reevaluating the evolution of epigyny: data from ... - Mark Fishbein

Int. J. Plant Sci. 164(5 Suppl.):S251–S264. 2003. 

� 2003 by The University of Chicago. All rights reserved. 

1058-5893/2003/16405S-0005$15.00 

REEVALUATING THE EVOLUTION OF EPIGYNY: DATA FROM 

PHYLOGENETICS AND FLORAL ONTOGENY 

Douglas E. Soltis, 1 Mark Fishbein, and Robert K. Kuzoff 2 

Department of Botany and the Genetics Institute, University of Florida, Gainesville, Florida 32611, U.S.A.; Department of 

Biological Sciences, Mississippi State University, Mississippi State, Mississippi 39762, U.S.A.; and Department of 

Plant Biology, University of Georgia, Athens, Georgia 30602, U.S.A. 

A long-standing perspective of many botanists has been that there is a unidirectional trend in the evolution 

of ovary position from superior to inferior and that reversals are rare if at all possible. Recent studies that 

formally investigate the problem of gynoecial diversification in a rigorous phylogenetic context demonstrate 

that the evolution of ovary position is more complex and dynamic than this traditional view suggested. It is 

well known that a hypogynous ground plan characterizes a vast majority of angiosperms having superior 

ovaries and that within a hypogynous ground plan, flowers with inferior ovaries can be produced by a 

developmental plan termed receptacular epigyny. However, most angiosperms with inferior ovaries have an 

appendicular-epigynous ground plan in which a distinctive concavity appears in the center of the floral apex 

during perianth initiation. Recent investigations have shown that a diverse array of ovary positions ranging 

from completely inferior to what superficially appear to be superior ovaries, as well as intermediate ovary 

positions, can all develop from flowers having an appendicular-epigynous ground plan. A wide range of ovary 

positions among closely related species can be produced by allometric shifts in development, entailing greater 

relative growth in either the superior or inferior regions of an ovary. We have termed those ovaries produced 

via appendicular epigyny that appear superior or nearly superior “pseudosuperior ovaries.” Such ovaries are 

not developmentally homologous with truly superior ovaries produced via a hypogynous ground plan. We 

have observed, however, that errors in homology assessment of apparently superior ovaries are not uncommon, 

such that a number of angiosperm lineages with ovaries that have been termed superior are actually pseudosuperior. 

Finally, recent studies have demonstrated that reversals from an appendicular-epigynous to a 

hypogynous ground plan can occur but are rare. 

Keywords: floral development, epigyny, gynoecium, hypogyny, inferior ovary, phylogeny, character mapping. 

Introduction 

A fundamental aspect of floral diversification is the evolution 

of ovary position (Grant 1950; Stebbins 1974; Cronquist 

1988). The position of the ovary has a major impact on floral 

architecture, concomitantly impacting various interactions 

with animals that include predation, pollination, and seed dispersal 

(Grant 1950; Stebbins 1974; Thompson 1994). In general, 

ovary positions have been treated as either superior or 

inferior on the basis of the point of attachment of the perianth 

and androecium relative to the ovary in an anthetic (i.e., open 

or mature) flower (fig. 1). A superior ovary is situated above 

the point of attachment of the perianth and androecium to 

form 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 to 

form an epigynous flower. Flowers in which the outer floral 

appendages are basally fused are often called perigynous and 

can have either superior or inferior ovaries. 

In angiosperm systematics, ovary position has been used as 

1 Author for correspondence; e-mail dsoltis@botany.ufl.edu. 

2 Author for correspondence; e-mail rkuzoff@plantbio.uga.edu. 

Manuscript received August 2002; revised manuscript received May 2003. 

S251 

a key descriptive feature of families. It has often been considered 

a relatively stable character (Grant 1950; Stebbins 1974) 

sometimes used to distinguish closely related families. For example, 

in Lythraceae, the position of the ovary is generally 

described as superior whereas in the closely related Onagraceae, 

the ovary position is inferior. As a result, those welldefined 

angiosperm lineages in which considerable ovary position 

variation has been observed, usually described as 

families or orders, have been the source of considerable 

interest. 

A commonly espoused view in the plant systematic literature 

is that in the great span of angiosperm phylogeny, ovary position 

has evolved in a unidirectional manner from superior 

to greater inferiority, generally via congenital fusion of the 

outer floral appendages to the ovary wall; furthermore, reversals 

were considered rare or impossible (Bessey 1915; Grant 

1950; Stebbins 1974; Cronquist 1988; Takhtajan 1991). For 

heuristic purposes, we will refer to this as the “unidirectional” 

model of ovary position evolution. 

Before the mid-1990s, only a handful of investigators presented 

results that conflicted with the traditional view of unidirectional 

ovary position evolution. Tetraplasandra gymnocarpa 

(Araliaceae) has flowers that appear superior, but the 

species occurs within a family characterized by near pervasive

S252 INTERNATIONAL JOURNAL OF PLANT SCIENCES 

Fig. 1 Diagrams of hypogynous and epigynous flowers at anthesis 

(A) and hypogynous and epigynous ground plans (B). A, Hypogynous 

flower (ovary is superior) and epigynous flower (ovary is inferior). 

Modified from Judd et al. (2002). B, Hypogynous and epigynous 

ground plans. Flowers begin development with either a hypogynous 

ground plan or an epigynous ground plan and result in flowers with 

a superior or an inferior ovary, respectively. In a hypogynous flower, 

all of the floral organ series are initiated on a convex floral apex. There 

are two types of epigynous ground plans. In a receptacular-epigynous 

flower, the ground plan is also hypogynous, and the floral organs are 

again initiated on a convex floral apex, but just after organ initiation, 

the floral apex expands and raises, causing the floral axis to fold around 

the apex. In contrast, in an appendicular-epigynous flower, the floral 

apex flattens early in floral organogenesis and shifts to a concave 

formation during or just after perianth initiation. 

epigyny (Eyde and Tseng 1969). Similarly, Gaertnera (Rubiaceae) 

has ovaries that are largely superior, but it is also considered 

to be derived in an epigynous family (Igersheim et al. 

1994). Because both taxa are thought to be derived within 

families that are predominantly epigynous, their ovaries are 

considered secondarily superior (Igersheim et al. 1994) or the 

flowers have been termed secondarily hypogynous (Eyde and 

Tseng 1969). However, developmental data were not provided 

in the later study, and neither investigation evaluated the presumed 

phylogenetic hypotheses. Until recently, the factors underlying 

the evolution of ovary position had seldom been explored 

in both phylogenetic and developmental contexts, 

leaving the unidirectional model virtually unchallenged. 

