What's so primitive about Acorus?

So first of all what is Acorus, and why would anyone think it primitive?

Acorus is a marginal aquatic with sword-shaped leaves
typical of monocots, and flowers densely packed onto
a thick spike resembling the spadix of an aroid.  Photo
by H. Zell, posted in Wikimedia commons.

Acorus, commonly known as Sweet Flag, is a widespread marginal aquatic plant native to North America and Asia.  A marginal aquatic is essentially one in which the roots are in soil that is waterlogged most of the time. So they occupy shallow water at the edges of streams, lakes and swamps, as well as marshes and intermittently wet prairies. The leaves of Acorus are flattened into a fan-like arrangement at right angles to the rhizome, similar to many members of the Iris family.  It's flowers, however, are small and crowded onto a dense spike resembling the spadix of an aroid (e.g. Calla lily or Anthurium).  It was in fact classified as an aroid until recently, generally as its most archaic member, but now has been placed in its own family and order.

In this simplified phylogenetic tree of the monocots,
Acorus is the first clade to branch off.  It is the
 sister clade to the common ancestor of all the
 remaining monocots.  Alismatales includes
mostly aquatic plants, but also the mostly
terrestrial aroids (Araceae).  The Commelinoids
 include palms, gingers, and grasses (among others),
while the Lilioides include lilies, irises and orchids.

This new placement is based on recent phylogenetic studies which suggest that Acorus is the sole representative of the most ancient lineage of monocots.  In technical parlance, we say that the single genus Acorus, in its own family and order, is sister group to all the rest of the monocots.   In other words, the ancestor of Acorus split from from the common ancestor of all other monocots 120 million years ago or more.  So we look at it and we say, "so this is what the first monocots looked like!"

Well, probably not.  The truth is that we know very little about what the first members of the Acorus clade looked like, or what kind of habitat they lived in, let alone earlier monocots.  We have no fossils of any of them. The modern genus Acorus is the end points of over 100 million years of evolution, and the lineage certainly has changed in some way over that time, possibly with earlier genera now extinct.

As an analogy, Homo sapiens is the sole surviving species of the family Hominidae, but does that mean that the first members of the family looked or behaved just like us?  We happen to have a pretty good fossil record of our own history, and know that we were preceded by Australopithecus and even more ancient forms.  These early hominids walked upright, but other than that looked a lot more like chimpanzees that like us, and we are separated from them by a mere 5-6 million years.

What we can say is that the common ancestor of the Acorus clade, as it split from the main monocot line, already had the basic features of all monocots:  leaves with parallel veins that grow from the base, a single seedling leaf ("cotyledon") in the embryo, a clonal herbaceous growth form lacking in secondary growth ("wood"), and an entirely adventitious root system (no taproot or other permanent root system).  (See How the Grass Leaf Got its Stripes, January 26, 2012).  Monocots mostly also have flower parts in 3s - 3 sepals, 3 petals, 6 stamens, and 3 carpels. This also appears to have been established by the time the Acorales split off the family tree.

We know even less about the "stem monocots," early monocots that preceded the origin of the Acorus clade and bridged the transition from dicotyledonous plants.   Phylogenetic studies indicate that the monocots originated in or near the Magnolid clade. This clade includes diverse kinds of plants, from the lofty Magnolia trees to the herbaceous or semi-herbaceous members of the Aristolochiaceae and Piperaceae, but no aquatics similar to Acorus.  So there was a kind of "evolutionary wormhole" into which went plants with broad, dicotyledonous leaves and embryos with two cotyledons, and out of which emerged true monocots with sword-shaped leaves and a single cotyledon.

So in what ways might the modern Acorus species be like stem monocots?  And in what ways are they likely more specialized?  Were the first Acoroids  marginal aquatics, like the modern species?  They likely were, since the next clade to branch off the monocot  tree, the Alismatales, consists largely of  aquatics as well. This vast assemblage ranges from marginal wetland plants like Sagittaria to fully-submerged sea grasses.  It includes also the aroids, which range from marginal aquatics to rain forest epiphytes.

The sword-shaped monocot leaf, which pushes upward from a basal growth zone (basal intercalary meristem) appears, however, to have been shaped by a strongly seasonal environment subject to grazing and fires.  It is a leaf adapted for rapid regeneration from an underground stem system.  If the leaf tips of young grass leaves are burnt or bitten off, for example, the basal growth zone can reactivate and restore the blade.

The  unifacial leaves of Iris, Acorus, and many
other monocots are "folded" with the two
halves  in the  lower part pressed together to
forming a flat, narrow sheath.  The upper part
is solid, as if the two sides were glued
together.  Each new leaf emerges through
the sheaths of adjacent leaves.

Also, as monocot seeds germinate, the single cotyledon usually remains within the seed.  It lengthens at its base like monocot leaves in genera, but this serves to push the rest of the embryo deeper into the soil, rather than to push itself into the light.  This suggested to the great evolutionary botanist G.L. Stebbins (1974) that the first monocots were adapted to environments that were alternately very wet and very dry, like a modern savanna.  Seeds germinated when the soil was wet, with the embryo being "planted" deeply in the mud.  The embryo was thus protected from desiccation when the soil later dried out.  So most likely the early monocots evolved within a range of savanna to marshy habitats, where a great many monocots, from grasses to cat-tails, live today.

