Friday, February 21, 2014

The Birthplace of the Angiosperms

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

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

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

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

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

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

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

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

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

A tale of stem and crown

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

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

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

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

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

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

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

Thursday, December 5, 2013

Mosses of Central Florida 5. Syrrhopodon incompletus

Syrrhopodon incompletus growing on the spongy trunk
of a date palm (Phoenix dactylifera) on the University
of South Florida campus
Syrrhopodon incompletus Schwaegr.  is a relatively common moss found throughout the coastal plain of the southeastern U.S., occurring mostly on tree trunks, including palms, and exposed roots. It has a short upright stem with relatively large leaves, typically 3-5 mm in length, crowded into a circular pattern called a rosette ("rose-like"), and thus superficially resembles Octoblepharum.  The leaves are thinner, however, just one cell thick except for the prominent midrib, with small teeth along the margins, and are translucent green.  
The leaf cells of this species are small, roundish and thin-walled.  The marginal
cells are similar in size, shape, and coloration, but with an occasional short
The leaf cells are roundish or polygonal and thin-walled.  This genus is also characterized by an extensive and conspicuous basal region of large rectangular clear cells.  Leaf cells and the midrib have tiny rounded outgrowths called papilli, particularly on the back side.  When dry, the leaf margins roll inward, creating an almost tubular configuration, and this then twists and curls irregularly.

The large leaves have a strong midrib (or costa) and the basal region is composed of large, empty, rectangular cells.
When dry, the leave roll into a tube and then twist and curl.
The capsules (sporangia) arise from the tips of the stems, and are upright, symmetrical, and narrowly ovoid to cylindrical (when dry).  Teeth of the capsule mouth (peristome) are short and attached below the rim.  
The sporophytes arise from the tips of the stems, and the sporangia are upright and symmetrical.
Several other species of Syrrhopodon occur in Florida.  S. incompletus is characterized by the marginal cells of its leaf, which are slightly thickened but green and shaped more-or-less like the other cells of the leaf.  The other species have distinctive elongate, clear cells along the margin. S. texanus also has much more prominent spines along the margins and particularly on the lower midrib.  

Friday, November 1, 2013

A leaf by any other name

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

Many brown algae produce large, leaf-like fronds.
Line drawing from Allen & Gilbert, 1917, A textbook
 of botany. 
To be fully convincing as a leaf, a structure must not only be flat and photosynthetic, but also limited in size and shape (determinate), and produced in a regular pattern around a central stem.    Leaves also have a certain lifespan, after which they fall off of the plant, or sometimes remain as a dead skirt, as in Washingtonia palms.  New leaves are produced at the tips of stems that continue to elongate over time.  This would rule out leaf-like cacti, in which the flat segments are produced one from another like links in a chain.  They are parts of indeterminate, branching stem systems - stems in leaf’s clothing. 

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

The "leaves" of leafy liverworts, like this Lejeunea, are
flat extensions of the thallus.
The first flattened, photosynthetic structures to appear in land plants were the thalli of ancient liverworts.  A thallus is a plant body that is not clearly defined into organs like stems and leaves.  A thalloid liverwort is flat and photosynthetic, but grows and branches at its tip like a stem.  Some liverworts are called “leafy liverworts,” because their thalli are subdivided into small leaf-like segments with slender stem-like sections in-between.   Mosses are more convincingly leafy, with
determinate, leaf-like structures attached spirally around a stem,  but purists prefer to not call any bryophyte structures leaves because they evolved independently of the “true leaves” of other land plants.
Mosses, like this Barbula agraria, have distinct leaves produced one at a time by the stem apex.
Club mosses, like this Lycopdiella cernua
 from Florida, have small scale-like leaves
called microphylls.
However, the true leaves of vascular plants evolved at least twice from scratch, and were subsequently completely remodeled several times.   Early land plants had perennial creeping stems, called rhizomes, plus short-lived upright shoots adapted for gathering light and producing spores.   The early upright shoots were little more than green, forking stems, but competition for light soon forced them to evolve more efficient light-gathering structures.  In clubmosses (Lycophytes) the answer came in the form of flat but narrow leaves with a single vein of vascular tissue running through them.  They are referred to technically as microphylls, and are believed to have evolved as simple outgrowths of the surface tissues of ancient stems.  A more recent hypothesis is that microphylls evolved from sporangia that were “sterilized” and flattened.  Precursors of lycophytes produced numerous sporangia on short stalks along the sides of their upright leafless stems.  So converting some of them into leaves would have been a fairly simple adaptation.  In either case, leaves of lycophytes can grow in length, but cannot develop complex shapes or much breadth.