A clearer understanding of the evolution of ovary position 

requires a firm phylogenetic underpinning as well as detailed 

analyses of development and structural homologies within 

flowers. Considerable progress toward this end has been 

achieved recently through multidisciplinary studies of this type. 

Phylogenetic relationships and studies of floral development 

in several lineages that are remarkable for their ovary position 

diversity suggest a much more dynamic picture of floral diversification. 

Here, we review the insights gained through these 

recent studies and provide a synthesis of phylogenetic and ontogenetic 

data pertaining to ovary position evolution. Additionally, 

we suggest a dynamic alternative to the classical model 

of ovary position diversification for the angiosperms. 

Ovary Position Terminology 

Varying degrees of ovary inferiority are standardly recognized 

(e.g., one-half inferior, one-quarter inferior), but this 

practice has led to some confusion. It may indicate to some 

that such ovaries are not structurally homologous with deeply 

inferior ovaries. For clarity, we wish to draw attention to a 

landmark in floral morphology, which is the insertion point 

(IP) of the perianth and androecium on an ovary (figs. 1, 4). 

If any portion of an ovary extends below the IP, then it is 

inferior. We also wish to clarify the terms we employ to refer 

to mature and developing flowers. At anthesis, the terms “superior” 

and “inferior” describe ovaries whereas “hypogynous” 

and “epigynous” describe floral architecture, in keeping with 

standard botanical terminology. In contrast, “hypogynous 

ground plan” and “epigynous ground plan” (fig. 1) describe 

developmental pathways. Morphologists have sometimes used 

the term “ground plan” to refer to the organization of the 

flower in a broad sense (Endress 1994). We are using the term 

“ground plan” to refer specifically to the conformation of the 

floral apex during organogenesis. 

Phylogenetic Data 

Phylogenetic analyses and character mapping studies have 

provided key insights into trends in ovary position evolution 

and diversification, challenging the unidirectional model of 

ovary position evolution. Character mapping studies have now 

been conducted at several different taxonomic levels including 

across all major lineages of flowering plants (Gustafsson and 

Albert 1999) as well as within families and genera (M. Fishbein, 

L. Hufford, and D. E. Soltis, unpublished manuscript; 

Kuzoff et al. 1999, 2001; Mort and Soltis 1999; Soltis et al. 

2001b). We will first review the mapping studies of Gustafsson 

and Albert (1999) that span angiosperms as a whole and proceed 

to more recent findings for one well-defined clade, Saxifragales 

(sensu APGII 2003), summarizing several phylogenetic 

analyses as well as character mapping studies. Within 

Saxifragaceae, we summarize an analysis conducted on Lithophragma, 

a particularly well-characterized genus. Additional 

examples will be drawn from ongoing investigations of Melastomataceae 

(D. Penneys, M. Hils, and D. E. Soltis, unpublished 

manuscript). 

Angiosperms 

Gustafsson and Albert (1999) analyzed ovary position diversification 

across the angiosperms and mapped ovary positions 

obtained from selected secondary sources onto the rbcL

SOLTIS ET AL.—EVOLUTION OF EPIGYNY S253 

Fig. 2 Mapping of ovary position using MacClade (Maddison and Maddison 1992) onto the maximum likelihood tree obtained for Saxifragales 

(Fishbein et al. 2001), illustrating the evolution of ovary position (modified from M. Fishbein, L. Hufford, and D. E. Soltis, unpublished 

manuscript). 

tree of Chase et al. (1993) for 499 angiosperms. Although their 

analysis is not the most current estimate of angiosperm phylogeny, 

recent changes in our understanding of angiosperm 

phylogeny (Soltis et al. 2000; reviewed by Kuzoff and Gasser 

2000) do not strongly impact the conclusions of Gustaffson 

and Albert (1999). In one set of mapping studies, two states 

were employed: hypogyny (including perigyny) and all degrees 

of epigyny (e.g., half-inferior, one-quarter inferior), treated as 

a single character state. However, these categories probably 

obscure some diversity. For example, many perigynous flowers 

should have been treated as epigynous rather than hypogynous. 

Additionally, the authors do not clarify their use of the 

terms “hypogynous” and “epigynous” and probably relied on 

homology assessments presented in the secondary sources, 

which have numerous errors. We have therefore attempted to 

examine developmental ground plans for ovary position (see 

appendix). 

These qualifications notwithstanding, the mapping studies 

of Gustafsson and Albert (1999) indicated that ovary position 

evolution at this broad scale was dynamic. They found 64 

unambiguous changes from hypogyny to epigyny, with 24 such 

changes from epigyny to hypogyny. Although their figures indicate 

that reversals are less frequent than are transitions from 

hypogyny to epigyny, these results would indicate that on a 

broad scale, ovary position evolution is not unidirectional. 

Importantly, the apparent reversals observed are not evenly 

distributed; whereas some groups are essentially fixed for epigyny, 

others appear more labile. Clades indicated to exemplify 

this lability in ovary position evolution include Goodeniaceae 

and Saxifragales (Gustafsson and Albert 1999); other clades 

could be added to that list including Rhamnaceae, Rhizophoraceae, 

and families of Myrtales including Melastomataceae 

and Vochysiaceae. 

Saxifragales 

Saxifragales provide an excellent system to investigate ovary 

position diversification because a range of ovary positions from 

superior to inferior is present. To reconstruct phylogeny for 

Saxifragales, sequences from five nuclear and chloroplast genes 

were used (ca. 9000 bp; Fishbein et al. 2001). M. Fishbein et 

al. (unpublished manuscript) reconstructed the diversification 

of ovary position on the basis of the morphology of flowers 

at anthesis (developmental data are discussed in “Saxifragales” 

in “Ontogenetic Data”). Gustafsson and Albert (1999) earlier 

reconstructed ovary position evolution in Saxifragales, but the 

more recent phylogenetic analysis of Fishbein et al. (2001) 

provides greater resolution of relationships as well as a better 

understanding of the composition of the clade. 

In contrast to the traditional view of unidirectional ovary


position evolution, mapping studies across Saxifragales reveal 

several possible reversals from inferior ovaries to those that 

appear to be superior (fig. 2; M. Fishbein, L. Hufford, and D. 

