MODERN BOTANY — P. RAVEN — 1990

SECTION VIII. EVOLUTION

CHAPTER 29. EVOLUTION OF FLOWERING PLANTS

Among modern plants, angiosperms occupy a prominent place. Trees and shrubs, meadows and gardens, wheat and corn fields, wildflowers, vegetables and fruits on display stands, colorful arrangements in florist shop windows, geraniums on the windowsill, duckweed and Water lilies in a pond, eelgrass in the bay, cacti in the desert—wherever we might be, we encounter them everywhere.

Class="center">Fig. 29-1. A. A pollen-covered longhorn beetle (fam. Cerambycidae) on the flowers of an umbellifer (Apiaceae) in the mountains of northeastern Arizona. B. Beetle elytra from deposits containing *Archaeanthus*, an angiosperm that went extinct 95 — 98 million years ago (see Appendix 1 to Ch. 29). The evolution of flowering plants is largely a METABOLISM/13.html">History of the increasing specialization of relationships between flowers and insect pollinators, in the Cytology/cytology/16.html">Early stages of which beetles played a major role.

In a letter to a friend, Charles Darwin called the sudden appearance of representatives of this major group in the fossil record an "abominable mystery." In the oldest deposits containing plant remains, primitive vascular forms with very simple structures are found. Then, in the Devonian and Carboniferous periods, ferns, clubmosses, horsetails, and progymnosperms rapidly spread. The first seed plants appeared in the late Devonian, and by the Mesozoic, gymnosperms were already dominant. Finally, in the first half of the Cretaceous period—that is, toward the end of the Mesozoic era—angiosperms, or flowering plants, emerged, gradually taking over a dominant position across the entire planet. About 75 million years ago, many modern families and even some currently living genera of this division already existed (Fig. 29-2).

Fig. 29-2. Fossil remains of a gymnosperm (A) and two angiosperms (B, C) from Late Cretaceous deposits (about 70 million years ago) in Wyoming. A. A branch and individual cone scales of *Araucarites longifolia*, an extinct conifer of the araucaria family (Araucariaceae), which today is restricted to the Southern Hemisphere. Widely cultivated species of this family include the Norfolk Island pine (*Araucaria heterophylla*). B. A leaf of the extinct fan palm *Sabalites montana*, distantly related to the palmettos of the southeastern US. C. A leaf of the extinct species *Viburnum marginatum*, belonging to the widely distributed shrub genus *Viburnum* (viburnums).

What enabled angiosperms to claim a dominant position in the plant world and achieve such staggering diversity by the present day? In this chapter, we will attempt to answer this question by focusing on three points: THE ORIGIN OF this group, the Evolution of the flower, and The Role of certain chemical compounds in the evolution of angiosperms. In doing so, we will illustrate the evolutionary process that we began describing in the previous chapter.

Origin of Angiosperms

It is now widely accepted that flowering plants arose from some primitive, most likely shrubby, gymnosperms.

No remains of the probable ancestors of angiosperms have been found in Cretaceous deposits, but A number of earlier Mesozoic and Paleozoic gymnosperms already possessed certain combinations of features close to the characteristic traits of flowering plants. This suggests that angiosperms appeared earlier than the date of their oldest known fossils.

The earliest remains that can be reliably attributed to angiosperms date to the Early Cretaceous (around 125 million years ago) and consist of monosulcate pollen grains. They resemble fern spores and gymnosperm pollen, yet are distinct from them. Apparently, the pollen of most earlier angiosperms can no longer be recognized among the remains of other groups. In all monocots and most primitive dicots, the pollen resembles that of the earliest known flowering plants. In layers at least 120 million years ago, tricolpate pollen grains appear, which are characteristic of all dicots except the most primitive ones. And as early as 80 — 90 million years ago, angiosperms were more numerous everywhere in the world than representatives of any other plant group. What do we actually know about their origin?

Phylogenetic Relationships of Angiosperms

Since Darwin's time, scientists have attempted to determine the ancestors of angiosperms. One approach to this task was to search for them among the fossil remains of seed plants. Particular emphasis was placed on how easily the hypothetical transformation of ovule-bearing structures in gymnosperms into carpels could occur. Recently, a different approach has been proposed: instead of hunting for ancestors, simply identify the major natural groups of seed plants and trace their relationships to one another. The degree of relationship can then be used to judge how long ago they diverged from a common ancestor. This field is currently led by P. Crane of the Field Museum of Natural History in Chicago, who provided much of the data used in compiling our section.

In the simplest case, discussing phylogenetic (evolutionary) relationships involves just three different plant groups. In ferns, cycads, and pines, for example, the xylem consists of tracheids, which suggests that long ago in the distant past they shared a common ancestor (also possessing tracheids). One can ask: which two of these three groups diverged later? In this case, we have only three possibilities, graphically represented by three diagrams (Fig. 29-3). Cycads and pines have seeds and wood (secondary xylem); neither of these is present in ferns. Thus, we can infer that the common ancestor of cycads and pines existed more recently than the common ancestor of each of these groups and ferns (Fig. 29-3, A). Traits considered inherited from a common ancestor (e.g., seeds, wood, tracheids) are called homologous. If an additional plant group is introduced into the diagram, such as Douglas-fir, to clarify its relationship with cycads and pines, it becomes necessary to find narrower homologies. What pines and Douglas-firs share is the presence of resin canals in their leaves; this suggests that the two genera diverged evolutionarily later than either of them did from cycads (Fig. 29-4). When this type of analysis is expanded by increasing the number of traits and plant groups, the Conclusions are often different from those obtained with a more limited scope of data. In such cases, the simplest explanation of relationships must be adopted—that is, the one supported by the greatest number of homologies. This solution can be tested, and sometimes modified, by considering additional traits and plant groups.

Fig. 29-3. Three possible Phylogenetic relationships among ferns, cycads, and pines. Variant A is likely correct; it is based on the indicated traits.

Fig. 29-4. Phylogenetic relationships among ferns, cycads, pines, and Douglas-fir, indicating the shared traits underlying this specific scheme and the approximate divergence times of the groups.

Elucidating relationships in this manner leads to the creation of schemes in which large (higher) groups encompass several smaller (lower) ones. This is called a hierarchical level. Each group, or clade, is characterized by one or more homologies and includes all descendants of a single hypothetical common ancestor. Graphic representations of evolutionary relationships among such groups in the form of branching systems are called cladograms. Vascular plants are a clade within which seed plants form a lower-order clade, and conifers within seed plants form an even lower-order clade (Fig. 29-4). Such a scheme simultaneously predicts the possible sequence of the appearance of homologies in the fossil record. In our simple example, paleobotanical data fit the cladogram: tracheids first appeared no later than 400 million years ago, seeds and wood about 350 million years ago, and resin canals approximately 50 million years later.

In some cases, similarities that at first glance appear to be signs of relationship do not reflect the evolutionary connections depicted by a cladogram. For example, the female cones of cycads, on the one hand, and pines and Douglas-firs, on the other, are very similar, but this similarity is merely superficial. In cycads, each scale is simply a modified leaf bearing a seed, whereas in conifers it is a complex Structure (see Ch. 18). Thus, the cones of cycads and conifers apparently did not evolve from a common ancestor and cannot be used to characterize a clade. Such structures are called analogous. Their external similarity is due to convergent evolution (see p. 72). Conversely, the complex female cones of pine and Douglas-fir are homologous and serve as a diagnostic trait of the conifer clade.

Another potential source of confusion when establishing similarities is too narrow an understanding of specific Homology. For example, in clubmosses, horsetails, and ferns, spores are free (i.e., they disperse rather than remain on the parent sporophyte), but this trait cannot be used to define a clade because the spores of these plants are simultaneously homologous to part of the seed in seed plants. A group characterized by free spores would be incomplete and would not include all descendants of a single common ancestor that presumably also gave rise to seed plants. In this example, There are two homologies: the presence of spores and the presence of megaspores modified into seeds; these correspond to two clades, one of which is nested within the other, while free-spored vascular plants do not form a clade on their own.

The approach discussed here, known as Phylogenetic Analysis or cladistics, relegates The problem of finding the ancestors of flowering plants (which may not yet have been discovered or may not have been preserved in the fossil record at all) to the Background. Its goal is to identify the major clades of seed plants and assess their relationships in terms of the relative times when their common ancestors existed.

Analysis is best initiated with modern seed plants, which are generally better studied than their fossil relatives. A recently proposed cladogram is shown in Fig. 29-5. It clearly indicates that gymnosperms do not form a distinct clade and that traits potentially characterizing this division are apparently shared by angiosperms as well. Indeed, gymnosperms are simply what remains of the seed plant clade after the angiosperms diverged.

Fig. 29-5. Phylogenetic relationships among the four living gymnosperm divisions and angiosperms

The next step after analyzing modern plants is incorporating data from fossil seed plants. While many of these can be assigned to groups known from extant forms, others represent major extinct clades. The latter can play a crucial role in tracing homologies and thus prove extremely valuable for elucidating evolutionary relationships. Fig. 29-6 presents two recently proposed cladograms illustrating the affinities of major living and fossil seed plants. Naturally, these schemes will be refined through future research—particularly by incorporating new data on several key extinct groups—yet even in their present form, they reflect current views on THE POSITION OF flowering plants in seed plant evolution.

Fig. 29-6. Two possible schemes of phylogenetic relationships among divisions of extant seed plants and certain related groups. These cladograms were constructed by P. Crane from the Field Museum of Natural History in Chicago

Evolutionary Radiation of Angiosperms

Several years ago, paleobotanist D. Axelrod of the University of California at Davis suggested that the early evolution of angiosperms may have taken place far from the lowland basins where their fossils are typically found. It is quite probable that in tropical hills and uplands, flowering plants produced a wide spectrum of forms that had little chance of being preserved in the geological record. According to Axelrod, angiosperms attained a dominant position in the Earth's vegetation approximately 120 million years ago, when they descended into the lowlands.

