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Department of Botany, Washington State University, Pullman, Washington, 99164-4238 USA
Received for publication November 16, 1999. Accepted for publication May 11, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allometry • epigyny • floral evolution • floral ontogeny • Lithophragma • ovary position • Saxifragaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In order to arrive at the most accurate judgement of the homology of the inferior ovary in different plant groups, it is necessary to combine the closely related approaches of comparative morphology, vascular anatomy, and ontogeny.—D. R. Kaplan (1967)
The evolution of floral architecture has captivated naturalists at least since Goethe (1790)
and Darwin (1877)
. From a single common ancestor that arose over 130 million years ago, greater than 250 thousand different species of angiosperms have evolved, generating an enormous array of floral forms (Crane, Friis, and Pedersen, 1995
). The phylogenetic, morphological, and developmental details of this protracted process are an enduring enigma. A fundamental aspect of floral diversification is the evolution of ovary position, because the structure and manner of insertion of the gynoecium strongly affect the overall conformation of the flower and the array of shapes that the outer floral appendages can assume. However, the factors underlying the evolution of ovary position have seldom been explored in a phylogenetic context and are not yet well understood.
Progress in elucidating the evolution of ovary position relies on an accurate understanding of the relationship between ovary position and patterns of floral development as well as structural homologies within flowers. In general, ovary position has been treated in two categories: superior and inferior. Different ovary positions are distinguished based on the point of attachment of the perianth and androecium relative to the ovary in a mature flower. A superior ovary is one that is situated entirely above the point of attachment of the perianth and androecium (sometimes basally fused into a hypanthium) in a hypogynous flower. In contrast, an inferior ovary has the perianth and androecium (also sometimes basally fused into a hypanthium) attached above the base of the ovary in an epigynous flower. Inferior ovaries vary from those that are deeply inferior and have the perianth and androecium attached at or above the apex of the ovary to those having these outer floral appendage series attached between the base and apex of the ovary. Frequently, decisions concerning floral homology have been made primarily on the basis of mature floral structure. Although it is crucial to evaluate mature floral architecture, this is not the only line of evidence that should be consulted in floral homology determination (Kaplan, 1967, 1984
; Stevens, 1984
).
Several authors have argued that early floral development serves as an additional line of evidence to help differentiate between flowers that are hypogynous, on the one hand, and epigynous, on the other, as well as discriminating between different forms of epigyny (Payer, 1857
; Boke, 1963, 1964, 1966
; Kaplan, 1967, 1984
). For example, Boke (1964, 1966)
and Kaplan (1967)
maintained that hypogynous and epigynous flowers differ in form from the time of organogenesis. Hypogynous flowers generally exhibit a convex floral apex throughout organogenesis (Fig. 1), as is the case in most Caryophyllales, Magnoliales, Proteales, Ranunculales, and Winteraceae (e.g., Payer, 1857
; Sattler, 1973
; van Heel, 1981, 1983, 1984
; Endress, 1994
; orders sensu Angiosperm Phylogeny Group, 1998
).
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; Kaplan, 1967
). Stamen primordia initiate on the flanks of the resultant concavity. As it deepens, carpel primordia are also initiated on the flanks of this concavity proximal to the stamen primordia. This is the most common type of epigynous floral development (Boke, 1964, 1966
; Kaplan, 1967
; Magin, 1977
; Hufford, 1988
; alternative interpretations are discussed in Douglas, 1944, 1957
; Weberling, 1992
). In contrast, receptacular-epigynous flowers have a convex floral apex throughout organogenesis. However, just after gynoecial primordia emerge, the base of the floral axis expands and its periphery rises, creating a basin in its center, and inverting the shape of the flower (Fig. 1; Boke, 1963, 1964
; Kaplan, 1967
; Endress, 1994
; Weberling, 1992
). This uncommon type of floral development characterizes the Cactaceae and Aizoaceae (Kaplan, 1967
; Weberling, 1992
). Hence, early floral ontogeny is an additional line of evidence that can be used to distinguish between alternative floral architectures, whether hypogynous, appendicular-epigynous, or receptacular-epigynous (Fig. 1).