E. Soltis, unpublished manuscript). Inferior (or partially inferior) 

ovaries typify most members of the clade (fig. 2), but 

several reversals to ovaries that are or appear to be superior 

have occurred (fig. 2). The actual number of reversals is unclear 

because of uncertainty in phylogenetic relationships at the base 

of the clade. In Daphniphyllum, character state reconstructions 

indicate that a reversal to a superior ovary, or plesiomorphy, 

is equally parsimonious. Unambiguous reversals to hypogyny 

are seen in Crassulaceae and in Tetracarpaea (fig. 2). In Saxifragaceae, 

a family in which ovary position evolution appears 

to be so labile that it merits separate discussion, ovary position 

has evolved toward greater superiority in some lineages and 

greater inferiority in others, contrary to the predictions of the 

unidirectional model. 

Saxifragaceae 

Considerable variation in ovary position is present even 

within individual genera of Saxifragaceae (e.g., Saxifraga, Micranthes, 

Lithophragma, Chrysosplenium). The model of unidirectional 

ovary evolution has been invoked to account for 

the remarkable range of ovary positions seen in some genera, 

for example, Saxifraga (Stebbins 1974) and Lithophragma. 

Well-resolved and strongly supported topologies are now available 

for the entire family Saxifragaceae (Soltis et al. 1993, 

1996b, 2001a) as well as for many well-supported intrafamilial 

clades (e.g., Heuchera group: Soltis and Kuzoff 1995; R. K. 

Kuzoff, D. E. Soltis, and L. Hufford, unpublished manuscript; 

Boykinia group: Soltis et al. 1996a) and individual genera (e.g., 

Saxifraga: Soltis et al. 1996b; Micranthes: Soltis et al. 1996b; 

Mort and Soltis 1999; Lithophragma: Kuzoff et al. 1999; 

Chrysosplenium: Soltis et al. 2001b), providing the opportunity 

to evaluate critically trends in ovary position diversification. 

Mapping ovary position at anthesis onto phylogenetic trees 

again reveals repeated reversals from inferior ovaries to those 

that appear to be superior. This dynamic nature of ovary position 

evolution was detected across the entire family as well 

as within several genera including Chrysosplenium (Soltis et 

al. 2001b), Lithophragma (Kuzoff et al. 1999, 2001), and Micranthes 

(Mort and Soltis 1999) as well as within well-defined 

clades of genera such as the Heuchera group (R. K. Kuzoff, 

D. E. Solits, and L. Hufford, unpublished manuscript) and 

across Saxifragaceae as a whole. We provide an overview of 

the results for Lithophragma. 

Lithophragma includes only 10 species but exhibits extensive 

variation in ovary position from what has been termed 

superior to completely inferior, with a range of intermediate 

forms present (Taylor 1965). Hence, Lithophragma represents 

an ideal group with which to study ovary position diversification 

in a phylogenetic context. Kuzoff et al. (1999) provided 

a well-resolved phylogenetic hypothesis for the genus and subsequently 

interpreted ovary position evolution. On the basis 

of the results of Kuzoff et al. (1999) as well as broader phylogenetic 

surveys (Soltis and Kuzoff 1995; R. K. Kuzoff, D. E. 

Soltis, and L. Hufford, unpublished manuscript), the closest 

relatives of Lithophragma are well known. Parsimony recon- 

structions indicate that the hypothesized ancestor of Lithophragma 

possessed an ovary that was inferior, with approximately 

half of its ovary situated below the point of insertion 

for the perianth and androecium (hereafter, the “insertion 

point”). From this ancestral condition, there has been evolution 

toward increasing the portion of the ovary below the 

insertion point (fig. 3) in some species (L. affine, L. parviflorum, 

L. trifoliatum) and also toward increasing the portion of 

the ovary above the insertion point in several other species 

such as L. heterophyllum, L. campanulatum, and L. glabrum 

(fig. 3). Statistical analyses of the ovary position versus the 

relative positions of species in the phylogeny indicate that 

ovary position evolution in the genus does not fit a pattern of 

a trend toward greater superiority (Kuzoff et al. 1999). These 

results indicate that ovary position evolution in Lithophragma 

(fig. 3) has been highly labile, moving toward greater superiority 

in some lineages and greater inferiority in others, again 

contrary to the unidirectional model. 

Variation in ovary position is evident not only within small 

genera such as Lithophragma and Chrysosplenium but also 

across Saxifragaceae, with considerable variation also present 

among genera and clades of genera such as the Heuchera and 

Boykinia groups and within the three largest genera in the 

family, Micranthes, Chrysosplenium, and Saxifraga. There is 

no clear trend in gynoecial evolution from superior to inferior 

ovary position within Saxifragaceae as a whole or within individual 

genera or clades of genera; evolutionary shifts in the 

opposite direction appear to be common in some lineages. 

Fig. 3 Mapping of ovary position using MacClade (Maddison and 

Maddison 1992) onto the shortest phylogenetic trees obtained for Lithophragma, 

illustrating the evolution of ovary position (modified from 

Kuzoff et al. 1999, 2001).

Melastomataceae 

A similar, highly dynamic picture of ovary position diversification 

is emerging for Melastomataceae. When we focus on 

just one well-supported clade within the family that consists 

largely of section Miconeae, mapping studies (D. Penneys, M. 

Hils, and D. E. Soltis, unpublished manuscript) employing 

most parsimonious trees on the basis of analysis of ITS sequences 

do not indicate a unidirectional trend in ovary position 

evolution. Beginning with an inferred ancestor that was halfinferior, 

mapping studies indicate that in several instances, 

there has been evolution toward increasing inferiority; significantly, 

there has been evolution to what appear to be completely 

superior ovaries in two separate instances: in the Monochaetum, 

Tibouchina, Pilocosta clade and also again, 

independently in the Meriania, Axinaea, Graffenrieda clade 

(D. Penneys, M. Hils, and D. E. Soltis, unpublished manuscript). 

Thus, on the basis of this character analysis for the 

taxa sampled, we can infer multiple changes in ovary position. 

The evolution of ovary position from inferior to half-inferior 

has occurred as least five times, and our data support two 

reversals to a superior ovary position. This example is comparable 

to those reviewed for clades within Saxifragaceae and 

illustrates well just how labile ovary position can be within 

some groups of angiosperms. 

Ontogenetic Data 

Typically, ovary positions have been described and decisions 

concerning structural homology made exclusively on the basis 

of anthetic floral structure; i.e., superior and inferior ovaries 

typically are distinguished on the basis of the point of attachment 

of other floral appendages relative to the ovary through 

the examination of anthetic flowers. Although anthetic floral 

structure is important, early floral development serves as an 

additional line of evidence to differentiate among flowers that 

are hypogynous and those that are epigynous (Kuzoff et al. 