The fronds of ferns are
upright shoots flattened into
a leaf-like configuration.  From
Smith, 1955, Cryptogamic Botany.
The complex fronds of ferns, which bear sporangia on their.

The large complex leaves of ferns are called megaphylls.

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

The upright shoots of horsetails are equivalent to the fronds of ferns,
 but consist of repeated whorls of small leaf-like branchesand
elongate stem segments.
From Kerner & Oliver, 1904, The natural history of plants.
The upright shoots of horsetails, cousins of the ferns, evolved a little differently.  They too are determinate, photosynthetic, and spore-bearing, and are discarded after a defined period of time, but they remained stem-like with smaller leaf-like segments.  Though modern horsetails don’t have leaves, their earliest ancestors had short, fan-shaped leaves born in a circular arrangement at intervals along the upright shoots.   They evolved a unique, bamboo way of growth, in which stem segments elongate to extend the entire shoot quickly upward (see The first “bamboos,” 28 Mar, 2012). These smaller leaves are also called megaphylls, though each is equivalent to only part of the fern megaphyll.  Spores are produced, not on the leaves, but in specialized cones at the ends of upright shoots. 
  This is an
ancient horsetail ancestor called Lilpopia,
with small megaphylls, each equivalent
to just a small part of a fern frond.

Cycads have compound leaves
descended from the fronds of seed ferns.
The leaves of the cycad Bowenia are doubly compound, and
the most like ancient seed ferns.
The leaves of flowering plants, as well as cycads, are
Archaeopteris was an ancient spore-bearing
tree that may have been a precursor to
both seed ferns and conifers. These lateral
leafy systems may have evolved directly into
seed fern fronds or into branch systems of
small needle-like leaves in the conifers.
also considered to be full  megaphylls, having evolved from the large fern-like fronds of plants known as “seed ferns.”  Seed ferns evolved in much the same ways as ferns, though probably independently from leafless ancestors, and bear seeds and pollen sacs directly on the leaves.    In conifers and ginkgos, however, needle-like and fan-shaped  leaves may represent segments of ancient megaphylls that became more twig-like.  Short leafy shoots of these plants would then be evolutionarily equivalent to entire seed fern fronds.  The common ancestors of all seed plants, the progymnosperms, had leafy systems that were complex and frond-like, but not clearly defined as either determinate or indeterminate.   Thus both types of systems could have evolved from them. 
The leaves of conifers, such as this
Araucaria, are
simple, and flat or needle-like.

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

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

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

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

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

Wednesday, October 9, 2013

Beyond Natural Selection –Shortcuts in Plant Evolution

In Darwin’s understanding of evolution, change in the characteristics of organisms occurred very slowly through the painstaking action of natural selection.  In the 20th century such change was defined genetically as the spread of favorable mutations through a population.  That simple view of evolution prevailed until relatively recently, but we now know that there are a number of ways in which dramatic changes in an organism’s genome, or in the expression of that genome, can occur virtually overnight and lead to a dramatic evolutionary change.  This is sometimes referred to as evolutionary saltation (jumping).

One of the simplest, and most familiar examples of overnight change in plants, is the hybridization of crop plants and garden flowers.  Such hybrids, when guided and selected by plant breeders, exhibit the best attributes of the parents and typically great vigor. Hybridization also occurs between related species in nature, and sometimes gives rise to permanent new kinds of plants.  Hybrids are often sterile, because the different chromosome structures of the parents are incompatible and cells cannot undergo meiosis to initiate the reproductive cycle.  However, if the chromosomes of such a hybrid are doubled, either through an accident of cell division, or on purpose by plant breeders, the chromosomes can then pair up and reproduce normally.  Such plants are called polyploids, because they have multiple complete sets of chromosomes.  The earliest form of wheat, emmer wheat, originated as an accidental natural hybridization before it was cultivated by humans.  Seedless bananas are from sterile, triploid plants that also originated from natural hybrids thousands of years ago.

