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Structure and Development |
2Department of Biology, New York University, New York, New York 10003-6688 USA; 3The Lewis B. and Dorothy Cullman Program for Molecular Systematic Studies, The New York Botanical Garden, Bronx, New York 10458-5126 USA
Received for publication May 23, 2003. Accepted for publication January 8, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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Key Words: Araliaceae • floral anatomy • floral ontogeny • Hawaiian Islands • inferior ovary • superior ovary • Tetraplasandra
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). Reversals from epigyny to hypogyny are relatively rare, and in many large groups, the condition is fixed.
One exception is found in the Araliaceae in the Hawaiian endemic genus Tetraplasandra in which positions range from completely inferior (T. hawaiensis A. Gray, T. flynnii Lowry and Wood, T. oahuensis A. Gray, T. waialealae Rock, and T. waimeae Wawra) to partially superior [T. kavaiensis (H. Mann) Sherff] and fully superior [T. gymnocarpa (Hillebr.) Sherff]. Tetraplasandra gymnocarpa is the only member of the Araliaceae with a completely superior ovary (Eyde and Tseng, 1969
). The nested position of Tetraplasandra within the Araliaceae (Plunkett et al., 1996
, 1997
) and T. gymnocarpa within Tetraplasandra (Costello and Motley, 2001
) phylogenetically corroborates Eyde and Tseng's (1969)
hypothesis that hypogyny is secondarily derived in Tetraplasandra. This reversal contradicts a major trend in floral evolution toward epigyny (Coulter et al., 1910
; Stebbins, 1974
; Cronquist, 1981
; Takhtajan, 1991
; Gustafsson and Albert, 1999
).
Although the derivation of epigyny historically has been controversial (Douglas, 1944
, 1957
; Puri, 1951
, 1952
; Kaplan, 1967
), developmental and anatomical series in various plant families (e.g., Rosaceae—Bonne, 1928
; Jackson, 1934
; MacDaniels, 1940
; Palser, 1961
; Ericaceae—Eames, 1931
; Onagraceae—Bonner, 1948
), including the Araliaceae (Eames and MacDaniels, 1947
; Singh, 1954
), have shown that most epigynous flowers are appendicular in nature, implying that the inferior ovary originated through fusion with the bases of the outer floral organs. Nevertheless, in a small number of plant groups, the inferior ovary has been interpreted as receptacular (e.g., Calycanthaceae—Smith, 1928
; Cactaceae—Leinfellner, 1941
; Tiagi, 1955
; Boke, 1964
; Santalaceae—Smith and Smith, 1942
), which implies that the ovary is embedded in the tissues of the floral receptacle.
Anatomical studies of floral vasculature support both types of development (Douglas, 1957
; Kaplan, 1967
). In receptacular epigynous flowers, the vascular bundles providing traces to the floral appendages run upward through the length of the ovary wall and then descend sharply to supply the ovule traces (Fig. 1A). In appendicular epigynous flowers, the vascular strands ascend from the pedicel to supply the ovule traces and diverge in an acropetal sequence to supply the stamens, petals, and sepals, just as they do in a typical hypogynous flower (Fig. 1B).
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considered epigyny to be largely a response to bird pollination. In epigynous flowers, the ovules are protected from foraging birds that eat superior floral parts. Stebbins (1974)
proposed two hypotheses. One is that the inferior ovary provides developing ovules better protection against environmental stresses. Secondly, epigyny might enable quicker floral development and maturation of seeds.
Based on these hypotheses, is there evidence suggesting that the shift to hypogyny in Tetraplasandra was a response to natural selection? Eyde and Tseng (1969)
suggested that the switch to hypogyny was probably not driven by selective pressure, but might simply reflect the relaxation of selection pressures on hypogynous mutants in an isolated island habitat. However, recent phylogenetic analyses of Tetraplasandra derived from morphological, ITS, and 5S-NTS sequence data (Costello and Motley, 2001
; Costello, 2002
) provide evidence that the change to hypogyny may have evolved over time in response to underlying selective forces. Within the T. gymnocarpa clade (see Fig. 2), T. flynnii has an inferior ovary, T. kavaiensis has a partially superior ovary, and T. gymnocarpa has a fully superior ovary. The range of ovary positions found in this clade suggests that hypogyny was a gradual transformation that evolved in a stepwise fashion. All three species have a substantial reduction in floral parts, most notably decreases in stamen number, and T. flynnii also shows a switch to andromonoecy. The shift to hypogyny, combined with a reduction in floral parts and a change in sex expression, provides evidence suggesting that the trend toward hypogyny in Tetraplasandra corresponds with changes in reproductive biology. Members of the sister clade to T. gymnocarpa (e.g., T. waimeae and T. waialealae) have a suite of morphological features that suggest a switch to ornithophily (Lowry, 1990
). A shift from insect to bird pollination has occurred several times in the Hawaiian flora (e.g., Scaevola, Geranium, Hibiscadelphus, Kokia; Carlquist, 1980
).