In what other ways might Acorus either resemble or differ from early monocots?  Most likely the flowers were larger, fewer in number, and more loosely arranged than they are in the present dense spike.   The trend from loose clusters of flowers to dense spikes, as far as we can see, is a one-way trip.  The spike is an efficient reproductive structure, a "super-flower" if you like, that becomes more and more specialized.  It often becomes surrounded by other structures, like the spathe of the aroids, that not only protect the flowers, but also serve to attract pollinators or manipulate their movement over the stamens and stigmas.  It is hard to imagine any selective pressure that would cause that trend to reverse.  Families that contain small flowers in dense spikes include the Araceae, some Arecaceae (palms), Cyclanthaceace, Pandanaceae, Piperaceae, Saururaceae, and to a smaller degree many other families.  In none of these has the trend ever reversed.

Also, we might expect that the carpels (the chambers in which the seeds develop) of the ancestral monocots were separate from one another (apocarpous).  Most ancient angiosperms, including most Magnolids, and most Alismatales (other than aroids), have separate carpels. The three carpels of Acorus, however, are solidly fused together and share a common stigma, the way it is in more advanced angiosperms in general.  Once carpels are fused together, they rarely revert back to separate entities, except sometimes to produce specialized fruit types like the schizocarps of the Apiaceae (carrot family) or the follicles of Asclepiads (milkweeds).  So in this way modern Acorus is more advanced than the Magnolids that preceded it and the Alismatales that followed it.

Tofieldia, in the Alismatales, grows in moist meadows. Its
carpels are only loosely joined together, retain separate
stigmas, and separate as they mature into seed capsules
 (follicles).

What about the fan-shaped clusters of leaves?  The leaves of Acorus are unifacial, which means that the leaf blades appear as if they were folded and fused together, so that both sides are really the back side (abaxial) of a normal leaf.  The apparent fusion of the two sides of the leaf occurs just above the opening of the narrow sheath through which newer leaves emerge.  Leaves like this are common in the iris family, in Butomus and Tofieldia in the Alismatales, and scattered among other monocot families.  Butomus and Tofieldia incidentally both have carpels more separate from one another than in Acorus, and so in that sense are more archaic.

The flowers of Butomus, in the Alismatales, are larger, in
looser clusters, and have separate carpels, and so
are probably more like the ancient monocot flowers than
are those of Acorus.

It is possible that the common ancestor of Acorus and other living monocots had unifacial leaves.  More ordinary open leaves, as found in grasses, cat-tails, daylilies, etc., could have evolved from them by increasing the growth of the open sheath region and reducing the growth of the unifacial blade.  Or the reverse could have occurred, as it evidently has happened multiple times in different families, perhaps as an adaptation to the marginal aquatic environment.  The stiff fan-shaped cluster of leaves may be more sturdy in the face of moving water or flooding.

 Monocot leaf development is highly flexible, as growth emphasis can easily be shifted from one part of the leaf to another, resulting in the vast array of monocot leaves from grass blades to palm fronds, paddle-shaped banana leaves, and heart-shaped yam (Dioscorea) leaves.  This perhaps more than anything, is the key to the great diversity of monocots today.

A very young monocot leaf resembles the hood
of a sweatshirt.   The tissues surrounding the opening
represent the young leaf sheath, with the next younger leaf and
apical meristem (AM) visible within.
The tissues around the opening will form the sheath of
the mature leaf.  A zone of dividing growing cells
(meristem) that forms around the base of zone A will
 form a  cylindrical leaf sheath.  If a meristem  forms
 in zone B, but not zone C, an open leaf sheath flattening
into a long, grass-like blade will develop.  But if growth
 is largely focused at the base of the solid tip (C),
 a long unifacial blade will form.  

A mixture of primitive and specialized features is common is to be expected in surviving members of ancient lineages, the specialized features no doubt the reason why these plants are still around!  The dense flower spike and fused carpels of Acorus, and possibly the unifacial leaf blade, are likely specialized features that have allowed it to not only survive, but still flourish today.



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

The long and short of it - the story of internodes

The structural units of a higher plant consist of a node,
an internode, and one ore more buds and leaves at the
node.  These units can be repeated indefinitely to form
a shoot, or modified in various ways to alter the
architecture of the plant.

Plant stems are organized into repeated units consisting of nodes and internodes.  Nodes seem to be where all the action is.  Leaves are attached at the nodes, and most often there is also a bud at the base of each leaf that has the potential to develop into a new shoot.  The new shoot also will develop as a series of nodes and internodes.


Internodes are essentially the sections of stem between nodes. Ho humm - end of story.  Not quite!  The internode in fact is a dynamic part the plant, the part responsible for most actual growth in height.  You can see the lengthening of internodes most dramatically in vines, which are adapted to extend themselves as rapidly upward as possible to reach the light zone.  In vines, cell division and expansion continue in the internodes well below the tip, propelling several sets of expanding leaves ahead of them.  Once reaching the light zone, internodes will end growth sooner, resulting in a bushier crown suitable for gathering light.  Tree saplings also show dramatic internode elongation in the shade, and many more humble plants will send their flowers rapidly upward by means of strikingly elongate flower stalks.

Internodes are quite distinct in most trees and shrubs (left), but are extraordinarily
elongate in vines like the Clematis (right).

The bamboo's elongate internodes are the secrets to its
height.

Bamboo shoots contain all the
nodes of a full stem packed close
together.  Expansion of all the
internodes, more-or-less
simultaneously, results in very
rapid growth.

Bamboos are grasses evolutionarily adapted to compete with trees, and they do so with the most extraordinary internodal elongation of all.   Each bamboo shoot begins as a compact bud, the "bamboo shoot" of culinary commerce.  Within that massive bud, the nodes and internodes for the entire shoot (culm) are preformed, but the internodes are extremely short.  When growing conditions are right, the entire bamboo shoot elongates through simultaneous elongation of all of its internodes, reaching full height in a matter of days.  The legendary "Chinese bamboo torture" consisted of strapping a prisoner over a bamboo shoot just beginning its expansion phase.  The sharp point of the shoot tip pressing against the back quickly became horribly painful.

