Integrative Biology 335:
Systematics of Plants
Origin of the Angiosperms

Announcements:
Lecture Assignment 5 is due Monday, May 4th. Lecture Assignment 6 is due Monday May 11th.
The final lecture exam is on Thursday, May 14th, from 8 to 11 AM in this room. This exam will be comprehensive, but with emphasis on the last third of the course. It will be worth 20% of your final grade. There is a sample final exam in the back of your Class Notes (pp. 269-284) and the exam will be similar in style to what you saw in Lecture Exam 2. If there is interest, there will be a final lecture exam review (time and place TBA).
Final lab exam on Tuesday, May 5th (stations in lab) and Wednesday, May 6th (slides in lecture). Your final lab exam will also be comprehensive, but again with emphasis on the last half of the course. There will be a lab review on Sunday, May 3rd (time TBA) and I will review families in lecture on Monday, May 4th.
After our lectures conclude, access the General Course Announcements link on the course homepage to obtain any late-breaking class announcements.
Don't forget to complete an ICES teaching evaluation for this course! This year, this evaluation is web-based, and no doubt you would have already received email announcements from the Center for Teaching Excellence. Your comments are important!

Text and Web Resources:
Chapter 7 in Judd et al. (2008), Plant Systematics: A Phylogenetic Approach, pp. 173-181 (Angiosperms). Also, review Chapter 9, pp. 225-229.
The origin of angiosperms is still a mystery, from UC Berkeley
The Abominable Mystery, from Science Magazine
Science at NASA, Solving Charles Darwin's "Abominable Mystery"
View Origin of the Angiosperms, a lecture outline developed for IB 335 by Dr. Jason Koontz and Karyla Trester (formerly of the Illinois Natural History Survey). Much of the information presented, however, duplicates that provided below.

General Objectives:
After studying this material you should be able to:

Know the major morphological synapomorphies shared by angiosperms.
Explain when, where, and how angiosperms may have originated and subsequently migrated.
Explain some ideas on why angiosperms radiated rapidly.
Discuss Charles Bessey's contribution to understanding early angiosperm evolution.
Differentiate among the catkin-bearing, woody magnoliid, paleoherb and Amborella/ANITA Grade hypotheses of early angiosperm evolution.
Describe what is believed to be the most basal extant angiosperm (i.e., Amborella).
Place the ANITA Grade in a phylogeny of extant angiosperms, and know the relationship between this group and the other major clades we've studied this semester. You should be able to construct a simplified cladogram showing the relationships among all the major clades we've studied this term, provide an example or two of a family for each of these major clades, and provide a few synapomorphies for each of these groups.
Explain how we are solving Darwin's abominable mystery today, and what groups (extinct or extant) are candidates for the title "ancestor of the angiosperms."

The Origin of Angiosperms

"The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery." Charles Darwin, in a letter to Sir Joseph Hooker, 1879.

The origin of flowering plants is one of the major unsolved problems of plant phylogeny and an enigma in which most major groups of vascular plants (extinct or extant) have been implicated. This has been what Darwin has called an "abominable mystery."
Why? It's because of the lack of available fossil evidence, including transitional fossils, linking flowering plants with gymnosperms, seed ferns, or other extant or extinct groups. Until rather recently, the fossil record failed to provide reliable clues, and early methods of phylogenetic analysis yielded equivocal or incongruent results. The origin of the angiosperms is indeed "mysterious!"

What is an angiosperm?

A Greek word for "vessel seed."

A vascular seed-bearing plant that bears its ovules enclosed in an ovary derived from the bases of one or more carpels (and also with a stigmatic surface designed for pollen germination). Also defined as "a leaflike megasporphyll with infolded or inrolled connate margins bearing one or more ovules on the inside."
Evolutionary development of the carpel

Over 280,000 (to maybe 400,000) extant species in about 400 families; dominant vegetation type in most terrestrial ecosystems; variable in habit, floral biology, etc., but shares many distinct features, such as:

A. Flowers
Carpels [some magnoliids have open or partially fused carpels]
Reduced megagametophyte (8 nucleate embryo sac)
Double fertilization and triploid endosperm formation
Pollen structural characters

B. Vascular tissue
Vessel elements in secondary xylem for efficient and rapid conduction of water. [Some magnoliids do not have vessel elements. Vessel elements occur in Gnetales.]
Sieve tube elements and companion cells in phloem derived from the same mother cell

C. Leaves
Parallel or netted (reticulate) venation with intercostal (branching) veins

When and where did angiosperms evolve?
Geologic Time Scale. Angiosperms underwent a major radiation starting in the early (lower) Cretaceous, with many angiosperm lineages recognized by the mid-Cretaceous (110 mya). By the end of the Cretaceous, angiosperms had diversified extensively and were the dominant plants in many terrestrial environments.

Unequivocal angiosperm pollen evidence dates to 135 mya (Lower Cretaceous Period).

Macrofossil evidence also dates to about 135 mya (Lower Cretaceous Period).