Ancient flowering plants possessed numerous adaptive traits that made them particularly resilient to drought and cold. These included leathery, typically small leaves, vessel elements (efficient water-conducting Cells), and a tough, durable seed coat protecting the young embryo from desiccation. While these traits are not universal among angiosperms, nor exclusive to them, they played a pivotal role in the diversification of this division.

A number of other factors appear to have been critical to the initial and subsequent success of angiosperms, some of which are discussed in greater detail later in this chapter. The appearance of sieve tube elements enhanced the efficiency of sugar transport through the phloem, while more sophisticated conducting elements—vessel elements—replaced tracheids in the xylem. Perhaps an even greater role was played by the finely tuned pollination and seed dispersal systems characteristic of this group, which enabled widely separated individuals to thrive in diverse habitats. The tremendous chemical diversity of angiosperms, which produce numerous compounds defending them against diseases and herbivores, was likewise of major significance (see below). These and other features are directly related to the faster and more efficient reproduction of angiosperms compared to other plants.

An important evolutionary innovation of flowering plants was deciduousness. Deciduous forms do occur among gymnosperms—such as larch and bald cypress—but they are exceptionally rare relative to the total size of the group. Among angiosperms, such plants are very numerous. Deciduousness apparently first emerged in tropical regions characterized by periodic droughts. Descendants of the earliest deciduous plants migrated northward, where winters became too cold and water unavailable for growth. Another beneficial modification in flowering plants was the evolution of herbaceous perennials and, subsequently, annuals, enabling survival in harsher conditions than those tolerated by their woody ancestors. All of these adaptations proved especially crucial during the climatic stresses of the past 50 million years of Earth's history—a period that played a vital role in the evolution of flowering plants.

About 125 million years ago (the age of the earliest angiosperm pollen finds in the geological record), Africa and South America were connected to each other, as well as to Antarctica, India, and Australia, forming a vast southern supercontinent known as Gondwana (Fig. 29-7). Around this time, Africa and South America began to drift apart, forming the South Atlantic Ocean, though they were not completely separated in the tropical zone even 90 million years ago. Concurrently, India began moving northward, colliding with Asia some 45 million years ago, which drove the uplift of the Himalayas. Approximately 55 million years ago, Australia began to separate from Antarctica, though their complete detachment occurred later.

Fig. 29-7. Continental positions at the time of the earliest angiosperm fossils. In the mid-Cretaceous, about 100 million years ago, South America was connected to Africa, Madagascar, and India, and via Antarctica to Australia. This combined landmass, highlighted in brownish tones on the map, constituted the supercontinent of Gondwana

The central regions of western Gondwana, corresponding to modern Africa and South America, evidently featured a diverse array of habitats ranging from arid to subhumid types, which—according to Axelrod and others—served as a major center for the early evolution of angiosperms. By the time the two continents finally separated, roughly when fossil evidence shows angiosperms had already become widespread globally, the Earth's climate had changed dramatically, particularly in equatorial regions, where it grew milder with less extreme fluctuations in Temperature and moisture. This shift is believed to have driven the evolutionary success of early angiosperms as they tightened their dominance over the world's floras.

When India and Australia occupied high southern latitudes, their vegetation was typical of a cool-temperate climate. The distribution ranges of several unique PLANT AND ANIMAL groups currently shared by southern South America and southeastern Australia-Tasmania were shaped by migration across Antarctica long before its complete glaciation around 20 million years ago (Fig. 29-8). As Australia drifted northward over the past 55 million years, it entered a broad arid zone bordering the tropics; it was then that the desert plant communities so characteristic of this continent experienced massive expansion. Upon approaching Asia, Australia's northern tip entered a tropical climate zone, allowing tropical Asian plants and animals to invade. Nevertheless, Asian and Australian biotas remained largely geographically segregated; the boundary separating their respective domains is known as Wallace's Line, named after Alfred Russel Wallace, one of the earliest naturalists to explore these regions (also renowned for co-proposing The Theory of evolution by natural Selection alongside Darwin). The native flora and fauna of cool-temperate Australia survived in the southeastern extremity of the continent, in Tasmania, and in New Zealand, which had separated from the Australia-Antarctica landmass about 80 million years ago and drifted northeastward.

Fig. 29-8. A. Hard beech (Nothofagus menziesii) in the upper Caples River valley (South Island, New Zealand)—a relict of the cool-temperate forests that once spanned from southern South America across Antarctica to Australia and New Zealand approximately 80–30 million years ago. Throughout this period, their range fragmented, and the gaps continue to widen to this day. B. The nipa palm (Nypa fruticans) at the edge of a tidal mangrove swamp. Some 40–50 million years ago, when Africa and South America remained closely juxtaposed, this genus was widespread across all warm Regions of the globe, but its range gradually contracted and is now restricted to southeastern Asia, northern and northeastern Australia, and certain Pacific islands

India's original flora and fauna fared far less well, with only a handful of relicts surviving to the present day. India drifted much farther than Australia, traversing the southern arid zone, the tropics, and the northern arid zone in the process. As a result, nearly all Gondwanan organisms perished, replaced by Eurasian desert, tropical, and montane plants and animals.

Evolution of the Flower

Floral Parts

The single feature distinguishing angiosperms from all other groups is the flower—a structure discussed in considerable detail in Chapter 18. As noted previously, it represents a shortened SHOOT bearing various leaf-like appendages. The evolutionary homology between leaves and floral parts is examined below. Most of our conclusions regarding floral evolution are based on comparative studies of extant forms, although The Significance of fossil flowers in unraveling angiosperm history is steadily growing as more discoveries are made.

Carpel

In its simplest form, a carpel is a folded leaf blade. As illustrated somewhat schematically in Fig. 29-9, there are no specialized structures for catching pollen grains. Both margins of the folded blade are covered with stigmatic hairs. Such a carpel encloses ovules borne on its inner surface. In all modern angiosperms, carpels are closed, although various stages of closure can still be traced across different groups. In primitive flowering plants, extensive stigmatic surfaces run along the margins of the carpels. More specialized groups (comprising nearly all living species) possess much smaller stigmas located on a style above the Ovary.

Fig. 29-9. Evolutionary modifications of the carpel. A primitive carpel is folded along its axis. Its blade encloses numerous ovules attached to its inner surface. The margins are unsealed, and the stigmatic surface lacks distinct boundaries, although stigmatic hairs are strongly developed along the crest, i.e., the carpel margins. In carpels derived from this primitive type, the margins fuse to varying degrees, and the pollen-receptive stigmatic surface occupies only a portion of the crest

In early angiosperms, ovules were presumably arranged in rows along the margins of the carpel on its inner surface. In more advanced groups, their placement became more diverse. Primitive flowering plants possessed numerous ovules, whereas advanced ones have relatively few. The gynaecium in the flowers of ancient angiosperms consisted of A large number of separate carpels; through evolutionary specialisation, their number decreased, and they fused with one another (Fig. 29-10).

Fig. 29-10. Proposed course of gynaecium evolution

Androecium

Although the stamens of modern plants (see, for example, Fig. 18-39) rarely resemble leaves, some resemblance between these structures can be found in magnolias and their relatives. Much like them, primitive stamens may have been flat in shape, bearing sporangia near the centre of the blade (Fig. 29-11). According to one theory, the blade differentiated into a slender stalk (the filament) with sporangia at the apex; another equally plausible theory suggests that stamens arose from systems of fine branches bearing terminal sporangia (which gradually fused and, in some cases, became leaf-like).

Fig. 29-11. Stamens of primitive angiosperms. In these woody plants, anthers are formed on the lower or upper surface of leaf-like microsporophylls. The first pattern occurs in the genera Himantandra and Degeneria (viewed from below), while the second is found in Austrobaileya and Magnolia (viewed from above). In most modern angiosperms, the stamens are no longer leaf-like, contain much less sterile tissue, and bear anthers at the tip of a slender filament. These differences are difficult to explain, leading to the hypothesis that leaf-like stamens, such as those shown here, may have evolved through the fusion of branching systems with terminal sporangia.

In a number of specialised flowers, stamens—much like carpels—have undergone fusion. This has led to The formation of columnar structures, such as those seen in Fabaceae, Cucurbitaceae, Malvaceae (see Fig. 29-13, D), and Asteraceae. In some cases, stamens became adnate to the corolla, notably in the Polemoniaceae, Scrophulariaceae, and Lamiaceae families.

In certain evolutionarily advanced flowers, stamens became secondarily sterile—that is, they lost their sporangia and transformed into specialised structures, such as nectaries, which are glands secreting a sugary fluid that attracts and feeds pollinators. (It is important to note, however, that in most cases nectaries are not modified stamens, but rather originate from other PARTS OF THE flower.) As will be discussed below, stamens also played a specific role in the evolution of petals.

Perianth

The perianth consists of sepals and petals. In most plants, the sepals are green and photosynthetic. For this reason, and because they receive the same number of vascular bundles as the leaves of the given species (often, though not always, more than one), sepals are leaf-like, and are generally considered to have evolved directly from leaves.

In a few families, such as the Nymphaeaceae, petals apparently originated from sepals. However, in the majority of angiosperms, petals likely evolved from stamens that had previously lost their sporangia and acquired a new function—attracting potential pollinators to the flower. Most petals, like stamens, are supplied by a single vascular bundle, thus differing from sepals which, as mentioned earlier, typically possess as many bundles as the leaves of the same species (often three or more). In both sepals and petals, vascular bundles usually branch, making it impossible to determine the number of bundles entering the organ simply by counting the Veins on the blade.

During the evolution of many angiosperm groups, petals underwent fusion to form a tubular corolla characteristic of numerous families. The stamens frequently fused with this tube as well (appearing to arise from the corolla). In a number of evolutionarily advanced families, the sepals have also united into a tube.