This Pachypodium, in the Apocynaceae,
has virtually no internodes, but grows
slowly through the accumulation of
tissues at the base of each leaf.

This Neoregelia in the Bromeliad, forms a concise rosette
of leaves.

Many plants effectively have no internodes.  They are very short, or slowly build up trunks just from the bulk of the tissues around the leaf bases.  Palms and cycads are prime examples, as are many desert succulents.  Plants that hug the surface of the ground have short stems with leaves crowded into a rounded pattern referred to as a rosette (named for its resemblance to the crowded petals of a rose).  Strawberry plants, bromeliads, venus fly traps, sundews, and African violets are examples.

This tiny Drosera  rosette is dwarfed by its much larger flowers.  The flower
stalks consist of greatly elongate internodes, in contrast to the virtual lack
of internodes within the rosette of leaves.

The stalk of the Egyptian papyrus plant
(Cyperus papyrus) is a single elongate
internode.  The tassle at the top consists
of several dozen nodes packed closely
together through lack of any internode
elongation.

The growth of internodes is controlled by hormones, particularly gibberellin.  Dwarf forms of vegetables or other crops can be created by genetically limiting the plant's ability to produce or respond to gibberellin.  And plants that are normally compact, such as cabbages, can be stretched out like vines by applying the hormone to the young plants.

Gaillardia daisies are normally compact rosettes, but
under the influence of gibberellins can stretch out via
elongate internodes.

Internodes are therefore the unsung heroes of plant growth.  They determine whether a plant will be a skinny, stretched-out vine, a squat mound of leaves, or something in-between.

The first plants

Who were the first plants?   At the risk of a scolding from some of my fellow botanists, I’m going to define plants broadly as organisms that use sunlight to make carbohydrates, and release oxygen gas as a byproduct -   in other words, organisms that photosynthesize.   There is in fact a diverse array of organisms that photosynthesize, including some bacteria and various kinds of algae that are only remotely related to one another; not to mention photosynthetic sea slugs!  So used in that way, "plant" is more of an ecological term for organisms that provide the base of the global food chain, not a precise taxonomic category. (see my post of October 5, 2011, "Plants and animals and kleptoplasts - oh my!")

My goal today is in fact to explore where photosynthesis came from, and we won't be distracted by taxonomic issues.  The first organisms to practice photosynthesis were bacteria, and the cyanobacteria were the first to employ modern photosynthesis, in which oxygen is released as a byproduct.  Bacteria are prokaryotic organisms that have a simple cell structure without nucleus or internal organelles.  They don’t have chloroplasts like true plants or algae, but their entire cell is adapted to conduct photosynthesis.  In my October 5, 2011  post, I described how cyanobacteria in fact were captured and domesticated to become the first chloroplasts.   I also argued as devil’s advocate that cyanobacteria are the only true plants – the multicellular organisms that we call plants are merely the luxury condominiums in which those captured cyanobacteria live!

Cyanobacteria come in many different forms and resemble true eukaryotic algae.  Mat-forming cyanobacteria
 that build stromatolites are similar to to A and B, in which cells are bound by a mucilaginous matrix. on the
surface of a rock.  Drawing from Haupt, Plant Morphology, McGraw-Hill, 1953.

Photosynthesis was invented only once, and passed on to various eukaryotic organisms as chloroplasts, which have been captured, stolen, and recaptured many times.  But when did it all start?  We travel to Australia, where we find some important clues.

In a few shallow, highly saline lagoons along the west coast of Australia, peculiar knobby pillars of rock called stromatolites stand like the disarrayed remnants of a terracotta army, eroded and distorted beyond recognition.  These monoliths were not carved by some ancient civilization, however, but are built up very slowly by microscopic living organisms.   On the tops of the knobs, you can find mats of living microorganisms, held together by a mucilaginous glue.  The glue is secreted primarily by cyanobacteria.  Many bacteria form mats like this.  It’s a good way to anchor yourself to a suitable location.  

Stromatolites at Shark Bay, Western Australia.  Photo by Paul
Harrison via Wikipedia.

Cyanobacteria are massively abundant organisms.  Many live as free-floating plankton or tangles of filaments, and account for as much as 50% of the photosynthesis occurring in open waters (Fig. 2). Others are attached to rocks as filaments or mats.   They are easily confused with true algae, which are eukaryotic organisms with nuclei, chloroplasts, and other organelles.  Before electron microscopy showed us the difference, cyanobacteria were called “blue-green algae.”

Microbial mats on the tops of stromatolites form deposits that extend the knobby pillars slowly upwards.  Particles of sediment and lime precipitated from the water get trapped in the sticky matrix, and periodically bury the living microbes.   The resourceful cyanobacteria in those instances migrate to the top of the sediment and begin a new mat.  This results in a fine structure of alternating light and dark bands.  Stromatolites are thus, like coral reefs, built by the living organisms that inhabit them.   There is a website devoted to Shark Bay in Western Australia (www.sharkbay.org) that includes facts, photos and a video swim through a grove of stromatolites.

             
Stromatolites turn out to be one of our most important clues as to the origin of plant life.  They have been around for about 3.5 million years.  Ancient fossilized stromatolites, which can also be found in parts of Australia, are in fact among the earliest signs of any kind of life on this planet.  They are abundant throughout much of the geological record, but became rather scarce around 500 million years ago.  This was the time of the  “Cambrian Explosion”, when many new kinds of animals appeared.  Stromatolites came under attack by voracious grazing animals equipped with hard, scraping mouth parts.  After that, they survived only in restricted sites too salty for such animals. 

