a medication against malaria almost
as long. Photo by B. Navez, posted in Wikipedia.

So it was a personal surprise to me - even though I teach a course in Medicinal Botany - that a plant frequently found in my own backyard has within it compounds that may cure malaria.  The plant is Argemone mexicana, the prickly poppy. The new information was featured in the recent issue (June 2014) of Scientific American, in the article "Seeds of a Cure," by Brendan Borrell.  The article describes the efforts by researchers working in the field in Africa, Mali to be specific, to document the effectiveness of the plant among people taking this natural medicine as an herbal tea.  The researchers documented a successful cure rate of about 89%, which compares quite favorably with the 95% rate of the much more expensive conventional treatments based on artemisin.

I went back to my classic textbook on medicinal botany by Lewis and Lewis, and found mention of prickly poppy as treatment for heart arrhythmias, but not malaria.  So I didn't feel so stupid then, but a still little bit ignorant compared with the native African healers who have been using this for over a century. The plant is native to tropical America, and was introduced into Africa sometime in the 19th century, which means the native healers there caught onto its medicinal properties fairly quickly!  We tend to think of traditional healers in general as following procedures cast in stone hundreds or thousands of years ago - a clearly unjustified stereotype.  In this instance at least, there were  intellectually flexible experimenters in the profession.

So what are the active principles in  prickly poppy tea? The Lewis text indicates a-allocrytopine obtained from the roots as the active principle in treatment of heart arrhythmia.  It also indicates that a more toxic mix of sanguinarine, berberine, protopine is present in the plants, and that prickly poppy occasionally contaminates grain.   This may be from the seeds of the prickly poppy, which have been implicated in poisoning events in India.  Sanguinarine is considered the primary culprit.

The leaves, however, have little sanguinarine, and the herbal tea, according to Borrell, is fairly non-toxic.  Isolated berberine has shown some anti-malarial effect, but much weaker than that of whole leaf infusions. So it is not known exactly what mix of compounds in the leaves is so potent against malaria.

Argemone mexicana might  turn out to be the tip of an iceberg.  There are 32 species in this genus, native mostly to tropical America, with one species in Hawaii.  Relationship among plants is highly predictive of similarity in secondary plant compounds.  These other species may have similar or even better combinations of compounds for treating malaria or other parasites.

This is not to mention the numerous other genera and species of the poppy family.  One must of course be very careful to steer away from the dangerous compounds found throughout this family, including the opiates in Papaver somniferum.  As I say on the first day of my medical botany course: "DO NOT TRY THIS AT HOME!"  Self-experimentation with natural plant compounds is exceedingly risky. If you can get a hold of the Lewis text, there is an excellent section on all the ways people inadvertently poison themselves.

The study of medicinal botany is both ancient and very new.  The new part is applying the modern scientific method to finding and verifying the curative or preventative properties of plant compounds.  The possibilities and opportunities in this field are endless.

References:

Borrell, Brendan.  2014.  Seeds of a Cure.  Scientific American 310 (#6): 64-69.

Lewis, W. H. and M. P. F. Elvin-Lewis. 2003.  Medical Botany, 2nd Ed., John Wiley and Sons.

The Birthplace of the Angiosperms

The Fynbos of South Africa consists of
drought-resistant evergreen shrubs and
ephemeral herbaceous wildflowers.

One of the great thrills for any botanist, gardener, or wildflower enthusiast is a visit to the southwestern tip of Africa in the springtime, as featured in the current series on my wildflower page.  Rain falls mainly in the winter here, as it does in southern Europe or California, creating a Mediterranean type of climate at the tip of a largely tropical continent.  Rainfall varies, creating relatively lush shrublands, locally called Fynbos, along the southern coast, and these grade into desert to the north and west.  The isolation, rough terrain, and diversity of microhabitats has resulted in one of the richest and most spectacular floras to be seen anywhere in the world.  The moistening of the soil in the winter releases a frenzy of growth and reproduction in plants that have been dormant for 9 to 11 months, blanketing the usually barren fields and rocky hillsides with brilliantly colored wildflowers.  In a month or two, the show is over and the Fynbos sleeps again.

