Relationships Among Flowers, Fruits, and Seeds

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RELATIONSHIPS AMONG FLOWERS, FRUITS, AND SEEDS Richard B. Primack Department of Biology, Boston University, Boston, Massachusetts 02215

INTRODUCTION The development of diverse reproductive structures has been one of the major factors in the evolution of the angiosperms (11, 78, 90). This diversity of reproductive structures, especially in flowers, is the primary means of identifying and classifying flowering plants. Systematists, ecologists, and evolutionary biologists have traditionally treated reproduction in flowering plants as constituted by three distinct phases, each associated with a large literature: flowers and pollination (21, 47, 68), fruits and seed dispersal (20, 43, 60, 88, 91 ) , seed and seedling establishment (39, 42). Specialized studies that consider only one phase of reproduction are typical in the botanical literature. As an example of the viewpoint that justifies specialized studies, Cronquist (16, p. 79) says 'The 'morphological integra­ tion' which often permits students of vertebrates to reconstruct an entire animal from a few bones simply does not exist among the angiosperms. Another facet of this same situation is that higher plants, being non-motile and lacking a nervous system, do not have their structure so precisely prescribed by their environmental requirements as do the animals." This viewpoint that characters of flowering plants are not closely integrated in the whole plant is echoed in the writings of virtually all other systematic botanists and is found in current introductory biology textbooks. At the same time, field researchers in reproductive ecology are beginning to extend the scope of their studies into a broader context, blurring the edges of the three phases of reproduction. For example, in a study of the lily, Clintonia borealis, floral ecology is shown to have significant effects on both fruit set and seed size (25). Alpine biennial and perennial gentians differ in aspects of their pollination ecology and 409

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flowering phenology, which in turn are related to seed production and viabil­ ity (76). The purpose of this paper is to present arguments supporting the idea that there are close relationships among flowers and pollination, fruits and seed dispersal, and seed and seedling establishment. These arguments are sup­ ported with diverse evidence drawn from the literature. Finally, six selected published monographs of plant genera are examined to provide specific examples. RELATIONSHIP BETWEEN FLOWERS AND FRUITS A morphological continuity exists among flowers, fruits, and seeds. After all, it is the ovary of the flower that develops into the fruit, which in turn contains the seeds. At the extreme are naked pistillate flowers, such as the oak (Quercus) and many species of Moraceae, such as Antiaris, in which most of the biomass of the pistillate flower is in fact ovary tissue. Flower parts, in particular the sepals of many species in the Rhizophoraceae and Dipterocarpa­ ceae, remain attached to the developing fruit and may function in increasing the photosynthate available to the fruit (8). In addition, the sepals often fold over the enlarging ovary and function as an additional layer of protection for the immature seeds. In many species with inferior ovaries, the outer layer of fruits develops from floral tissue derived from the sepals, petals, and fila­ ments (11). In general, the individual flower parts form an integrated structure that must be effective in pollen donation and receipt. In any comparison across either a phylogenetic grouping or a community, species with large flowers possessing large petals also tend to have large sepals, filaments, anthers, ovary, stigma, and style. Positive correlations among stigma depth, style length, and pollen grain size have also been noted (17, 92). One simple explanation for many of these correlations is pleiotropic effects (31), possibly for genes controlling increases in cell size and cell number in floral parts. The resources (i.e. carbohydrates, proteins, minerals, etc) contained within the ovary are incorporated into the developing fruit after fertilization. It is reason­ able that species with large flowers and associated ovaries will tend to have large fruits, because it is unlikely that the fertilized ovary will get smaller during fruit development. If resources from other flower parts, in particular the sepals, are translocated jnto the developing fruit following fertilization, again it is reasonable that species with large flowers will tend to have large fruits. This can be stated in the following way: Prediction 1 Species with large flowers will almost always have large fruits. Species with small flowers may have either small or large fruits (Figure 1).

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Figure I

Relationships among reproductive and vegetative characters during selection for larger

sizes of structures (above) and smaller sizes of structures (below). A thick line predicts a strong relationship between pairs of characters, while a thin line represents a weaker predicted relation­ ship.

RELATIONSHIP AMONG FRUITS AND SEEDS A major component of many fruits is the seeds contained inside. While in certain species, such as blueberries (Vaccinium). the seeds only constitute a small percent of the final fruit volume, in many other species of nuts, drupes, and achenes, such as chestnut (Castanea) and sunflower (Helianthus), the seed forms the majority of the final fruit volume and weight. Consequently, fruit size will immediately be affected by any selective forces acting on seed size. While it may be rather obvious to say, for a particular species fruit size

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can never be less than seed size. Species with small seeds can have either small fruits with one or a few seeds or fruits ranging up to larger sizes with numerous seeds. Species with large seeds, such as mango (Mangifera), avocado (Persea), and rambutan (Nephelium) have large fruits with resulting specialized modes of dispersal. This is illustrated by a survey of tropical bird-dispersed fruits, demonstrating that birds with specialized feeding habits tend to feed on large fruits containing large seeds while birds with a greater

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dietary range tend to feed on smaller fruits containing smaller seeds (55, 75). This can be stated as follows:

Prediction 2 Species with large fruits will either contain one large seed or larger numbers of smaller seeds per fruit. Species with small fruits will always have one or a few small seeds per fruit (Figure

I).