Trends in Flower Evolution

Among modern plants, the flowers most closely resembling the primitive type in overall structure are found in the Magnoliaceae (Fig. 29-12). Their flowers feature numerous carpels, stamens, and perianth parts, all of which are distinctly separate from one another. Furthermore, their spiral arrangement on a conical receptacle remains clearly discernible. However, the pronounced elongation of the receptacle and the 'cone-like' packing of the carpels are clearly secondary features, reflecting the specialisation of magnoliids and are not characteristic of other primitive angiosperms.

Fig. 29-12. Floral structure of southern magnolia (Magnolia grandiflora). The conical receptacle bears numerous spirally arranged carpels with recurved styles. Below them lie the light-cream stamens (A, B). An unopened bud; parts of the perianth in the foreground have been removed to reveal the stigmas and stamens, which are not yet shedding pollen. B. The floral axis on the second day of anthesis; the stigmas are no longer receptive, and the stamens are shedding pollen. C. Fruits; carpels and bright red seeds on slender stalks are visible.

Comparing such flowers with more specialised ones allows us to trace four major evolutionary trends in floral structure (Fig. 29-13; see also Fig. 18-43).

1. From a large and indefinite number of parts to a small and fixed number.

2. From four types of floral parts down to three, two, and occasionally one in more advanced groups. The floral axis shortens, and the original spiral arrangement becomes obscured. Floral parts undergo fusion.

3. From a superior ovary to an inferior ovary.

4. From radial Symmetry, or actinomorphy, to bilateral symmetry, or zygomorphy.

Fig. 29-13. Examples of specialised flowers. A. Pipsissewa (Chimaphila umbellata); the number of sepals (not visible) and petals is reduced to 5, stamens to 10, and 5 carpels are united into a single compound gynaecium with a single stigma. B. American lotus (Nelumbo lutea). Undifferentiated sepals, numerous petals, and stamens are arranged in a spiral; carpels have fused into a compound gynaecium. C. Hairy honeysuckle (Lonicera hispidula). The ovary is inferior, two- or three-locular; sepals are reduced to small Teeth at its apex. Petals are united into the corolla tube of a zygomorphic (bilaterally symmetrical) flower. Five stamens protrude from the tube and are attached to its inner wall. The style is longer than the stamens, and the stigma is positioned above them. Before a pollinator visiting the flower can reach the anthers, it must Touch the stigma, leaving behind pollen carried from another flower. The fruits of this plant are shown in Fig. 29-46. D. Floral diagram of cotton (Gossypium) with stamens united into a Column surrounding the style.

Examples of Specialized Families

Among the groups with the most evolutionarily specialized flowers are the Asteraceae (or Compositae) within the dicotyledons and the Orchidaceae among the monocotyledons.

Asteraceae (Compositae)

The epigynous flowers of this family are relatively small and densely crowded into a HEAD, or capitulum, inflorescence. Their inferior ovary is unilocular and formed by two fused carpels enclosing a single ovule (Fig. 29-14).

Fig. 29-14. Asteraceae (Compositae). A. Diagram of a head inflorescence in a representative of this family. The structure of individual flowers is subordinated to the overall architectural plan of the head, which Functions as a single large, pollinator-attracting flower. B. Cirsium pastoris (thistle). Species of this tribe possess only tubular (disc) florets. In this thistle, the florets are bright red and regularly visited by hummingbirds, its primary pollination agents. C. Agoseris, a relative of the dandelion (Taraxacum). In the inflorescences of members of this tribe (a group of composites that includes dandelions, chicory, and related species), tubular florets are absent, and only ligulate (ray) florets are developed, which are larger at the periphery of the inflorescence. D. Sunflower (Helianthus annuus)

The number of stamens per flower is reduced to five, and they are typically fused to one another and to the corolla. There are also five petals, fused to each other and to the ovary, while sepals are absent or reduced to rows of bristles or scales forming the so-called pappus. The pappus frequently AIDS in wind dispersal of seeds, as seen in the dandelion (Fig. 29-14, C; see also Fig. 29-42), which belongs to the Asteraceae. In other members of this family, such as beggar-ticks (Bidens), the pappus may bear barbs that serve to attach the fruit to the fur or clothing of animals, thereby increasing the probability of dispersal to a new Location. In many composites, the head contains Two Types of flowers: tubular florets in the central region and ligulate florets along the margin. The latter often possess an ovary but are sometimes completely sterile. In some composites, such as daisies, sunflowers, or chamomile, their fused corolla takes the form of a long "petal."

In general, the composite head resembles a large solitary flower; however, unlike a solitary flower, it matures over the course of several days, with individual flowers opening in a centripetal sequence. As a result, the ovules within a single head can be fertilized by pollen from multiple sources. The success of this evolutionary strategy is evidenced by the species richness of this family—likely the largest among flowering plants—which comprises approximately 22,000 species.

Orchidaceae

A different, highly successful floral structural plan is demonstrated by the orchid family (Orchidaceae), which, in contrast to the Asteraceae, belong to the monocotyledons. Comprising at least 17,000 species—though the Classification of many genera remains poorly resolved—this is likewise one of the largest plant families. The majority of its species are tropical; only about 140 species have ranges extending into the United States and Canada. As in the Asteraceae, the three carpels of orchids are fused, and the ovary is inferior (Fig. 29-15). However, the ovary contains many thousands of tiny ovules, meaning that pollination can result in The production of an enormous number of seeds. Typically, only a single stamen is present (two in the subfamily Diandra), which is fused with the style and stigma into a complex structure called the column. All the Contents of the anther are held together and transferred as a single unit known as a pollinium (see Fig. 29-26, B). Of the three petals, two lateral ones are modified into wings, while the third forms a cup-shaped lip (labellum), which is often very large and brightly colored. There are also three sepals, frequently colored and petal-like in appearance. The flowers are invariably bilaterally symmetrical and in many cases exhibit a bizarre or intricate Morphology.

Fig. 29-15. A. An orchid of the genus Cattleya (species 143). The Orchidaceae are one of the most specialized monocot families. B. Comparison of floral parts in an orchid (left) and a radially symmetrical flower (right). The "lip" is a modified petal that serves as a landing platform for insects

Orchid flowers range in size from that of a pinhead to more than 20 cm in diameter. Saprophytic plants are known within certain genera; two Australian species lead a completely subterranean lifestyle, their flowers emerging in soil cracks where they are pollinated by flies (Fig. 29-16). In commercial cultivation, orchids are cloned by dividing meristematic tissue, rapidly producing thousands of identical plants in this manner. More than 60,000 hybrids have been registered in this family, many of them involving crosses between two or more genera. Fruits of the genus Vanilla serve as the natural source of the popular spice vanilla (Fig. 29-17).

Fig. 29-16. Rhizanthella, a subterranean orchid from Western Australia. Its flowers, which never emerge above the surface, can be seen in soil fissures formed during the dry season. A. Top view (debris and leaves cleared away): three diverging bracts through which pollinators (flies) squeeze. B. Flowers surrounded by protective bracts

Fig. 29-17. Vanilla (Vanilla) is an orchid from which the spice of the same name is produced on an industrial scale. It was first used by the Aztecs in the territory of present-day Mexico. Today, vanilla is cultivated primarily in Madagascar, other islands of the western Indian Ocean, and the Old World generally. Chocolate is a mixture of cacao and vanilla. The synthetic flavoring agent vanillin is now widely used instead of the natural product extracted from the dried and cured fruits of this orchid. A. Flowers of Vanilla planifolia. B. Artificial pollination of vanilla in Mexico; this practice is employed even with wild plants to ensure a high yield of the fruit from which the spice is extracted

Agents of Evolution

Unlike animals, plants cannot move from place to place in search of food, shelter, or a mating partner, and are forced to satisfy these "needs" through growth processes and specialized structures. Nevertheless, angiosperms have evolved a suite of traits that ensure a degree of active searching for a sexual partner—namely, floral features. By using flowers to attract insects and other animals and directing their behavior to increase the probability of cross-pollination (i.e., the mating of distantly related organisms), angiosperms are, in a sense, no less motile than animals. How was this achieved?

The earliest seed plants—various groups of gymnosperms—were pollinated passively. Their pollen was carried by the wind and only by chance came into the vicinity of ovules. Located on leaves or inside cones, the ovules secreted droplets of sticky fluid from their micropyles. These droplets served to capture pollen grains and draw them into the micropyle, much as in extant gymnosperms. Insects (likely beetles, see Fig. 29-1) that fed on sap and resinous secretions on stems and leaves encountered protein-rich pollen grains and the sticky droplets exuded by ovules. By regularly exploiting these novel food sources, insects began, through their visits, to transfer pollen from one plant to another. This mode of pollination evidently proved far more effective right from the start than passive wind pollination.

The more attractive plants were to beetles, the more frequently they were visited and the more seeds they were able to produce. Any phenotypic change that enhanced the frequency or efficiency of such visits immediately conferred a selective advantage. This drove several important evolutionary changes. For example, plants with flowers that offered a particularly valuable food source for pollinators gained a selective advantage. In addition to pollen, the sticky fluid around the ovules, and edible parts of the flower itself, flowers began to evolve nectaries—glands secreting nectar, a nutritious sugary liquid that serves as an energy source for insects and other animals.

Attracting pollinators to flowers created a new challenge: the need to protect the ovule from being eaten. The Emergence of a closed carpel was likely one solution to this problem. Subsequent modifications in floral architecture, such as the evolution of an inferior ovary, may also have served as mechanisms to protect the ovule.

Another major milestone was the appearance of the bisexual flower. The presence of both carpels and stamens within the same flower (in contrast to, for example, the separate male and female cones of conifers) made each pollinator visit far more efficient, as the animal could now simultaneously remove pollen from the plant and deposit foreign pollen upon it.

