Wednesday, November 26, 2014

Why we must teach botany

Those of you who follow this blog site regularly may be wondering where I've been for the past several months.  Aside from teaching this semester and having to move my office, I've been finalizing the manuscript of a new book: “Plant Life – A Brief History,” which will be published this winter by Oxford University Press.  My reason for writing this book is the same as for doing this blog site – to explore the mysteries of why plants are the way they are, and to help people around the world to better understand this fascinating and important group of organisms. 

I hope my efforts will also contribute to the Botanical Society of America’s fight against “plant blindness,” and its campaign to “reclaim the name” of botany. (go to So what’s all that about?  There has been a serious decline in the teaching of botany in university biology departments over the past 40 years.  The  reasons for that are complex, but primarily the result of the burgeoning growth of cellular, genetic, and developmental biology, as well as advances in theoretical ecology, that have come to occupy an increasing share of an undergraduate’s budget of course requirements.  This is on top of the traditional bias that plants are less interesting or less important than animals.

Like fine arts and PE in elementary schools, botany and other taxonomically defined classes are viewed as luxuries that can be cut if needed – and they have been. In some universities, even the introductory botany course has fallen by the wayside, leaving only a week of plants in an introductory biology sequence.  Even that is typically taught reluctantly by a young (or old) faculty member who is only one chapter ahead of the students in his or her own removal from plant blindness.  

The excuse is often given that “most of our undergraduates these days are pre-med.” That doesn’t excuse a department from providing a well-rounded background for those who plan to go into research or teaching.  Moreover, when courses in medical botany are offered, they are very popular, and provide to our future doctors, nurses, etc., a vital broadening of perspective on the nature of medicine.

Plant blindness then refers to a general lack of awareness of plants, particularly of their diversity and the many unique ways they contribute to the balance of the natural world, as well as to our own societal and individual well-being.  It is akin to other forms of blindness, like the much deplored inability of young people to point out Iraq, or even Texas, on a map.  Our undergraduates, graduate students, applicants for our vacant positions, and ultimately our fellow faculty members increasingly have less working knowledge of plants.

There’s no question that this is bad at all levels.  At the general level, failure to understand both the fundamental biology of plants, and the significance of plant diversity, leads to superficial and erroneous interpretation of environmental issues, abuse of our food supply chain, nutritional and medicinal resources, poorly designed and maintained landscapes, and numerous other issues vital to our survival.   K-12 teachers turned out by universities without a good background in plants will reinforce and amplify the blindness. 

At the professional level, biologists may overlook cellular, genetic, and developmental processes, or environmental adaptations, unique to plants.  Consideration of how plants do things can provide a breakthrough when animal or microbial models hit a dead end.  A great comedian draws upon his or her own accumulation of diverse observations of culture and human behavior to synthesize a unique and entertaining routine.  A master medical diagnostician draws upon a vast pool of specific information about symptom and their causes, to identify and cure an ill patient.  And so too, the most brilliant and imaginative biological researcher will draw upon his or her knowledge of diverse organisms to ask new questions, or to find different solutions to existing questions. 

We must of course teach critical thinking and the scientific method in science, but there must also be a place for teaching awareness of diversity, and providing opportunities to build a pool of knowledge about different organisms. 

In addition, the lack of awareness of plant diversity and the fact that every species interacts uniquely, whether subtly or dramatically, with its environment can lead to serious errors.  It can lead researchers to oversimplify the role of plants in ecosystems, or worse to fail to obtain accurate identifications of the plants studied (see Bortolus 2008, for some classic blunders).  Misidentification links the study plants, as well as the results of the study, to the wrong body of literature.
The “reclaim the name” movement reflects the parallel decline of respect for botany among our biological colleagues, and the impression that botany as a subject matter is old-fashioned and no longer important.  Will a name change help?  It seems that everything in our society gets renamed every few years in order to buy new respect.  Used cars are now “pre-owned” and I’m not sure what graveyards are called these days.  Some of my colleagues insist that we call our discipline “Plant Science,” but to me that has an applied, agricultural ring to it.  I haven’t seen any of my zoologist friends opt for “Animal Science,” which if I remember correctly from my years at Cornell is the study of dairy cows! 

The counterpart to zoology is “phytology,” which has never caught on as the name of our discipline.  If we ditch botany, what do we do with botanical gardens?  “Plant gardens” just sounds dumb, and people would just drive past a ”phytarium,” having no idea what the heck it was.  