RELATIONSHIP BETWEEN SEED SIZE AND SEED NUMBER An individual plant would achieve its maximum fitness by producing an infinitely large number of big seeds. The availability of photosynthate, miner­ als, protein, and water limits the resources that can be devoted to reproduc­ tion. The total amount of resources available for reproduction is used in the production of a certain number of seeds. Increases in seed size may come at the expense of producing fewer seeds per fruit and fewer fruits per plant (61,

65, 72). Prediction 3 An evolutionary trade-off exists between seed size and seed number (Figure 1). Seed size and subsequent seedling size are important determinants of success in seedling establishment (39, 53). As a general rule, larger seeds will have larger cotyledons and nutritional reserves (23, 44). Comparisons of habitats have shown that plant species of stable, shady, and moist habitats generally have larger seeds than plant species of sunny, disturbed, and dry habitats (3, 72). Also, species groupings based on growth form, i.e. herb, shrub, and tree, show increased average seed weight with plant size in tropical floras (24, 70). Analysis of covariance using 203 woody species from a Peruvian forest show that species that establish in canopy gaps tend to have smaller seeds than species that establish in the shade, though tree height, dispersal syndrome, and growth form also influence seed size (24). The importance of seed size in determining establishment success is suggested by its lower phenotypic and genetic variability in comparison to many other plant characters less closely associated with fitness (39, 64).

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Prediction 4 Species with small seeds tend to occupy habitats that are more sunny, dry, and disturbed than are those of species with large seeds (Figure I).

RELATIONSHIP BETWEEN FLOWERS AND MODE OF POLLINA TlON

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Each species of plant possesses a syndrome of characteristics that are adapted to a particular mode of pollination, such as by birds, moths, bees, flies, bats, butterflies, or wind. These syndromes have been extensively described (21), and they explain variation both across communities and within individual plant families such as the Polemoniaceae (35) and Rhizophoraceae (85). Descriptions of syndromes emphasize flower color, odor, shape, and timing of anthesis. Clear differences in flower size also exist among these pollination syndromes. In general, the flowers visited by large, energy-demanding ver­ tebrates, such as bats and birds, tend to be large and produce copious amounts of food reward in the form of either nectar or pollen. Flowers visited by small insects such as flies and small bees tend to be small in size and produce only small amounts of food reward. Wind-pollinated species typically have very small flowers in which elements of the perianth have been reduced or even lost during evolution. These are general tendencies, though exceptions do occur. Species that have small flowers grouped into dense inflorescences that mimic large flowers, such as many members of the Compositae, are obvious exceptions to the generalization. Even within categories of pollinators, varia­ tion in pollinator size is correlated with flower size. For example, bumblebee species with longer tongues tend to visit larger flowers than do species with shorter tongues (38). Large species of Australian honeyeaters tend to forage more often than do smaller honeyeater species on plant species with large flowers containing abundant nectar (58).

Prediction 5 Species with large flowers tend to be visited by larger pollina­ tors than those that visit species with small flowers (Figure 1).

RELA TlONSHIPS BETWEEN FRUITS AND DISPERSAL SYNDROME Fruit size, shape, and color are related to the type of dispersal syndrome (26 45). At the extremes, fruits that are wind-dispersed tend to be small and light-weight (2), while fruits eaten and dispersed by vertebrate animals tend to ,

be much larger. Within the category of animal dispersal, fruit characteristics of color, nutrient content, odor, size, and general morphology have been related to the specific type of vertebrate disperser (60, 75). Detailed animal!

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fruit surveys from rainforest communities show that fruit characteristics tend to match the size, visual abilities, and gape width of the vertebrates (45, 87). In general, large, husked fruits are often dispersed by mammals, mainly monkeys and bats, while birds tend to disperse smaller fruits that are not protected by a husk. Only large vertebrates are strong enough to pull apart the spiny valves of large, husked fruit, such as durians (Durio) and to tear apart the rind in huge leathery fruits such as jack-fruit and chempedak (Artocarpus)

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(12, 63). Prediction 6 Vertebrate-dispersed fruit types tend to be larger than wind­ dispersed fruits. Species with large, fleshy fruits tend to be dispersed by vertebrate dispersers larger than those that disperse species with smaller, fleshy fruits (Figure I).