Though there is still debate about whether the earliest stromatolites were formed by cyanobacteria or some earlier form of life, or even by some physical process, there is no doubt that they were building stromatolites  by 2.7 billion years ago – still a heck of a long ago!   Fossilized cells identifiable as cyanobacteria have also been found in slightly different types of rocks, the Warrawoona and Apex cherts of Australia, and these appear also to date back to 3.5 billion years ago.   Cyanobacteria were the plants, the photosynthetic organisms, that supported the Earth’s early ecosystem.  They did so virtually alone form almost 2 billion years, after which the first signs of eukaryotic algae began to appear.

The early photosynthesizers must have gradually built up enormous populations, for the oxygen they produced eventually transformed the vast oceans of our planet, and then the very atmosphere itself.  The scarcity of oxidized (“rusted”) minerals in the Earth’s oldest rocks (older than 3 billion years), indicates that there was very little free oxygen in the atmosphere at that time, so the oxidizing of crustal rocks is also evidence of plant life.  Iron is particularly abundant on Earth, and quite prone to rusting.  In the ancient seas there was a steady supply of iron bubbling up from underwater volcanic fissures, and from eroding surface rocks.  In its unoxidized state, iron is soluble in water, but when it oxidizes it forms insoluble molecules of hematite or magnetite, which sink to the bottom of the sea.  When oxygen became available in comparably huge quantities there were spectacular depositions of iron.  This resulted in distinctive and extensive rock layers known as the Banded Iron Formations.  The “rusting of the earth,” as it was called by Schopf (2006), is the source of most of the iron ore that is being ravenously consumed by modern civilization.

There is some evidence of limited iron formations about 3.5 billion years ago, but they did not become truly massive until the mid-2-billions.   This suggests that oxygen buildup may have occurred sporadically and slowly at first, but became overwhelming between 2.7 and 2.5 billion years ago.  Oxygen makes up 21% of our current atmosphere, but 20 times as much plant-generated oxygen may be tied up in banded iron formations.  The formation of iron deposits declined rapidly after about 2 billion years ago, as the supply of dissolved iron was depleted, and oxygen then began to build up in the atmosphere.   The transformed atmosphere made it possible for more complex organisms to evolve, leading to eukaryotic cells and the modern world of algae, plants, fungi and animals.

So cyanobacteria invented photosynthesis as we know it today, and were the first functional plants.  The story does not end there.  In the two billion years of their unchallenged domination of the Earth, cyanobacteria also invented the rudiments of aerobic respiration and nitrogen-fixation, two other essential metabolic processes - cyanobacteria had to do virtually everything themselves!  Aerobic respiration is the process by  which organisms “burn” carbohydrates to fuel their metabolic processes.  It is obviously essential  for animals, but also for plants.  How else could they  utilize the carbohydrate reserves that they produced for themselves?

In terms of starting ingredients, photosynthesis is easy.  All you  need are carbon dioxide and water, and both are abundant on the planet.  But to make certain other things, like protein, DNA, ATP and other vital organic molecules, you also need nitrogen, which isn’t so easy to come by.  Wait-a-minute, isn’t the Earth’s atmosphere about 70% nitrogen?  Yes, it is, but it’s nitrogen that is hard to use.  Nitrogen gas consists of two nitrogen atoms bound tightly together by a triple bond.  Most organisms can’t break those bonds to make use of the abundant nitrogen supply.  Enter the cyanobacteria.  Somewhere along the way they acquired the genes to split nitrogen, either through mutation and natural selection, or from some other bacterium that invented it first.   Bacteria freely share genes through the process of horizontal gene transfer, a process we exploit in genetic engineering.

Once the nitrogen molecule has been split, cyanobacteria are able to attach hydrogen atoms to the nitrogen, making ammonia, and ammonia then can become the amino group required to make the building blocks of protein – amino acids.  So cyanobacteria, arguably the most successful and certainly the most long-lived group of organisms, make carbohydrates, metabolize carbohydrates for energy, and make their own protein.  The rest of us have only stolen from them!

References:

Schopf, J. W. 2006.  Fossil evidence of Archaean life.  Phil. Trans. R. Soc. B 361: 869–885.

Website for images and more information about stromatolites in Australia: www.sharkbay.org  (under "Nature of Shark Bay")

Mosses of Central Florida 2. Octoblepharum albidum

Leaves of Octoblepharum are crowded in upward-facing rosettes,
resembling tiny bromeliads. 

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


Octoblepharum albidum Hedw. is one of the more common and distinctive mosses in our area.  Its long, thick, strap-like leaves, typically pale green in color, and arranged in tight rosettes make it easily recognizable.  In local flatwoods and sandhill associations, it occurs in relatively dry banks, on roots or the bases of trees.  I have recently found it also growing on the trunks of date palms planted on the University of South Florida campus.

Octoblepharum is one of the few genera of mosses with leaves more than one cell thick.  Large, water-storage cells lie above and below 1-2 layers of thin photosynthetic cells in the center. Ovoid sporangia are erect and symmetrical (compare with those in Leucobryum, which are bent to the side).

The pale-colored, strap-shaped leaves of Octoblepharum are readily recognized.

 According to Reese (1984) the species is found throughout the tropics, but outside of Florida has been found only in a few places around New Orleans, Louisiana, and long ago near Matagorda Bay in Texas.  In the herbarium at the University of South Florida, the species is represented by collections as far north as Levy and Marion Counties, and is abundant in the southern and west-central part of the state.


Reference: Reese, W. D. 1984.  Mosses of the Gulf South.  Louisiana State University Press.  Baton Rouge and London.