At the beginning of the Tertiary period, i.e., 40–60 million years ago, the Abundance and diversity of specialized flower-visiting insects—such as bees and butterflies—increased significantly, having already coevolved with angiosperms for nearly 50 million years. The population growth and diversification of these animals are directly linked to these same processes in the angiosperms. In turn, insects exerted a profound influence on the evolution of flowering plants, contributing in large part to the dramatic increase in their diversity.

If a particular plant species is pollinated by only one or a few insect species, it benefits from specializing in accordance with the traits of these visitors. Many modifications of the primitive angiosperm flower were specialized adaptations that helped "secure" specific pollinators to flowers with distinct characteristics.

Below, we examine several evolutionary modifications of the flower that arose as adaptations to specific pollinators.

Beetle-Pollinated Flowers

A number of modern angiosperm species are pollinated exclusively or primarily by beetles (Fig. 29-18; see also Fig. 29-1). Their flowers are either large and solitary (as in magnolias, certain Liliaceae, California poppy, and roses) or small and clustered into inflorescences, as in dogwood, elderberry, spiraea, and many Apiaceae (see Fig. 29-1, A). Representatives of 16 beetle families frequently visit flowers, although, as a rule, their main food source consists of sap from vegetative plant parts, fruits, excrement, and decaying matter. Beetles rely far more on their SENSE OF SMELL than on sight; consequently, beetle-pollinated flowers are often white or drab in color yet possess a strong fragrance (Fig. 29-19, A)—typically fruity, spicy, or reminiscent of unpleasant Fermentation, which sets them apart from the sweet scents of bee- and butterfly-pollinated flowers. Some beetle-pollinated flowers secrete nectar, whereas in others these insects feed directly on the petals, specialized nutritional bodies (clusters of cells On the surface of various floral parts), or pollen. In most cases, the ovules here are well protected by the ovary and remain out of reach of the chewing mouthparts of the pollinators.

Fig. 29-18. A pollen-feeding beetle (Asclera ruficollis) on an open, saucer-shaped flower of the round-lobed hepatica (Hepática americana). All adult species of this beetle family (false blister beetles — Oedemeridae) are obligate pollen-eaters.

Fig. 29-19. A. The skunk cabbage (Lysichiton americanum) is pollinated by small, actively flying beetles of the family Staphylinidae, which are attracted by the plant's very pungent odor. Other species of the same family (Araceae) feature inflorescences with a scent reminiscent of rotting fish or carrion and are pollinated by blowflies. B. One such plant is Symplocarpus foetidus. Several species from other families produce a similar odor and are likewise pollinated by carrion flies; excellent examples include Stapelia schinzii (C) and its close relatives, predominantly African members of the milkweed family (Asclepiadaceae).

Flowers Pollinated by Bees, Wasps, and Flies

Bees are the most important group of flower-visiting animals, pollinating a greater variety of plant species than any other group. Bees subsist on nectar, and worker bees also gather pollen to feed their larvae. Their mouthparts, body setae, and other appendages are specialized adaptations that facilitate the collection and transport of these resources (Fig. 29-20). As Karl von Frisch and other researchers of insect behavior have demonstrated, bees quickly learn to distinguish colors, scents, and external shapes, although—like most insects—their visual spectrum differs somewhat from ours. Unlike humans, bees perceive the ultraviolet range and cannot detect red, which tends to blend into the background for them.

Fig. 29-20. Bees are as highly specialized as the flowers with which they have coevolved. Their mouthparts have evolved into a sucking tube equipped with a Tongue. The first segment of each of the three pairs of legs bears a tuft of bristles on its inner surface. On the First and Second pairs, these comb-like brushes collect pollen adhering to the bee's hairy body. The brushes on the third pair of legs clean the pollen from the brushes of the first pairs and the abdomen, from which it is pushed into the corbicula—a pollen basket framed by hairs on the upper segment of the third leg pair. The illustration shows a honey bee (Apis mellifera) foraging on a rosemary flower (Rosmarinus officinalis). Its stamens and stigma project from the corolla and curve upward, coming into contact with the hairy back of any adequately sized bee visiting the flower; pollen grains left behind by the anthers are clearly visible on the insect.

Many bee species—especially solitary ones, which make up the majority of this group (Fig. 29-21)—exhibit a high degree of floral constancy. This fidelity enhances the efficiency of the individual insect or species as a pollinator. In connection with this specialization, bees with rigidly fixed foraging behaviors frequently display distinct morphological and physiological adaptations. For instance, if they visit plants with large pollen grains, their pollen-collecting apparatus is equipped with coarse bristles, whereas if they gather nectar from flowers with long tubes, their mouthparts are elongated. By achieving such a high level of constancy in their "preferences," bees become a powerful evolutionary force driving the specialization of the plants they visit. There are approximately 20,000 known species of bees, the majority of which feed on flowers.

Fig. 29-21. A sweat bee (family Halictidae) gathering pollen from the stamens of an Echinocereus cactus flower (Baja California, Mexico). The stigmas are visible in the center of the flower above the stamens.

Flowers that coevolve with bees feature conspicuous, brightly colored petals—typically blue or yellow—often marked with distinct patterns that allow insects to recognize them effortlessly. These patterns sometimes include "nectar guides," i.e., specialized markings that indicate the LOCATION OF THE nectar (Fig. 29-22). Such flowers are never purely red. Specialized photography techniques have revealed that they frequently bear characteristic patterns invisible to the human eye (Fig. 29-23).

Fig. 29-22. "Nectar guides" on foxglove flowers (Digitalis purpurea) serve to attract insect pollinators. The lower lip of the sympetalous corolla forms a "landing platform," a feature commonly found in bee-pollinated flowers.

Fig. 29-23. The color perception of most insects differs somewhat from that of humans. For example, bees clearly distinguish ultraviolet light, which is invisible to us. The photograph shows that a marsh marigold flower (Caltha palustris), which appears bright yellow to us (A), reflects ultraviolet rays only in the region that appears light-colored in Fig. B. It also reflects yellow rays which, combined with the ultraviolet, produce what is known as "bee's purple." The dark regions of the flower absorb ultraviolet light and therefore appear yellow to the bee (see also p. 217).

Typical of "bee flowers" are nectaries located at the Base of the corolla tube; these are often positioned so deeply that they are accessible only to the specialized mouthparts of bees and remain unreachable, for instance, by the chewing mouthparts of beetles. Such flowers typically possess some form of landing platform (see Fig. 29-22).

Among the most common flower visitors in the northern temperate zone are bumblebees (Fig. 29-24). These are also social hymenopterans. Their queens overwinter and lay eggs in the spring to establish a new colony. Bumblebees are unable to fly until the temperature of their flight Muscles reaches 32°C; to maintain this temperature, they must continuously forage on nectar-rich flowers. In the cool regions of North America and Eurasia, many plants—including lupines, larkspurs, and fireweed—are regularly pollinated by bumblebees throughout their range.

Fig. 29-24. Bumblebees (Bombus). These social hymenopterans are vital pollinators for many plant genera in the cool regions of the Northern Hemisphere and have been introduced beyond their native range to pollinate forage crops such as white clover (Trifolium repens). A. A bumblebee gathering pollen on the California poppy (Eschscholzia californica). B. Part of an underground bumblebee nest showing the cells in which the worm-like larvae complete their development. Bumblebees provision these cells with pollen and regurgitated nectar. While an entire bumblebee colony may service flowers of A wide variety of species over the course of the season, individual insects frequently visit only specific plants encountered along a single, established route leading from the nest.

Some of the most evolutionarily advanced flowers, particularly among orchids, have developed intricate pathways and traps that force bees to crawl inside and exit along a specific route. As a result, the anther and stigma brush against the insect's body at precise points and in a strict sequence (see Fig. 29-20).

An even more remarkable pollination strategy has evolved in orchids of the genus *Ophrys*. Their flowers bear a striking resemblance to female bees, wasps, or flies (Fig. 29-25). Males of these insects emerge in early spring, well ahead of the females. As the *Ophrys* bloom concurrently, the male insects attempt to mate with the flowers. In the process, pollinia adhere to the insect's body and are transferred to the stigma of the next flower visited, thereby effecting pollination.

Fig. 29-25. A bee-mimicking orchid flower (*Ophrys speculum*) from Sardinia attracts male bees so thoroughly deceived by its resemblance to a female of their species that they attempt to copulate with the bloom. During these attempts, pollinia frequently attach to the insects and are subsequently carried to other *Ophrys* plants.

A wide variety of structurally diverse flowers are pollinated by various dipterans, including mosquitoes. These insects feed on nectar but do not gather pollen or provision food for their larvae. Examples of flowers pollinated by mosquitoes and flies are shown in Fig. 29-19, B, C.

Butterfly-Pollinated Flowers

Flowers coevolved with butterflies share many similarities with bee-pollinated flowers, primarily in using visual patterns and scents to attract insects. However, some lepidopterans can perceive the color red, and the flowers they pollinate are often red or orange.

In species typically pollinated by moths, the flowers are white or pale, highly fragrant, as seen in certain tobacco species (*Nicotiana*), with their intense sweet scent often intensifying only after sunset. Such plants also include evening primrose species (*Oenothera*) with yellow flowers (see Fig. 9-13, B) and the bright pink belladonna amaryllis (*Amaryllis belladonna*).

In butterfly-pollinated flowers, nectaries are frequently located at the base of a long, narrow corolla tube or spur, from which nectar can generally be reached only by these insects with their elongated sucking mouthparts. Hawk moths, for instance, typically do not crawl into the flower like bees; instead, they hover above it, inserting their long proboscis into the floral tube. Consequently, these flowers lack the "landing platforms," traps, and complex internal architecture sometimes seen in bee-pollinated plants. Among less specialized butterfly pollinators, smaller species that do not require as much energy as hawk moths are common; the flowers they visit tend to be smaller with relatively short tubes, allowing the insects simply to crawl over them. One of the clearest examples of a close mutualistic relationship between a plant and a lepidopteran is illustrated in Fig. 29-28.