I, for one, am a BOTANIST.

The term botany has indeed evolved into something that encompasses the big picture of plant life, of the unique attributes that unite plants, as well as of the multiplicity of unique ways in which plants have adapted for survival.  This is what distinguishes those of us who call ourselves botanists from cell biologists, geneticists, etc. who happen to be working with plant models at present.  Being a botanist, however, is not a research specialty, but a label that can be appended to any researcher who has had a broad training in botany, and/or a sufficient interest in the big picture to self-educate.  

That broad training – a full curriculum in plant anatomy, morphology, physiology and taxonomy, is harder to find these days, but does survive in departments affiliated with agricultural colleges and a few other refuges of enlightenment.  Let’s hope they continue the tradition!

So outside of those botanical monasteries, what do we do with our 15 minutes in the spotlight?  What are the essentials of botany that every undergraduate should have?  Earlier, I posted the “Essential features of plants.”  Those, at least, we need to impart in our week in introductory biology.  We need to avoid getting bogged down at that level in too much descriptive details, but perhaps demonstrate, with some well-chosen examples,  how different plants can provide radically different solutions to the same problems of survival.

If we are able to provide a full semester introduction to botany, we should do so aimed at a broad audience of science majors, from biology to geology and anthropology, with minimal prerequisites.  Beyond that, botanists in our faculty can craft more specialized courses based on their own background and experience. 

The introductory course, beyond the essentials, will have an emphasis on evolution,  diversity and ecology.  Discovery and explanation of adaptive differences among plants is what makes botany so exhilarating, and what can come as startling revelations to the plant blind.  Again, we must pull back a bit from the details that fill textbooks designed for botany majors. 

I leave you with a simple comparison of plants and animals, which borrows from the biblical model of “begats.”  A framework like this can serve as the starting point for a lecture, a class, or an entire botanical curriculum.

For plants:

  1.       In the beginning was photosynthesis.
  2.       Photosynthesis begat indeterminate growth.
  3.       Indeterminate growth begat immobility.
  4.       Immobility begat hydrostatic engines, spores, and passive defense.
  5.       Hydrostatic engines begat maple syrup, fresh salad, bamboo, and venus fly traps.
  6.     Spores begat alternation of generations, pine cones and orchids.
  7.       Passive defense begat curry, digitalis and marijuana, as well as cactus spines and walnut shells.

The resources required for photosynthesis are diffuse:
light and carbon dioxide from above, and water and
minerals from below.  How does that dictate virtually
every aspect of plant biology?
For animals:
  1.      In the beginning was the mouth.
  2.       The mouth begat food-sensing organs and locomotion.
  3.       Food-sensing organs and locomotion begat the head.
  4.       The head begat response, behavior, instinct, sex, thought, and blog postings.

Finer iterations of this model can lead us to understand the difference between Acacia trees and savanna grasses, both struggling to survive in an African savanna, or the difference between mussels and barnacles vying for a spot on an intertidal rock.

Your homework is to think about these chains of cause and effect.  How does photosynthesis lead to curry?  I’ll return with a fuller discussion in the near future.

Literature cited:

Bortolus, A.  2008.  Error Cascades in the Biological Sciences: The Unwanted Consequences of Using Bad Taxonomy in Ecology.  Ambio 37 (2): 114-118.

Monday, August 18, 2014

Were the first carpels plicate or ascidiate?

[This article extends the discussion begun in my post "What's so primitive about Amborella?"]

The carpel is the distinctive seed chamber of the angiosperms, or flowering plants.  It is in fact the definitive feature of this major group.  When the first carpel evolved, the first angiosperm came into existence.  The carpel encloses, protects, and facilitates the fertilization of the ovules, which then mature as seeds. The carpel then becomes the fruit, and participates in the dispersal of the seeds.  In the flower, carpels occupy the center and are surrounded by stamens and tepals (petals and sepals).  In most modern angiosperms the carpels are joined together into a compound pistil (see "Were the first monocots syncarpous?)"