2001; Soltis and Hufford 2002). Boke (1964) and Kaplan 

(1967) demonstrated that hypogynous and epigynous flowers 

actually differ in form from the time of organogenesis, although 

the significance of their criteria for homology assessment 

has often been overlooked. There are two basic ground 

plans of floral development, hypogynous and epigynous; we 

review each in figure 1. Perigynous flowers may be a source 

of confusion to some. A perigynous flower may have an ovary 

that is partially inferior, or the ovary could be truly superior 

in some taxa. Perigynous flowers with partially inferior ovaries 

have an epigynous developmental ground plan; those with 

truly superior ovaries have a hypogynous ground plan. 

The early floral conformation of most hypogynous flowers 

(see “Complexities and Caveats”) represents what is termed a 

hypogynous ground plan. Hypogynous flowers generally exhibit 

a convex floral apex throughout organogenesis (fig. 1; 

van Heel 1981, 1983, 1984; Endress 1994). This ground plan 

is common in the angiosperms and likely accounts for many 

flowers with ovaries described as superior on the basis of the 

examination of anthetic flowers. For example, a hypogynous 

ground plan characterizes many basal angiosperm lineages 

such as Piperaceae and Alismataceae as well as some earlybranching 

eudicots such as members of Ranunculaceae and 


Papaveraceae (the appendix summarizes some of the diversity 

in gynoecial development). Ontogenetic studies have also 

shown a hypogynous ground plan to be present in many core 

eudicot lineages, including families of Caryophyllales such as 

Caryophyllaceae and Chenopodiaceae (Sattler 1973) as well 

as many eurosids such as Fabaceae (Tucker et al 1985; Tucker 

1987), Malvaceae s. l. (Jenny 1988), and Brassicaceae (Sattler 

1973) and also asterids such as Solanaceae (Sattler 1973, 1977; 

appendix). 

A modification in the final stages of development of a hypogynous 

ground plan is represented by what is termed receptacular 

epigyny. Receptacular epigyny arises when a floral 

apex remains convex throughout organogenesis, but just after 

gynoecial primordia emerge, the periphery of the floral apex 

expands and rises, creating a basin in its center (Boke 1963, 

1964). Although a modification of a hypogynous ground plan, 

this type of floral development yields inferior ovaries at anthesis. 

Floral development of this kind is very uncommon, 

characterizing Cactaceae and Aizoaceae (Kaplan 1967; Weberling 

1992). 

Most inferior ovaries (see “Complexities and Caveats”) are 

the result of an appendicular-epigynous pattern of floral development 

(fig. 1). Appendicular epigyny also begins floral organogenesis 

with a convex floral apex, but during or just after 

perianth initiation, a concavity develops in the center of the 

floral apex. The concavity forms as the emerging perianth and 

androecium rise up from the floral axis as an annular meristem 

that elongates through zonal growth (fig. 1; Kaplan 1967; 

Leins 1972; Magin 1977). Stamen primordia initiate on the 

flanks of the resultant concavity. As it deepens, stylar primordia 

are also initiated on the flanks of this concavity below the 

stamen primordia. This appendicular-epigynous pattern is the 

most common type of epigynous floral development (Kaplan 

1967; Magin 1977), characterizing a large number of families 

including Apiaceae (Magin 1977; Leins and Erbar 1985), Araliaceae 

(Erbar and Leins 1988), Asteraceae (Leins and Erbar 

1987), Calyceraceae (Erbar 1993), Campanulaceae (Kaplan 

1967), Goodeniaceae (Leins and Erbar 1989), Rhamnaceae 

(Medan 1988), Rhizophoraceae (Juncosa 1988), Saxifragaceae 

(Kuzoff et al. 2001; Soltis and Hufford 2002), Stylidiaceae 

(Erbar 1992), Vitaceae (Gerrath and Posluszny 1988), Vochysiaceae 

(Litt 1999; A. Litt and D. W. Stevenson, unpublished 

manuscript), Begoniaceae (Charpentier et al. 1989), and 

Rubiaceae (Igersheim et al. 1994; see appendix for a summary 

of numerous examples of an appendicular-epigynous ground 

plan). 

Recent ontogenetic studies conducted in a phylogenetic context 

have extended our understanding of how shifts among 

ovary positions occur developmentally. They show that in lineages 

characterized by appendicular epigyny, it is possible to 

create a wide range of ovary positions (Leins 1972), including 

some ovaries that appear superior, through allometric shifts in 

the amount of relative growth in superior and inferior portions 

of the ovary. These recent results are reviewed for Saxifragaceae 

and Saxifragales, respectively. 

Saxifragaceae 

Studies of floral development in Lithophragma have helped 

elucidate the evolution of ovary position in Saxifragaceae (Ku-


Fig. 4 SEM photographs illustrating the structural diversity in inferior ovaries in Lithophragma. A, Lithophragma glabrum, exhibiting a 

pseudosuperior ovary. B, Lithophragma tenellum, exhibiting a half-inferior ovary. C, Lithophragma trifoliatum, exhibiting a deeply inferior 

ovary. For each flower, the insertion point (IP) of the perianth and androecium, which divides the superior and inferior regions of an inferior 

ovary, is designated with an arrow. H p hypanthium; Se p sepal; P p petal; S p stamen; St p style (modified from Kuzoff et al. 2001). 

zoff et al. 2001). Importantly, Kuzoff et al. (2001) found that 

all ovaries in Lithophragma are derived from an appendicularepigynous 

ground plan and there are no truly superior ovaries 

in the genus. Those species that possess flowers with ovaries 

that appear superior are actually inferior, representing pseudosuperior 

ovaries (fig. 4; Kuzoff et al. 2001). 

Kuzoff et al. (2001) also compared developmental patterns 

among Lithophragma species through static and ontogenetic 

allometry and scanning electron microscopy. These comparisons 

revealed that the diversity of ovary positions in this small 

genus resulted from shifts among species in the rate of growth 

between superior and inferior regions during floral development 

(fig. 4). Greater relative growth in the superior region 

results, at anthesis, in an ovary that appears superior or nearly 

superior (a pseudosuperior ovary), whereas greater relative 

growth in the inferior region results in a completely inferior 

ovary. When growth is nearly equal in the two regions, a halfinferior 

ovary is produced (fig. 4). Hence, the wide range of 

variation in ovary position in Lithophragma results from simple 

allometric shifts in relative growth above and below the 

position where the perianth and androecium are inserted. Allometric 

changes have been shown to be an important component 

in other aspects of floral evolution (Lord 1981; Guerrant 

1982; Diggle 1992; Niklas 1994). Our results reinforce 

the suggestion of Simpson (1998) that allometric changes are 

important in ovary position diversification. 