Bird-Pollinated Flowers

Certain birds regularly visit flowers to feed on plant Tissues, nectar, and resident insects; many of these birds act as pollinators. In the Americas, these are predominantly hummingbirds, whereas in other parts of the world, representatives of other specialized families fill this role.

Bird-pollinated flowers secrete copious liquid nectar (in some species, it even overflows by the time the pollen matures), yet they typically lack a strong scent, reflecting the poor sense of smell in birds. Conversely, birds have excellent Color Vision (spanning roughly the same spectral range as humans), so it is hardly surprising that the coloration of most bird-pollinated flowers is conspicuous, typically yellow and red (see Fig. 29-14, B). Examples include red columbine (Fig. 29-31, A), fuchsia, passionflower, eucalyptus, hibiscus, poinsettia (Fig. 28-31, B, C), and numerous cacti, bromeliads, and orchids. Such flowers are generally large or aggregated into robust inflorescences to attract avian visitors visually and to accommodate large volumes of nectar.

Fig. 29-31. Examples of bird-pollinated flowers. A. Columbine (*Aquilegia canadensis*). Elements of the perianth alternate with conventional petals, modified into nectar-filled tubes. Hummingbirds visiting these pendulous flowers sip nectar while hovering; it remains inaccessible to most other animals. B, C — Poinsettia (*Euphorbia pulcherrima*). Native to Mexico, this well-known plant bears small, greenish, clustered flowers, each featuring a large yellow nectary that secretes abundant nectar. Modified upper leaves, with their brilliant red coloration, attract hummingbirds to the clustered flowers.

Birds and other animal pollinators typically visit flowers of a specific plant species for short periods, but this is only one factor promoting outcrossing (cross-pollination between individuals of the same species). It is also necessary that the pollinator does not restrict its visits to a single flower or to flowers of the same individual plant. If large, high-energy-demand birds, hawk moths, or bats feed regularly on these plants, nectar must be produced in quantities sufficient to sustain the metabolic requirements of these animals and thereby ensure repeat visits. However, if abundant nectar were readily available to lower-energy animals, such as small bees or beetles, they would likely linger at a single flower and, once satiated, fail to fly to other plants to effect outcrossing. Consequently, flowers regularly pollinated by large species, particularly hummingbirds, tend to produce nectar deep within corolla tubes or in otherwise sequestered locations inaccessible to smaller animals. Similarly, red coloration attracts birds while remaining largely invisible to most insects. Birds, in turn, share with humans a poor sense of smell. Thus, unscented red flowers are inconspicuous to insects and generally fail to attract them—an advantageous adaptation for plants that produce large quantities of nectar.

Bat-Pollinated Flowers

Flower-visiting bats are well-documented in the tropical regions of the Old and New Worlds. More than 250 species of these animals (roughly a quarter of their total species diversity) incorporate nectar, fruit, or pollen into their diet, at least to some extent. Chiropterans that feed exclusively or primarily on flowers possess narrow, elongated snouts and long, highly protrusible tongues, the tips of which sometimes resemble a brush, while their front teeth are frequently reduced or entirely lost.

Bat- and bird-pollinated flowers share many similarities: they are large, sturdy, and produce abundant nectar (Fig. 29-32). Because bats are strictly nocturnal, "their" flowers are typically drab in color and often open only after sunset. Many are tubular or possess other structural adaptations to protect the nectar. In numerous plants that rely on bats for pollination or seed dispersal, the flowers and fruits either hang on long pedicels below the foliage, making flight access easier for the bats, or grow directly on the trunks (cauliflory). Bats locate flowers primarily by scent, rendering a very strong musky or fermented fruit odor characteristic of these blossoms. As these animals fly from tree to tree, they lap up nectar, consume floral parts and pollen, and simultaneously transfer pollen on their fur from one plant to another. They pollinate and/or disperse seeds for at least 130 genera of angiosperms.

Fig. 29-32. Thrusting its snout into the tubular corolla of a cactus flower (*Lemaireocereus*), this bat of the genus *Leptonycteris* laps up nectar with its long, papillae-covered tongue. Pollen grains dusted onto the bat's Head and Neck are subsequently transferred to the next flower it visits. Bat-pollinated flowers are dull in color, emit a musty odor (resembling the scent used by these animals for mutual attraction), and open at night.

It has recently been discovered that certain bats derive a significant portion of their dietary protein from ingested pollen. The pollen of plants pollinated by these bats was found to contain markedly higher protein levels than that of insect-pollinated plants, providing yet another striking example of coevolution.

Wind-Pollinated Plants

At the turn of the last century, many botanists believed that the flowers of wind-pollinated plants were the most primitive, and that all other types evolved from them. In conifers, which at the time were considered by some scientists to be the direct ancestors of angiosperms, the small, inconspicuous, odorless unisexual cones are wind-pollinated. Many wind-pollinated flowers are similarly drab, relatively odorless, and nectarless. Their petals are small or entirely absent, and such flowers are frequently unisexual. However, The Study of other traits in wind-pollinated angiosperms (particularly their specialized wood) has convinced most botanists that they did not descend from conifers, but rather evolved from insect-pollinated flowering plants.

Fig. 29-33. Unlike most angiosperms, grasses are wind-pollinated. In corn (*Zea mays*), the male inflorescences (tassels) are borne at the top of the stalk (A), whereas the female inflorescences (B), with their long protruding stigmas, are located lower down. C. Grasses are characterized by large, feathery stigmas that efficiently capture windborne pollen shed by dangling anthers, as shown here for the wheatgrass genus (*Agropyron*). D. Scanning electron micrograph of a corn pollen grain, revealing its smooth wall—typical of most wind-pollinated plants—and a single aperture, characteristic of monocots.

According to current understanding, their evolution proceeded independently from several ancestral groups. Wind-pollinated species are best represented in temperate regions and are relatively rare in the tropics. In the former case, trees of the same species often grow in dense stands and bloom in early spring while still leafless, which facilitates the windborne dispersal of pollen. In the tropics, a comparable area Supports a much greater diversity of species, and individual specimens of the same kind may be widely separated from one another. Furthermore, in many tropical communities trees are evergreen, making wind pollination far less effective than in deciduous temperate forests. Under these conditions, pollination by insects capable of locating plants of the same species is much more efficient,

which in some cases are separated by distances of 20 km or more.

Because wind-pollinated plants do not rely on insects to transport pollen, they do not expend energy on producing nutritional rewards for them. However, anemophily is highly inefficient and is only adaptive where a large number of conspecific individuals grow sufficiently close to one another. Nearly all pollen caught by the wind falls to the ground within a radius of a few hundred meters from the parent plant; consequently, if individual specimens of a given species are isolated, the chances of a pollen grain reaching a receptive stigma are extremely slim. Many wind-pollinated plants are dioecious (i.e., having male and female flowers on separate plants), such as willows; monoecious (male and female flowers on the same plant), notably oaks (see Fig. 18-45); or genetically self-incompatible (many grasses).

Fig. 29-34. Grass flowers typically develop in groups. A. When such a group completes its development, a pair of dry, rigid bracts (glumes) slightly parts, exposing an elongated spikelet consisting of one to many flowers (depending on the grass species) attached to a central axis. B. Each flower is surrounded by two of its own bracts—the lemma and palea. These diverge to reveal the internal floral Organs (C), driven by the turgidity of lodicules (small, rounded bodies at the base of the pistil), and open widely by anthesis. The stamens (usually three) feature slender filaments and elongated anthers; the stigmas are typically elongated and feathery, an adaptation for efficiently capturing wind-borne pollen

Thus, despite the random nature of pollen dispersal, these plants possess mechanisms that promote a high degree of outcrossing.

In wind-pollinated flowers, the stamens are usually prominently exserted so that the released pollen is readily caught by air currents. In some plants, the anthers dangle on long filaments and sway freely in the breeze (Figs. 29-33 and 29-34). The numerous pollen grains are typically smooth and small, avoiding the clumping characteristic of insect-pollinated species. Large stigmas are generally exposed outside the flower and are often branched or feathery to trap wind-borne pollen. In most wind-pollinated plants, the ovary contains a single ovule (and consequently produces a one-seeded fruit), meaning that the deposition of just a single pollen grain on the stigma is sufficient for Fertilization. For instance, each oak flower produces a single acorn, and each grass flower a single grain; however, wind-pollinated plants with very small flowers compensate for this through pluriflory and/or numerous inflorescences (Figs. 29-33, 29-34, and 29-35).

Fig. 29-35. Common tree species in temperate regions are predominantly wind-pollinated. The staminate flowers of the paper birch (Betula papyrifera) are borne in drooping catkins—flexible, slender inflorescences several centimeters long. Wind sways them, dispersing the shed mature pollen

Floral Coloration

The remarkable diversity of floral colors is produced by a very small set of pigments. Red, yellow, and orange hues are attributed to carotenoids, which are similar to those found in leaves. However, the principal floral pigments are Flavonoids—compounds in which two aromatic rings are linked by a three-carbon bridge. Flavonoids are present in presumably all angiosperms, though they occur only rarely in other vascular plant groups, as well as in Algae and animals. In leaves, they filter out ultraviolet radiation, which is destructive to Nucleic Acids and Proteins, and generally absorb blue-green and red light, which are vital for Photosynthesis.

One of the largest classes of flavonoids, the anthocyanins (Fig. 29-36), plays a leading role in determining floral color. They comprise the majority of red and blue plant pigments. Water-soluble, they reside within Cell vacuoles. Carotenoids, by contrast, are lipid-soluble and located in Plastids. The hue of an anthocyanin pigment depends on the pH of The Cell sap within the vacuoles; for example, cyanidin is red in acidic media, purple in neutral, and blue in alkaline. In some plants, flower color changes after pollination, typically mediated by anthocyanins that render the flowers less conspicuous to insects. Ken Paige and Thomas Whitham of Northern Arizona University near Flagstaff recently reported that individual plants and populations of the perennial herb Ipomopsis aggregata produce darkly colored flowers early in the blooming season, when their primary pollinators are hummingbirds, and lighter-colored flowers somewhat later, when hawk-moths become the principal pollinators (Fig. 29-37). This shift is likely regulated by intracellular pH under plant control.