The comparative study of chromosomes has provided extensive evidence of polyploids resulting from both hybridization (allopolyploids) and from duplication of an ordinary genome (autopolyploids) throughout the history of plants.  Such events can jumpstart new evolutionary trends.  Even without the novel combination of traits inherent in hybrids, a simple doubling of chromosomes creates duplicate sets that can accumulate new mutations, and eventually new useful traits.  

Cyanobacteria, such as this Anabaena,
are photosynthetic bacteria that came
about through the combination of
electron transfer chains from two
different sulfur bacteria through
horizontal gene transfer.
Photo by Elapied.
A more technological version of hybridization is the direct transfer of DNA from one organism to another thorugh genetic engineering.  In this way, DNA from unrelated organisms can be combined. Though such genetically modified crops are much maligned, this technology has ancient origins and has been practiced by bacteria for billions of years.  This bacterial form of hybridization is called horizontal gene transfer.  This is the promiscuous practice of bacteria gathering up DNA from other dead bacteria and incorporating it into their own genome.  Though the results might be disastrous at times, this process has resulted in a number of major evolutionary breakthroughs, such as the invention of modern oxygen-releasing photosynthesis.   The complex photosynthetic machinery of cyanobacteria and modern plants combines the abilities of at least two, and probably three distinct bacterial ancestors.   

When more complex eukaryotic organisms evolved – organisms with nuclei and an internal cytoskeleton capable of ingesting other smaller cells – a remarkable series of symbiotic events occurred.  Bacteria capable of aerobic respiration were taken into the larger cells, where they were domesticated and became mitochondria.   Later, cyanobacteria were ingested and gradually modified into chloroplasts.  Here whole organisms are combined into one, not just their DNA.  This process of endosymbiosis resulted in the first photosynthetic eukaryotes, or algae.

Euglenas are protists that relatively recently acquired
chloroplasts through a process akin to the original
endosymbiosic event between an ancient protist and
a cyanobacterium.  In this case, chloroplasts were taken
from green algae fed upon by a carnivorous euglenoid.
The event created a new line of  plant-like organisms.
Photo by Deuterostome (Own work) [CC-BY-SA-3.0
via Wikimedia Commons.  
In addition to these various ways of combining the genomes of different organisms, are equally dramatic changes resulting from changes in how genes are expressed.   Every cell in an individual’s body has exactly the same set of genes.  Your left toe, for example, has the genes for making a complete, functional eyeball.  Though it might come in handy when looking for a lost sock under the bed, nature has thought better of it and the genes for eyeball development are turned off during toe development. Developmental of an individual organism involves the turning on and turning off of particular genes in a precisely controlled sequence, sometimes in response to environmental cues.  A system of regulatory (homeotic) genes is responsible for that orderly process, insuring that genes are turned off and on at the right time and in the right place.  Mutations in homeotic genes therefore can have dramatic effects. Diabolical fruit fly geneticists, for example, have been able to tamper with those genetic controls, resulting in eyes, wings, and various other organs popping up where they don’t belong. 

Mutations in key regulatory genes are evident, or at least suspected, in the history of plant life. Some of those have affected the behavior of haploid and diploid cells during reproductive processes.  In animals, the haploid cells that result from meiosis have the specialized shape and behavior of gametes: sperm or egg, which have the single goal of finding one another and combining into one.  The diploid cell (zygote) that results from that union is programmed to start dividing and undergo development into a new individual, though it doesn't have any genes that are absent from the gametes' nuclei.   

Ulva and other forms of algae may have evolved alternation of generations
through mutations that allowed vegetative growth in the diploid zygote that
normally (in most algae) divide directly through meiosis to produce spores.
In this new diploid generation, meiosis and spore-production are delayed
until a full-sized plant identical to the original haploid plant has formed.
Plants differ from animals in that they have two distinct multicellular bodies during their life cycle, one that is diploid and one that is haploid.  Most green algae go about their daily lives as haploid individuals.  Sperm and egg combine, much as they do in animals, but the zygote does not divide to form a new multicellular individual as it would in animals.  Instead, it goes directly into meiosis, usually to produce specialized dispersal cells called zoospores.  Zoospores then settle to produce new haploid individuals, which may be unicellular or multicellular.  Being haploid or diploid determines which developmental genes are turned on, via some key regulatory gene.  In some green algae, such as the sea lettuce (Ulva), however, the zygote, which in other algae is programmed to do nothing more than undergo meiosis, goes through a developmental process identical to that of the haploid plant.  So Ulva populations exist as a mixture of haploid and diploid plants.  The only difference is that the diploid plants (sporophytes) eventually produced zoospores through a much delayed meiosis, and the haploid plants (gametophytes) produce gametes through ordinary cell division.  This alternation of multicellular haploid and diploid generations apparently resulted from a mutation in the regulatory gene that previously prevented the diploid zygote from developing into a multicellular individual.