According to some theories, the flowering plants, or angiosperms, began their existence in an environment similar to the semi-arid hills of southern Africa today.  Such regions provide varied challenges to both survival and reproduction. The short growing season and limited rainfall in particular force plants to economize in numerous ways, to shorten their reproductive cycles and decrease their exposure to the long dry summers.  Many go dormant, surviving underground as bulbs, corms, or tubers.    Adaptations to such habitats by early angiosperms opened the door to herbaceous life styles not available to the slow-growing and slow-reproducing gymnosperms.   

  

The Iris family, represented here by this brilliant Gladiolus,
is one of the families that has diversified recently in semi-arid
regions of Africa.

          Semi-arid habitats also tend to be fragmented by rocky terrain into patches of varying moisture, temperature, and soil conditions.   The north side of a rock, for example, has less sun exposure than the south side and remains moist longer.  Streambeds and marshes remain wet longer and provide additional habitats.  This breaks up populations of plants into small localized subpopulations, which may become further isolated through adaptation for specialized pollinators.  Isolation is key to the birth of new species, and promotes rapid evolution among plants.  Plants inhabiting such areas today are among the most progressive and diverse of angiosperms, and include members of the legume, sunflower, iris, and grass families, to name only a few.  These families represent the current cutting edge of plant evolution. 

The rough terrain of the South African uplands creates numerous microhabitats.

For these reasons, botanists such as Daniel Axelrod (1952) and G. Ledyard Stebbins (1974) proposed that semi-arid subtropical uplands similar to those seen in South Africa today serve as “cradles” of evolutionary innovation, where successive waves of plant innovation have occurred.  The cutting edge of plant evolution 120-180 million years ago consisted of the precursors of flowering plants.  Lowland moist forests, long thought to be the home of the first flowering plants, would have provided no incentives to shorten the life cycle or invent new forms of vegetation.  Diversification of early flowers and modes of pollination also would have been favored in semi-arid environments, where insects are abundant late in the wet season and compete fiercely with one another for limited resources. 

If this model of evolutionary cradles is correct, it helps to explain Darwin’s “abominable mystery.”In the fossil record, angiosperms appear rather abruptly, and in great diversity.  There is no sign of the “missing links” between earlier seed plants and those with flowers.  If early angiosperms and their precursors lived in hilly, semi-dry environments, where fossilization rarely takes place, they would not have left any traces in the rocks. Flowering plants, and the seed plants leading up to them, may have lived in upland environments for millions of years before some of their descendants moved into the forests and swamps of the lowland flood plains, where fossilization was more likely.  The fossil record of angiosperms began with those lowland immigrants, and by that time there were already many different kinds. 

Before this “semi-arid upland” theory, it was generally believed that angiosperms had evolved in moist lowland forests.  This is where we find the most archaic living angiosperms, such as Amborella, the Austrobaileyales, and many magnolids. To Stebbins, however, such forests were “museum” habitats that harbored refugees from earlier waves of evolution in the dry uplands as they were replaced by newer forms of plant life.  Successful new kinds of plants tend to radiate into different habitats, including moist forests and wetlands.  One early wave led to the waterlily order (Nymphaeales), a very ancient lineage, but one that is still quite successful and widespread today.

Think of a department store as an analogy.  The newest fashions are on the front-line, full-price racks.  This is where the action is – where new fashion trends evolve and all the cool people buy their clothes.  As these fashions are replaced by newer designs, the remnants migrate to the bargain racks in the back of the store.  The clearance racks are the museum habitat for clothing fashion.  Most will gradually disappear, but a few of the more interesting ones may persist in actual museums featuring clothing fashions of past eras.

Despite that attractive logic, there are still arguments that angiosperms may have in fact evolved in moist lowland habitats.   Taylor Feild (yes, his name is Feild, not Field, as I’ve had to explain numerous times to my spell-checker and one reviewer of my manuscript!) and colleagues (Feild et al., 2004)  have examined the physiology of living archaic angiosperms, representing diverse families, and found them fundamentally adapted to moist, shady, and disturbed habitats.  According to the “dark and disturbed” hypothesis, habitats subject to frequent disturbance would have promoted the shorter life cycles and vegetative flexibility inherent to angiosperms.  Genetic evidence indicates that these forest adaptations appear to have been inherited from a common ancestor, suggesting that they stemmed from the earliest angiosperms.  So the ecology of angiosperm origins is not yet fully agreed upon.