TIMING OF FLOWERING, FRUITING, AND SEED GERMINATION The selective forces that affect flowering phenology have been debated extensively in the literature (6, 62, 67). Particularly controversial has been the idea that the flowering phenology of individual species is linked to the abundance of pollinators and competition for those pollinators with other plant species (69). Several examples in which the succcssive flowering of species appears to be controlled by competition for pollinators have been shown to be indistinguishable from random patterns (62, 66, 67). Also, the fruit set of many temperate woodland herbs is not limited by pollinator visitation rates (54), suggesting that pollinator activity is not the factor determining flowering phenology at the present time. The timing of fruit maturation often appears to be closely linked to syn­ dromes of dispersal. For example, the maturation of fleshy fruited plants in the temperate zone appears to be closely linked to the seasonal abundance and nutritional requirements of bird dispersers (83). In southern Spain, species with watery fruits commonly mature in the hot summer when birds require more water, while species with high-lipid fruits typically mature in the winter when the caloric requirements of the birds may be high and the relative availability of food is low (41). These correlations readily suggest that species with bird-dispersed fruits have come under selection to match their time of ripening to the activities of the birds. Physiological factors, such as water availability, have often been cited as influencing the fruiting patterns of tropical plants, particularly in seasonally dry habitats (6, 62). Such explanations for flowering and fruiting times may be incomplete as a result of a tendency to focus on one phase of reproduction in isolation. The major factor determining flowering time in the temperate zone may simply be

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the size of the fruit. In the flora of Britain, large-fruited species flower

(62). (Hamamelis virginiana), which has large

significantly earlier in the growing season than do small-fruited species The fall-flowering witch hazel

fruits, at first appears to be an exception to this generalization. However, this species does not mature its fruits until the following year, and it appears to be derived from spring-flowering ancestors under strong selection to flower even earlier. In the flora of South Florida, large-fruited species take longer to

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mature their fruits than do small-fruited species

(62). Fruit development in

seasonal climates must take place within a growing season defined by such limitations as the periods free from killing frosts and from drought conditions. The differences among families in flowering sequence described by Kochmer

& Handel (49) need to be reanalyzed to determine if differences in fruit size among these families can explain a significant proportion of the pattern. The tendency of wind-pollinated trees to nower in the early spring, usually explained by the lack of leaves on the trees

(89), may also be partially

explained by the tendency of these species to have large fruits that require many months to mature. The small fruit and seed size

of many weeds is

probably related to the fact that their unpredictable life history places a high premium on rapid fruit maturation as well as on high seed numbers. When selective pressure does operate for particular fruiting times, as seems probable for many temperate bird�dispersed fruits, then selection will indirectly act on flowering time since these two characters are linked due to the more-or-less fixed time required for fruit maturation.

Prediction 7 Species with large fruits will require a greater period of time for fruit maturation than will species with smaller fruits. In the temperate zones, large-fruited species will be forced to flower early in the spring in order to have sufficient time for fruit maturation before the onset of cold weather in the fall. Small­ fruited species may flower anytime during the growing season but will tend to flower and fruit at the times when carbohydrate levels in the plant are highest (Figure

1).

In species-rich tropical rain forests, the main factor determining flowering and fruiting times may be the need of individuals within a population to coordinate their reproduction in order to attract pollinators to effect cross­ pollination, attract fruit dispersers, and satiate seed predators

(1, 46, 62).

Physiological mechanisms, such as drought-stress and the onset of the rainy season, are the proximate mechanisms controlling the flowering response but may not be the driving selective force themselves (l).

It would be valuable to

know for a community of species if flower buds and immature fruits can remain in an arrested state of development for many months once reproduc­ tion has begun. It seems reasonable that flower and fruit development should

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proceed without interruption in order to minimize the time of exposure to flower and seed predators. Such an uninterrupted reproductive development would more closely link seed germination with the other phases of reproduc­ tion. Prediction 8 Fruit development will normally be as rapid as possible to minimize exposure to seed predators and to minimize metabolic cost. This prediction could be tested either by comparing related species which differ in their rate of fruit maturation or by manipulating experimentally the rate of fruit maturation.

The factors affecting flowering and fruiting times might also be extended to include the best time for the seed to land on the ground. Factors of weather, leaf litter, and pests in the soil might affect the viability of seeds in the soil and determine the best time for seed dispersal in temperate species. As an example of this complex linkage, the red maple (Acer rubrum) and the sugar maple (A. saccharum) in New England could be cited (73a). The red maple f10wcrs in April; the samaras then develop rapidly and are shed in June. The samaras lack dormancy and germinate immediately, with several months remaining in the growing season. The sugar maple flowers a few weeks later in May when the danger of frost is past. Fruits are matured over a several­ month period and are finally shed in September. The sugar maple seeds have a chilling requirement and do not germinate until the following spring. This example illustrates the relationship among flowering and fruiting times and germination requirement. Variation in seed size, physiology, timing of germination, and morphology among species allows each species to specialize in its germination require­ ments, and such variation hence contributes to the maintenance of species diversity (37, 95). Among species in the British flora, larger seed size is associated with lower rates of germination and lower relative growth rates of the seedlings (36). Families differ in their rates of germination, and this suggests that phylogenetic constraints are important (36). A tendency for immediate germination and a corresponding lack of dormancy is typical of many large-seeded tropical tree species which establish in shady conditions (23, 57). Selection on the optimum time for seed germination might be particularly important in many habitats, such as the seasonally dry forests in the western Ghats of India. Large-seeded, indigenous species that lack any seed dormancy, such as jack-fruit (Artocarpus heterophyllus). may be under selection to disperse their fruits at the time of year most suitable for the germination of these vulnerable seeds. Prediction 9 The time of year that is best for seed germination will influence fruiting and flowering times, particularly in species lacking