Making the Ancestor Problem Go Away

At the end of my recent post entitled “The Great Botanical Butter Battle Book” (which you would be well-advised to review before plunging into the even murkier aspects of the debate that follow!), I ended with the implication that, in the traditional taxonomic view, a classification system consisting entirely of monophyletic taxa  is not only undesirable, but also impossible.  Every genus, it is argued,  logically must have originated from a species in an earlier genus, rendering the earlier genus paraphyletic. All efforts to correct this by eliminating paraphyletic genera cause the system to collapse into a single genus. This is sometimes referred to as the “ancestor problem.”  It is a problem that arises with a steadily improving fossil record and actual knowledge of ancestor-descendant relationships.

Recall that monophyletic taxa are complete branches, or clades, of a phylogenetic tree, beginning with the founding ancestral species and including all the descendant species of the common ancestor (all twigs of the branch).   According to the prevailing practice of phylogenetic taxonomy, a clade-taxon at one taxonomic rank (e.g. family) can be subdivided into smaller clade-taxa (e.g. genera) using the same criteria, but none of the subclades can be given the same rank as the main clade (e.g. there cannot be a family within a family).   That is why birds and reptiles cannot  both be ranked as formal classes, as was done traditionally.

A similar example involves dogs and cats, which represent two of the several modern families in the mammal order Carnivora.    The common ancestor, and most likely a group of related species that preceded the split into dog and cat clades (along with the others that don't need to be mentioned), are in a taxonomic no-man’s land.  If we place that ancestral cluster of species, or "stem group," into a family, that family will by definition be paraphyletic, because both the dog and cat clades that we now consider formal families developed as subclades from within that ancient family.

Phylogenetic taxonomy has the logical goal of accurately incorporating the actual branching pattern of evolutionary history into a formalized classification system.  Attempting to put traditional taxonomic boxes (i.e. genera, families, etc.) around clades, however, does create some awkward situations, particularly as we know more and more about ancestral groups of organisms.

As we envision the process of evolution, clades
branch to beget new clades.  Successful
clades further branch into  bushy clusters of
species that  we recognize as genera.   

The hypothetical diagram at the right  represents a common pattern of evolution, with new clades arising from older clades, each in turn developing distinctive adaptations, blossoming out into a diverse group of species, and then declining into extinction as still newer groups come to dominate.  Assuming a fairly complete fossil record of this group, traditional (also called "evolutionary") and phylogenetic taxonomists would have rather different ideas about how to classify them.

Traditional taxonomists would view the four groups as a succession of distinct genera, one on top of the other.  They would see nothing wrong with new genera arising from older genera in sequence over time – it is necessary in fact, if we are to simultaneously believe in evolution and have a system of classification.

Phylogenetic taxonomists view the diagram differently.  A clade is a clade, from the founding species through all of its descendants.  Subclades are viewed as nested within the main clade, rather than emerging on top of them. If all four were considered genera, both A and C would be paraphyletic, because some parts have been removed. "A" can be considered a monophyletic genus, only if B, C, and D are included within it.  If so, the latter 3 genera must be given lower rank than A (e.g. subgenera).   Traditional taxonomists charge that this "lumping" solution would result in a collapse of the entire taxonomic system, for surely genus A itself evolved from some earlier genus, and so on back to the first genus of organisms.

Alternatively, B and D could be recognized as genera, but C and A would have to have higher rank (e.g. C as a subfamily that included genus D, and A as a family that included subfamily C and genus B).  In that scenario, the remaining contents of A and C would have to be split into comparable subgenera and genera.  However, "splitting" like that would just result in even more small, unclassifiable stem groups, and not really solve the problem.  

Many taxonomists, particularly botanists, contend that the ancestor problem is not worth worrying about, because we are highly unlikely to ever have a specimen of an actual ancestor to classify and name, and if we do we won’t know it and it won’t matter.  It’s true that we really don’t have a lot of fossil plants with which to “connect the dots,” and may never directly confront the ancestor problem. Zoologists, however, with a better fossil record, don’t get off so easy.

For example, wee now know quite a lot about our own family of primates, the hominids.  Before the genus Homo existed, there was another genus of hominids, traditionally known as Australopithecus.  Unless you believe in special creation of humans, there has to be a connection between our genus and earlier genera.  The very first species of Homo most certainly descended from a species of Australopithecus, which therefore would be paraphyletic and illegal in phylogenetic classification.  Some anthropologists have dutifully tried to weed out the paraphyly, but no matter how you lump or split the various parts of the hominid tree, there is some part of it that is still directly ancestral to the first Homo.  Is that ancestor unnamable?  Can it be placed in a genus at all?

In the end, the best that hominid taxonomists can do is to “minimize paraphyly” by making the ancestral stem genus as small as possible.  This was the approach of Cela-Conde and Ayala (2003), who recognized the genus Praeanthropus for the stubbornly paraphyletic residue (5 species) of Australopithecines that directly preceded the first humans and the more narrowly defined Australopithecus.  So it seems that in this perspective of evolutionary history, paraphyletic taxa are logically unavoidable.

Yet monophyletic taxa are the foundation of phylogenetic taxonomy.  Is there no way out of this dilemma?

Proponents of the Phylocode movement, advocate simply naming all the branches of a phylogenetic tree, without ranking the parts as families, genera, etc.  This might effectively avoid the conflict of taxonomic philosophies.  Clades can and do arise from one another (e.g. birds from dinosaurs).  Each clade and subclade at every level can have a name, as long as we don't try to rank them as genera, families, classes, etc.  Paraphyly, it can be argued, is an artifact of trying to fit clades into the boxes of traditional classification.

