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,
 1948. 

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
Stevenson.

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.


References: 

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.