A tale of stem and crown

Perhaps, however, the real story will turn out to be a combination of the dry upland theory and the dark and disturbed theory.   Those advocating a dry upland origin for angiosperms, were suggesting that the fundamental features of angiosperms evolved gradually in upland habitats in the early angiosperms or even pre-angiosperms.  Feild, on the other hand, suggested only that the angiosperms we know today had a common ancestor that evolved in a dark, disturbed environment.  What’s the difference between these two statements? 

All living angiosperms have a hypothetical common ancestor, and together constitute the “crown group” of angiosperms.  That common ancestor was not the very first angiosperm, however.  It emerged from a long line of early angiosperms and transitional pre-angiosperms, which constituted the “stem group.”  Aside from the crown group ancestor and the living angiosperms that descended from it, all stem angiosperms, by definition, are now extinct.  

 

The angiosperm stem group (yellow) consists of various extinct pre-angiosperms and early angiosperms. Modified from general diagram provided by Wikimedia commons.

  Early development of the angiosperms, and the evolution of their key features, may very well have evolved among stem angiosperms living in semi-dry uplands, as proposed by Axelrod and Stebbins.  That environment still offers the greatest stimulation for evolutionary change, and in particular for the types of changes that led to the angiosperms.  The early angiosperm that was destined to give rise to all modern angiosperms, however, apparently migrated into a “dark, disturbed” environment, where the finishing touches of angiospermy were applied, giving rise to a diverse, flexible and aggressive group of plants that came to dominate the earth.  So the different theories, like blind men feeling different parts of an elephant, described different parts of the story: one begins where the other leaves off.  The real story may prove to be even more complex, however, for plants have repeatedly moved from wet habitats to dry habitats and vice versa.  Only time will tell.

This article is a modified excerpt from "A Brief History of Plant Life," to be published next year.

References:

Axelrod,  D. I.  1952. A Theory of Angiosperm Evolution. Evolution 6(1): 29-60.

Feild, T. S., N. C. Arens, J. A. Doyle, T. E. Dawson, and M. J. Donoghue. 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30: 82­107.

Stebbins, G. L.  1974.  Flowering Plants.  Evolution above the species level.  Belknap Press of Harvard University Press.  Cambridge, MA.

Mosses of Central Florida 5. Syrrhopodon incompletus

Syrrhopodon incompletus growing on the spongy trunk
of a date palm (Phoenix dactylifera) on the University
of South Florida campus

[For other mosses in this series, see the Table of Contents]

Syrrhopodon incompletus Schwaegr. (Calymperaceae) is a relatively common moss found throughout the coastal plain of the southeastern U.S., occurring mostly on tree trunks, including palms, and exposed roots. It has a short upright stem with relatively large leaves, typically 3-5 mm in length, crowded into a circular pattern called a rosette ("rose-like"), and thus superficially resembles Octoblepharum.  The leaves are thinner, however, just one cell thick except for the prominent midrib, with small teeth along the margins, and are translucent green.

The leaf cells of this species are small, roundish and thin-
walled, and each has a small, hard, pimple-like outgrowth
called a papilla.  The marginal cells are similar in size, shape,
and coloration, but with an occasional short tooth.

The leaf cells are roundish or polygonal and thin-walled.  This genus is also characterized by an extensive and conspicuous basal region of large rectangular clear cells.  Leaf cells and the midrib have tiny rounded outgrowths called papilli, particularly on the back side.  When dry, the leaf margins roll inward, creating an almost tubular configuration, and this then twists and curls irregularly.

The large leaves have a strong midrib (or costa) and the basal region is composed of large, empty, rectangular cells.

When dry, the leave roll into a tube and then twist and curl.

The capsules (sporangia) arise from the tips of the stems, and are upright, symmetrical, and narrowly ovoid to cylindrical (when dry).  Teeth of the capsule mouth (peristome) are short and attached below the rim.  

The sporophytes arise from the tips of the stems, and the sporangia are upright and symmetrical.