See Science Article (1998). A date of 140 million years has also been proposed for the first macrofossil (Late Jurassic), but this is likely incorrect. Recent data suggest that this fossil, called Archaefructus (meaning "ancient fruit"), was actually from the Cretaceous.
A more recent Science article (2002) The 125-million-year-old plant (minimum) suggests that the forebears of flowering plants may have been aquatic, weedy herbs.

Earlier reports of pre-Cretaceous angiosperm fossils were rejected or regarded as uncertain relevance due to lack of critical information. Fossils from ca. 130 mya have unequivocal angiosperm reproductive structures that are similar to those found in some extant woody Magnoliales or herbaceous aquatic plants (paleoherbs). Archaefructus actually combines features of both the woody Magnoliales and the paleoherbs!

It's possible that the angiosperms originated in the Jurassic (more than 140 mya); it is also thought that the lineage that gave rise to angiosperms may have been separate from other extant plants for twice that long (see text for further discussion).

At the time of the origin of angiosperms, the continental positions were much different than they are now. West Gondwana (South America and Africa) is thought to be the place of angiosperm origin. Severe deserts existed in the vast continent of Gondwana.
West Gondwana

Climate changes due to the breaking up of Gondwana (continental drift) and subsequent migration via landbridge connections resulted in the migration of these plants into new areas.

Migratory Routes

Angiosperms are thought to have arisen in dry, upland areas; these areas were not optimal for the preservation of fruits, flowers, leaves, etc., thus fossils are either very rare or are difficult to interpret. Though this idea has long been accepted, it has not been well-investigated and so remains to be tested. Because the fossil record is sparse, theories regarding the ancestral stock from which the angiosperms originated are speculative and contradictory (an "abominable mystery!").

Angiosperms appear suddenly and are dominant in the fossil record about 110 mya (mid-Cretaceous Period), and by the end of this Period (65-70 mya) most flowering plant families had evolved. Why this rapid radiation?

Possible reasons for rapid radiation of angiosperms
Angiosperms appear suddenly in the fossil record, probably as a result of rapid adaptive radiation. It has been suggested this occurred because of:

co-evolution with many insect groups (more efficient pollen transfer leads to reproductive isolation);

the advantages conferred by having a shorter life cycle than gymnosperms; and

the probable evolution of the group in regions of diverse habitat types and edaphic factors.
Many features of flowering plants seem to be correlated with successful growth under arid conditions (e.g., closed carpels, vessel elements for highly efficient conduction of water, pollen distribution not dependent upon water [as in gymnosperms; 85% angiosperm spp. insect pollinated], seed resistance and dormancy, efficient fruit dispersal methods, well-protected leaves). Severe deserts led to environmental stress on plants. To survive, these adaptations were necessary.

What groups are candidates for the title "ancestor of the angiosperms?"
Nearly all groups of plants, extant or extinct, have been implicated using morphological, anatomical, and molecular data.

Gnetales. Many analyses have suggested that the Gnetales are the closest living ancestors to the angiosperms (i.e., Gnetum, Welwitschia, Ephedra). These plants also show features of the angiosperms, such as vessel elements and double fertilization. Broad leaves with reticulate venation are found in Gnetum; Ephedra has angiosperm-like reproductive morphology. Analyses based on wood anatomy and some molecular data sets, however, place these plants alongside the conifers.

Conifers. Comparisons were made in the early literature between the strobili (cones) of the Coniferales and the reduced, wind-pollinated flowers of catkin-bearing plants (which were then regarded as the most primitive angiosperms). Anatomical data have shown that the catkin-bearing plants to be advanced, and no support for these candidates as ancestors of the angiosperms are found today.

Cycads. Evidence from fossils indicates that some primitive cycads bore rows of ovules that were partly covered by a leaf blade, thus representing an early stage of carpel evolution.

Seed ferns. Fossils of these ancient, extinct plants caused considerable interest when comparisons were made between their reproductive structures and the angiosperm carpel. They possessed distinct megasporophylls and microsporophylls, with ovules borne on the margins. These plants were abundant in the Carboniferous Period (300 mya). Seeds ferns are often regarded as possible angiosperm ancestors on the basis that all other groups can be eliminated. The "Mesozoic (Jurassic and Triassic) seed ferns," such as the Bennettitales and Caytoniales, had a basal whorl of perianth-like bracts and a whorl of pinnately compound microsporophylls below an ovuliferous region.

None of the above. No living group of seed plants is very closely related to the angiosperms. Therefore, more and better fossils are required to identify the "ancestor of the angiosperms."

What are the most primitive extant angiosperms?
1. Catkin-bearing Plants (Amentiferae)
Adolf Engler & Karl von Prantl (Die natürlichen Pflanzenfamilien, 1887-1915) thought catkin-bearing plants with simple flowers are the most primitive (e.g., Salicaceae, Betulaceae, and Fagaceae).
SIMPLE equals PRIMITIVE.