Something similar appears to have happened in the early land plants, though this is somewhat speculative at this point.  The ancestors of land plants were green
Aglaophyton, an early diploid land plant.
Such plants originated when genes for
indeterminate growth and branching were
turned on in the zygote of normally
haploid plants similar to modern liverworts,
much as occurred in Ulva.
 Drawing by Griensteidl
[GFDL ( 
algae that had typical haploid bodies.  While the zygotes of algae go directly into meiosis to produce a handful of spores, those of early land plants delayed meiosis, and instead divided through ordinary division to produce a mass of diploid cells called a sporangium.  Within the sporangium, many cells underwent meiosis, producing a large number of spores.  The direct descendants of plants with this strategy are the bryophytes (mosses, liverworts and hornworts), which have all remained as haploid vegetative plants (gametophytes) alternating with simple, diploid, spore-producing bodies (sporophytes). 

In one ancient land plant, however, a mutation occurred that allowed the diploid zygote to grow like the haploid plant, branching  to ultimately produce many sporangia.  This event was probably much like that occurred in the ancestors of Ulva. These diploid branching plants were the ancestors of the vascular plants (ferns, gymnosperms, and flowering plants).  Their alternate haploid generations shrank over time to become minimal sperm and egg producing structures.  So modern land plants consist of haploid bryophytes and diploid vascular plants.

The most common form of carpel in
flowering plants was like these in Eranthis,
appearing as leaves folded around
developing seeds (ovules).
Another “giant leap for plantkind” may have come during the evolution of flowers.  It has
Early stamens may have
been flat and leaf-like,
as in this Degeneria
always been a mystery as to where the signature structure of angiosperms - the closed seed chamber known as the carpel - came from.  It has long been assumed to be a leaf-like structure that folded around a series of embryonic seeds (ovules), which were borne directly on the leaf as in ancient seed ferns, or on a branching structure that became enclosed by a leaf.  According to the “mostly male theory” of  Michael Frohlich (2002), however, the first floral organs to form in a flower-like, spiral arrangement were the male structures (stamens).  These were at the time flat and leaf-like.  Ovules were produced elsewhere on the plant, but another genetic accident had the ovule-development genes turn on during stamen development, forming ovules instead of pollen sacs on some of the stamens.  This is comparable to eyeballs forming on toes!  These transsexual stamens then became carpels as they folded around the developing ovules.

More recently,  maize (or corn in America), Zea mays, originated rather suddenly through modification of just a few genes that controlled the location of the female flower spikes, and the nature of the seeds, in a wild plant called Teosinte.
Teosinte, on the left, has very hard grains in simple spikes
located just below the male tassels.  Early forms of maize appeared rather
suddenly with mutations that relocated the cobs lower down
on the stem and that gave the grains a softer, more edible texture.  The center
specimen is a teosinte X maize hybrid that may be similar to early maize.
 Human selection gradually developed the larger cobs we know today.
Photo by John Doebly.

Finally, I must mention the rapidly growing field of epigenetics.  In the broadest definition, epigenetics includes the processes that turn genes on and off to result in different organs, phenotypes, or environmental responses. Genetic changes that enable plants to start producing flowers instead of leaves, for example, are most often triggered by changes in temperature, day length, or other factors.  Epigenetic phenomena can results in rather different looking individuals without any change in their DNA code.  Current focus in epigenetics concerns patterns of gene suppression that adapt individuals to varying environmental conditions, and which sometimes can be passed on to future generations.   Ironically, this resembles the long-discredited Lamarckian idea that characteristics acquired during an individual's lifetime can be passed on to its descendants. For long-term evolutionary trends, true genetic change is required, but heritable epigenetic changes in the short term may allow populations to adapt to changing conditions, after which mutations and ordinary natural selection can reinforce those changes and make them permanent.  The extent to which epigenetics can influence the bigger picture of evolutionary change is still being hotly debated.