Several other species of Syrrhopodon occur in Florida.  S. incompletus is characterized by the marginal cells of its leaf, which are slightly thickened but green and shaped more-or-less like the other cells of the leaf.  The other species have distinctive elongate, clear cells along the margin. S. texanus also has much more prominent spines along the margins and particularly on the lower midrib.  

A leaf by any other name

The leaf-like segments of Schlumbergera, are parts of the
stem system.

What is a leaf?  For practical purposes, it might be any flat, photosynthetic plant organ.  Yet we know that there are certain “stems in leaf’s clothing” in the botanical world.  Cacti evolved in deserts, where leaves were a liability, and thick, succulent stems took over the job of photosynthesis.  Many cacti that have adapted as epiphytes in the tropics, such as Schlumbergera (Christmas cactus) and  Epiphyllum, however, have “reinvented leaves” by making their stem segments flat and thin. 

Many brown algae produce large, leaf-like fronds.
Line drawing from Allen & Gilbert, 1917, A textbook
 of botany. 

To be fully convincing as a leaf, a structure must not only be flat and photosynthetic, but also limited in size and shape (determinate), and produced in a regular pattern around a central stem.    Leaves also have a certain lifespan, after which they fall off of the plant, or sometimes remain as a dead skirt, as in Washingtonia palms.  New leaves are produced at the tips of stems that continue to elongate over time.  This would rule out leaf-like cacti, in which the flat segments are produced one from another like links in a chain.  They are parts of indeterminate, branching stem systems - stems in leaf’s clothing. 

Even within that more restrictive definition, flat photosynthetic appendages that are commonly referred to as leaves have evolved independently many times.  The leaf-like shape, not surprisingly, is nature’s most efficient light gathering antenna, and so has been reinvented over and over again. Many algae have adopted this highly successful growth form.  Kelp, for example, form underwater forests of long stems bearing many leaf-like fronds produced in sequence from an embryonic tip (an apical meristem).

The "leaves" of leafy liverworts, like this Lejeunea, are
flat extensions of the thallus.

The first flattened, photosynthetic structures to appear in land plants were the thalli of ancient liverworts.  A thallus is a plant body that is not clearly defined into organs like stems and leaves.  A thalloid liverwort is flat and photosynthetic, but grows and branches at its tip like a stem.  Some liverworts are called “leafy liverworts,” because their thalli are subdivided into small leaf-like segments with slender stem-like sections in-between.   Mosses are more convincingly leafy, with

determinate, leaf-like structures attached spirally around a stem,  but purists prefer to not call any bryophyte structures leaves because they evolved independently of the “true leaves” of other land plants.

 

Mosses, like this Barbula agraria, have distinct leaves produced one at a time by the stem apex.

Club mosses, like this Lycopdiella cernua
 from Florida, have small scale-like leaves
called microphylls.

However, the true leaves of vascular plants evolved at least twice from scratch, and were subsequently completely remodeled several times.   Early land plants had perennial creeping stems, called rhizomes, plus short-lived upright shoots adapted for gathering light and producing spores.   The early upright shoots were little more than green, forking stems, but competition for light soon forced them to evolve more efficient light-gathering structures.  In clubmosses (Lycophytes) the answer came in the form of flat but narrow leaves with a single vein of vascular tissue running through them.  They are referred to technically as microphylls, and are believed to have evolved as simple outgrowths of the surface tissues of ancient stems.  A more recent hypothesis is that microphylls evolved from sporangia that were “sterilized” and flattened.  Precursors of lycophytes produced numerous sporangia on short stalks along the sides of their upright leafless stems.  So converting some of them into leaves would have been a fairly simple adaptation.  In either case, leaves of lycophytes can grow in length, but cannot develop complex shapes or much breadth.

The fronds of ferns are
upright shoots flattened into
a leaf-like configuration.  From
Smith, 1955, Cryptogamic Botany.

The complex fronds of ferns, which bear sporangia on their.

The large complex leaves of ferns are called megaphylls.

lower surfaces, as well as conducting photosynthesis are  upright shoots that became leaf-like
through fine-branching and  flattening.  Such leaves are called megaphylls.  Megaphylls can be called leaves because they are produced sequentially at the tips of the ongoing rhizomes, have a definite size and shape, and fall off of the plant after one or a few seasons

The upright shoots of horsetails are equivalent to the fronds of ferns,
 but consist of repeated whorls of small leaf-like branches and
elongate stem segments.
From Kerner & Oliver, 1904, The natural history of plants.