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criteria of homology (cf. Remane, 1952
) to determine whether the divergent ovary positions in Tetraplasandra are or are not homologous. Our goals are to elucidate the developmental transformations involved in shifting from an inferior to superior ovary, assess homology of ovary position in developing flowers, and reexamine the adaptive significance of hypogyny in Tetraplasandra. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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; Berlyn and Miksche, 1976
). Permanent slides were made using Permount (Fisher Scientific, Fair Lawn, New Jersey, USA) and photographed using a Nikon FX-35 (Nikon, Tokyo, Japan).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). The stamens alternate with the petals (e.g., T. gymnocarpa, T. kavaiensis, T. flynnii), are opposite and alternate with the petals (e.g., T. hawaiensis, T. waimeae, T. waialealae) and are equal to the number of petals (e.g., T. gymnocarpa, T. kavaiensis, T. flynnii), or are 2–8 times the number of petals (e.g., T. hawaiensis, T. waimeae, T. waialealae). The stamens are attached to the edge of a nectary disk that lies on top of the inferior ovary. The styles are fused, forming a stylopodium, which is confluent with the disk (see Fig. 3B). The stylopodium is greatly reduced in the superior ovary species T. gymnocarpa (Fig. 3F). In general, the ovary consists of 2–10 carpels, with an equal number of locules, each with a single pendulous ovule. Ovary positions of mature flowers vary among species of Tetraplasandra (Fig. 3C–F).
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, 1966
; Kaplan, 1967
; Fig. 1 in Kuzoff et al., 2001
). In contrast, in T. gymnocarpa the floral bud becomes increasingly concave (Fig. 5E) as development progresses, comparable to an epigynous flower (see Fig. 1 in Kuzoff et al., 2001
).
This pattern of gynoecial development can be explained based on the "principle of variable proportions" (cf. Troll, 1948
, 1949
; Leins, 1972
; Leins and Erbar, 1985
; Igersheim et al., 1994
). The variability of proportions is interpreted by using a series of three lines (a, b, and c) and by measuring the changes in their length, angle, and distance to one another during ovary development (Igersheim et al., 1994
). Line "a" is perpendicular to the median longitudinal axis of the ovary, running from the insertion point of the perianth and androecium to the median longitudinal axis. Line "b" is also perpendicular, running from the base of the ovary to the median longitudinal axis (cf. Leins, 1972
). Line "c" connects line "a" (insertion point) and line "b" (ovary base). As Igersheim et al. (1994)
point out, in a truly superior ovary, line "b" would be above line "a," and line "c" would obliquely approach the longitudinal axis toward the distal end (i.e., farthest from the insertion point of the perianth and androecium). The opposite is expected in an inferior ovary; line "a" would be above line "b," and line "c" would obliquely approach the longitudinal axis toward the proximal end. If the floral axis is flat, lines "a," "b," and "c" would be superimposed.
By applying this paradigm to T. gymnocarpa, the shift from an inferior to a superior ovary seems to be a result of differential growth of the ovary causing expansion of the top of the ovary. In a typical inferior ovary, such as in T. oahuensis, there is a deep floral cup. Consequently, during development, the distance between lines "a" and "b" becomes greater and greater (Fig. 8A, B) as the base of the ovary expands. Alternatively in T. gymnocarpa, the floral cup is relatively shallow during early carpel development (Fig. 9A). As development progresses (Fig. 9B), the distance between lines "a" and "b" barely increases. By late development, the vertical distance between lines "a" and "b" decreases dramatically (Fig. 9C). Apical expansion of the ovary as well as extension of the floral axis (i.e., below the ovary base) causes the ovary to become superior. This is a very similar pattern to what has been shown in Gaertnera [e.g., G. macrostipulata Baker, G. oblanceolata King and Gamble var. diversifolia (Ridl) van Beusekom, G. vaginans (DC.) Merr. subsp. junghuhniana (Miq.) van Beusekom, G. vaginans (DC.) Merr. subsp. vaginans] in which the superior ovary is also a consequence of the expansion of the ovary apex (Igersheim et al., 1994
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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characterizes three phases of floral organ development: (1) the floral organs are initiated, (2) the organs attain their shapes by differential growth, and (3) they differentiate their specific tissues. Regardless of the "nature" of the inferior ovary, phase two indicates that the inferior position results from pronounced dilation of the ovary base but little dilation of the ovary apex (Leins, 1972
). Several ontogenetic studies of different epigynous groups have confirmed this observation (e.g., in the Campanulaceae [Kaplan, 1967
], Apiaceae [Leins and Erbar, 1985
], and Araliaceae [Erbar and Leins, 1988
]).