Fig. 29-36. Three anthocyanins serve as primary pigments determining the flower color of many angiosperms: pelargonidin (red), cyanidin (purple), and delphinidin (blue). Related compounds, flavonols, are yellow or cream-colored, while carotenoids are red, orange, or yellow. Betacyanins (betalains) are red pigments found within a specific group of dicots. The blending of these diverse pigments across varying cellular pH levels generates the full spectrum of angiosperm floral colors. Color shifts act as "signals" to pollinators, communicating which flowers have opened recently and thus are more likely to contain food rewards

Fig. 29-37. Ipomopsis aggregata of the phlox family (Polemoniaceae) on Fern Mountain near Flagstaff in northern Arizona blooms from mid-July to September. A. In the early and middle stages of flowering, individual plants and populations produce dark red flowers visited by hummingbirds. Throughout August, the regional hummingbird population gradually declines and disappears by early September. B. Late in the season, plants produce paler flowers that are more attractive to hawk-moths, their primary pollinators at that time. Differences in floral coloration are almost certainly attributable to shifts in cellular pH rather than the synthesis of new types of anthocyanins

Flavonols, another group of flavonoids, are also very common in leaves and flowers. Many of these are entirely or nearly colorless, yet they can impart an ivory or whitish hue to flowers.

Across all angiosperms, characteristic floral pigmentation depends on a mixture of flavonoids and carotenoids in varying proportions, cellular pH, and the structural—i.e., reflective—Properties of the tissues. Brilliant autumn foliage colors result from The conversion of large quantities of colorless flavonols into anthocyanins as chlorophyll breaks down. The flower of the marsh marigold (Caltha palustris) is entirely yellow. However, the peripheral region of the petals, which reflects ultraviolet light, contains carotenoids, whereas the ultraviolet-absorbing central zone appears yellow to our eyes due to the presence of the flavonoid chalcone. To bees and other insects, the outer zone appears as a mixed yellow-ultraviolet color (the so-called "bee's purple"), while the non-reflecting central zone appears pure yellow (see Fig. 29-23). Most often, though not invariably, the ability of flowers to reflect ultraviolet light is associated with the presence of carotenoids, meaning that UV patterning is more characteristic of yellow flowers.

In members of the Chenopodiaceae, Cactaceae, Portulacaceae, and other families of the order Chenopoidiales (Centrospermae), the reddish pigment is neither of anthocyanin nor even of flavonoid origin. It belongs to a more complex class of Aromatic Compounds known as betacyanins (betalains). These are the pigments responsible for the red flowers of bougainvillea (Bougainvillea) and the tissues of beets. Anthocyanins are entirely absent in the plants of these families, and their biochemical traits point to a close phylogenetic affinity.

Diversity of Fruits

A fruit is a mature ovary, sometimes incorporating other floral parts as well (in the latter case termed an accessory fruit). Although seeds are typically contained within, occasionally they fail to develop, giving rise to parthenocarpic fruits. A well-known example of the latter is the cultivated banana.

Fruits are traditionally classified as simple, aggregate, or multiple, depending on the arrangement of the carpels. Simple fruits develop from a single carpel or several fused carpels, whereas aggregate fruits (such as those of magnolia, raspberry, and strawberry) develop from several separate carpels of a single gynoecium, which in this case produce fruitlets (the aggregate fruit of magnolia is shown in Fig. 29-12, C). A multiple fruit is formed from the gynoecia of multiple flowers. For instance, a pineapple is a multiple fruit derived from numerous, initially separate Ovaries borne on the axis of an inflorescence, which press tightly against one another as they enlarge along with other floral parts.

Simple fruits exhibit the greatest diversity. At maturity, they may be succulent and fleshy, dry and woody, possess parchment-like walls, and so forth. The three MAIN TYPES OF fleshy fruits are the berry, drupe, and pome. The formation of a berry—such as in tomatoes, dates, and grapes—may involve one or several typically multi-seeded carpels, with the inner layer of the pericarp remaining fleshy. Drupes may also comprise one or several carpels, but are usually single-seeded, with the inner layer of the fruit (endocarp) becoming stony and typically tightly fused to the seed. Peaches, plums, olives, and cherries are familiar examples of drupes. Coconuts are also drupes, but possess a fibrous rather than a fleshy outer layer (Fig. 29-38). A pome is a specialized fleshy fruit characteristic of one of the subfamilies of the Rosaceae; it develops from an inferior ovary fused with the base of the perianth, which forms the bulk of the fleshy tissue. The endocarp here forms a tough, cartilaginous core familiar to anyone who has eaten apples or pears, which are classic examples of this fruit type.

Fig. 29-38. The fruit of the coconut palm (Cocos nucifera) is a drupe. Coconut water is liquid endosperm; cellular walls form within it by the time of germination. The intact fruit floats easily on seawater, enabling coconut palms to disperse widely across the globe and reach the most remote islands. For commercial transport, the outer husks are typically stripped from the coconut "nuts," exposing the hard inner "shell" directly enclosing the seed, which is what people in temperate regions usually see

Simple dry fruits are subdivided into dehiscent (Figs. 29-39 and 29-40) and indehiscent (Fig. 29-41). In dehiscent fruits, the wall of the mature ovary—the pericarp—splits open to release the seeds, whereas in indehiscent fruits, the seeds remain inside the fruit even after it detaches from the parent plant. Most fleshy fruits are indehiscent and typically contain a single seed.

Fig. 29-39. Dehiscent fruits. A. Dehisced follicles of milkweed (Asclepias). B. In certain members of the poppy family (Papaveraceae), such as poppies (Papaver), seeds are shed from the capsule through pores near its apex. C. The Brassicaceae family is characterized by a fruit called a silique, in which seeds are attached to a central partition, while the two Valves covering it detach upon maturation

Simple dry fruits are diverse. A follicle is formed by a single carpel and splits open along one suture when mature (examples include columbine and milkweed, Fig. 29-39, A). Follicles are also characteristic of the extinct mid-Cretaceous plant Archaeanthus (see Appendix 1 to this chapter) and magnolias (see Fig. 29-12, B). Fabaceae (legumes) feature a legume fruit, which is similar to a follicle but dehisces along both sutures (Fig. 29-40). In the Brassicaceae family, the fruit is a silique, formed by two fused carpels. Upon maturation, the two halves of the fruit separate, while the seeds remain attached to the persistent central partition (Fig. 29-39, B). The most common type of dehiscent simple dry fruit is the capsule, which develops from a compound superior or inferior ovary. Seeds are dispersed from it in various ways. In Papaveraceae, this often occurs through longitudinal splitting of the capsule, whereas in some members of the family, it happens through pores at the top of the fruit (Fig. 29-39, B).

Fig. 29-40. A legume is a type of dehiscent fruit characteristic of Fabaceae (Leguminosae). Comprising about 18,000 species, this family is one of the largest among flowering plants. Many of its representatives are capable of symbiotic Nitrogen Fixation due to the presence of ROOT nodule Bacteria of the genus Rhizobium on their roots (see p. 145). For this reason, legumes are often pioneer plants on relatively barren soils, such as in the tropics, where they can grow rapidly. The seeds of several members of this family, such as peas, beans, and lentils, are important food crops. A. Pods of the garden pea (Pisum sativum). B. Pods of the silk tree (Albizia polyphylla) native to Madagascar; each seed is located in a separate compartment of the fruit. C. Legume of the West African tree Griffonia simplicifolia. Its two valves have separated, revealing two seeds inside

Indehiscent simple dry fruits occur in many families (Fig. 29-41). The most common are small, single-seeded achenes featuring a cavity where the seed lies loosely, attached only by the funiculus. They are typical of Ranunculaceae and Polygonaceae. Winged achenes, such as those of elms and ashes, are commonly called samaras (Fig. 29-41, A). The fruits of grasses (Poaceae) are caryopses, in which the seed coat is fused tightly to the fruit wall. In Asteraceae, a complex achene-like fruit develops from an inferior ovary¹ (Fig. 29-41, B; see also Fig. 29-43). Acorns and hazelnuts are examples of nuts, which resemble achenes but have a stony fruit wall and develop from a compound ovary. Finally, in Apiaceae, Aceraceae, and several other unrelated families, the fruit is a schizocarp, which splits at maturity into two or more single-seeded segments (Fig. 29-42, A).

¹In Soviet literature, this is also referred to as an achene. — Ed. note.

Fig. 29-41. Indehiscent fruits. A. A samara, characteristic of ashes (Fraxinus) and elms (Ulmus), retains a single seed when mature. These fruits are wind-dispersed. B. Achenes of burdock (Arctium) from the Asteraceae family attach to passing animals and are thus dispersed

Fig. 29-42. Wind-dispersed fruits. A. In maples (Acer), each half of the schizocarp is equipped with a long wing. B. Fruits of dandelion (Taraxacum) and many other Asteraceae possess a modified calyx (pappus) attached to the mature achene, forming a parachute-like tuft that facilitates wind dispersal of the fruits

Fruit and Seed Dispersal

Just as flowers can be classified according to their pollinators, fruits are grouped depending on their dispersal agents.