Additional studies (Soltis and Hufford 2002) indicate that 

the pattern and mechanism of ovary position evolution elucidated 

in Lithophragma are directly applicable to the entire 

Saxifragaceae. SEM studies of floral ontogeny across a diverse 

array of taxa in Saxifragaceae indicate that many species reported 

previously to have superior ovaries actually have an 

appendicular-epigynous ground plan. Thus, these ovaries are 

not “truly superior” but again represent pseudosuperior ovaries 

(fig. 4). These pseudosuperior ovaries should not be considered 

homologous with truly superior ovaries derived from 

a hypogynous ground plan. There is also evidence suggesting 

that true reversals to hypogynous development may have occurred 

on rare occasions (e.g., Saxifraga nipponica) in Saxifragaceae 

(fig. 5). 

Thus, developmental studies demonstrate that nearly all ovaries 

in Saxifragaceae are technically inferior (Kuzoff et al. 

2001; Soltis and Hufford 2002), although in the literature, 

they are described as ranging from superior to inferior. Differences 

in mature ovary position throughout Saxifragaceae 

may typically be the direct result of allometric shifts in the 

growth proportions of these regions of the ovary (fig. 4; Kuzoff 

et al. 2001). These findings also have important implications 

for phylogeny reconstruction and floral evolution across the 

angiosperms, indicating that not all ovaries described as superior 

are homologous. 

Saxifragales 

Phylogenetic data (fig. 2) indicated several reversals from 

inferior to superior ovaries within Saxifragales. Ontogenetic 

data provide critical, additional insights into ovary position 

diversification within the clade. Studies of floral ontogeny (M. 

Fishbein, L. Hufford, and D. E. Soltis, unpublished manuscript) 

reveal that appendicular epigyny typifies most Saxifragales 

and is ancestral for most of or possibly the entire clade 

(fig. 5). Significantly, reversals to a superior ovary have occurred 

in Crassulaceae, Tetracarpaea, and perhaps also in 

Daphiniphyllum (fig. 5). Cercidiphyllum is actually a special


Fig. 5 Maximum likelihood tree for Saxifragales (from Fishbein et al. 2001) that also shows diversification in the modes of early floral 

meristem development. Darker branches are well supported and insensitive to data combination and method of phylogenetic analysis (see Fishbein 

et al. 2001). Vertical bars indicate derived floral ontogenies affecting ovary position. 1, Derivation of pseudosuperior ovary from appendicularepigynous 

ground plan; 2, ground plan in which carpels initiate on a flattened meristem, producing superior ovaries; 3, hypogynous pattern; 4, 

anomolous ground plan associated with nearly superior ovaries, which is currently under further investigation. SEM photographs (Soltis and 

Hufford 2002; M. Fishbein et al., unpublished manuscript) of Saxifraga nipponica (Saxifragaceae), Itea japonica (Iteaceae), Kalanchoe blossfeldiana 

(Crassulaceae), Tetracarpaea tasmanica (Tetracarpaeaceae), Penthorum sedoides (Penthoraceae), Paeonia daurica (Paeoniaceae), and 

Daphniphyllum sp. (Daphniphyllaceae) depict early stages of floral development. The ancestral state for the clade is equivocal. The dashed bar 

indicates that there is uncertainty in the phylogenetic position of Daphniphyllum, and this makes determination of the phylogenetic homology 

of the superior ovary in this species and the ancestral state of the clade uncertain (from M. Fishbein, L. Hufford, and D. E. Soltis, unpublished 

manuscript). 

case in that the flowers are unisexual and each female flower 

is essentially no more than a carpel; hence, the terms “superior 

ovary” and “inferior ovary” are not truly applicable. In Crassulaceae, 

the floral meristem is raised on a central platform 

with a reversal to a superior ovary also associated with derived 

apocarpy (fig. 5). In Tetracarpaea, the floral apex remains convex 

throughout organogenesis, so it would seem appropriate 

to refer to this as a hypogynous ground plan. Thus, Tetracarpaea 

represents a true reversal from an appendicular-epigynous 

ground plan to a hypogynous ground plan (M. Fishbein et al., 

unpublished manuscript). However, in Crassulaceae, as noted 

in “Complexities and Caveats,” the underlying ground plan 

is less clear. 

Other Relevant Angiosperm Lineages 

The same developmental processes occurring in Saxifagaceae 

may also occur in other eudicot families exhibiting variation 

in ovary position. Studies of ovary development in Vochysiaceae 

similarly reveal that despite considerable ovary position 

variation, all taxa examined possess an appendicularepigynous 

ground plan and, hence, are technically inferior (Litt 

1999; A. Litt and D. W. Stevenson, unpublished manuscript). 

Although studies of allometry were not conducted, we hypothesize 

that this variation in ovary position is again the 

consequence of the relative amount of vertical extension of 

inferior versus superior region of the ovary (fig. 4). 

Similar allometric shifts in development may explain the 

transition to a superficially superior ovary observed in Gaertnera 

(Rubiaceae). All Rubiaceae possess ovaries that are inferior, 

and ontogenetic studies indicate appendicular epigyny 

as the underlying developmental ground plan (Igersheim et al. 

1994). Igersheim et al. (1994) refer to the ovary of Gaertnera 

as “secondarily superior”; on the basis of ontogenetic studies, 

they conclude that the “superior” ovary is achieved in this


taxon via increased growth or development in the superior 

region of the ovary, a process that they state follows the principle 

of variable proportions. 

We suggest that modifications of appendicular-epigynous 

ground plans have yielded a diverse array of ovary positions 

not only in the clades and families we have emphasized here 

(Saxifragaceae and other Saxifragales) but many other families 

as well. This process may be responsible for the diversity of 

ovary positions observed in Melastomataceae. In addition, 

Vochysiaceae, Rhamnacae, and Rhizophoracae have considerable 

ovary position variation, and developmental studies of 

one or a few taxa suggest that an appendicular-epigynous 

ground plan may be present in these families (Sattler 1973; 

Juncosa 1988; Medan 1988; Litt 1999). However, establishing 

the underlying mechanism in these and other families will require 

additional detailed investigation of floral ontogeny. 

Synthesis: The Evolution of Epigyny 

To summarize the emerging picture, the patterns of ovary 

position diversity in the context of phylogenetic data reveal 

that ovary position evolution is not unidirectional. At both 

higher levels across the angiosperms and even within individual 

families and genera, a more dynamic picture of ovary position 

diversification has emerged with several examples of transitions 

from deeply inferior ovaries to those that are either shallowly 

inferior or truly superior. Ovary position lability is not 

evenly distributed, however, across the angiosperms. Some 

clades such as Saxifragales, Myrtales, and Goodeniaceae appear 

to have more developmental flexibility in terms of ovary 

position evolution than do other clades (Gustafsson and Albert 

1999). 