Based on the evidence reported here for Tetraplasandra, the shift from an inferior to a superior position results mostly from pronounced dilation of the ovary apex but little dilation of the ovary base. Developmental studies in the Haemodoraceae (Simpson, 1998
), Rubiaceae (Igersheim et al., 1994
), and Saxifragaceae (Kuzoff et al., 2001
) corroborate that the switch from an inferior to a superior position can be explained by differential growth. The superior ovary in Gaertnera (Rubiaceae) and the nearly superior ovary found in species of Lithophragma (Saxifragaceae) arises from differential growth from the insertion point of the perianth and androecium to the apex of the ovary. In Wachendorfia (Haemodoraceae), the superior ovary is derived primarily from extension of the central axis of the receptacle (Simpson, 1998
). In Tetraplasandra, as well as Wachendorfia and Gaertnera, the ontogeny of the superior ovary reflects phylogeny. All three genera are nested well within epigynous families, and floral development indicates that the superior ovary found in these genera is really a modified inferior ovary.
Homology of ovary position
Remane (1952)
considers structures homologous if they fulfill one or more of three criteria: (1) equivalent positions within the general ground plan, (2) equivalent special quality, and (3) connection of differing structures by intermediates. According to Remane's criteria of homology, the superior ovary of T. gymnocarpa is homologous to an inferior ovary. The ovary of T. gymnocarpa arises inferior, but subsequently becomes displaced (i.e., superior) by differential growth. Kaplan (1984)
points out that when a character state changes during the ontogeny of the structure, developmental stages can function as intermediates linking the two divergent character states. According to Kaplan, this criterion is the most useful in determining homologies. In T. gymnocarpa, the ovary is inferior initially, partially superior (i.e., intermediate) at middle stages of floral development (Fig. 4E), and fully superior by anthesis. Structural intermediates can also be found between different species of closely related taxa (Kaplan, 1984
). As mentioned earlier, Tetraplasandra gymnocarpa shares a clade with the hemi-epigynous species T. kavaiensis and the epigynous species T. flynnii (see Fig. 2). Based on the intermediate criterion of homology, the partially superior ovary of T. kavaiensis may represent a phylogenetic intermediate connecting the inferior ovary (T. flynnii) and the fully superior ovary (T. gymnocarpa).
The developmental pathway of least resistance
Stebbins (1950)
proposed that most of the trends of plant evolution are best expressed by the fourth and fifth of Ganong's (1901)
"cardinal principles of morphology." Ganong's (1901
, p. 428) "principle of indeterminate anatomical plasticity" states that in all anatomical characters (including position), plant organs "... are not limited by anything in their morphological nature, but under proper influence may be led to wax and wane indefinitely in any of these respects" (p. 429). His principle of "metamorphosis along the lines of least resistance" further states that when a change in environmental conditions necessitates the performance of a new function, it will be assumed by that part which is "... most available for that purpose, regardless of its morphological nature, either because that part already has a structure most nearly answering the demands of the new function, or because it happens to be set free from its former function by change of habit, or for some other non- morphological reason" (p. 429).
Although Stebbins (1974)
advocated Ganong's "principle of indeterminate anatomical plasticity," he pointed out that the developmental pattern of an epigynous flower is so complex that reversion to the hypogynous condition is difficult to achieve. He argued that adaptive modifications along the pathway of least resistance can give rise to a number of modifications of the epigynous pattern, rather than its abandonment. For example, epigynous flowers can give rise to fruit structures that are functionally analogous but not homologous to various kinds of fruits derived from hypogynous flowers (e.g., dehiscent capsules, many-seeded berries, stone fruits).
Evidence from this study and other developmental studies in epigynous groups (e.g., Igersheim et al., 1994
; Simpson, 1998
) validate Ganong's point of view regarding anatomical plasticity and indicate that the inferior ovary is a labile character state that can be modified along a developmental pathway of least resistance, well before fruit development. The superior ovary in Tetraplasandra, Wachendorfia, and Gaertnera is an inferior ovary that has been modified developmentally simply by differential growth. Tetraplasandra and Gaertnera are endemic to island environments, which can foster the development of unique adaptations through founder effects and genetic drift (Mayr, 1954
, 1965
; Carson, 1981
). Gaertnera is endemic to Madagascar, Borneo, and Sri Lanka. Tetraplasandra is endemic to the Hawaiian Islands where another putative secondarily hypogynous species, Hillebrandia sandwicensis in the Begoniaceae (Charpentier et al., 1989
), occurs.