2. Magnoliaceae and Relatives
Charles Bessey (1915) established a set of dicta (assumptions) that indicated his interpretation of evolutionary trends in angiosperms; he showed these relationships by way of a "cactus-like" drawing ("Bessey's Cactus"). Trends in the evolution of the flower have come about by reduction, fusion, specialization, and changes in symmetry. Simple structures are not primitive, but have become simple as a result of reduction from more complex parts.
SIMPLE does NOT equal PRIMITIVE.

He suggested that Magnolia (Magnoliidae) and its relatives are among the most primitive living angiosperms. These flowers are large, showy, and unspecialized, with many spirally-arranged parts. There is no adnation or connation of parts. While many of the relationships Bessey proposed were flawed, his dicta provided the theoretical base and guiding principles for many other systems of classification that followed (e.g., the systems proposed by Arthur Cronquist [1982] and Armen Takhtajan [1988]).
The Woody Magnoliid Hypothesis
This hypothesis suggests that the basal lineages were small to medium-sized trees with slower life cycles.

3. Paleoherbs
This group includes the monocots plus several "dicot" orders, such as the Nymphaeales and Piperales, as well as the family Aristolochiaceae. These flowers tend to be small, with few simple, perianth parts. Evidence supporting this hypothesis is based on morphology and, to a lesser extent, early molecular data.

Phylogeny of Angiosperms from Zomlefer (1994)
The Paleoherb Hypothesis
This hypothesis suggests that the basal lineages were small herbs with rapid life cycles. They had uncomplicated flowers with a mixture of monocot and dicot features.

4. Amborella and the ANITA Grade
The monotypic genus Amborella has been implicated on the basis of recent phylogenetic analysis of molecular data to represent the most basal angiosperm group. It is classified in family Amborellaceae, order Amborellales.

Figure 7.16 from Judd et al. (2008) showning phylogenetic relationships at the base of the angiosperm clade.
ANITA GRADE
Click here to see Plate 9.1 in your textbook, the ANITA Grade

Amborellaceae (Amborella family, consisting of only Amborella trichopoda)

Nymphaeales (family Nymphaeaceae, water lily family)

Austrobaileyales (families Illiciaceae, Trimeniaceae, and Austrobaileyaceae; star anise family)
Collectively, the group known as the ANITA Grade forms a paraphyletic assemblage at the base of the angiosperms. The remaining well-supported clade that includes the rest of the flowering plants is called the "core angiosperm" clade, or the Mesangiospermae. The latter is characterized by completely fused carpels, rather than carpel margins sealed by only a secretion layer in the basalmost lineages.
Members of the ANITA grade, along with the somewhat morphologically similar Magnoliid clade, have been considered to retain the greatest number of plesiomorphic features within the angiosperms.
Recent evidence suggests that the monocots and eudicots may be sister taxa, with the Magnoliids and ANITA Grade successively basal to them.
You should be able to construct a simplified cladogram showing the relationships among all the major clades we've studied this term, provide an example or two of a family for each group, and list some synapomorphies for each of these clades. Such major clades include:

ANITA Grade
Magnoliids
Monocots
Eudicots

Basal tricolpates
Rosids
Asterids
Caryophyllales

See a previous lecture for more information on angiosperm classification. Remember, some families are not assigned to any of these major eudicot subclades. See Figs. 9.1, 9.2, 9.3 and 9.4 in your textbook.
Amborella trichopoda is a shrubby plant from the island of New Caledonia, with small unisexual flowers and spirally-arranged floral parts. The plants are dioecious. Staminodes are present on the carpellate flowers, suggesting that this species evolved from ancestors with perfect flowers. The flowers are actinomorphic and hypogynous, and the gynoecium apocarpous. Its tepals are distinct. Its numerous stamens are poorly differentiated (i.e., laminar). Its leaves are evergreen, simple and alternate. Only tracheids are found, suggesting that the first angiosperms lacked vessel elements. The absence of aromatic (ethereal) oil cells is significant in light of other basal groups that have them.

Amborella trichopoda (Amborellaceae), is a tropical, dioecious shrub.
Modern representatives of Amborella and Austrobaileyales live in moist forest understory environments and show various adaptations to low-light environments. It has been argued that the first angiosperms grew in disturbed understory habitats or in shady streamside settings and that movement out into more diverse environments might have stimulated diversification (Judd et al., 2008, p. 180). The herbaceous habit evolved multiple times, possibly correlated with the movement into aquatic habitats.

How are we solving Darwin's "abominable mystery" today?
Cladistic analyses of morphological and molecular data, plus the discovery of older and better fossils, are helping to solve Darwin's "abominable mystery." The issue is now close to being resolved, with current data from molecular systematics shedding new light on this subject.
Many molecular studies now point to the gymnosperms (with included Gnetales) as a monophyletic sister group to the flowering plants.
Once more, view the link Origin of the Angiosperms, to learn the results of several recent studies.

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