In sum,  through the tricks of horizontal gene transfer, endosymbiosis, hybridization,  mutation in regulatory genes, and epigenetics, the evolution of photosynthetic organisms has periodically taken dramatic leaps forward. 


Frohlich, M. W. 2002.  The Mostly Male theory of flower origins: summary and update regarding the Jurasssic pteridosperm Pteroma, in Developmental Genetics and Plant Evolution, C. B. Cronk, R. M. Bateman, and J. A. Hawkins, Eds., Taylor and Francis.  London and New York.

Friday, September 27, 2013

Why are there so many kinds of plants?

(first published at, updated with additional photos here)

Estimates vary, but there are about 300,000 named species of plants, with more being discovered daily.  There may ultimately be as many as 500,000, if and when all are catalogued.  Some botanists include some 10,000 species of red and green algae in such estimates, but others include only the land plants.  Either way, it’s a lot.   Theoretically, each species differs from every other enough to create a unique niche for itself.  Species with very similar niches in the same location will compete with each other for resources, and the stronger species will drive the other to adapt to a different niche or else go extinct.   Hence, “no two species can occupy the same niche.”   Yet it is sometimes difficult to tell what is unique about each species, and why each maintains a seat at life’s table. 

I’d like to do a thought experiment to get a picture of how many possible plant niches there might be.  Imagine a multidimensional “niche space,” each dimension representing a variable plant characteristic.  Suppose first that there were just one dimension, such as a gradient of temperature regimes running from the equator to the pole.  For simplicity, let’s say that this gradient is occupied by 10 different species, each specialized to make the best use of a particular combination of summer warmth and winter cold.  In reality of course there would probably be more, but we’ll keep all of our hypothetical niche dimensions at 10 for easy calculation.

Now let’s add another dimension, let’s say a moisture gradient.  At the equator, we might have 10 different plants, adapted to habitats ranging from evergreen rain forest to barren desert.  There would likewise be 10 such possible niches for each of the other temperature regimes, and so in this 2-dimensionsal niche space there would be a possibility of 100 different plant species worldwide.  Remember that in this simple array the plants differ only in their temperature and moisture requirements.

Now we can add a 3rd  dimension for growth form: trees, vines, shrubs, epiphytes, etc.   In biological communities one growth form creates subhabitats for other growth forms.  Trees create shade for understory plants, as well as support for light-seeking vines and epiphytes.  So, multiply our previous niche matrix by 10 again, and you have room for 1,000 species of plants in the world. 

Adaptations for pollination and seed dispersal create still more niche dimensions.  For flowers adapted for specific pollination vectors (e.g. by bird, butterfly, bumblebee, wind, etc.) and for seeds adapted for different means of dispersal (bird, wind, mammal fur, rodents, etc.) add two more dimensions, bringing us to 100,000 different possible kinds of plants. 

There are many other ways in which plants differ from one another: how they protect themselves from herbivores (spines, fuzzy coverings, toxic secretions, etc.), leaf shape and texture (for balancing light reception,  CO2 absorption, keeping cool, and avoiding water loss).  Each of these could be another niche dimension, but if we throw in just one, we multiply our possibilities by 10 again to have over a million.

We’re not quite done yet, however.  We also need to take into consideration geographical isolation, for similar species occupying similar niches tend to occur on different continents and major islands. Assuming just 10 more-or-less isolated geographical regions, each with warm wet lowlands, dry deserts, and cold mountain tops, we’re up to a possible 10,000,000 species in our matrix. In reality, individual mountain tops and isolated valleys frequently contain unique endemic species, adding even more diversity. 

 Even if this estimate is only moderately accurate, we can see that the number of potential plant niches vastly exceeds what actually exist.  Using 10 spots within each niche dimension is of course a simplification; for some dimensions there will be more, and for some there may be fewer.  Subarctic environments, for example, don’t support trees, vines, etc., so the number of growth forms is much fewer. Our model may seriously underestimate the options for pollination.  In a tropical rainforest, for example, there may be hundreds of possible pollinators. And there are niche dimensions that I just brushed to the side.  Nevertheless, the exercise provides a good perspective on the vast range of possibilities.  We in fact start to wonder why there are so few species of plants! 

Most likely, not every possible kind of plant can exist because the total resource “pie” of the ecosystem can only be sliced into so many pieces.  There is a minimum amount of energy, mineral resources, etc., required to maintain each species as a viable, genetically diverse population.  Those that are more aggressive, or that happen to be at the right place at the right time, are the ones that have actually succeeded.