The two basic underlying ground plans of floral development, 

hypogynous and appendicular-epigynous ground plans, 

yield superior and inferior ovaries, respectively. There are developmental 

complexities, however, as noted in more detail in 

“Complexities and Caveats.” Furthermore, modifications of 

both underlying ground plans are possible, providing greater 

flexibility in terms of floral morphologies. Thus, receptacular 

epigyny represents a modification of a hypogynous ground 

plan that ultimately results in an inferior ovary. These inferior 

ovaries are not homologous with those derived from an 

appendicular-epigynous ground plan. This modification appears 

rare, however, occurring only in Cactaceae and Aizoaceae 

(Boke 1963, 1964; Kaplan 1967). Virtually all inferior 

ovaries occur in flowers having an appendicular-epigynous 

ground plan. However, this ground plan can also be modified 

through allometric shifts in development (figs. 1, 4) to produce 

a diverse array of ovary positions ranging from completely 

inferior to varying degrees of inferiority to ovaries that appear 

completely superior (pseudosuperior ovaries following our terminology). 

Adding further to the dynamic nature of ovary 

position evolution is the recent discovery that reversals from 

an appendicular-epigynous to a hypogynous floral ground plan 

can occur. 

Complexities and Caveats 

Although recent studies have greatly improved our understanding 

of the evolution of epigyny, new complexities have 

emerged. We know, for example, that there are developmental 

complexities present in Rosaceae, where species of Physocarpus 

and Oemlera have flowers that exhibit a concave floral 

apex before gynoecial initiation yet have clearly superior ovaries 

at maturity (Evans and Dickinson 1999a, 1999b). However, 

other Rosaceae such as Fragaria appear to have a convex 

floral apex throughout organogenesis (Sattler 1973), as would 

be expected with a hypogynous ground plan. The anomalous 

situation in the Rosaceae clearly indicates the need for additional 

investigation of development in a phylogenetic context 

in other lineages. Kuzoff et al. (2001) speculated that the remarkable 

pattern of growth of some rosaceous species may, 

for example, be the result of precocious toral upgrowth around 

the periphery of the floral apex associated with the pronounced 

hypanthium in this family. 

As noted briefly, a caveat associated with the reversals from 

inferior to superior ovaries in Saxifragales (fig. 5) involves 

whether the developmental ground plan involved is best 

termed a hypogynous ground plan. In Crassulaceae, the floral 

apex appears flat throughout organogenesis rather than convex 

(fig. 5). Is this a hypogynous ground plan of floral development? 

Perhaps because the Saxifragales are developmentally 

labile, there are several distinct mechanisms by which reversals 

to superior ovaries may occur, and the underlying patterns of 

development associated with these reversals are not identical. 

Evolutionary Implications 

The relative ease with which allometric shifts may occur in 

the course of evolution readily explains the wide range of ovary 

positions in Saxifragaceae as well as the numerous reversals 

that have occurred in the group. Our data also indicate that 

gynoecial evolution in Saxifragaceae may be more rapid than 

generally inferred for angiosperms. Ongoing studies suggest 

that a similar highly dynamic picture of ovary position evolution 

also characterizes Melastomataceae (D. Penneys, M. 

Hils, and D. E. Soltis, unpublished manuscript) and perhaps 

other families characterized by considerable variation in ovary 

position (e.g., Rhamnaceae, Rhizophoraceae). 

Although our developmental studies provide a process by 

which a wide range of ovary positions may be produced, it is 

not clear what selective forces may be driving this diversification. 

Perhaps the most commonly proposed selective force 

has been protection from herbivorous birds or insects with 

biting mouth parts, with epigyny resulting in the increased 

protection of ovules (Grant 1950; Stebbins 1974). Another 

possible cause for the evolution of epigyny would be selection 

mediated by pollinators. J. Thompson (personal communication) 

has suggested that the diverse array of ovary position 

observed may be the result of coevolutionary interactions with 

pollinators. Greya moths, which are close relatives of yucca 

moths, are the major pollinators and, in some cases, the only 

major herbivores of their Lithophragma host plants (Thompson 

and Cunningham 2002). In some species and populations, 

the pollination services of Greya can be swamped by a small 

number of copollinator species (Thompson and Pellmyr 1992; 

Thompson 1994), making the outcome of the interaction between 

the moths antagonistic in some environments and mutualistic 

in others (Thompson and Cunningham 2002). Since 

some of these Greya species lay their eggs in Lithophragma

flowers, they may pose important selection pressures on Lithophragma 

flowers both as mutualists and antagonists. Additional 

research is needed to identify the nature and outcome 

of such mutualisms (Thompson 1994). 

Summary and Future Studies 

Recent documentation of gynoecial development in several 

lineages of eudicots has broad implications for understanding 

floral diversity in the angiosperms. An exciting recent discovery 

is that a diverse array of ovary positions ranging from completely 

inferior to what superficially appear to be superior ovaries, 

as well as the entire range of intermediate ovary positions, 

can all be produced via an appendicular-epigynous ground 

plan of development. This wide range of ovary positions may 

be produced via allometric shifts in development in several 

investigated species and perhaps in many more as well (fig. 5). 

We have termed those ovaries that are produced via appendicular 

epigyny and appear to be superior “pseudosuperior.” 

Such ovaries are not homologous with truly superior ovaries 

produced via a hypogynous ground plan. 

Most of the recent work summarized here is in Saxifragales. 

Saxifragales appear to occupy a critical phylogenetic position 

in the core eudicots, perhaps as sister to the large eurosid clade 

(Soltis et al. 2000). Importantly, within the eurosids, several 

families and small clades of families similarly exhibit extensive 

variation in ovary position ranging from superior to inferior. 

Examples include Melastomataceae, Memecylcaceae, Vochysiaceae, 

Flacourtiaceae, Dichapetalaceae, and Rhizophoraceae. 

Recent studies demonstrate that not all ovaries that 

appear superficially to be superior are homologous. We predict 

that ovaries described as superior in other groups, such as the 

eurosid families noted, may not be homologous with truly 

superior ovaries derived from a hypogynous floral ground plan 


Appendix 

Table A1 

but are also derived from within an appendicular-epigynous 

ground plan. As one avenue of future investigation, it will be 

important to conduct ontogenetic studies in other groups in 

an effort to differentiate between truly superior ovaries (derived 

via a hypogynous ground plan) and pseudosuperior ovaries 

(derived from an appendicular-epigynous ground plan). 