Although these three patterns of early floral ontogeny may be useful starting points for categorizing diversity and are generally indicative of mature floral architecture (Payer, 1857
; Sattler, 1973
; van Heel, 1981, 1983, 1984
; Endress, 1994
), in actuality, floral development in some families appears to be more complex. For example, some flowers in the Rosaceae (e.g., Physocarpus, Oemleria) exhibit a more-or-less concave floral apex prior to gynoecial initiation, but have superior ovaries at maturity (Evans and Dickinson, 1999a, b
). Rauh and Reznik (1951)
observed that growth of the hypanthium, relative to the timing of floral organogenesis, is delayed in flowers of some Rosaceae species (e.g., Rosa), but much advanced in others (e.g., Pirus). However, they noted that the center of the floral apex remains convex throughout organogenesis in investigated Rosoideae species, which have a superior ovary, and becomes concave in Maloideae species, which have inferior ovaries. Evans and Dickinson have identified some morphologically transitional species in the phylogenetically intermediate Amygdaloideae (1999a) and Spiraeoideae (1999b). The anomalous pattern of early floral development in some Amygdaloideae and Spiraeoideae may be the result of precocious toral upgrowth around the periphery of the floral apex associated with the pronounced hypanthium in this family. This recent discovery illustrates the need for caution when interpreting patterns of early floral development and the need for additional studies of floral ontogeny.
The great diversity of ovary positions reported in Saxifragaceae has attracted much attention (e.g., Morf, 1950
; Klopfer, 1968, 1970, 1972, 1973
; Stebbins, 1974
; Cronquist, 1988
). For example, the single genus Lithophragma, comprising ten species, encompasses ovary positions reported to range from inferior to superior, with an array of intermediates (Taylor, 1965
; Hitchcock and Cronquist, 1973
; Elvander, 1993
). The concentration of such diversity in Lithophragma makes it an attractive genus with which to explore the evolution of ovary position (Taylor, 1965
). Phylogenetic relationships in Lithophragma have recently been assessed using restriction site (Soltis et al., 1992
) and ITS sequence data (Kuzoff et al., 1999
). Prior analysis of ovary position within Lithophragma (Kuzoff et al., 1999
) indicates that (1) the ancestor of Lithophragma had an ovary that was half inferior; and (2) ovary position has evolved toward greater inferiority in some species (e.g., L. affine, L. parviflorum, and L. trifoliatum) and greater superiority in others (e.g., L. glabrum, L. heterophyllum, and L. campanulatum), and thus is not the result of a unidirectional trend.
Here we explore the diversity of ovary positions in Lithophragma in terms of both mature floral architecture and patterns of development. Our goals are to assess structural homology in mature flowers, characterize patterns of early floral development, estimate relative rates of development in superior and inferior regions of the ovary, and uncover developmental transformations responsible for the evolution of ovary position in Lithophragma.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Lithophragma maxima was, until recently, considered extinct, and is still quite rare; therefore, anthetic flowers for this rare taxon could only be obtained from herbarium specimens (Table 1). Adult flowers for the outgroup species, Bensoniella oregona and Tellima grandiflora, were obtained from greenhouse specimens. In addition, developmental (i.e., immature) material of flowers was collected for eight species of Lithophragma (Table 1) and preserved in FAA; developmental material for the narrow endemics L. trifoliatum and L. maxima was not collected, because the problems we wished to address in this study did not require disturbing their fragile populations.
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). Herbarium specimens of flowers of L. maxima were reexpanded using Pohlstoffe rehydrating medium (Wagner, 1981
) and measured under a dissecting microscope.
Floral specimens for scanning electron microscopy (SEM) were dehydrated in a graded ethanol series, critical-point dried, mounted on metal stubs with double-stick tape, and sputter-coated with gold (following Hufford, 1988
). Specimens were examined using a Hitachi S570 SEM at 10–15 kV. SEM was used to examine both organogenesis and longitudinal sections of anthetic floral specimens. Preserved specimens were sectioned by hand with razor blades, prior to critical-point drying, and subsequently viewed under SEM. Additional flowers viewed under SEM were collected in very early stages of floral development and dissected to remove outer floral appendages and expose the floral apex.
Allometry
Longitudinal microtome sections and SEM micrographs were evaluated to determine the location of the ovary relative to the point of insertion of the perianth and androecium (henceforth the insertion point or IP). The length of the superior region was assessed by measuring the distance from the level of the IP, specifically from the midpoint of a line connecting the axils on opposite sides of the flower formed by the hypanthium and the ovary wall, to the apex of the ovary chamber (Fig. 2). The length of the inferior region was assessed by measuring the distance from the same midpoint between opposite IPs to the base of the ovary chamber (Fig. 2). For each species, flowers were measured to assess the length of the inferior and superior portions of ovaries from several specimens. The length of the inferior region was plotted against the length of the superior region using Microsoft Excel 5.0. To assess relationships between the lengths of superior and inferior regions, a trendline was inserted on the scatter plot with Microsoft Excel 5.0 using linear regression (Sokal and Rohlf, 1995
).