In those flowers in which the carpels remain separate, there are two fundamental shapes: plicate - resembling leaves that have folded with the opposite edges sealed together, and ascidiate - shaped like a vase or an urn.
The ascidiate carpels of Amborella
contain a single seed, and have a
large, folded stigma. A. the carpel
at the time of pollination.  B. the
 mature fruit, which is a drupe.
Drawing from Bailey and Swamy,
It is now clear that the three clades of the ANITA grade (Amborella, Nymphaeales and Austrobaileyales) are the most ancient branches of the flowering plants.  We assume that whatever characteristics they have in common were inherited from their common ancestor.   The carpels in this group are mostly ascidiate, which is variously described as vase-, urn-, or bottle-shaped.  The wall of the ascidiate carpel is smooth and seamless, tightly enclosing the contents but open at the top in the stigmatic region.  It resembles a sock pulled up around a foot.

Above the opening, which is blocked only by a drop of fluid, the stigma is typically prolonged along what can be described as the backbone of the carpel,  and ovules are attached in a line on the opposite side (i.e. in what might be called the "belly"), within the urn-shaped base.  Sometimes, as in Amborella, the stigma  is folded at the backbone, forming narrow flaps along each side.  During the growth of the carpel, tissues at the base (“a meristematic cross-zone between the primordium margins” – Endress & Doyle 2009) push the wall upward around the ovules.
After pollination the carpels of
Austrobaileya spread apart as they
swell with the developing seeds
within. Photo courtesy Dennis

The carpels of Austrobaileya are ascidiate, but
contain two rows of ovules opposite the
backbone.  The stigmas are pushed together
to form a common head for receiving pollen.
Photo courtesy Dennis Stevenson.
Ascidiate carpels contrast with carpels described as plicate, or folded.  A folded carpel, like a pea pod has the structure of a folded leaf.  Opposite the midrib or backbone of the carpel, the  margins of the hypothetical leaf blade are figuratively sewn together in a suture.  The suture is actually more like a zipper, as it forms as alternating cells from the two margins  expand and interlock with one another.  Many plicate carpels dry out as they mature, and split open along the suture to release their seeds, though just about any kind of fruit can develop from them. Plicate carpels are common among the higher branches of angiosperms: the magnolids, monocots, and eudicots.
Simple plicate carlpels, called follicles,
 can be seen most readily in the
 Ranunculaceae,  in genera like 
Aquilegia (columbine), Delphinium
Eranthis, and others. Drawing from 
Asa Gray's Botanical Textbook, 1879.
The pea pod is somewhat more specialized
than a follicle, as it has adapted to split
along both the suture and the backbone
 when it opens to release its seeds. The seeds
alternate along the two margins.  Drawing 

from Thomé 1877, Textbook of Structural and
Physiological Botany.

Follicles of the genus Eranthis
(Ranunculaceae) are quite leaf-like.
Because the earliest branching angiosperms have primarily ascidiate carpels, the simplest (most parsimonious) interpretation about the earliest carpels is that they were ascidiate as well (Endress & Doyle 2009, and others).  The corollary of this interpretation is that  the plicate carpel of the magnolids, eudicots and monocots must have evolved from one of these ancient ascidiate carpels.

As I have argued in earlier posts, however, these theoretical conclusions based on probability need to be tesed in the adaptive arena. In other worids, do they make sense in terms of "adaptive parsimony?" (see "Were the first monocots syncarpous?" for an explanation of this term)

In ancient seed ferns, such as this
Sphenopteris, seeds were
borne directly on large, frond-
like leaves. Drawing from Brown,
1935, The Plant Kingdom.
Ovules were originally borne directly on the leaves of ancient seed ferns, and on modified seed-leaves (megasporophylls) in later gymnosperms such as the cycads. According to traditional theory, the first carpel came about as a simple blade-like megasporophyll, with ovules along both edges, rolled or folded together, enclosing the ovules within a protective chamber.  The structure would have been very similar to a pea pod or a follicle.

An interesting alternate idea is the "mostly male hypothesis" (see Frohlich and Chase 2007)  in which early blade-like stamens became carpels by the genetic accident of ovules popping up where pollen sacs should have been.  Such things do happen, and are reminders that leaves and seed-leaves were originally one and the same.

The third possibility raised by the current phylogentic conclusions is that, instead of simply folding around the ovules, the first carpels formed by an ascidiate growth pattern, i.e. the base of the ancient ovule-bearing structure, or a leaf below it, formed a cup-like base that grew up around a group of ovules (or conceivably a single ovule as in Amborella, but I have already argued agains that in "What's so primitive about Amborella?").  At the same time, the backside of this cup-like structure would develop as a strong backbone, resembling the mid-rib of a leaf, the open top  developed a folded structure, and the ovules would come to be placed in two rows opposite the backbone. In terms of genetic and developmental processes, this seems to be a much more complex scenario than simply folding a leaf together. If this is indeed what happened, we need fossil evidence and/or genetic-developmental evidence to confirm it.