The phylocode makes a lot of sense, and in practice, we don’t worry so much about ranking the bigger clades of life any more.  We talk of Magnolids, Eudicots, Monocots, Amborellids, etc.  in discussions of the evolution of flowering plants, but it seems that no one is seriously trying to squeeze them into classes, subclasses, etc. any more.  There seems to be no point to it. 

There is a snag, however, in going totally rank-less.   Our conventional binomial (“two-name”) system  for naming species requires the genus name plus a specific epithet (e.g. – Quercus is the name of the genus that includes Quercus rubra, the red oak).  So all species must be in a genus.   Attempts to find an alternate species naming system to accompany the Phylocode have failed to achieve any consensus.  So my further discussion and proposed resolution of the ancestor problem assumes that we need formally-defined genera in order to create names for all species, past and present.

It would appear that the prospects for monophyletic-only genera destabilize and collapse the more information we have about ancestral organisms.  But does it really?  Perhaps all this discussion of ancestors having names, and genera evolving from genera, is putting the cart before the horse. 

Going back to the “father” of modern phylogenetic taxonomy, Willi Hennig, we see that his system centered around the process of cladistics and the resulting cladograms.  Cladistics is an objective mathematical process for comparing taxa by coding each for a very specific set of characters (e.g. leaves simple vs compound, stamens 6 vs 5, etc.).  The cladogram is generated by comparing taxa pair by pair.  It superficially resembles a phylogenetic tree as it consists of lines connecting taxa in a branching pattern. Taxa most similar in terms of shared character states come out close together on the cladogram, while those sharing relatively few character states come out distant from each other on the cladogram. 

The difference between a cladogram and a traditional phylogenetic tree (though the two are often considered the same these days) is that the cladogram is purely a diagram of similarity among the taxa being compared.  The cladistics process itself is not prejudiced by whether or not any of the taxa in the comparison are ancestors of any other taxa.  Though we call the stem line that precedes each branch point the “hypothetical common ancestor” (probably a poor choice of words), it is only a mathematically generated line, and does not need to be classified or named.  In a traditional phylogenetic tree (as in the first diagram above, or the diagram published in the study of hominid evolution discussed above), there are built-in hypotheses about ancestors and descendants. 

Now suppose, by chance, that we actually had a common ancestor in a cladistic analysis.  It would be coded and compared like any of the other taxa in the analysis.  It could be classified by putting a box around its line on the cladogram, and named according to conventional rules.  Like the exasperated phylogenetic plant taxonomists mentioned above, we would not know for sure if any taxon were ancestral to any other, and it wouldn't matter.  The cladogram is "ancestor-neutral." 

After the cladogram is made and carved into genera, however, we can then make hypotheses about common ancestors.  This is a separate, secondary process.  At the right is a small portion of a cladogram, with two genera that are sister taxa.  The short horizontal lines on the branch leading to genus B, indicate new adaptations, (technically character state changes or apomorphies), that evolved in the common ancestor of B after its split from A.   There are no comparable character changes indicated on the line leading to genus A, indicating that A has not changed since the split, and is therefore not measurably different from the actual common ancestor.  A and B can be classified as genera based on the cladogram, but then as a separate process we can hypothesize that genus B evolved from a species in genus A.   Genus A is monophyletic by the rules of cladistic classification, but still can be considered ancestral to B.

There is one important assumption in this “solution” of the ancestor problem.  In the simplified diagram above, it is  genera that are the units of cladistic comparison.  The short horizontal lines on the line going to genus B in the diagram are generic level characters.  For  purposes of recognizing genera, we must assume that characters that distinguish genera from one another are of a greater magnitude than, or perhaps qualitatively different from, characters that distinguish species, otherwise we might logically be led to make genera out of smaller and smaller groups of species, even of individual species, following the branching pattern alone.  

The determination of generic-level characters is a subjective judgement that in this context inevitable.   Otherwise, how do we decide that our own genus, Homo, is in fact a genus, not just a section of Australopithecus?  Anthropologists (some at least) have emphasized the "minimization of paraphyly" by lowering the threshold for generic characters.  Other systematists might choose to minimize the proliferation of small, barely-distinguishable genera by raising that threshold.  I have argued that minimal ancestral genera, such as Praeanthropus, are not taxonomically paraphyletic, as they are not identified as ancestral in the cladistic process.  How broadly or narrowly such ancestral genera are defined becomes an issue of how much difference should be required to distinguish genera from one another. This issue is far less cataclismic than the black-and-white battle between pro- and anti-paraphyletic forces that has unnecessarily preoccupied systematists for so many decades.

I would not necessarily extend these arguments to higher levels of classification, to talk about “class-worthy” characters, or “phylum-worthy” characters, for example.  It is not necessary to go there.  It may be that un-ranked clade names are a better option at those levels.  Genera are uniquely important in the taxonomic hierarchy, however, as they are necessary for naming species by the binomial convention, so we must do what we can to  maintain their universal application for all appropriately characterized clusters of species, be they current or ancestral. 

References:

Cela-Conde, C. J. and F. J. Ayala. 2003.  Genera of the human lineage PNAS 100: 7684-7689. 

Mosses of Central Florida 1. Leucobryum albidum

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

To take a break from the more theoretical posts of late, I'd like to begin a series on the mosses of Central Florida, the subject of one of my current projects. This will ultimately be part of a pictorial key and guide to the mosses of this area. So far about 77 species have been recorded in our area, centering on Hillsborough County, and including the neighboring counties of Pasco, Hernando, Pinellas, Manatee, and Polk. More are sure to show up as we look more closely.