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). Allometric plots comparing the rate of growth between the inferior and superior regions of each ovary were combined into a single graph for interspecific comparison.
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75% of the ovary chamber is below the IP), and so on. We will also distinguish those flowers that externally appear to be superior, but internally have some portion of their ovary extended below the IP as pseudosuperior. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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77% of the variation in the SL can be explained in terms of the IL according to this allometric equation. In contrast, the two outgroup species, Bensoniella oregona (SL = 1.33 ± 0.03 mm; IL = 0.38 ± 0.01 mm) and Tellima grandiflora (SL = 1.67 ± 0.05 mm; IL = 1.87 ± 0.08 mm), do not have ovaries with an SL that fits the pattern observed in species of Lithophragma. The SL is too short in Bensoniella oregona and too long in Tellima grandiflora to fit the equation derived from static allometric comparisons of Lithophragma species.
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1.68 mm as the inferior region elongates to 0.22 mm. The two regions lengthen at highly proportional rates throughout development as expressed by the following allometric equation; SL = 6.409 IL + 0.167 (r2 = 0.8399, df = 17, P = 9.16 x 10-8; Fig. 7). In contrast, L. parviflorum, which has the greatest proportion of its ovary below the IP, has a superior region that attains a length of 0.45 mm as the inferior region elongates to 2.6 mm. The two regions of the ovary in L. parviflorum lengthen at highly proportional rates throughout development as expressed by the following allometric equation: SL = 0.162 IL + 0.0159 (r2 = 0.9537; df = 21, P = 8.15 x 10-15; Fig. 7). Thus, the rate of growth in the superior region relative to the inferior region in L. heterophyllum is 40 times greater than that of L. parviflorum. The six additional species investigated show a similar pattern of proportional growth in the two regions of the ovary and have slopes ranging between those of the two most extreme species (Fig. 7).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hitchcock and Cronquist, 1973
; Elvander, 1993
) describe ovaries of L. campanulatum and L. heterophyllum as superior. Taylor (1965)
used two criteria to determine ovary position in these two species: (1) their ovaries are positioned almost entirely above the IP; and (2) there are no ovules below the point of fusion of hypanthium and ovary (Fig. 4a). While these lines of evidence are explicit and reasonable, we feel that they are not the most reliable grounds for recognition of truly superior ovaries. Taylor (1965)
noted that his homology decisions concerning the ovary should be tested further, particularly through ontogenetic data. Hitchcock and Cronquist (1973)
and Elvander (1993)
also described ovaries of these two species as superior, but did not reveal the criteria they used to assess homology of ovary position in species of Lithophragma.
Truly superior ovaries can readily be distinguished from those that are pseudosuperior, and this is important because equating the two implies a false homology that obscures our understanding of angiosperm diversification. Additionally, such a mischaracterization can negatively impact phylogeny reconstruction. Truly superior ovaries (1) are positioned entirely above the IP in a hypogynous flower; and (2) are generally associated with a convex floral apex throughout organogenesis (but recent findings suggest exceptions in the Rosaceae [Evans and Dickinson, 1999a, b]
). Examples of truly superior ovaries can be found in flowers of species in ancestrally hypogynous lineages, including the Caryophyllales, Magnoliales, Proteales, Ranunculales, and Winteraceae (orders sensu Angiosperm Phylogeny Group, 1998
). Ovaries that are mostly situated above the insertion point, but do not meet these criteria, are not structurally homologous with truly superior ovaries. To avoid the problems mentioned, we suggest distinguishing all ovaries that externally appear superior but are found in epigynous flowers as pseudosuperior.
Truly superior ovaries are not present in Lithophragma, because all species (1) have ovaries partially situated below the IP, and (2) have a shift to a concave conformation in the floral apex during organogenesis. Hence, all flowers in species of Lithophragma are epigynous and have ovaries ranging from deeply inferior (e.g., L. affine, L. parviflorum, and L. trifoliatum) to pseudosuperior (e.g., L. campanulatum, L. glabrum, and L. heterophyllum). Additionally, hypogyny is probably not the plesiomorphic state in this lineage, because the common ancestor of Lithophragma very likely had an ovary that was half inferior (Kuzoff et al., 1999
). It is noteworthy that Small and Rydberg (1905)
, in their treatment of Lithophragma, refrained from describing any ovaries in Lithophragma as superior and, instead, used the phrase "hypanthium adnate only at the base of the ovary" to describe the flowers of L. campanulatum and L. heterophyllum. Our findings indicate that the conservative language of Small and Rydberg (1905)
was appropriate.