If there were a selective pressure for enclosing ancient ovules, the principle of evolution along the lines of least resistance (Stebbins 1974) would clearly favor the easier path of a folding leaf.  (see "G. L. Stebbins and the process of adaptive modification" for a full and detailed explanation of this evolutionary principle).

Though not directly ancestral to the angiosperms, the seed-leaves of the living gymnosperm genus Cycas illustrate the kinds of structures that might have folded together to form the first carpels.  Drawing from Asa Gray, 1879.
So is there a clash between cladistic parsimony and adaptive parsimony with respect the first carpels?  Yes and no.  First the "no" part.  We must remember that the cladistic studies that place ascidiate carpels at the base of the angiosperm tree were based on living angiosperms -  the crown group, and so have no bearing on what might have been happening in the stem group (the extinct angiosperms that preceded the common ancestor of all living angiosperms - see "the birthplace of the angiosperms").  There were probably carpels among extinct angiosperm ancestors long before the crown group ancestor evolved.  Therefore, there is no conflict between the idea that the first carpels were folded and the idea that the common ancestor of the living angiosperms had ascidiate carpels.  We are free to choose the folded leaf model for the first carpels.

Ascidiate carpels most likely evolved among early crown group angiosperms, and presumably evolved for a reason. Most ascidiate carpels, at least those in Amborella and most Austrobaileyales, mature as drupes or berries.  These brightly colored fleshy fruits may have been adaptations for improved dispersal by birds in shady forest environments, where these archaic plants survive today.

A number of gymnosperms, such as this yew (Taxus) has
a fruit-like layer that grows up around each seed. Similar
features can be found widely among different
angiosperms, including magnolids, eudicots and
 monocots, and may have been present in the
earliest angiosperms.  Photo by
Didier Descouens, posted on Wikipedia.
In the the first hypothetical leaf-like carpels, the unsealed edges probably simply reopened to release the mature seeds.  Quite possibly, these seeds were covered with colorful fruit-like layers called arils.  These arils were comsumed by birds, who in the process dispersed the seeds. Many gymnosperms, including cycads, junipers, podocarps, and yews have similar adaptations. As fleshy fruits evolved among the early members of the crown group, the fruity function of the aril was genetically transferred to the wall of the carpel itself.

In this scenario, the evolution of the ascidiate growth form was an adaptation to embed the ovules more securely within a uniform, sealed wall. The lower tissues could have grown together while leaving the open folded region just at the top.  Something similar happened in the evolution of both roses and apples, where tissues of the receptacle were extended up and around the separate carpels.

Now I return to the apparent re-evolution of plicate carpels from ascidiate carpels, as predicted by cladistic analysis. It is odd that simple, leaf-like carpels with marginal rows of ovules would have evolved from the decidedly less leaf-like ascidiate structure, rather than directly from an ancient carpel of essentially the same design.  The nature of the suture in modern plicate carpel strongly suggests the joining of opposite edges, and that ovules were attached in rows along those edges.

The carpels of Illicium are folded and split open
to release seeds, but only one seed is produced
per carpel, rather than a row along each margin.
They may have evolved from an ascidiate
carpel through expansion of the folded stigmatic
region. Drawing from Kerner & Oliver, 1895. The
Natural History of Plants.
 One possible scenario is suggested by an exceptional member of the Austrobaileyales, Illicium (star anise), which does have plicate carpels. If these evolved from ascidiate carpels, it is conceivable that the ascidiate portion contracted while the folded stigmatic region expanded.  Though the edges are pressed together and partially fused, this does not seem to be the same suture structure as found in other plicate angiosperms (Robertson and Tucker, 1979).  Also, there is only one seed in each Illicium carpel.  Evolution of carpel with marginal rows of ovules would require a different path, i.e. extending the stigmatic split down between two rows of ovules in something like Austrobaileya,  followed by union of the margins into a suture.  This again is a rather cumbersome scenario with no apparent adaptive value.