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seed dormancy and in tropical habitats with a pronounced dry

season. CONTINUITY AMONG FLOWERS, FRUITS, AND SEEDS

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Anatomical Evidence The vascular connections of the fruit to the stem are generally fully formed in the ovary at the time of anthesis. Vascularization of individual flower parts

can be related to the size of the parts as well as their subsequent development or abscission during fruit development ( II). Following anthesis, fruit de­ velopment consists primarily of cell expansion rather than cell division in most species (19). Obviously, a flower with a well-developed vascular system in the ovary and the pedicel will be able to develop rapidly into a fruit with a

well-developed vascular system. The anatomy of the flower and fruit are used to support various in­ terpretatio ns of the evolution of the angiosperm flower (11, 18, 19). Flower parts may be viewed as modified leaves, some of which became specialized for support (sepals), attraction of pollinators (petals), presentation of pollen (stamens), and protection of the ovules (carpels). The leaflike qualities of these structures, particularly in primitive angiosperms, as well as the vascula­ ture can be used to support this viewpoint. An alternative explanation is that leaves as well as individual flower parts are derived from reduced branches. Whichever explanation is correct, a close anato mical affinity exists between these structures, in terms of vascularization and surface features, which suggests but does not prove that the structures are homologous. The flower, fruit, and seeds also have an anatomical and morphological

continuity in protective mechanisms. Resin canals afld 'latex ducts in the ovary and ovules are laid down at the stage of flower formation, and they simply enlarge during fruit development. Secondary compounds, such as alkaloids, resins, and aromatic oils, which may serve to protect the flowers against herbivores, will remain throughout the fruit maturation phase and often be

incorporated into the mature seed. These protective compounds may be broken down or removed from the fleshy tissue of animal-dispersed fruits during the final days of the ripening process. Floral glands and protective hairs on the ovary wall or a persistent calyx will also remain on the developing and even mature fruit (10). As another example, the inferior ovary has been interpreted as an a da pta tion to protect the ovary from i nju ry during pollination

(33), Wrapping the ovary in additional layers of floral tissue may give the developing fruit added protection and allow correlated evolutionary changes to occur in the morphology of the final fruit. It would be in teresting to determine if the evolution of the inferior ovary is associated with greater

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ovary size at the time of anthesis, more ovules per flower, and more rapid fruit development.

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Genetic Evidence Pleiotropic effects may link variation in reproductive characters (14, 31 , 34, 78). For example, the S gene in Nicotiana tabacum affects the size and shape of the leaves, petals, and capsule (77). Such genes may operate through effects on ce\1 size, possibly associated with changes in the number of chromosomes. If the number of ce\1s per part is constant, then increases in chromosome number and cell size may result in larger flowers, fruits, and seeds (48). Another mode of action is for increases in the number of cells in all flower parts as a result of increased numbers of cell divisions in the flower primordium. A doubling of the cell number in the flower primordium will result in larger perianth and androecium parts as well as a larger ovary, which would develop into a larger fruit with larger seeds. Larger numbers of cells in the ovary might also allow greater numbers of ovules to be formed. Through such pleiotropic effects, selection for either increased or decreased size at one phase in reproduction would have corresponding effect� on the other phases of reproduction. The effects of pleiotropy may be particularly strong among reproductive characters, since, as mentioned earlier, all floral parts are prob­ ably homologous. Similarly, the major constituent of many seeds is the cotyledons, which are modified leaves. Consequently, many of the genes controlling the development of these structures must be the same.

Physiological Evidence The same essential physiological factors affect the three phases of reproduc­ tion. Certain of these factors are external, such as temperature, water, and light. Internal factors, which may be regulated by the external factors, include carbohydrate and nitrogen levels, and plant hormones. The same basic plant hormones play a dominant role in regulating plant reproduction and indicate a physiological continuity in reproduction (50). Auxin, gibberellin, cytokinin, and ethylene have all been implicated in the initiation of flowering and flower development (50). Auxin produced by germinating pollen grains stimulates early fruit development. Auxin, cytokinin, and gibberellin produced by the developing ovules further stimulate fruit development following fertilization. Fruit maturation is induced by the ethylene, with the other hormones probably also playing significant roles. Seed germination is stimulated by the pro­ duction of gibberellin and cytokinin and is inhibited by the production of abscissic acid. Early seedling leaf development and phototropic responses are regulated by auxin and gibberellic acid. At each successive stage in development, these same hormones interact with each other as well as in-