During the development of an epigynous flower, the periphery of the floral apex grows upwardly as a torus, or ring (e.g., Payer, 1857
; Klopfer, 1968, 1970, 1973
; Leins, 1972
; Magin, 1977
; Leins and Erbar, 1985
; Weberling, 1992
; Endress, 1994
). Whether such a torus includes carpellary and receptacular tissue (Payer, 1857
; Klopfer, 1968, 1970, 1973
; Leins, 1972
; Weberling, 1992
) or is solely appendicular tissue (van Tieghem, 1871
; Langdon, 1939
; Gauthier, 1950
; Kaplan, 1967
) has been contended on both anatomical and ontogenetic grounds (reviewed in Douglas, 1944, 1957
; Weberling, 1992
). Developmental morphologists advocating the appendicular theory have contended that zonal growth results from the elongation of congenitally fused floral appendages rather than an annular extension of axial tissue fused to the abaxial surface of the ovary wall (Payer, 1857
; Puri, 1952
; Klopfer, 1968, 1970, 1972
; Weberling, 1992
) or to the carpellary base (Leins, 1972
; Magin, 1977
; Leins and Erbar, 1985
). As was described in Downingia bacigalupii (Kaplan, 1967
), development of the floral apex in Lithophragma is consistent with an hypothesis of zonal growth centered in a synorganized region of congenitally fused floral appendages, because (1) zonal upgrowth commences only after sepal initiation (Fig. 6); (2) the emerging floral cup is unequally enlarged around the floral apex, consistent with phyllotactic initiation of perianth appendages (Fig. 6); and (3) the floral apex shifts to a concave conformation during perianth initiation, rather than after gynoecial initiation as is the case in receptacular-inferior ovaries (Boke, 1963, 1964, 1966
; Kaplan, 1967
). A similar interpretation was applied to other Saxifragaceae by Werle (1984)
. On the basis of observed patterns of floral vascularization, Taylor (1965)
suggested that the inferior ovary in Lithophragma was appendicular but stressed the need for further ontogenetic research.
It would be desirable to test this hypothesis of the structural homology of the inferior ovary of Lithophragma using molecular markers of carpel and perianth tissues. Potential molecular tools include orthologs of AGAMOUS, which is expressed in stamen and carpel primordia in diverse eudicots (Bowman, Smyth, and Meyerowitz, 1989, 1991
; Coen and Meyerowitz, 1991
; Bowman, 1997
) or CRABS CLAW, which is expressed specifically on the abaxial surface of carpels in Arabidopsis thaliana (Alvarez and Smyth, 1999
; Bowman and Smyth, 1999
; Sessions and Yanofsky, 1999
), and APETALA 1 or APETALA 2 (Bowman, Smyth, and Meyerowitz, 1989, 1991
; Coen and Meyerowitz, 1991
), which are expressed in perianth tissue in diverse eudicots. If our hypothesis is correct, we suspect that AGAMOUS and CRABS CLAW expression, detected through in situ hybridization, would be evident in the interior layers of the inferior region of the ovary, and APETALA 1 and APETALA 2 would be expressed in its external layers. Similar strategies have been employed successfully to explore structural homologies of petals in basal eudicots (Kramer and Irish, 1999
) and monocots (Ambrose et al., 2000)
. Gustafsson and Albert (1999) review recent studies of MADS box gene expression in derived eudicots and their implications for inferior ovary homology assessment. They conclude that interpretation of such data is complex, but seems inconsistent with some models of appendicular epigyny.
Developmental transformations
The diverse ovary positions observed in Lithophragma arise through allometric shifts in the amount of vertical growth in the inferior (appendicular floral cup and its carpellary interior) and superior (from the point of insertion of the unfused carpellary primordia to the apex of the ovary, subadjacent to the style) regions of the ovary (Figs. 3, 7). Greater relative growth in the superior region results in an adult flower having a nearly superior (or pseudosuperior) ovary, and greater relative growth in the inferior region results in a deeply inferior ovary (Figs. 3, 7). When net growth is nearly equivalent between these two regions, an approximately half-inferior ovary results (Figs. 3, 7). Shifts in the proportion of the ovary above and below the insertion point are, therefore, explicable entirely in terms of differential growth in the inferior and superior regions (Figs. 7, 8).