Adaptive significance of shifting ovary position
Eyde and Tseng (1969)
suggested that the switch to hypogyny was probably not a response to selection pressures, but that selection pressures against hypogynous mutants might have been relaxed on the Hawaiian Islands. Random mutations could be fixed extremely rapidly in small island populations as a result of founder effects and drift (Mayr, 1954
; Carson, 1981
). Carlquist (1969)
also suggested that the switch to hypogyny was probably quick, because intermediate stages would be expected if the transition had developed over a long period of time. The partial hypogyny in T. kavaiensis (Fig. 2) may represent an intermediate state. In that case, the switch to hypogyny may have occurred over time as a result of natural selection.
Based on the distribution of the extant species and the geological age of the Hawaiian Islands, the possibility that the change occurred quite rapidly, perhaps as the result of a single mutation cannot be ruled out. Among the members of the T. gymnocarpa clade, T. flynnii is a recently discovered species of only three known individuals endemic to Kauai (Lowry and Wood, 2000
), the oldest of the Hawaiian Islands (5.1 million years [my]; Carson and Clague, 1995
). Tetraplasanda kavaiensis is common on Kauai and apparently rarer on the younger islands (Lowry, 1990
). Tetraplasandra gymnocarpa is an extremely rare species restricted to Oahu (Lowry, 1990
), an island several million years younger (3.7 my) than Kauai. Given the phylogenetic relationships and biogegraphy of the modern species of Tetraplasandra as well as the age of the Hawaiian Islands, the superior ovary evolved at least 2.6 my ago. This change is a fairly recent evolutionary event and is found in a single population along the crest of the Koolau Mountain Range.
Additionally, Eyde and Tseng (1969)
suggested that selection for increased outcrossing, an important evolutionary trend on oceanic islands (Carlquist, 1966
, 1980
), may have played a role in the secondary derivation of the superior ovary. In buds of herbarium specimens of T. gymnocarpa, they observed that the stigma is separated from the anthers, and at anthesis the stigma remains above the anthers. This arrangement seems well adapted for inhibiting self-pollination. In the inferior ovary species of Tetraplasandra, the stigma is located below the anthers.
Alternatively, increasing evidence supports a shift in pollination strategy. Tetraplasandra gymnocarpa, T. kavaiensis, and T. flynnii show decreases in the number of ovary cells (2– 5) and a substantial reduction in the number of stamens (equal to the number of petals). The reduction in floral parts is probably not associated with developmental constraints due to the changes in ovary position, because T. flynnii has both a reduction in the number of floral parts and an inferior ovary. Interestingly, T. flynnii is the only species in the genus that is andromonoecious (Lowry and Wood, 2000
). Although the adaptive significance of andromonoecy in T. flynnii is unknown, changes in sexual system are usually associated with changes in pollination biology (Bawa and Beach, 1981
). It is plausible that the derived floral character states found in members of the T. gymnocarpa clade reflect a response to changes in pollination or dispersal opportunities.
The Kauai endemics, T. waialealae and T. waimeae, have a suite of specialized floral character states that suggest the development of ornithophily (Lowry, 1990
). The ovary is inferior and the large fuchsia flowers are clustered in dense compound umbellules, producing abundant quantities of nectar. As mentioned earlier, the epigynous species of the Tetraplasandra group have a nectary disk surmounting the inferior ovary. Both T. waimeae and T. waialealae have prominent nectary disks. In longitudinal sections of flowers, the nectary disk is indicated by a darkened staining pattern at the top of the ovary (Fig. 3C, D). In longitudinal sections of flowers of T. gymnocarpa, there is no such staining pattern at the top or base of the ovary indicating a nectary disk (Fig. 3F). The absence or a reduction of the nectary disk may be associated with the transformations involved in the development of the superior ovary. A loss or reduction in the nectary disk provides further evidence supporting the hypothesis that the switch to hypogyny corresponds with changes in reproductive ecology.
Based on differences in floral morphology and their sister- clade relationship, the T. gymnocarpa and the T. waimeae–T. waialealae clades may represent lineages that diverged in response to different pollination opportunities. Bird flowers produce relatively large amounts of nectar consisting of almost entirely of hexose sugars, with very little or no sucrose (Baker and Baker, 1983
). Qualitative differences in floral nectar would be expected among members of the T. gymnocarpa and T. waimeae–T. waialealae clades if there are differences in reproductive biology. Our future research will focus on the reproductive ecology of Tetraplasandra to test whether the differences in floral morphology reflect differences in pollination biology.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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FOOTNOTES |
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4 E-mail: acostello{at}ross.org
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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