Wind-Dispersed Fruits and Seeds

In some plants, lightweight fruits or seeds are carried by the wind (Figs. 29-39, A; 29-41, A; 29-42), such as the dust-like seeds of orchids or winged fruits that sometimes form from perianth parts. For instance, in maples with a gynaecium composed of two united carpels, each carpel in the schizocarp forms a long wing (Fig. 29-42, A). Upon maturation, the carpels separate and fall. In many Asteraceae, such as dandelions, a fluffy, parachute-like pappus helps the lightweight fruit stay afloat in the air (Figs. 29-41, B and 29-43). In some plants, the wing or tuft of hairs is borne not by the fruit, but by the seed itself; toadflax (Linaria), in particular, has winged seeds, whereas willowherb (Epilobium) and milkweed (Asclepias, see Fig. 29-39, A) have tufted seeds. In willows and poplars (Salicaceae), the entire seed coat is covered with a felt-like layer. In tumbleweed species (e.g., within the genus Salsola), the entire plant (or a part of it) is blown across the ground by the wind, scattering seeds along the way (Fig. 29-44).

Fig. 29-43. The familiar small indehiscent fruits of the dandelion are achenes dispersed by means of a calyx modified into a tuft (pappus). The photograph shows flower heads of a plant from the genus Agoseris, closely related to dandelions, bearing fruits

Fig. 29-44. In tumbleweed-type plants (pictured here: genus Salsola), the aerial shoot detaches from the root and is driven across open terrain by the wind, releasing seeds in the process. Such species are native to Eurasia but have become widespread as weeds in North America and other parts of the world

Some plants "shoot" their seeds. For instance, in touch-me-nots (Impatiens), seeds are forcefully ejected some distance away by suddenly separating capsule valves. In witch hazel (Hammamelis), as the fruit dries, the endocarp contracts, scattering seeds with such force that they can travel up to 15 m. Another example of this mechanism is shown in Fig. 29-45. In contrast to these active dispersal Methods, the seeds and fruits of many plants simply drop to the ground and are subsequently transported more or less passively, particularly by periodic agents such as floods.

Fig. 29-45. Arceuthobium is a parasitic dicot that is a major cause of reduced forest productivity in the western United States. A. A plant of this genus on a pine branch in California. B. Seed ejection. Extremely high hydrostatic pressure builds up inside the fruit, causing seeds to be shot away from it up to a distance of 15 m with an initial velocity of about 100 km/h. This is one way seeds are transferred from tree to tree, although they are sticky and can be dispersed much farther by adhering to the feet or feathers of birds

Water-Dispersed Fruits and Seeds

The fruits and seeds of many species, particularly those growing in or near aquatic environments, are capable of floating. This is due to the presence of either specialized air chambers or spongy tissues with air-filled intercellular spaces. Some fruits are specifically adapted for dispersal by oceanic currents, such as the coconut palm (see Figs. 29-38); this is why it rapidly colonizes nearly all relatively young atolls in the Pacific Ocean. Rain is also a common agent of fruit and seed dispersal, being especially important for plants growing on slopes of mountains and hills.

Fruits and Seeds Dispersed by Animals

Sweet and often brightly colored fleshy fruits are a clear testament to the coevolution of animals and plants. In most cases, those species in which a significant portion of the pericarp is fleshy (e.g., plums, raspberries, dogwood, grapes) are eaten by vertebrates (typically mammals or birds). As a result, the seeds they contain pass through the digestive tract or are regurgitated by the animal, ending up far from the place where they were swallowed (Figs. 29-46). Sometimes, incomplete Digestion softens the seed coat, thereby promoting seed germination.

As they ripen, fleshy fruits undergo a series of characteristic changes triggered by the hormone Ethylene (see Ch. 24). Their sugar content increases, tissues soften due to The breakdown of pectic substances, and the inconspicuous, leaf-like greenish color is replaced by bright red (Fig. 29-46, A), yellow, blue, or black. The seeds of certain plants, especially in the tropics, bear brightly colored fleshy appendages known as arils. Their succulence and coloration, much like those of fruits, facilitate seed dispersal by vertebrates. The arils of yew (Taxus; see Figs. 18-26) are not homologous to the similarly named structures in angiosperms—meaning they have a different evolutionary origin—yet they perform the same function.

Fig. 29-46. Seeds of fleshy fruits are typically dispersed by frugivorous vertebrates. In the process, seeds are either regurgitated or pass out with feces. A. Wild strawberry (Fragaria) is an example of an aggregate fruit with achenes on The surface of a fleshy receptacle. Unripe, these fruits—like many others dispersed by birds and mammals—are green. They turn red when the seeds mature and become ready for dispersal. B. Berries of many cacti, such as the prickly pear (Opuntia) in southern Mexico, become conspicuous upon ripening. C. Berries of the honeysuckle Lonicera hispidula; in this species, the fruits develop from an inferior ovary and incorporate the fused parts of the outer whorls of the flower shown in Fig. 29-13, B

Often, the green or camouflage coloration of unripe fruits provides some degree of protection against premature consumption by animals. At the same time, they may be unpalatable, such as very sour unripe cherries (Prunus), which also deters animals. By changing color upon fruit ripening, the plant "signals" their edibility—that is, that the seeds are mature and ready for dispersal (Fig. 29-46). It is no coincidence that red predominates at this time. Thanks to this color, the fruits remain inconspicuous to insects, seemingly blending into the green background of the leaves. These animals are too small to effectively disperse the large seeds of fleshy fruits, and it is not advantageous for the plant to attract them. At the same time, red fruits are highly visible to vertebrates, which consume them and thereby transport mature seeds over long distances.

The fruits or seeds of many angiosperms are dispersed by attaching to the fur or feathers of animals (Figs. 29-47; 29-41,5), being equipped for this purpose with hooks, barbs, spines, bristles, or sticky coatings.

Fig. 29-47. Fruits of the African plant Harpagophytum, a member of the sesame family (Pedaliaceae), are equipped with clinging hooks that attach to the fur on the legs of large mammals, allowing them to be carried from place to place

Biochemical Coevolution

Another important factor in angiosperm evolution is associated with so-called plant secondary metabolites, which were previously considered Metabolic waste products. These include a multitude of compounds from various classes—Alkaloids, Quinones, Essential Oils (including terpenoids), Glycosides (including cyanogenic compounds and saponins), flavonoids, and even raphides, i.e., needle-like crystals of calcium oxalate. Some of these are characteristic of entire families or groups of flowering plant families (Fig. 29-48).

Fig. 29-48. Plant secondary metabolites: sinigrin from black mustard (Brassica nigra); calactin, a cardiac glycoside from the milkweed Asclepias curassavica; nicotine from tobacco Nicotiana tabacum, a representative of The Nightshade family; caffeine from the coffee tree (Coffea arabica) of The Madder family; theobromine, the main alkaloid of coffee, tea (Thea sinensis), and cacao (Theobroma cacao). Nicotine, caffeine, and theobromine are alkaloids, representing a diverse class of nitrogen-containing cyclic compounds that are physiologically active in vertebrates

In nature, these substances presumably play a major role in limiting the edibility of the plants that contain them, causing many animals to avoid them (Fig. 29-49). If plants of a certain family contain specific secondary metabolites, only insects from particular families can feed on them. For example, Brassicaceae are characterized by the presence of mustard oil glycosides and Enzymes that break them down, releasing pungent compounds characteristic of cabbage, horseradish, and mustard. Most phytophagous insects avoid plants of this family despite their nutritional needs. However, certain bugs, beetles, and lepidopteran larvae feed exclusively on the leaves of Brassicaceae; for instance, the caterpillars of many butterfly species from the subfamily Pierinae (which includes the large white, small white, and others). The very same chemical substances that repel the vast majority of phytophagous insects stimulate the feeding activity of species with narrow dietary specialization. For example, if larvae of certain Lepidoptera that feed on cabbage are placed on Agar or filter paper moistened with cabbage juice, they extend their mouthparts and perform characteristic feeding movements.

Fig. 29-49. Toxicodendron radicans produces the secondary metabolite 3-pentadecadienylcatechol, which causes an itchy Skin rash in many people. The ability to synthesize this compound likely evolved under selection pressure exerted by herbivores. Fortunately, this plant is easily recognized by its characteristic compound leaves with three leaflets

Clearly, the ability to produce these chemical substances and accumulate them in tissues is an important evolutionary acquisition for the respective plants, providing them with biochemical defense against most herbivores. This is certainly the function of mustard oil glycosides in Brassicaceae. As for herbivores, for any group of insects resistant to these poisons or capable of breaking them down, plants protected in this manner represent an abundant food source due to the lack of competition from other insects. Thus, the rapid evolutionary diversification of the subfamily Pierinae probably began only after ancestral forms acquired the ability to feed on Brassicaceae by detoxifying their toxins.

Phytophagous insects whose diet is restricted to a narrow range of plants with specific secondary metabolites often feature bright coloration, thereby warning predators of the presence of toxic compounds in their bodies. For instance, insects that feed on milkweed during the day include bright green leaf beetles, bright red longhorn beetles and bugs, and black danaid butterflies. Members of the milkweed family (Asclepiadaceae), to which this plant belongs, are rich in alkaloids and cardiac glycosides—poisons that strongly affect vertebrates, the potential enemies of these insects. A bird that swallows a danaid will experience severe gastrointestinal distress accompanied by vomiting, and the predator will subsequently learn to avoid the orange-and-black pattern characteristic of this butterfly's wings. Other insects, such as the viceroy butterfly (Basilarchia archippus), have evolved a similar wing coloration, thereby escaping enemies by mimicking the appearance of the toxic danaid. This phenomenon, known as mimicry, ultimately depends on chemical defense substances. Various drugs and psychotomimetic preparations, such as the biologically active compounds of hemp (Cannabis sativa) and the opium poppy (Papaver somniferum), are also plant secondary metabolites whose role in nature is to deter herbivores (Fig. 29-50).

