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.