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ternal levels of carbohydrates in complex ways that are often specific to each plant species. The fruit wall may determine many aspects of seed germination behavior (42). The fruit wall may split open at maturity in capsules, pods, and follicles; it may remain as a hard protective layer in nuts, caryopses, and achenes; or it may envelop the seeds in a soft nutritious flesh in berries and pomes. The remnants of fruit structures that remain associated with the seed will de­ termine the immediate physical and chemical environment of the seed. At one extreme, seeds released from a capsule are free of the fruit tissue, while seeds enclosed in nuts and achenes are still completely surrounded by maternal tissue which can have a dominant effect on germination behavior. The rate at which this fruit wall deteriorates and releases the seed will play a dominant role in determining the timing of seed germination. In many weedy and herbaceous species, the green tissues of the sepals and ovary walls that remain around the seed even after dispersal determine the light requirements for germination of the developing seeds (15). Species with a high chlorophyll content in the tissues surrounding the seeds typically cannot germinate in the dark, while species with a low chlorophyll content in these tissues are capable of germination in the dark. The seed coat itself, which is so important in seed germination, has its origins in the integuments of the ovule, which is floral tissue (86). So, the tissues of the flower, fruit, and seed are often de­ velopmentally and physiologically integrated in controlling germination. Resources are necessary for construction of flowers and production of nectar for pollination, construction of fruit tissues to aid in seed dispersal, and provisioning the seed for germination and establishment in a new habitat. Each of these three reproductive phases places demands on the resource budget of the adult plant. The resources may be measured in terms of such constituents as carbohydrates, minerals, proteins, and water (30), though calories are the most universal unit and probably the most appropriate (9). The usual method of measuring reproductive cost by weighing individual parts typically overestimates reproductive costs, since the flower and the develop­ ing fruit are photosynthetic and produce a substantial proportion of their own calories (8). In any case, each phase in plant reproduction does have some cost, which places limits on reproduction. A plant must devote resources to growth and maintenance, so only a limited amount of resources remains available for reproduction. A trade-off between flowering, fruiting, and seedling establishment may occur, leading to the most efficient and maximal overall reproduction. If too much of the resources are used in producing numerous, large flowers, then not enough resources will be available to mature the developing fruit (79). Alternatively, if only a few, small flowers are produced, a plant will not be able to mature many fruits and the resources available for reproduction will go unused. A key factor may be the relative maternal investment in the ovary at the time of anthesis (52, 92).

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Within the fruit itself, there may be a trade-off between the resources devoted to seed formation and resources devoted to dispersal processes (76a). At one extreme are capsules and achenes in which only a small proportion of the fruit is devoted to dispersal, while in other fruits, such as berries and pomes, most of the fruit is devoted to dispersal, with only a small seed volume. Natural selection should act on the relative proportions of resources devoted to flowers, fruit tissues, and seeds, depending on the relative advan­ tages to the plant of high levels of outcrossing, dispersal of the seeds to new sites far from the parent plant, and the production of numerous, large seeds. EMPIRICAL EVIDENCE FROM SIX LARGE GENERA Selection for optimal characteristics within an evolutionary grouping may be constrained by phylogenetic factors, such as shared morphology, anatomy, and life history characteristics that limit the potential for natural selection and speciation (22, 32). Phylogenetic constraints affect such angiosperm charac­ teristics as flowering time (49) and leafing phenology (51). Studies of changes in size and shape using statistical techniques such as allometry have been useful in determining constraints on animal evolution (40, 59) and the process of speciation in plant species (37a). These statistical techniques can be applied to variation in reproductive characters among plant species within genera. Six large genera were examined in detail to determine evolutionary correlations among the sizes of flowers, fruits, and seeds (R. B. Primack, unpublished). Allometric analysis was used to determine how natural selection operated on correlated plant characters in order to determine whether there are any de­ monstrable limitations on evolutionary changes. The raw data for this study were extracted from published monographs (R. B. Primack, unpublished). The genera selected were all relatively large and included a mixture of tropical and temperate genera as well as, woody and herbaceous genera. For each species, data were extracted on the length of flower parts, fruits, and seeds as well as other reproductive and vegetative characters. When a petal length for a species was listed as "3 to 7 mm in length," then 5 mm was recorded. Unusual extreme values were not included in the recorded values. Spearman Rank Correlation was used to examine pairs of variables. Analy­ sis was used to determine if the relationship between pairs of variables was significantly allometric (59). The developmentally earlier stage was always considered the independent variable. For example, petal length would be considered as the independent variable in a relationship with fruit length. Each species is treated as a separate data point in this analysis. Such an assumption may lead to an overestimate of the sample size if the evolutionary changes in the studied characters were fewer than the number of species (40).

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Only a detailed numerical taxonomy study of each genus could possibly reveal such information. For our present purposes, highly significant rela­ tionships between pairs of characters repeated in many genera are accepted as valid evidence.

Genera Examined

Annu. Rev. Ecol. Syst. 1987.18:409-430. Downloaded from www.annualreviews.org Access provided by CONRICYT EBVC and Econ Trial on 09/23/15. For personal use only.