Fig. 29-50. Certain plants that produce hallucinogenic and medicinal substances. A. Mescaline from the peyote cactus (Lophophora williamsii) is used in ritual ceremonies by many indigenous groups in northern Mexico and the southwestern United States. B. Tetrahydrocannabinol is the primary biologically active substance in hemp (Cannabis sativa). C. Quinine, a valuable drug for the Treatment and Prevention of malaria, is extracted from tropical trees and shrubs of the genus Cinchona. D. Cocaine, a heavily abused narcotic, is obtained from the coca plant (Erythroxylon coca) cultivated in northwestern South America. The photograph shows a Peruvian woman harvesting the leaves of this plant. Secondary metabolites likely protect it from phytophagous insects, but they are also physiologically active in vertebrates, including humans

More complex defense systems are also known. When the leaves of tomato or potato plants are damaged, for instance by the Colorado potato beetle, the concentration of proteinase inhibitors—which block the insect's digestive enzymes in plant tissues exposed to air—increases rapidly. Other plants produce molecules structurally similar to the Hormones of insects or other herbivores, thereby disrupting the normal GROWTH AND DEVELOPMENT of the animals. Of great human interest is the structurally complex compound diosgenin, obtained primarily from wild yams native to Mexico, and to a lesser extent from Indian and Chinese yam species. Chemically, diosgenin is very close to the well-known chemical compound 16-dehydropregnenolone (16D), the main active ingredient in many oral contraceptives. Wild yam was formerly the primary raw material for its production. Unfortunately,

it grows very slowly, and its natural reserves may soon be depleted. Researchers in the USSR, Ecuador, and other countries have investigated the cultivation potential of certain nightshade species (Solanum) containing solasodine, a substance that is easily converted into 16D. Some of these plants are already cultivated on a commercial scale.

As discussed earlier, during the coevolution of pollination systems, each type of pollination emerged not just once, but typically multiple times. The resulting diversity of pollen-transfer mechanisms vastly expanded the opportunities for angiosperm diversification. However, in the case of biochemical traits, evolutionary stages can be traced very clearly. Entire plant families can be characterized from this perspective, demonstrating their associations with Major Groups of phytophagous insects. It is quite possible that these biochemical interactions played a pivotal role in the initial success of angiosperms.

Conclusion

The oldest fossil remains of angiosperms—currently the dominant group of vascular plants—date back about 125 million years (to the Early Cretaceous). Approximately 80 to 90 million years ago (Late Cretaceous), they came to dominate the globe. Among the plant remains in deposits from this period, many modern angiosperm families and even distinct modern genera can be identified. It is possible that angiosperm pollen from more than 125 million years ago is indistinguishable from the pollen of gymnosperms or the spores of ferns, making it difficult to pinpoint the earlier presence of flowering plants on the planet with absolute certainty; however, the group is undoubtedly somewhat older.

Angiosperms may have originated in the semi-arid highlands and dry inland basins of western Gondwana—the supercontinent that gave rise to South America and Africa. By the time these continents fully separated (about 90 million years ago), their climate had changed significantly, and angiosperms began their rise to global dominance. Among the probable reasons for their success are various adaptations that enhance drought tolerance, as well as the emergence of efficient and highly specialized pollination systems.

A defining feature of angiosperms is the flower, which played a crucial role in their evolution. The carpel—a longitudinally folded, leaf-like structure that protects the ovules (containing megasporangia)—differentiated into a basal expanded portion (the ovary), an elongated style, and a pollen-capturing stigma. Stamens likewise evolved from leaf-like structures or thin, branched systems bearing terminal sporangia. Sepals are specialized leaves that protect the flower in the bud. In some angiosperms, petals are sterilized stamens that assumed the function of attracting insects, whereas in others they evolved from sepals. The spiral arrangement, multiplicity, and Separation of floral parts characteristic of primitive angiosperms were largely replaced in most modern forms by a whorled arrangement of a fixed number of parts and their fusion within a single whorl or even between different whorls.

Examples of specialized families include Asteraceae (composites), in which numerous highly specialized flowers are grouped into a head (capitulum) functioning as a single insect-attracting structure, and Orchidaceae (orchids), which feature bizarrely shaped parts in a bilaterally symmetrical flower boasting the most specialized pollination system.

Insect pollination is one of the most crucial traits of angiosperms; its earliest agents may have been beetles or similar animals. The closure of the carpel margins is likely associated with the protection of ovules from being eaten by pollinators. More specialized insect groups emerged later, coevolving with angiosperms; wasps, flies, butterflies, and moths have all left their mark on the floral morphology of certain groups. However, the most specialized and steadfast flower visitors are bees, which have probably exerted the greatest influence on floral evolution. Each group of flower-visiting animals is associated with a specific suite of traits that appeal to their vision and sense of smell. Some angiosperms became wind-pollinated, dispersing large quantities of small, non-clumping pollen; they feature well-developed, often feathery stigmas that efficiently capture pollen from the air.

In plants regularly visited and pollinated by animals requiring energy-rich food (such as hummingbirds), flowers must produce abundant nectar while concealing and protecting its sources from other potential visitors with lower energy needs—those that could satisfy themselves with the nectar of a single flower (or flowers of a single plant) and are highly inefficient in terms of cross-pollination. Wind pollination is less reliable; furthermore, individual plants must grow close together in large groups, whereas insects, birds, and bats can transport pollen even between flowers separated by vast distances.

Fruits are as diverse as the flowers from which they develop. They can be classified based on both their MORPHOLOGY AND ANATOMY, as well as their dispersal mechanisms. Fruits are mature ovaries, sometimes retaining other parts of the flower (accessory fruits). Simple fruits develop from a single carpel or several fused carpels, aggregate fruits from the free carpels of a single flower, and multiple fruits from the carpels of several (sometimes many) flowers. Dehiscent fruits scatter their seeds by splitting open, while indehiscent fruits do so by other means.

Wind-dispersed fruits or seeds are lightweight, often winged or bearing tufts of hairs, which facilitates their dissemination. Some fruits scatter their seeds by bursting open. Many fruits or seeds are water-dispersed; these must be buoyant and possess water-resistant coats. Others are dispersed by animals, primarily vertebrates, and feature a fleshy pericarp whose taste and often conspicuous appearance attract frugivores. Some fruits are dispersed by clinging to the fur of mammals or the feathers of birds.

A third reason for the success of angiosperms and the increase in their diversity is biochemical coevolution. Certain groups of flowering plants developed the ability to produce secondary metabolites (such as alkaloids) that protect them from most herbivores. However, some herbivorous species (typically with a narrow diet) are capable of feeding on these plants and consistently accompany them. Meanwhile, competition from other herbivores is eliminated due to the plants' toxicity. Thus, coevolution may have proceeded in a stepwise fashion, and it is likely that early flowering plants were defended by compounds toxic to animals.

Appendix 1. Ancient Angiosperms and Their Flowers

Archaeanthus linnenbergeri, the only known representative of an extinct angiosperm family, grew during the mid-Cretaceous (90–95 million years ago) in what is now central Kansas. The subtropical coastal plains stretching across the region abounded with dinosaurs. The dense flowers of Archaeanthus featured an elongated axis bearing 100 to 130 spirally arranged follicles, with 10 to 18 seeds in each. The perianth consisted of three outer parts and 6 to 9 inner parts; numerous stamens were arranged in a spiral. This was likely a deciduous tree or shrub whose floral morphology broadly resembled modern representatives of families related to magnoliids (see Fig. 29-11). A — impression of the reproductive axis; B — fossil leaf; C — reconstruction of a twig with a flower; D — reconstruction of a twig with fruits. Reconstructions are based on the work of D. Dilcher of Indiana University; drawings by M. Rohn. Careful research by Dilcher and his students has contributed immensely to our understanding of The Nature of early angiosperms and their flowers.

Appendix 2. Genetic Self-Incompatibility

The recombination of Genes from different individuals during sexual reproduction generates diversity in natural populations, equipping them to adapt to environmental changes through gradual evolutionary transformations. Self-pollinating plants have fewer opportunities in this regard. At the dawn of flowering plant history, many of their families evolved mechanisms that make cross-pollination mandatory, even in plants with bisexual flowers or monoecy.

Among modern species, Two main mechanisms promote this process. Most frequently (for example, in economically important plants such as grasses and legumes), The Fate of a pollen grain is determined by its own (haploid) genotype. If it carries the same Gene in the incompatibility locus as is found in the corresponding locus of the diploid stigma and style, the pathway for the pollen tube is blocked. If the gene at this locus in the pollen grain differs from that in the stigma tissue, it germinates normally.

In a different type of system, found in the Brassicaceae and Asteraceae families, the future of the pollen is determined by the GENES OF THE parent plant that produced it rather than the individual grain—that is, by the match between the diploid tissues of both parents. In both cases, the possibility of fertilization is determined by the combination of genes at the incompatibility locus.

Although much remains to be learned about the physiology of these mechanisms, it is already clear that they depend on recognition reactions between specific Proteins of the pollen grains and the Tissues of the stigma or style. In grasses, this reaction often takes place on the surface of the stigma. A scanning electron micrograph (A) shows a portion of the stigma of orchard grass (Dactylis glomerata). It is covered with numerous papillae, each capable of capturing several pollen grains. In Fig. B, a transmission electron micrograph reveals a cross-section of the wall of such an outgrowth in another grass, rye (Secale cereale). Above the cuticle lie two additional layers: an inner layer of mucilaginous pectic substances and an outer proteinaceous layer. Incompatibility is known to manifest when the pollen tube comes into contact with the outer layer or shortly thereafter. Two other micrographs (C, D) taken with a fluorescence Microscope show the stigmas of meadow foxtail (Alopecurus pratensis) stained with a fluorescent dye to detect callose, a Cell wall polysaccharide. Fig. C shows compatible pollination (the tube can be seen growing toward the ovary after penetrating the stigma), whereas Fig. D shows incompatible pollination: after the tip of the tube made contact with the protein layer, its growth stopped, and its interior became filled with callose, signifying the "rejection" of the pollen grain.