Another question, closely related to that posed earlier, will be 

to determine whether allometric shifts in development similarly 

account for the diverse array of ovary positions observed in 

other families. 

Undoubtedly, future developmental studies will illustrate additional 

complexities in gynoecial development. For example, 

the recognition of two basic ground plans, appendicularepigynous 

and hypogynous, may be an oversimplification. In 

addition, comparisons of transitions among floral ground 

plans are needed because dissimilar mechanisms may be responsible 

for changes in different lineages. 

The underlying genetic factors that result in hypogynous 

versus appendicular-epigynous floral ground plans are unknown, 

as are the underlying genetic causes for the developmental 

changes that occur just within appendicular epigyny 

and generate substantial ovary position variation. Hence, another 

important area of future research involves developmental 

genetic investigations to identify the genes controlling ovary 

position. 

Acknowledgments 

This research was supported by DEB 9726225 to D. Soltis 

and L. Hufford and a Fulbright Award to D. Soltis and P. 

Soltis. The authors thank L. Hufford and P. Endress for helpful 

discussions and R. Evans and an anonymous reviewer for helpful 

comments on the manuscript. 

Partial Listing of Families of Angiosperms for Which Ontogenetic Data Are Available 

Family 

Ground 

plan Reference 

Basal lineages: 

Monocots: 

Acorales: 

Acorus calamus Acoraceae HGP Sattler 1973; Buzgo and Endress 2000 

Alismatales: 

Asimina triviale Alismataceae HGP Sattler 1973 

Butomus umbellatus Butomaceae HGP Sattler 1973 

Liliales: 

Scilla violacea Liliaceae HGP Sattler 1973 

Asparagales: 

Ruscus hypoglossum Ruscaceae HGP Sattler 1973 

Allium sp. Alliaceae HGP Sattler 1973 

Habenaria clavellata Orchidaceae AGP? Sattler 1973 

Poales: 

Hordeum vulgare Poaceae HGP Sattler 1973 

Sparganium eurycarpum Sparganiaceae HGP Sattler 1973 

Scirpus validus Cyperaceae HGP Sattler 1973

Family 

Table A1 

(Continued) 

S260 

Ground 


Commelinales: 

Tradescantia sp. Commelinaceae HGP Hardy and Stevenson 2000 

Callisia navicularis 

Other basal lineages: 

Nymphaeales: 

Commelinaceae HGP Hardy and Stevenson 2000 

Cabomba caroliniana Nymphaeaceae HGP Tucker 1999 

Cabomba furcata Nymphaeaceae HGP Endress 2001 

Nuphar advena Nymphaeaceae HGP Endress 2001 

Victoria cruziana Nymphaeaceae HGP Endress 2001 

Nymphaea alba 

Austrobaileyales: 

Nymphaeaceae HGP Ronse Decraene and Smets 1993 

Austrobaileya scandens Austrobaileyaceae HGP Endress 2001 

Trimenia papuana Trimeniaceae HGP Endress 2001 

Schisandra glabra Schisandraceae HGP Tucker 1999 

Schisandra chinensis Schisandraceae HGP Endress 2001 

Illicium anisatum Illiciaceae HGP Endress 2001 

Illicium henryi 

Piperales: 

Illiciaceae HGP Ronse Decraene and Smets 1993 

Peperomia caperata Piperaceae HGP Sattler 1973 

Saruma henryi 

Winterales: 

Aristolochiaceae AGP Tucker 1999 

Drimys winteri 

Magnoliales: 

Winteraceae HGP Doust 2001 

Magnolia denudata 

Laurales: 

Magnoliaceae HGP Erbar and Leins 1983 

Laurus nobilis 

Eudicots: 

Early-branching eudicots: 

Ranunculales: 

Lauraceae HGP Ronse Decraene and Smets 1993 

Chelidonium majus Papaveraceae HGP Sattler 1973 

Ranunculus acris Ranunculaceae HGP Sattler 1973 

Cocculus laurifolius Menispermaceae HGP Ronse Decraene and Smets 1993 

Papaver somniferum Papaveraceae HGP Ronse Decraene and Smets 1993 

Decaisnea fargesii 

Proteales: 

Lardizabalaceae HGP Ronse Decraene and Smets 1993 

Persoonia myrtilloides Proteaceaea HGP Douglas and Tucker 1996a 

Bellendena montana Proteaceae a 

HGP Douglas and Tucker 1996a 

Placospermum corianum Proteaceae a 

HGP Douglas and Tucker 1996a 

Lambertia inermis Proteaceae a 

HGP Douglas and Tucker 1996b 

Nelumbo nucifera 

Core eudicots: 

Saxifragales: 

Nelumbonaceeae HGP Hayes et al. 2000 

Lithophragma sp. Saxifragaceaea AGP Kuzoff et al. 2001 

Boykinia sp. Saxifragaceaea AGP Soltis and Hufford 2002 

Suksdorfia sp. Saxifragaceae a 

AGP Soltis and Hufford 2002 

Micranthes sp. Saxifragaceae a 

AGP Soltis and Hufford 2002 

Saxifraga sp. Saxifragaceaea AGP Soltis and Hufford 2002 

AGP Klopfer 1970 

Tellima grandiflora Saxifragaceaea AGP Klopfer 1968; Kuzoff et al. 2001 

Rhodoleia championii Hamamelidaceae AGP Bogle 1989 

Daphniphyllum sp. Daphniphyllaceae Anom M. Fishbein, L. Hufford, and D. E. 

Soltis, unpublished manuscript 

Kalenchoe blossfeldiana Crassulaceae Anom M. Fishbein, L. Hufford, and D. E. 


Tetracarpaea tasmanica Tetracarpaeaceae HGP M. Fishbein, L. Hufford, and D. E. 


Penthorum sedoides Penthoraceae AGP M. Fishbein, L. Hufford, and D. E. 


Itea japonica Iteaceae AGP M. Fishbein, L. Hufford, and D. E. 

Soltis, unpublished manuscript

Family 

Table A1 

(Continued) 

S261 

Ground 


Aphanopetalum resinosum 

Caryophyllales: 

Haloragaceae AGP M. Fishbein, L. Hufford, and D. E. 