Because transitions among ovary positions have occurred frequently in Lithophragma (Kuzoff et al., 1999
), we hypothesize that they result from modification of one or a few genes affecting developmental processes. For example, a change in the timing of expression of C-class genes (i.e., orthologs of AGAMOUS in Lithophragma species) might explain some of the diversity in ovary positions in species of Lithophragma. C-class genes determine organ identity in both androecia and gynoecia in diverse eudicots (Bowman, Smyth and Meyerowitz, 1989, 1991
; Coen and Meyerowitz, 1991
; Weigel and Meyerowitz, 1994
; Bowman, 1997
). C-class genes also have an antagonistic (cadasteral) effect on A-class gene expression, which affects petal and sepal formation. Assuming that the closely related species of Lithophragma devote a similar amount of total metabolic energy and tissue mass to floral development, shifts in the timing of expression of C-class genes in developing flowers among species of Lithophragma might alter relative proportions of growth both among floral whorls and between ovarian regions. Earlier expression of C-class genes, relative to the common ancestor of Lithophragma, in the floral ontogeny of an extant species could result in increased size of stamens and the superior region of the ovary, because these organs could incorporate a larger proportion of the differentiating floral apex. A corollary effect would be relatively smaller perianth appendages. Alternatively, a delay in C-class gene expression, relative to the common ancestor, could result in a reversed effect with a decrease in the size of the stamens and superior region of the ovary but enlarged petals.
In Lithophragma, four lines of evidence are consistent with this hypothesis of shifts in the timing of C-class gene expression among the member species. First, stamens in flowers having pseudosuperior ovaries are longer than those in flowers having deeply inferior ovaries, consistent with early C-class gene expression and a greater portion of the floral mass being allocated to development of reproductive floral appendages (Taylor, 1965
; Fig. 4). Second, petals are shorter in species having pseudosuperior ovaries (e.g., L. campanulatum = 3–7 mm; L. glabrum = 3.5–7 mm; and L. heterophyllum = 5–12 mm; Taylor, 1965
) than in those that have deeply inferior ovaries (e.g., L. affine = 6–13 mm; L. parviflorum = 7–16 mm; L. trifoliatum = 9–11 mm; Taylor, 1965
; Fig. 4), also consistent with this hypothesis. Third, shifts in the lengths of superior and inferior regions among the species of Lithophragma conform to a pattern that suggests the lengths of these two regions are coordinated (Fig. 5), and it is most parsimonious to attribute this dual effect to a common cause (e.g., a change in the expression pattern of one gene or one suite of functionally related genes). Finally, among species of Lithophragma, shifts in the rate of growth of the inferior and superior regions are established early in floral development and maintained throughout floral ontogeny (Fig. 7), suggesting a change in gene expression very early in floral development, about the time that stamen and carpel primordia are initiated. Consequently, the derived pseudosuperior ovaries in L. campanulatum, L. glabrum, and L. heterophyllum might be, in part, the result of earlier expression of C-class genes, and the derived, deeply inferior ovaries of L. affine, L. parviflorum, and L. trifoliatum might be the result of delayed expression of C-class genes (Fig. 8). The molecular genetic hypothesis presented here could be tested through: (1) quantitative morphometric analysis of patterns of floral diversity; (2) direct analysis of expression of AGAMOUS orthologs in Lithophragma species via in situ hybridization; and (3) analysis of protein expression of these genes via immunolocalization. This hypothesis could also be tested in other Saxifragaceae, which exhibit a similar lability in floral architecture (Soltis et al., 1993, 1996
).