The upright shoots of horsetails, cousins of the ferns, evolved a little differently.  They too are determinate, photosynthetic, and spore-bearing, and are discarded after a defined period of time, but they remained stem-like with smaller leaf-like segments.  Though modern horsetails don’t have leaves, their earliest ancestors had short, fan-shaped leaves born in a circular arrangement at intervals along the upright shoots.   They evolved a unique, bamboo way of growth, in which stem segments elongate to extend the entire shoot quickly upward (see The first “bamboos,” 28 Mar, 2012). These smaller leaves are also called megaphylls, though each is equivalent to only part of the fern megaphyll.  Spores are produced, not on the leaves, but in specialized cones at the ends of upright shoots. 

  This is an
ancient horsetail ancestor called Lilpopia,
with small megaphylls, each equivalent
to just a small part of a fern frond.

Cycads have compound leaves
descended from the fronds of seed ferns.

The leaves of the cycad Bowenia are doubly compound, and
the most like ancient seed ferns.

The leaves of flowering plants, as well as cycads, are

Archaeopteris was an ancient spore-bearing
tree that may have been a precursor to
both seed ferns and conifers. These lateral
leafy systems may have evolved directly into
seed fern fronds or into branch systems of
small needle-like leaves in the conifers.

also considered to be full  megaphylls, having evolved from the large fern-like fronds of plants known as “seed ferns.”  Seed ferns evolved in much the same ways as ferns, though probably independently from leafless ancestors, and bear seeds and pollen sacs directly on the leaves.    In conifers and ginkgos, however, needle-like and fan-shaped  leaves may represent segments of ancient megaphylls that became more twig-like.  Short leafy shoots of these plants would then be evolutionarily equivalent to entire seed fern fronds.  The common ancestors of all seed plants, the progymnosperms, had leafy systems that were complex and frond-like, but not clearly defined as either determinate or indeterminate.   Thus both types of systems could have evolved from them. 

The leaves of conifers, such as this
Araucaria, are
simple, and flat or needle-like.

Angiosperm leaves, like this Tetrapanax,
can be large and complex.

Leaves in the eudicot family, Apiaceae, are typically
compound, and can be quite fern-like, as in this variety of
parsley.

The leaves of flowering plants, though evolving from seed-fern type ancestors, are extremely varied in structure.  Some are complexly branched, like their ancestors, others are small and simple, even scale-like in some cases.  Their extreme evolutionary plasticity demonstrates the innate potential for growth and complexity inherent to the original megaphylls.    Angiosperm leaves, moreover, develop in two different ways, in accordance with what we might call the “dicot model” and the “monocot model.” 

Dicotyledonous plants occur in several distinct clades, mostly in the Eudicot clade, but also in the more ancient Magnolid clade, and the most ancient clades of the ANITA grade (Amborella, Nymphaeales, and Austrobaileyaceae – another long story!).  In this developmental model, leaves begin as tiny peg-like primordia at the tips of the stems, after which they develop their characteristic shapes in miniature.  Complex, dissected, and irregular shapes develop through marginal meristems expanding locally at different rates.   After the shape has been formed (and in some climates after a period of dormancy within a protected terminal bud), the leaves expand two-dimensionally, increasing in size but retaining the shapes developed in their infancy.

In the eudicot, Liquidambar, leaves
develop their shape first in miniature,
then expand to their full size.

In the monocots, leaves being as hood-like primordial, with a basal sheath surrounding the apical meristem, then expand primarily through basal growth (see How the grass leaf got its stripes, 26 Jan 2012).  By growing only from the base, typical monocot leaves are long and strap-like and their veins of vascular tissue run parallel to one another.

The typical monocot leaf grows from the base,
 resulting in a strap-shaped structure and
parallel veins.
From Rost, et al., Plant Biology

All of these structures can be called leaves, though they develop in different ways.  Botanists will continue to use more precise technical terms for leaf-like structures that evolved independently.