A simpler adaptive scenario is that a folded carpel with marginal rows of ovules was retained in some ancient crown group angiosperm, and this evolved directly into the more advanced form of plicate carpel with sutures found in the higher angiosperms.  The folded nature of the stigmatic region in Amborella  may in fact be a remnant of the earliest folded carpels, and the two rows of ovules in Austrobaileya another remnant.  So the pieces of the earliest folded carpels are still present among the ANITA grade, and may have been still together in the ancestor of magnolids, monocots, and eudicots.

Bailey, I. W. and G. L. Swamy. 1948.  Amborella trichopoda Baill., J. Arnold Arbor. 23:245-254, plus plates.

Endress, P. &  J. Doyle. 2009.  Reconstructing the ancestral angiosperm flower and its initial specializations. Am. J. Bot. 96(1): 22-66.  

Frohlich, M. W. & M. W. Chase, 2007.  After a dozen years of progress the origin of angiosperms is still a great mystery.  Nature 450: 1184-1189.

Robertson and Tucker, 1979.  Floral ontogeny of Illicium floridanum, with emphasis on stamen and carpel development.  Amer. J. Bot. 66(6): 605-617.

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

Thursday, August 14, 2014

Mosses of Central Florida 8. Entodon seductrix

The small ovate leaves of Entodon seductrix are
pressed against the stem when dry, giving the stems
a rope-like appearance.  The sporangia are upright
and cylindrical, with two rows of teeth around the
[For other mosses in this series, see the Table of Contents]

Entodon seductrix (Hedw.) Müll. Hal. (Entodontaceae) is a common, straggling moss with horizontal stems covered with short leaves, and with sporophytes arising along the sides.  This species is found throughout eastern North America, as far north as Ontario, and extending westward from Florida to Texas.  Our collections are from the middle of the state northward, so it's not clear how far south it extends.  It characteristically forms lush mats at the bases of trees.

This species is easily confused with Isopterygium tenerum. Like that species, leaf cells are elongate and slightly curved, and there is no midrib (costa).   The short leaves of E. seductrix, however, press closely to the stem when dry, while those of Isopterygium are spread out.  The two species differ most obviously when sporangia are present.  In E. seductrix they are upright, nearly symmetrical, and cylindrical, in contrast with the strongly curved sporangia Isopterygium.

Another species of Entodon in our state is E. macropodus, which has slightly larger leaves that remain spread out when dry, but the sporangia are still upright and cylindrical. This species is more southern in its distribution, occurring northward to Virginia and southward into tropical America.  It is also found in Japan.
The slender leaf cells of Entodon are like tiny worms, with
thick, clear walls between them. Toward the base, they
become more rectangular, but not conspicuously

Sunday, August 10, 2014

Were the first monocots syncarpous?

In my recent post on Acorus, I suggested that one of the ways this genus is specialized is that the three carpels within each flower are joined together into a single pistil (syncarpous).  Acorus is at the end of the earliest branch of the monocot tree -  the sister clade to all other monocots. Its various characteristics are therefore of great interest when discussing the nature of the first monocots.  Carpels are mostly free of one another (apocarpous) in many members of the Alismatales, the next most ancient branch of the monocot tree after Acorus.  Because carpels are also free in the archaic angiosperms of the ANITA grade, many magnolids, and some basal Eudicots, it seems most logical that the common ancestor of Acorus and the rest of the monocots also had free carpels.  That logical assumption, however, has recently been challenged by Sokoloff et al. (2013).
Carpels in ancient angiosperms were separate structures, each of which had to receive pollen individually from a visiting insect. Butomus, on the left, is a monocot in the Alismatales that retains separate carpels.  In more advanced angiosperms, such as the tulip on the right, also a monocot, carpels are fused together, with a common stigmatic area where a single deposit of pollen can fertilize all the ovules in the ovary.  Left photo by Sten Porse, right photo by Bernd Haynold,  both posted on Wikimedia Commons

Tradition and conventional wisdom hold that the fusion of carpels has adaptive value and is a more-or-less irreversible process. This was confirmed by Armbruster et al. (2002), who explored the advantages of shifting from apocarpy to syncarpy and estimated 17-26 separate instances of this shift among angiosperms. The fusion of carpels brings stigmas together in such a way that pollen is deposited in a single central location by a visiting insect.  Pollen tubes can then pass through the common style and enter into any of the carpel chambers, which is said to increase competition among pollen tubes, but also insures more even fertilization among the ovules in the ovary as a whole. Carpel fusion also reduces material needs as only the outer walls need to be fortified for protection of the developing ovules. Monocots were not analyzed in the Armbruster study, but apparently were assumed to be fundamentally syncarpous