Looking closely is the key to finding and identifying the different kinds of mosses.  They are mostly small, and at first all look pretty much the same.  But there are huge differences in both vegetative and reproductive structures that make that closer look most rewarding.

I begin with one of the most abundant species in our area, Leucobryum albidum (Brid. ex P. Beauv.) Lindb. (Family Dicranaceae).  This species forms large, conspicuous mats on the dry ground of shady pine flatwoods and oak hammocks.  Like most mosses, Leucobryum soaks up water from rainstorms and dries out inbetween.  The leaves of this species are unusually thick.  There are several layers of cells, with only the single central layer green.  Above and below are essentially empty cells that fill up with water during a rainstorm.  In most mosses, leaves are just one cell thick, and dry up rather quickly during dry weather.  Mosses in general can tolerate desiccation for rather long periods of time, and spring back to life quickly when wet.

The distinctive succulent leaves of Leucobryum are short, stiff, and folded lengthwise, creating a distinct upper groove.  The leaves are crowded at the ends of upright stems, and the sporangia emerge from the tips of the stems after union of sperm and egg.  The sporangia are turned to the side and look distinctly like the heads of some kind of wading bird.

Another species, Leucobryum glaucum (Hedw.) Ångström has longer leaves, but is not as common, and grows in somewhat moister areas.

The Great Botanical Butter Battle Book

In recent decades, there have been many often drastic changes in the taxonomic system of flowering plants (and indeed all organisms).  This is due to radical changes in taxonomic philosophy that began in the middle of the 20^th Century, and which were in turn the result of vastly improved techniques for determining the pattern of evolutionary relationships among organisms.  Usually referred to as phylogenetic taxonomy, the primary philosophical goal of this approach is to make our classification system reflect the evolutionary history, or phylogeny, of organisms as exactly as possible.  Our traditional classification system deviated from this ideal in many of its details, and so the classification of organisms has changed considerably in the last 50 years. 

In a recent posting, I described the fate of the Snapdragon Family, which has been taxonomically “blown to smithereens” because it was polyphyletic.  A polyphyletic taxonomic group (taxon) is one that has members descended from very different ancestors, i.e. their resemblance to one another is superficial. Similar body forms in unrelated organisms with very different anatomy and chemistry, not to mention genetics, is due to independent adaptation to similar environmental conditions, or convergent evolution.  The former classification of whales and porpoises, along with tuna and salmon, in the category of “Fishes” is an extreme example.

No one really disagrees that such strange bedfellows need to be separated and returned to their true relatives, i.e. to be arranged in monophyletic categories - by definition a common ancestor and all its descendants.   Much of the taxonomic busywork of the past century has been to ferret out illicit polyphyletic associations and rearrange organisms into a classification based on true relationship.  That’s not where the butter battle comes in, however.

 The classic Butter Battle Book by Dr. Suess satirized the human propensity for escalating silly disagreements into cataclysmic space-time-continuum-threatening warfare.  The story began with an argument between two groups of whimsical creatures, one of which believed passionately that toast should be eaten butter-side up, and the other that it should be eaten butter-side down.  Something akin to this feud began in the botanical world during the latter part of the 20^th century, and it’s not over yet.  It wasn’t about polyphyletic groups, but about a much subtler distinction that results in some traditional taxa being called “paraphyletic.”

Both traditional and phylogenetic systems of classification have the form of a hierarchy of categories.  The level of the hierarchy is referred to as ranks.  Domains are currently the highest rank of taxon, and they are subdivided into Kingdoms.  Progressively smaller subcategories are given lesser rank.  The  principle ranks are Domain, Kingdom, Phylum, Class, Order, Family, Genus,  and Species, and in-between ranks (subclass, superorder, etc.) can be inserted as needed.  

Phylogenetic taxonomy has two basic rules designed to make a classification system explicitly reflect evolutionary history:

1.  Only monophyletic groups - by definition a complete branch, or clade, of the phylogenetic tree, with the common ancestor and all of its descendents, can be formally recognized as taxa at each level of branching.  

      
 2.  Each branch point on a cladogram results in two sister taxa, which must be given equal rank (genus, family, class, etc.).  

          

   Applying these two rules, it was found that many traditional taxa were neither polyphyletic nor monophyletic, but fell into a fuzzy gray area called paraphyletic.  Paraphyletic taxa are incomplete clades (violating rule 1) - some part of the clade that should be just a subclade has been improperly promoted to the same rank as the main clade (violating rule 2 since they are not sister clades).
     

The traditional classification of higher vertebrates was
simple and intuitive, but misleading about
evolutionary relationships.  Clades A through F
retain certain ancestral characteristics, such as
scaly skin, that we associate with reptiles, while
the birds evolved highly distinctive wings, flight
feathers and other specialized features
associated with flight.

     This is probably as clear as mud at this point.  Let me use a familiar  example from the animal world to quickly explain this concept.  Reptiles and birds are two of the traditional classes of vertebrates, but modern studies have overwhelmingly confirmed that birds descended from reptiles, in particular from a group of dinosaurs that included velociraptors and Tyrannosaurus.   While birds are a monophyletic group, the reptiles are paraphyletic (also referred to as a grade to differentiate it from a clade).  

In the greatly simplified diagram to the right, clades A through F are different groups of reptiles.  Technically, the sister group of birds is clade F, which includes their closest dinosaur relatives.  Therefore, according to the rules, birds must be have the same rank as group F.  Birds are still a distinct group, but taxonomically must be considered just a highly specialized subgroup of reptiles.  Note also that the traditional classification obscures the fact that group F is much more closely related to birds than it is to group A (turtles and their relatives).  Remember that it is the goal of phylogenetic taxonomy to better reveal these relationships in the classification system.

