Chapter 6. Darwin's Abominable Mystery - Origin of the Flowering Plants

The lack of fossil evidence led Charles Darwin to declare that the origin of flowering plants "an abominable mystery." A remarkable set of adaptations that brought male and female reproductive organs together in a compact strobilus, called the flower, revolutionized plant life on land. It led to a vast array of pollination strategies involving animal partners, but also led to a much shortened reproductive cycle, making short-lived herbaceous plants possible. 

1. The flower has a fundamental structure of four leaf--like organs, with protective sepals on the bottom, followed by animal-attracting petals,  ovule-bearing  pistils,and with pollen-bearing stamens above them, always in that order, though one or more sets of organs may be missing in specialized flowers.

2. Sepals enclose the other organs in bud, and are typically green and tough, though they may be colored to aid in the attraction of animal pollinators.

3. Petals commonly are colored, fragrant, and/or nectar-bearing, but may be reduced and inconspicuous in flowers specialized for wind or water-pollination.

 4. Sepals and petals are clearly leaf-like in structure and likely origin, but the origin of carpels and stamens from simple leaf-like ancestral structures, though likely, is sometimes disputed, with branch-like intermediaries proposed.

 5. Fossils of angiosperm ancestors or links with other seed plants are exceedingly rare, and so theories of their origins are somewhat speculative.

 

Figure 6.1 Angiosperms now cover much of the vegetated  planet, having driven earlier forms 

of life to climaticall marginalized habitats (gymnosperms), or to specialized microohabitats 

(bryophytes, seedless vascular plants). They have diversified into a vast array of vegetative 

body forms, as well as into a great variety of flower types htat coevolved with animal 

pollinators or adaptated for abiotic pollen dispersal, such as wind or water.

 

 

Figure 6.2.This phylogenetic diagram illustrates the general relationships of major groups of 

seed plants. The common ancestor of seed plants was a seed fern. The angiosperm stem group 

includes known and presumed seed plants in which the essential features of angiosperms evolved. 

  The angiosperm crown group includes all existing and extinct plants that descended from 

a common ancestor that possessed the essential features of flowering plants. 

 

 

Figure 6.3. The generalized layout of flowers consists of four series of organs: sepals, petals,  

stamens, and carpels (the latter, when joined together into a unified structure, the pistil). 

One or more of these series may be lacking in some specialized flowers. 

Drawings from Haupt 1953.

 

 

Figure 6.4. Magnolia is part of an ancient lineage with an archaic flower structure. Sepals and 

petals are not differentiated, but form a single spirally arranged series of "tepals.". Stamens 

likewise are indefinite in numbers and in a spiral sequence, as are the separate carpels.

 

 

Figure 6.5. Stamens commonly consist of a long, slender filament, and an anther with four

 pollen sacs arranged in a trapezoidal form as viewed in cross-section. Several more archaic 

forms of stamens are flat and leaf-like, with the four pollen sacs lined up on either side of 

the midrib. Drawings from Brown 1935 (A,B) and Mauseth 2014.

 

Figure 6.6. A follicle (A,B) is an elongate carpel that resembles a folded leaf, with the ovules 

arranged in rows on either side. In Eranthis (C), ripening follicles can be seen above leafy bracts 

after the other flower parts have fallen away. In Colchicum (D), a monocot, the carpels are 

of similar structure, but fused together into a unified pistil.  

Drawings from Gray 1879 (A,B) and Thome 1877 (D)

 

Figure 6.7. Comparing the ovule of gymnosperms with the ovule of angiosperms reveals some 

striking and consistant differences. The gymnosperm ovule (A) has a single integument and 

radial symmetry around its central axis (orthotropous), while the typical angiosperm ovule (B) 

has two integuments and is bent downwards (anatropous). The stored nutritive tissue of the 

gymnosperm ovule (colored gray here) is simple haploid gametophyte tissue and bears two egg 

cells near the opening at the top (the micropyle), while the storage tissue in the angiosperm 

ovule is a special triploid tissue (endosperm) resulting from the fusion of three nuclei in the

 center of the female gametophyte. 

 

 

Figure 6.8. Members of the extinct Bennetitales had bisexual strobili that superficially 

resembled angiosperm flowers, but their structure was completely different. They are now 

considered a parallel group descendant from ancient seed ferns. 

Drawing from Brown 1935. 

 

 

Figure 6.9. Though their reproductive structures were not flower-like, details of the pollen-

bearing and ovule-bearing structures suggest a close relationship with angiosperms. 

Pollen sacs were borne on branching stems (A), but each unit contained four chambers (B), 

like modern stamens. Ovules were borne in cupules on branched stalks (C). 

Drawings from Brown 1935 (A,C) and Harris 1937 (B).

Figure 6.10. The cupules of the Caytoniales contained several ovules of gymnospermous 

structure, arranged along the backbone of the chamber (A). A hypothetical transition to the 

angiosperm ovule would involve reduction of the number of ovules to one per chamber, attached 

to the top and suspended downward (B). With further refinement the wall of the cupule would

 become the second integument of the angiosperm ovule and also result in the "bent" 

(anatropous) shape characteristic of angiosperms.

 

 

Figure 6.11. The ANITA grade (more recently the ANA grade) consists of several 

orders of archaic Angiosperms that branched off before the three major clades. 

The "I" and "T" of the ANITA grade stand for  Illiciales and Trimeniaceae, 

which have now been lumped with the Australobaileyales. Note that the monocots, once 

considered an equal sister clade to the rest of the angiosperms ("dicots"), is a specialized 

branch from within all the others. 

Figure 6.12. Amborella trichopoda  is the single surviving species of a long clade that

branched off of the ancestral angiosperm lineage before any other known flowering 

plants. It has archaic flowers, but several specialized features as well:

it has unisexual flowers (separate male and female flowers) and fruits specialized 

as brightly colored drupes - single seeded fruits adapted for bird 

dispersal. The carpel (A) is ascidiate, unsealed at the top, with a single ovule hanging

 from  the top. The ovule develops into a small red-colored drupe (B). Because of their

 widespread occurrance in the ANA grade, ascidiate carpels are  presumed to be the ancestral 

type in flowering plants. The relationship between such ascidiate ovules, and the folded 

carpels, which are more common among monocots, magnolids and eudicots, and that seem 

to be more directly derived from ovule-bearing leaves in seed ferns, is still unclear. 

 Drawings from Bailey and Swamy 1948.