I.

2.

3.

4.

5.

6.

Calophyllum (Guttiferae) is a genus of about 175 tree and shrub species, mainly found in the lowland rain forests of Southeast Asia (80), character­ ized by relatively small white flowers with numerous stamens and an olive-like drupe with a fleshy rind covering a large stone. Agave (Agavaceae) is a genus of 300 species of woody herbs, known as "century plants," distributed throughout arid and often tropical regions of the Americas (27). Plants have a basal rosette of large, stiff, spiny leaves, tall inflorescences of funnelform flowers, and an oblong capsule contain­ ing numerous flattened seeds. Astragalus (Leguminosae) is a cosmopolitan genus of about 2000 annual and perennial species, known as "locoweeds," found usually in open xeric habitats (4). Species have pinnately compound leaves, flowers in spikes or racemes, and a legume pod containing ovoid seeds. Lesquerella (Cruciferae) is a genus of about 80 primarily herbaceous, annual, biennial, and perennial species, known as "cloth of gold," occur­ ring mainly in open, dry habitats in the western United States and Mexico (71). A basal rosette of leaves produces inflorescences of yellow flowers. The globous, two-locular silique contains round seeds. Phacelia (Hydrophyllaceae) is a genus of about 200 species of annual, biennial, and perennial herbs from the Americas known as "scorpion weeds" (56). The stem has simple or pinnate leaves and campanulate flowers in scorpiod cymes, followed by ovoid capsules. Asclepias (Asclepiadaceae) is a large genus of perennial herbs from the Americas and Africa, known as "milkweeds" because of the white latex (94). The complex flowers are produced in umbels, followed by follicles which split at maturity to release the numerous, flattened seeds, each containing a tuft of hair to aid in wind-dispersal. The milkweeds are particularly interesting here because they have been used extensively in studies of sexual selection in plants (93).

Variation Among Species Within a Genus A significant positive correlation exists between petal length and fruit length among species within each of the six genera (Table I), and the correlation is very·highly significant in four of the six genera (R. B. Primack, unpublished). The correlation coefficients range from a high of 0.59 in Agave to a low of 0.28 in Lesquerella. The high values for several of the genera show that

422

PRIMACK PHACElIA

E �

10

.

./

:J:: I" Z

'"

..J

'" ..J � rn 0""

/

5

y = 0.33

,. P. mitior

X'

I. 9 I

Annu. Rev. Ecol. Syst. 1987.18:409-430. Downloaded from www.annualreviews.org Access provided by CONRICYT EBVC and Econ Trial on 09/23/15. For personal use only.

0

0 30

15

0

PET AL LENGTH (mm)

Figure 2 Relationship between petal length and capsule length among species in the genus Phacelia. Each dot represents a species.

evolutionary changes in flower size are closely associated with changes in fruit size.

For example, species of Phacelia with small flowers have smaller with larger flowers (Figure 2). A highly significant positive relationship exists between fruit size and seed size in four of the six genera (Table 1). The very high correlation coefficient in Calophyllum is not surprising considering that the single seed forms a large frui ts than species

proportion of the drupe volume . However, there is also a high correlation coefficient for the genus

Agave, in which there are many seeds per capsule (Figure 3). Seed size and fruit size have a nonsignificant, negative correlation in the genera Asclepias and Phacelia. In the genus Asclepias, the main constituent of the follicle is the hairs attached to the seeds, and hair l ength is

correlated with fruit length (R. B. Primack, unpublished). Regression analysis was undertaken to determine if these relat ionshi ps are si mp le linear relationships or if changes in relative sizes have occurred during speciation (R. B. Primack, unpublished). In all genera except Agave, there is

AGAVE

IZ Y

E

=

.!: :I: le> z w ..J o W W '"

'

6

..... : : .

./ ..:

o

.

'. "

:

x

' I'

.'

.

�� ;/

'

/



. . .. /:::. "

/." .

.

�I

o

.

0.11

:

__----�I

40

----------�I----

BO

CAPSULE LENGTH (mm)

3 Relationship between capsule length and seed length among species of Agave. Each dot represents a spec ies

Figure

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Table 1

Spearman Rank correlations (r) and allometric values

(b) between pairs of characters among species within a genus.··b Leaf Length with:

Genus Calophyllum Agave Astragalus

NC 1 27

64 236

Lesquerella

62

Phacelia

67

Asclepias

81

Petal Length

Fruit Length

with Fruit Length

with Seed Length

r 0. 56**0.59*** 0. 49*** 0.28*

0. 57**" 0. 30**

b 0 . 70*0.97 0.62***

0.45*-*

0. 51 *** 0 . 24*-*

r 0.94*** 0.79*** 0. 50***

0 . 27* - 0 . 14 - 0 . 07

Petal

Fruit

Seed

Height

Length

Length

Length

b

r

r

r

r

0 . 9 1 ** 0.62*** 0. 1 9**-

0 . 29*** 0.66***

0.26***

-0.47**" - 0.06-*-

0 . 5 1 *** 0. 30*-

0.45***

0. 33*** 0. 37*** -0.08 0. 33 **

0 . 3 1 ***

0.40***

0. 33 *** 0.29*** 0.17 0 . 08 0 . 20

0. 39***

0.43*** 0 . 21** -0.03 0.45*** 0 . 25 *

aThe value b is reported from the equation y = ax", where x is the independent variable, y is the dependent variable, and a and b are constants. Each value of

b

was tested for significant differences from I. "One, two, and three stars indicate significance at the 0.05, 0.01, and 0.001 levels, respectively. C

For each genus, the minimum number of species (N) for each correlation is given.