The flowers of Bahia grass, Paspalum notatum, are specialized for pollination by the wind.  The feathery,
Christmas tree-like stigmas stand upright, while the pendant stamens dangle below.
For flowering plants, it is therefore not difficult to see how different sets of adaptations allow so many different kinds to coexist on our planet.  For example, consider three different kinds of plants from the monocot clade.  Their common ancestor was a creeping perennial herb with long, strap-like leaves with parallel veins, and embryos with a single cotyledon.  It had flower parts (sepals, petals, stamens and carpels) in sets of three.   Epiphytic orchids, savanna grasses, and succulent aloes are descendants of the ancestral monocot with quite different sets of adaptations. 

The butterfly orchid, Epidendrum radicans is adapted for
pollination by butterflies with well-developed color vision. Each orchid
species has uniquely shaped and colored flowers that attract a specific
bee, butterfly, hummingbird or other specialized pollinator.
They differ not only in where they grow (tree limbs or rocks for orchids, seasonally dry savannas for grasses, and deserts for aloes), but also most conspicuously in their mode of pollination.  The Epidendrum orchid pictured is pollinated by butterflies, and its tiny seeds are dispersed by the wind.  The grass is pollinated by the wind, and its seeds dispersed by grain-hoarding mammals and birds (and sometimes ants).   The Aloe dichotoma  (a relative of the familiar Aloe vera) is not only a succulent, but has also evolved a tree-like form. Its flowers are pollinated by birds and its flat seeds dispersed by the wind. 

The giant Aloe dichotoma has evolved a unique way to continue thickening its stem, allowing it to become tree-like.
Aloes in general have red, orange or
yellow flowers adapted for
bird-pollination.  The flowers of
Aloe dichotoma are yellow.
The other 60,000 species of monocots exhibit various combinations of these and many other adaptations. Agaves and Yuccas greatly resemble the African Aloes, but evolved in the Americas with different pollinators.  Palms and screwpines (Pandanus) are tree-like but with very different leaf structure and flowers from Aloe, Yucca or Agave, and prefer moister habitats.   Members of the ginger family have flowers that are often as elaborate as orchid flowers, but with a different growth habit and larger, animal-dispersed seeds. The orchid family itself has more than 20,000 species, each with a unique pollinator.  Sedges, cat-tails, and rushes are wind-pollinated like grasses, but adapted to different habitats and modes of seed dispersal.

Yuccas and their relatives live in similar climates
and have similar growth forms as Aloes,
 but  have colorless flowers adapted for pollination by moths.
We don’t have time to consider the other major groups of plants: eudicots, gymnosperms, ferns, mosses, etc., but you get the point.  There are seemingly endless ways for plants to vary – a multidimensional hyperspace of possibilities.  The half million or so living today are the fraction of those possibilities that through aggressiveness or chance maintain a tenuous foothold on our planet.

Friday, August 30, 2013

Mosses of Central Florida 4. Isopterygium tenerum

The asymmetrical capsules of Isopterygium rise on
long stalks from along the creeping stems, and curve to the side.
Isopterygium tenerum (Sw.) Mitt. is one of the most common mosses in Central Florida, yet easily confused with others of similar growth habit.  That habit is what we might call "creeping." as apposed to the upright habit of the three previous mosses in this series. Stems lie against the ground or flop over each other in a thick mat.  The numerous delicate leaves spread out, largely on the two sides of the stem so as to face upward and gather the maximum amount of light.  The leaves remain in that spread out condition when they dry.  They  lack a midrib and the cells are uniformly narrow and worm-like, with thick walls.  The sporophytes emerge from along the stem, lifting the sporangia, or capsules, high above the mat of vegetation.  The sporangia are asymmetrical and curve to the side.  When dry, the capsules are constricted below the mouth, which is lined with two rows of teeth.

The opening of the capsule is
surrounded by two rows of teeth, the
outer short, curved and stiff, and the
inner longer, thinner and straight.
These teeth change shape with changes
in humidity, and help to loosen and
eject the spores. This double row of
conspicuous teeth is characteristic
of the Hypnaceae and related
Isopterygium is found throughout Florida, commonly  at the bases of trees: on the lower trunk, roots, and surrounding wet soil.
The leaf cells of Isopterygium and its relatives are narrow and worm-like, with thick, clear walls.
The leaves are simple in structure, lacking a midrib (costa) or specialized cells at the base.