The general trend among seed plants is for gradually tighter and deeper enclosure of ovules within protective stuructures,including the tighter closure and fusion of carpels.  Because of the adaptive advantage attached to this trend, reversals back to apocarpy are considered unlikely:

ovules on open, leaf-like structures (ancient seed ferns)----->

     ovules on specialized leaf-like, cone-like, or shoot-like structures (gymnosperms) ------>
          ovules within loosely-closed, leaf-like carpels (stem angiosperms) ------->
                carpels apocarpous (early crown-group angiosperms and basal magnolids, eudicots, and monocots)                                   ------->
                     carpels syncarpous or unicarpellate, and sometimes surrounded by tissues of the receptacle                                                               ("inferior ovary") (most advanced angiosperms)

Armbruster and colleagues did detect two probable reversals from syncarpy to apocarpy among  eudicots (in the genus Crossosoma and members of the Saxifragales), and speculated that the advantage might be to extend the period of ovule fertilization so as to receive pollen from different sources. It's not clear that such an extension happens in these examples, however, as each only has a few carpels.  Likewise, in archaic monocots like Butomus (in the Alismatales), the small number of carpels are receptive at the same time and for only one day (Bhardwaj & Eckert 2001).   In Sagittaria, also in the Alismatales, the carpels are more numerous and physically spread out, but again are receptive at the same time for only one day.  If multiple visitors fail to arrive during that window, it potentially leaves carpels unfertilized. Multiple insect visitors are possible in one day, but does the potential advantage of genetically different pollen arriving in the same flower outweigh the usual advantages of syncarpy? The idea needs fleshing out with stronger selective arguments and actual examples of it working.   

From another perspective, if there is an advantage in spreading out the fertilization of ovules in either time or space, a much simpler way to effect that advantage in syncarpous flowers is to make the flowers smaller, with just one or a few ovules in each, and produce a series of them.  This has in fact happened many times, as in the Saururaceae, Piperaceae, Asteraceae, palms, aroids, etc. I am not aware of any series of carpels in an apocarpous flower functioning this way, let alone a syncarpous ovary splitting apart to do so.

 Despite the foregoing, Sokoloff et al. (2013) concluded that the earliest monocots were syncarpous and that apocarpous flowers evolved several times among them.  In some cases, according to this scenario, syncarpy re-evolved a short time later from newly-apocarpous ancestors. What is the basis for this counter-intuitive proposal?  It appears not to be based simply on the fact that the most ancient monocot lineage (Acorus) is syncarpous, but on a more extensive theoretical exercise involving cladistic analysis plus an additional step of "optimized parsimony analysis."

DNA-based cladistic analysis provides a clear, and increasingly accurate picture of the ancestral branching patterns of groups of organisms - - i.e. a phylogenetic tree.  When only DNA information is used, the tree tells us nothing about when and where new adaptive traits arose.  For this, we can "map" such physical characteristics onto the tree. For example, we can make a little mark on each branch containing only species known to be syncarpous.  If two adjacent (sister) branches have syncarpous flowers, we assume their common ancestor had the same.  It is also possible, however, that syncarpy evolved  independently on each branch from an ancestor that was apocarpous.  But this interpretation is less parsimonius, because it involves more independent evolutionary changes (syncarpy evolved twice instead of only once).  

Optimized parsimony  analysis takes into consideration a wide variety of tests, assumptions, taxa lists, character definitions, etc. for the same set of data and determines the most parsimonious interpretation of the evolution of particular characteristics.  Some of the tests  performed by Sokoloff et al. were ambiguous about the nature of the ancestors, but overall they suggested that syncarpous flowers were present first in the monocots.  Quite possibly, the basal position of syncarpous Acorus tilted the final results in this favor, raising again the questions I raised in my previous post.