Taxonomically, there are actually three choices in such a situation:  1) keep the status quo, recognizing the paraphyletic Reptilia and the monophyletic Aves as two equivalent classes.  This would be the preference of some traditional taxonomists; 2) combine the reptile and bird classes together into one class (“lumping”), in which birds become one of the subclasses of reptiles along with groups A through F; or 3) keep the birds as a class, but also promote each of  the main clades of reptiles to the rank of class, creating several additional classes (“splitting”). 

An acceptable solution in phylogenetic systematics
is to lump reptiles and birds into a single class, with
birds recognized as a subclass (along with clades A
 through F)

The alternate solution recognizes many classes of
reptiles along with the birds.

The second two options are equally acceptable to phylogenetic taxonomists, but this creates a dilemma with each paraphyletic situation encountered: Do we fragment the paraphyletic taxon (reptiles) into a number of smaller classes or submerge the distinctive group at the top (birds) into one big class with the reptiles?  Either way, the taxonomy reflects the phylogenetic history of the group, but one way ends up with a lot of smaller classes (harder to remember them all) or fewer big classes (obscuring the distinctive, sometimes revolutionary, adaptations of the top group).  This ranking decision is pretty much subjective.

This is all about the formal classification used primarily by scientists.  We can still talk about reptiles and birds informally.   No one is obligated to include birds in a field guide of common reptiles, for example. 

To finally get around to plants, I'll mention first in passing that the traditional classification of flowering plants into dicots and monocots created exactly the same situation as the reptiles and birds.  Dicots turned out to consist of a grade of separate clades, with monocots occupying the bird position at the top of the tree.  It still has not been fully agreed upon as to how to rank these clades.

Walter Judd, Roger Sanders and Michael Donoghue, in a truly landmark paper in 1994, identified a number of pairs of traditional angiosperm  families, of which one was paraphyletic and theo other monophyletic.  In most cases, the monophyletic family at the top of the tree was primarily temperate in distribution and consisted primarily of herbaceous plants, while the clades branching along the grade consist mainly of woody trees and shrubs.  The pairs include: Apocynaceae (oleander family)/Asclepiadaceae (milkweed family), Araliaceae (Aralia family)/Apiaceae (carrot family), Capparaceae/Brassicaceae (mustard family), among others.  To keep this posting under control, I’ll just talk briefly about the first case.

The Apocynaceae and Asclepiadaceae share a number of characters inherited from their common ancestor.  Each clade that branched off of the Apocynaceae grade had some distinctive characters, but were not deemed worthy of family status.  The upper subclade we call Asclepiadaceae, however, had some very innovative and distinctive floral characters that allowed this group to blossom into a “family” of many related genera.  The conclusion of Judd, Sanders, and Donoghue was however that the Asclepiadacease should be submerged into the Apocynaceae.

The traditional Apocynaceae, like this
Pachypodium, have relatively
conventional flowers with petals united
into a flaring tube that often twists like a
pinwheel.

I’ve provided this lengthy explanation as a prelude to getting into the real butter battle, which may take one or two more posts to explore fully.  It is first of all a battle between two views of how we divide up an undisputed diagram of relationship into taxonomic entities that are convenient, practical, and informative.  Phylogenetic taxonomists, in forbidding  paraphyletic taxa, are emphasizing information on phylogenetic branching patterns.  Clades are real entities that represent evolutionary history and groups of related organisms.  They are predictive of the characteristics to expect within the group.  Recognizing birds and reptiles as equivalent groups obscures the fascinating relationship of birds to dinosaurs, and the fact that Tyrannosaurus rex is much more closely related to ostriches than it is to turtles. 

The Asclepiadaceae, represented by this milkweed
(Asclepias), has the same basic features as the Apocynaceae,
but adds some unique floral features related to specialized
modes of pollination.

 Traditional taxonomists, while probably not much concerned about the reptile/bird issue anymore, believe that allowing some paraphyletic groups to be recognized as taxa is not only harmless, but also desirable in order to simplify classifications and create user-friendly, easily recognizable taxa, and  to recognize highly innovative groups, like the birds or the Asclepiadaceae, as distinctive taxa of higher rank.  Birds have achieved the level of distinctiveness that is worthy of a new class of organisms, while the other clades of reptiles are still basically reptilian.  The differences between them are technical and not readily evident to the non-expert.   They point out that if one wants to see the actual pattern of relationship, one can look directly at the phylogenetic trees.  There is no need to create cumbersome, non-intuitive classifications just to duplicate the information that is easier to see in the diagrams themselves.  This sentiment is probably stronger among botanists that among zoologists.  

  Phylogenetic taxonomists appear to be winning the day, but there are many holdouts among traditionalists.  For the latter, the distinctions between reptiles and birds, dicots and monocots, Apocynaceae and Asclepiadaceae, are all simple, intuitive,informative, and useful.

There is, moreover, another dimension to the debate brought up by traditionalists that is not so easily dismissed, and which we might sum up as the “ancestor problem.”  This arises when one views, theoretically at least, the entire sweep of evolutionary history.  The first member (common ancestor) of every genus (or family, etc.) logically had ancestors that were in an older genus.  Whenever a new genus-worthy group of species became distinct, it would have rendered its ancestral genus paraphyletic (just as the evolution of birds as a distinct new class of organisms rendered the reptiles paraphyletic).  So the evolution of new genera (or families or classes) appears to be impossible according to the rules of phylogenetic taxonomy, or else to force the retroactive fragmentation of the older taxa. I will take up this tricky issue in a future posting (See "Making the Ancestor Problem Go Away,"  October 18, 2012).