The delicate, feathery foliage of Isopterygium spreads out into a tangled mat.
The flat leaves  maintain their shape and orientation as they dry.
Similar common species include Sematophyllum adnatum and Entodon seductrix.  The Sematophyllum differs most conspicuously when it is dry, as the stems and the leaves curve toward the side. In Entodon, however, the leaves press against the stem when dry, makeing the shoots resemble little twigs of juniper. Their sporangia are also symmetrical and upright.  The less common Taxithelium planum is similar, but the leaves are covered with many small bumps, or papillae. Schwetskiopsis fabrona, also less common, is
similar, but has papillae at the upper end of each leaf cell, and the leaves are pressed to the stem when dry, like Entodon.

Friday, July 12, 2013

To self or not to self - the story of Drosera capillaris

What does it mean for a plant to "self?".  The expression is short for self-pollination. It's when the pollen of a flower lands on its own stigma or the stigma of a flower on the same plant, resulting in fertile seeds.  It's a feat only plants can pull off as they typically bear both male and female organs on the same flower. However it is not generally recommended even for them.  Most plants take measures to avoid self-pollination.  In some, the stigma is not receptive when pollen from the same flower is released. In others, the stigma recognizes its own pollen and rejects it. There are dozens of different ways to prevent selfing. Why? Because in general, populations that get into that habit become genetically, weak and eventually die out - they are evolutionary dead ends.

There are some times when it pays off , however. It is a way, similar to vegetative propagation, of quickly increasing the numbers of a population, and is especially useful in very transient habitats.

The carnivorous Drosera capillaris is seldom more
than an inch in diameter, and lives only in moist,
acidic, sandy soil.
Enter Drosera capillaris, a tiny carnivorous sundew common in Florida. Their sticky leaves trap tiny insects, supplementing their supply of nitrogen and other minerals in wet and nutrient-poor soils. Almost 200 species of this genus exist, mostly in Australia, southern Africa, and South America, but we have 5 species native to Florida.

These tiny plants appear by the millions in damp soil around swamps and freshwater marshes, seemingly out of nowhere.   Evidently the tiny seeds wait out dry periods in the sandy soil, sprouting when moisture returns.  I have even seen progressions of seedlings appear as the shoreline of a small pond receded over several months of a dry spell.

A few years ago, I became curious about how Drosera capillaris reproduced.  Lifespan can be pretty short for the moisture-loving plants as wet meadows come and go and shorelines recede.  They plants pretty much die when the soil dries out.  They can, however bloom within a couple of months of germination, while only about half an inch in diameter. In more stable moist areas, they can live for several years and get to be around 1.5 inches in diameter.

The flowers are small and white or pinkish, most commonly appearing in early spring.  A successfully pollinated flower can produce dozens of tiny seeds.  Because of the thousands of seedlings that can show up when the soil moistens, I assumed that pollination, presumably by some small bees or flies, was pretty common.

The flowers of Drosera capillaris, lifted well above
the sticky traps, stay open only for
a couple of hours, and only if the sun is shining.
I convinced a few of my botany students to spend a few hours in a large population of sundews during their blooming period in the USF Ecology Area.  Fortunately, it is relatively short.  Flowers typically open up in mid-morning, but only if the sun is shining, and close up by noon.  After several days of observation, one student caught a single small bee that might have been pollinating a flower.  Other than that - nothing.  We saw very few insects come near the flowers, and that has been my experience whenever finding these plants in the field.  So where do all the seeds come from to constantly regenerate the populations of sundews?

An accidental experiment suggested the answer.  I had started some sundews from seed in a pot, and eventually I had a single flower on one of them.  This was miles from any other sundews.  The flower closed up around noon and I figured that was the end of it.  A few weeks later, however, I noticed that a seed pod had formed, and eventually I had a crop of seeds from this single isolated flower.

That seemed to confirm my growing suspicion that these little plants self-pollinated.  Looking again at the flowers, it was clear that as the flowers closed, the stigmas and stamens would be pressed together, resulting in pollination.  It has not been verified by rigorous experiment, but it seems that this is the secret to the great fertility of these small plants and their success at inhabiting a fleeting habitat. Every so often, perhaps, an actual cross-pollination might occur, mixing different genotypes and boosting the genetic diversity of the population.