5



tTl �

[n



c:

a > z o [n



en

.j::. IV W

Annu. Rev. Ecol. Syst. 1987.18:409-430. Downloaded from www.annualreviews.org Access provided by CONRICYT EBVC and Econ Trial on 09/23/15. For personal use only.

424

PRIMACK

a significant allometric relationship between petal length and fruit length with a slope varying from 0.24 to 0.70 (Table 1). This result suggests that evolutionary changes in fruit length approach a maximum value as flower size continues to increase over evolutionary time. In the genera Calophyllum, Agave, Astra!?aius, and Lesquerella, the relationships between fruit length and seed length are significantly al10metric with a slope less than 1, suggest­ ing that evolutionary changes in seed length approach a maximum value as fruit size continues to increase over evolutionary time (Table 1). These allometric analyses demonstrate that changes in the relative size of flowers, fruits, and seeds are associated with speciation even though these characters arc closely correlated. Prediction 10 The evolutionary relationships of flowers, fruits, and seeds among species within a genus are allometric, presumably as a result of greater constraints on one character than another.

RELATIONSHIPS OF REPRODUCTIVE AND VEGETATIVE CHARACTERS Plant architecture examines the physiological, morphological, and biome­ chanical factors influencing plant form and function (29, 84). The emphasis of this field has been almost entirely on the vegetative morphology of the plant. Yet, plant reproduction is an important component in the life history of the plant that must also have an effect on plant architecture. At the least, flowers must develop at positions where they can make a suitable display and be located by pollinators. Further, these positions must be appropriate for the type of fruit dispersal found in that species. The net result is that the types of pollination and fruit dispersal must be related as a result of position effects on the plant. The characteristics of the flowers, fruits, and seeds must also be closely coordinated with the vegetative characters of the plant. Studies mentioned previously have shown that tree species tend to produce larger seeds than herb species (3, 70). As Corner (13) has described in one of his imaginative articles: "A big natural genus has massively constructed species with big buds, thick twigs, large leaves and large flowers, fruits, and seeds. It has, also, the slender which are small in all their primary parts." This idea was tested using the 6 genera mentioned previously (R. B. Primack, unpublished). Within each genus, the correlation of plant height with leaf length is very highly significant. Tall species have longer leaves than short species (Table 1). Vegetatively larger species also have bigger flowers and seeds in five of the six genera (Table 1). Only in the genus Lesquerella is this pattern not seen. In the genus Lesquerella, considerable variation in growth habits and

FLOWERS, FRUlTS, AND SEEDS breeding systems occurs

425

(71) which apparently obscures the trends observed

in the other genera. In three of the six genera, leaf length has a significant positive correlation with fruit length. These relationships of vegetative and reproductive characters have a mechanical as well as a natural history basis. Thick twigs are necessary to support

large flowers and heavy fruits without being bent or broken. In

addition, large flowers that are visited by large climbing and perching ver­

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tebrate pollinators need thick twigs to support the weight of the animal. For

example, African species of Erica that are pollinated by perch ing birds have thicker twigs than related species pollinated by insects (74). A striking contrast is also seen among bird-pollinated species of the same genus occur­

ring in the Americas and Australasia-for example, the genus Fuchsia. American species, such as F. simplicicaulis, are pollinated by hovering hummingbirds and have flowers produced outside of the foliage on slender

twigs. In

ntrast, Australasian species, such as F. excorticata, are pollinated

co

by larger, perching honeyeaters and have flowers produced inside the foliage layer on thick twigs. The thickness of the supporting twig can also be related to the size of the fruit. In

particular, large fruits must be produced on thick

twigs in order to support the weight of the fruit. The twig must also be able to support the weight of the disperser, in the case of vertebrate-dispersed fruits.

example, in the genus Artocarpus in Borneo, A. kemando has relatively (4 x 2.5 cm) produced at the ends of slender twigs (2-3 mm thick) and is dispersed by birds. A. odoratissimus has medium-size fruits (10 x 8 cm) produced at the end of thick twigs (4-10 mm thick) and A. integer has large fruits (25 x 12 cm), produced on the trunk and main branches, and is dispersed by large mammals (12, 63). In addition, specie s with large flowers, fruits, and seeds tend to have large

For

small fruits

,

leaves. Several potential reasons for this could be advanced. First, the genes controlling size may affect all of these structures, i.e. pleiotropy. Second, selection for large fruit size might require simultaneous selection on leaf size in order to support the fruit photosynthetically. And third, selection for thicker twigs to support bigger fruits might result in indirect selection on leaf size; thicker twigs are typically not as branched, so that the fewer leaves would have to be larger

in order to maintain the same photosynthetic area.