Pereskia aculeata Cactaceae RGP Boke 1963, 1964 

Chenopodium album Chenopodiaceae HGP Sattler 1973 

Fagopyrum sagittatum Chenopodiaceae HGP Sattler 1973 

Silene cucubalus Caryophyllaceaea HGP Sattler 1973 

Scleranthus perennis Caryophyllaceaea HGP Ronse Decraene and Smets 1993 

Gypsophila paniculata Caryophyllaceaea HGP Ronse Decraene and Smets 1993 

Silene colorata Caryophyllaceae a 

Asterids: 

Ericales: 

HGP Ronse Decraene et al. 1998 

Lysimachia nummularia 

Gentianales: 

Primulaceae Anom Sattler 1973 

Gaertnera sp. Rubiaceae AGP Igersheim et al. 1994 

Asclepias syriaca 

Lamiales: 

Apocynaceae APG Sattler 1973 

Syringa vulgaris 

Solanales: 

Oleaceae APG Sattler 1973 

Solanum dulcamara Solanaceae HGP Sattler 1973, 1977 

Sphenoclea zeylanica 

Apiales: 

Sphenocleaceae AGP Erbar 1995 

Levisticum vulgaris Apiaceae AGP Leins and Erbar 1985 

Astrantia major Apiaceae AGP Leins and Erbar 1985 

Hydrocotyle vulgaris Araliaceae AGP Erbar and Leins 1985 

Aralia elata 

Asterales: 

Araliaceae AGP Erbar and Leins 1988 

Bellis perennis Asteraceae AGP Erbar and Leins 1988 

Tragopogon pratensis Asteraceae AGP Sattler 1973 

Tagetes patula Asteraceae AGP Sattler 1973 

Acicarpha tribuloides Calyceraceae AGP Erbar 1993 

Campanula rotundifolia Campanulaceae AGP Erbar and Leins 1988 

Lobelia erinus Campanulaceae AGP Erbar and Leins 1988 

Downingia bacigalupii Campanulaceae AGP Kaplan 1967 

Selliera radicans Goodeniaceae AGP Erbar 1988; Leins and Erbar 1989 

Stylidium adnatum 

Dipsacales: 

Stylidaceae AGP Sattler 1973; Erbar 1992 

Valeriana officinalis 

Rosids: 

Valerianaceae AGP Sattler 1973 

Ampelopsis brevipedunculata Vitaceae HGP Gerrath and Posluszny 1988 

Fagonia cretica Zygophyllaceae HGP Ronse Decraene and Smets 1993 

Peganum harmala 

Cucurbitales: 

Zygophyllaceae HGP Ronse Decraene and Smets 1993 

Begonia dregei Begoniaceae Anom Gauthier 1950; Charpentier et al. 1989 

Hillebrandia sandwicensis 

Fabales: 

Begoniaceae Anom Charpentier et al. 1989 

Ceratonia siliqua Fabaceaea HGP Tucker 1992 

Bauhinia malabarica Fabaceaea HGP Tucker 1988a 

Neptunia pubescens Fabaceaea HGP Tucker 1988b 

Crudia choussyana Fabaceaea HGP Tucker 2001 

Albizia lophanta Fabaceae a 

HGP Sattler 1973 

Pisum sativum Fabaceaea HGP Sattler 1973 

Securidaca longepedunculata 

Rosales: 

Polygalaceae HGP Krüger and Robbertse 1988 

Rhamnus cathartica Rhamnaceae AGP? Sattler 1973 

Noltea africana Rhamnaceae AGP? Medan 1988 

Laportea canadensis Urticaceae HGP Sattler 1973 

Fragaria vesca Rosaceae HGP Sattler 1973 

Prunus virginiana Rosaceae HGP Evans and Dickinson 1999a 

Exochorda racemosa Rosaceae HGP Evans and Dickinson 1999a


Family 

Table A1 

(Continued) 

Ground 


Oemleria cerasiformis Rosaceae Anom Evans and Dickinson 1999a 

Physocarpus opulifolius Rosaceae HGP Evans and Dickinson 1999b 

Spiraea trilobata Rosaceae HGP Evans and Dickinson 1999b 

Sorbaria sorbifolia Rosaceae HGP Evans and Dickinson 1999b 

Fagales: 

Myrica gale Myricaceae HGP Sattler 1973 

Ostrya virginiana Betulaceae AGP Sattler 1973 

Quercus rubra Fagaceae AGP Sattler 1973 

Malpighiales: 

Carallia sp. Rhizophoraceae AGP? Juncosa 1988 

Euphorbia splendens Euphorbiaceae HGP Sattler 1973 

Hypericum perforatum Clusiaceae HGP Sattler 1973 

Geraniales: 

Pelargonium zonale Geraniaceae HGP Sattler 1973 

Geranium endressii Geraniaceae HGP Ronse Decraene and Smets 1993 

Brassicales: 

Cheiranthus cheiri Brassicaceae HGP Sattler 1973 

Iberis sempervirens Brassicaceae HGP Ronse Decraene and Smets 1993 

Sapindales: 

Schinus terebinthifolia Anacardiaceae HGP Ronse Decraene and Smets 1993 

Rhus typhina Anacardiaceae HGP Sattler 1973 

Melicope ternata Rutaceae HGP Ronse Decraene and Smets 1993 

Malvales: 

Malva neglecta Malvaceae HGP Sattler 1973 

Althaea rosea Malvaceae HGP Sattler 1973 

Helicteres isora Malvaceae HGP Jenny 1988 

Myrtales: 

Lythrum salicaria Lythraceae AGP? Sattler 1973 

Vochysia Vochysiaceae AGP Litt 1999; A. Litt and D. W. 

Stevenson, unpublished manuscript 

Fuchsia hybrida Onagraceae AGP Sattler 1973 

Santalales: 

Comandra umbellata Santalaceae AGP Sattler 1973 

Dilleniales: 

Hibbertia scandens Dilleniaceae HGP Sattler 1973 

Hibbertia huegelii Dilleniaceae HGP Tucker 1999 

Note. This is by no means a comprehensive compilation, but it illustrates the diversity of gyneocial development from a phylogenetic 

standpoint. The table indicates the presence of a hypogynous ground plan (HGP), receptacular-epigynous ground plan (RGP), or 

appendicular-epigynous ground plan (AGP). The abbreviation “Anom” indicates anomalous, which refers to unusual developmental 

programs that do not clearly fit into either HGP or AGP (see text). A question mark indicates that the ground plan is uncertain on the 

basis of evidence available—more research is needed (often the critical early stages of development are missing or not clearly illustrated). 

Order names follow APG II (2003); note that some families (Vitaceae) are still unassigned to order because of uncertainty regarding 

their phylogenetic position. 

a Families for which numerous representatives have been examined; only a fraction are indicated here. 

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Crane, S Blackmore, eds. Evolution, systematics and fossil history 

of the Hamamelidae. Vol 1. Introduction and “lower” Hamamelidae. 

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reevaluating the evolution of epigyny: data from ... - Mark Fishbein

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