So from this cladistic perspective, multiple evolution of apocarpous flowers from a syncarpous ancestor is more parsimonious than multiple origins of syncarpy from an apocarpous ancestor.  But does evolution necessarily follow the most parsimonious path?  In the real world, perhaps one evolutionary trend, because of its adaptive value, is more likely to occur multiple times than the opposite.  So to evaluate this proposal further, we need to consider the adaptive basis for each trend.   Sokoloff and colleagues in fact raised the question: “Assessing the functional and adaptive significance of evolutionary transformations is clearly important" ( p. 75). They proceed to reiterate the advantages of syncarpy, but made no suggestions as to why reversals might occur. They made another disturbing statement:  "Interestingly, in the monocot order Alismatales, congenital intercarpellary fusion was first lost and then re-appeared in three independent clades according to this scenario" (p. 64). One of those reversals would include the Butomus pictured above.

I recently outlined the principles advocated by Stebbins for evaluating alternate evolutionary scenarios (G. L.Stebbins and the process of adaptive modification).  These principles result in the "other parsimony," the parsimony in which sequences of adaptive changes are assumed to proceed along the simplest paths, or "along the lines of least resistance."  My example above, in which shifting to a series of small flowers, instead of splitting the ovary to make a series of separate carpels, is an example of such a simpler path.  Further, once a developmentally complex and highly functional structure like syncarpy evolves, one would need a rather powerful selective pressure to undo it, something giving an advantage to apocarpy strong enough to cancel out the documented benefits of  the syncarpous ovary.   No one has yet offered such an adaptive scenario.

Therefore, "cladistic parsimony" must be balanced against "adaptive parsimony."  Seventeen independent transformations from apocarpy to syncarpy may be more reasonable in view of selective pressures we know about than even one reversal.  I think it is therefore premature to dismiss apocarpy in the ancestral monocots.  Despite the fused carpels and other specializations of Acorus, apocarpy and looser forms of syncarpy (due to post-genital fusion) are widespread among the Alismatales, which are nearly as old as Acorus, and possibly more conservative with respect to the condition of their carpels.  In the palms as well, separate carpels occur in more archaic groups (Nypa and the Coryphoideae), though the first branch, the lepidocaryoid palms, are syncarpous. This is a more complex situation, however, as the palms appear to have originated among clades that were already syncarpous.  Still a scenario is needed for why fused carpels might become separate again in these palms.  Does such a scenario make sense in the real world of adaptive pressures?


Armbruster, W. S.  , E. M. Debevec & M. F. Willson. 2002. Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. Journal of Evolutionary Biology 15 (4): 657-672.

Bhardwaj, M., Eckert, C. G. 2001. Functional analysis of synchronous dichogamy in flowering rush, Butomus umbellatus (Butomaceae). Am. J. Bot. 88(12):2204-13.

Sokoloff, D. D., M. V. Remizowa and P. J. Rudall. 2013. Is syncarpy an ancestral condition in monocots and core eudicots? in Early Events in Monocot Evolution, Eds.  P. Wilkin & S. J. Mayo. Cambridge University Press.

Friday, July 18, 2014

Mosses of Central Florida 7. Thuidium delicatulum

The leafy stems of  Thuidium delicatulum branch into a fern-like pattern.
The leaves are boat-shaped and packed densely
along the stem.
[For other mosses in this series, see the Table of Contents]

Thuidium delicatulum (Hedw.) Schimp. (Thuidiaceae) is easy to recognize due to its strikingly fern-like appearance.  Its leafy structure of course is not a true compound frond as in actual ferns, but a finely branched stem system with tiny leaves.

The small leaves have a weakly-developed midrib (costa).
The leaves are roughened with tiny tooth-like papillae.

The leaves are small with a weakly-developed midrib, and roundish to oval cells that each have strongly developed papillae (small clear bumps).  Branched filaments, called paraphyllia, are also present among the leaves. Sporangia are uncommon, but described as "elongate, asymmetric, and inclined" (Reese, 1984, Mosses of the Gulf South).

Slender, sometimes
branched paraphyllia
are found among the leaves.

Thuidium delicatulum is distributed widely in northern and eastern North America, as well as South America. It extends westward from Florida into Texas.  Another species in Central Florida is T. allenii, which has a similar branching structure, but less regular and more straggly, not quite giving the appearance of a fern.  The papillae are also smaller.  T. minutulum is found further north, and also in Highlands County, and has mostly simple, unbranched stems, and short, unbranched paraphyllia.  T. pygmaeum is similar, and has been found only in Jackson County.

Wednesday, July 16, 2014

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.

Tuesday, July 1, 2014

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
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.
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.


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