Consequently, fruit and leaf characters might be linked indirectly via twig thickness.

Prediction 11 Vegetative characters, such as leaf size, twig thickness, and plant height, in addition to being positively correlated among species within a genus, are also evolutionarily linked with reproductive characters through a network of positive correla­ tions (Figure

I).

426

PRIMACK

BREEDING SYSTEMS AND FRUIT SET The intense interest in mating patterns and sexual selection in plants has led to the observation that dioecious species have a tendency toward fleshy dispersal units in the angiosperms

(5) and the gymnosperms (28). In tum, breeding

systems, fruit set, life fonn, and fruit type have been shown using large data sets to be interrelated

(8 1, 82). These studies demonstrate that fruit set is

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higher for species having the characteristics of self-compatibility, dioecy, annual habit, temperate distribution, and "inexpensive" fruits (i.e. capsules, follicles, achenes), in comparison with species that display self-incompatibili­ ty, hermaphroditism, perennial habit, tropical range, and "expensive" fruits (i.e. fleshy fruits, nuts)

(81). In general, "expensive" fruits appear to be larger

and heavier than "inexpensive" fruits. The correlations of breeding system with many plant characteristics suggest that the flower, fruit, and seed relationships presented already might also be correlated with breeding sys­ tems and fruit set. Such correlations are indicated by the well-known tendency of self-compatible species and populations to have smaller flowers than related self-incompatible species and popUlations

(73). These characters are

probably further linked with seed set, the proportions of ovules that develop into seeds

(7). The low fruit set in certain species with small flowers and large (Mangifera), could come about as a consequence of violating Prediction 1, that species with small flowers tend to have small

fruits, such as mangoes fruits.

Prediction 12 Self-fertilizing species with high fruit set will be found to have smaller flowers, fruits, and seeds, in comparison with out­ crossing species with low fruit set (Figure

1). Probably the

most critical determinant of fruit set is the relative dry weight of the ovary in relation to the dry weight of the fruit. Where the ovary-to-fruit ratio approaches

1, the average fruit set will 100% and fruit maturation will be rapid. Where the ovary-to-fruit ratio approaches 0, the average fruit set will approach 0% and fruit maturation will be slow. Absolute

approach

ovary size and fruit size should also be considered as variables in a multivariate test of this prediction.

CONCLUSIONS This study has presented arguments for close ecological and evolutionary relationships among pollination, seed dispersal, and seedling establishment. These arguments are supported by empirical data from six large genera showing patterns of positive correlations among flowers, fruits, and seeds among species. The only exceptions to this pattern are negative correlations

FLOWERS, FRUITS , AND SEEDS

427

between seed size and seed number in some groups. Vegetative characters are also frequently linked to this variation in reproductive characters . The evolu­ tionary implications of these arguments and results are obvious. First , it should be apparent that systematic studies of plant reproductive characteristics should not be too narrowly focused. For example, studies of floral evolution and pollination ecology within a taxonomically variable group, such as the Polemoniaceae

(35) and the Rhizophoraceae (85), should include parallel

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studies of fruit, seed, and vegetative evolution to determine the totality of the evolutionary change. Second, community surveys of plant reproductive ecol­ ogy and phenology should not examine only one aspect of reproduction if the three phases of reproduction are linked. For example, a survey of fruit types and dispersal syndromes at the community level in conjunction with studies of pollination ecology and seed establishment ecology may provide additional insights into the evolution of fruit characters and dispersal syndromes. It is quite possible that selective pressures for fruit size and type of dispersal are largely determined by selection on flower size and seed size. And third, the approach of determining the linear and allometric relationships among flow­ ers , fruits, and seeds allows predictions to be made of limits to natural selection. These predictions can provide a valuable starting point in further field studies and in investigations of plant evolution. Particularly valuable areas of further investigation would be to examine simultaneous evolutionary trends for flowers , fruits, and seeds among genera within large families and to examine parallel evolutionary trends within two or more large , closely related genera. The exceptions to these general trends and predictions might give significant insights into the process of speciation and the formation of higher taxonomic categories. ACKNOWLEDGMENTS

The most sincere appreciation is expressed to Kamal Bawa and David Lloyd, who unselfishly guided me throughout this project. Valuable advice was also given by Joseph Travis (on allometric analysis), Peter Stevens, Mary Willson, Judy Dudley, Elizabeth Shaw, Reed Rollins, Peter Ashton, Pamela Hall, Hyesoon Lee, and Mark Leighton. Paul Alloca, Sherry Booth , and Barbara Dorritie assisted in the data analysis.

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