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), Rubiaceae (Igersheim et al., 1994
), Rosaceae (Morgan and Soltis, 1993
), Hydrangeaceae (Soltis, Xiang, and Hufford, 1995
; Hufford, 1997
), and Haemodoraceae (Simpson, 1998
). For example, Tetraplasandra gymnocarpa (Araliaceae) has flowers with an IP near the base of the ovary but is nested in a family having epigynous flowers (Eyde and Tseng, 1969
). Similarly, Gærtnera (Rubiaceae) has flowers that bear an ovary that is largely situated above the IP, particularly in fruit, but is also believed to be highly derived in an epigynous family (Igersheim et al., 1994
). Because Tetraplasandra gymnocarpa and Gærtnera are thought to be derived in families that are generally epigynous, their flowers have been referred to as secondarily hypogynous (Eyde and Tseng, 1969
) and their ovaries as secondarily superior (Igersheim et al., 1994
) to distinguish them from superior ovaries in ancestrally hypogynous lineages. Within Hydrangeaceae, the basal-most branch in analyses based on molecular (Soltis, Xiang, and Hufford, 1995
) and morphological (Hufford, 1997
) characters has genera with ovaries that are about one-third inferior. Hydrangeaceae are derived within the Cornales (Soltis, Xiang, and Hufford, 1995
; Hufford, 1997
; Soltis, Soltis, and Chase, 1999
), for which deeply inferior ovaries are plesiomorphic, indicating that shallowly inferior ovaries are derived in this order. These examples illustrate that the evolution of shallowly inferior or pseudosuperior ovaries has occurred multiple times among flowering plants. Hence, the model of ovary position evolution described here for Lithophragma may well have broader applicability and should be tested in other angiosperm lineages.
Selection
Selective forces that might be driving the evolution of ovary position in this and other families remain poorly understood. Hypotheses concerning the evolution of more deeply inferior ovaries within a lineage are numerous (Grant, 1950
; Stebbins, 1974
; Cronquist, 1988
; Thompson, 1994
), but we are not aware of any proposed selective forces underlying evolution towards greater superiority. The primary visitors to flowers of Lithophragma species are Diptera and Hymenoptera (Taylor, 1965
; Pellmyr and Thompson, 1996
). In L. parviflorum, for example, Diptera and Hymenoptera account for greater than 98% of all visitations and an estimated 99.7% of all seed production (Pellmyr and Thompson, 1996
). Whether these present-day primary pollinators have a preference for a given ovary position has not been explored. Some Lepidoptera species, for example Greya politella, oviposit in flowers of Lithophragma species having deeply inferior ovaries and may have formed a mutualistic relationship with them (Thompson, 1994, 1997, 1999
). Such a coevolutionary relationship may have been a causal factor in the evolution of deeply inferior ovaries in L. affine, L. parviflorum, and L. trifoliatum. However, because the array of pollinators is large and varies among populations within species (Taylor, 1965
; Pellmyr and Thompson, 1992, 1996
; Thompson, 1997
), further research is needed to identify the nature and outcome of such mutualisms.
Conclusion
Analyses of adult floral architecture, floral ontogeny, and phylogeny indicate that (1) flowers of all Lithophragma species are epigynous with inferior ovaries; and (2) the remarkable range of ovary positions among the ten species of Lithophragma results from simple allometric shifts in the relative rate of growth in the inferior and superior regions of the ovary. The common ancestor of Lithophragma had an ovary that was approximately half inferior and, thus, had a nearly equal extent of growth in these two regions. Pseudosuperior ovaries in L. campanulatum, L. glabrum, and L. heterophyllum result from a shift toward greater relative growth in the superior region of the ovary. The reverse is true for species having deeply inferior ovaries, such as L. affine, L. parviflorum, and L. trifoliatum. Because developmental transformations among species of Lithophragma have been frequent, we propose that they may be the result of modification of expression patterns of one or a few genes. We hypothesize that heterochronic shifts in the expression of AGAMOUS orthologs in Lithophragma may be partly responsible for these allometric shifts. Further research is needed to identify any underlying selective forces that may explain the pattern of evolution observed in Lithophragma. Evolution toward greater superiority in ovary position has occurred numerous times among angiosperms and Lithophragma may serve as a model genus to explore this phenomenon in greater detail.
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FOOTNOTES |
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; the Rancho Santa Ana Botanic Gardens (RSA) for permission to examine floral tissue of Lithophragma maxima from herbarium specimens; John Bowman, Vince Franceschi, Chuck Gasser, Don Kaplan, Toby Kellogg, and Liz Zimmer for thought-provoking discussion; and Peter Endress, Pam Soltis, John Thompson, and Roy Taylor for critical reading of the text. We gratefully acknowledge the Higinbotham Trust Fund, Washington State University, Sigma Xi and the American Society for Plant Taxonomists for research awards to RKK; and the NSF for a doctoral dissertation improvement grant (9624507) to DES, RKK, and LH. 
2 Address for reprint requests: R. K. Kuzoff, Section of Molecular and Cellular Biology, One Shields Avenue, University of California, Davis, California, 95616 USA (rkkuzoff{at}ucdavis.edu)
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