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The evolution of unisexual flowers: morphological and functional convergence results from diverse developmental transitions¹

Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 USA

Received for publication September 17, 2004. Accepted for publication April 8, 2005.

ABSTRACT

Unisexual flower morphology was examined within a phylogenetic context in order to identify developmental transitions associated with the multiple origins of dioecy in flowering plants. Historically, two categories of unisexual flowers have been recognized: type I flowers exhibit rudiments of the nonfunctional organ type, while type II flowers bear no vestigial sexual organs. Mapping of these flower types onto a composite phylogeny shows that type II morphology is homoplasious and has resulted from at least four distinct evolutionary developmental pathways. The historical assignment of unisexual flowers into only two morphological types has masked important developmental and evolutionary dynamics.

Key Words: character evolution • dioecy • flower development • heterochrony • homeosis • homoplasy • unisexual flowers

Among angiosperms, dioecy (separate male and female plants) is thought to have evolved more than 100 times to account for the 160 plant families that include dioecious species (Charlesworth and Guttman, 1999 ). This number is likely an underestimate because dioecy may have multiple independent evolutionary origins within some families (e.g., Arecaceae, Rosaceae, Euphorbiaceae). Therefore, dioecy may be considered a preeminent example of homoplasy.

Homoplasy is the repeated evolution of the "same" character state in separate groups of organisms and results from convergence, parallelism, or evolutionary reversals (Hufford, 1996 ). Homoplasy has received considerable attention from phylogeneticists (e.g., Sanderson and Donoghue, 1989 ; Philippe et al., 1996 ; Ree and Donoghue, 1998 ; Wiens et al., 2003 ). Because homoplasy is difficult to identify, it is often viewed as noise that complicates analyses of phylogenetic relationships (Brooks, 1996 ). Recently homoplasy has become a subject of interest in its own right (e.g., Sanderson and Hufford, 1996 ) and is viewed as a critical source of information about a variety of evolutionary phenomena, including adaptation (Larson and Losos, 1996 ; Barrett et al., 1997 ).

The role of natural selection in the homoplastic origins of dioecy has been a focus of intensive research. Hypotheses for the origin of dioecy from hermaphroditism consider many genetic and ecological factors. These include avoidance of inbreeding (Charlesworth and Charlesworth, 1978b ; Thomson and Barrett, 1981 ), sexual selection (Freeman et al., 1980 ), and optimal resource allocation (Bawa, 1980 ; Charlesworth and Charlesworth, 1981 ; Thomson and Brunet, 1990 ; Brunet and Charlesworth, 1995 ; Seger and Eckhart, 1996 ). Empirical and theoretical studies also have identified possible evolutionary pathways to dioecy under these selective forces (reviewed in Barrett, 2002 ). Transitions to dioecy from distyly (e.g., Darwin, 1877 ; Barrett and Shore, 1987 ; Barrett, 1990 ), from monoecy (e.g., Lloyd, 1980 ; Renner and Ricklefs, 1995 ; Renner and Won, 2001 ; Dorken and Barrett, 2004 ), and from gynodioecy (e.g., Charlesworth and Charlesworth, 1978a ; Ashman, 1999 ; Charlesworth, 1999 ; Delph, 2003 ) have been explored. Despite multiple evolutionary forces and diverse intermediates, these evolutionary transitions all have the same end result—functionally unisexual individuals.

In contrast to the depth and sophistication of analyses of the advantages of dioecy and the multiple evolutionary pathways that result in dioecy, knowledge of the actual morphology and underlying developmental modifications associated with these transitions is surprisingly sparse. The ontogeny of hermaphroditic flowers has been modified repeatedly to result in developmental programs that yield either staminate or carpellate flowers. Yet, the changes that underlie the transition from bisexual to unisexual flower production have not been thoroughly investigated. Are there multiple developmental routes to unisexuality associated with the apparent functional convergence?

Since Darwin (1877) , two morphological types of unisexual flowers have been recognized (Fig. 1). One type exhibits "plain rudiments of male organs" in carpellate flowers and in staminate flowers "rudiments of the female organs," (p. 278) while the other type exhibits no rudiments of the opposite sex. The recognition of these two categories of unisexual flower morphology has persisted in the literature on unisexual flowers (e.g., Heslop-Harrison, 1957 , 1958 ; Dellaporta and Calderon-Urrea, 1993 ; Lebel-Hardenack and Grant, 1997 ; Ainsworth 2000 ), as has the notion that these distinct morphological types also differ in patterns of early development. The first type of flower, hereafter referred to as type I, is unisexual by abortion. Initiation of androecial and gynoecial organs occurs in all flowers, followed by the termination of development in one or the other organ set. The second type of flower, hereafter referred to as type II, is unisexual from inception. The floral meristem initiates only androecial or gynoecial organs and does not go through a hermaphroditic stage.

View larger version (16K): [in this window] [in a new window]   Fig. 1. Idealized diagrams representing the reproductive organs and receptacles of the two types of unisexual flowers. The staminate type I flower is shown with a nonfunctional, vestigial gynoecium in the center. The carpellate type I flower is shown with four nonfunctional, vestigial stamens. Type II flowers have only a single category of reproductive organ. Black = functional carpels; white = functional stamens; hatched = vestigial organs

View larger version (18K): [in this window] [in a new window]   Fig. 2. Four potential modes of developmental modification underlying the evolutionary transition from hermaphroditic to unisexual flowers: (1) sterilization of androecium or gynoecium postinitiation, (type I at maturity); (2) complete loss of organ type/whorl coincident with an origin of dioecy (type II at maturity); (3) initial origin of a type I intermediate with subsequent loss of organ initiation (type II at maturity); and (4) although seemingly unlikely, an initial loss of organ initiation with subsequent gain of rudimentary organs (type II at maturity) is also possible. Black = functional carpels; white = functional stamens; hatched = vestigial organs

MATERIALS AND METHODS

In order to address the distribution and frequency of unisexual flower types, it is necessary to compile a data set of the type of unisexual flowers characteristic of dioecious taxa. Because our ultimate interest is the homoplastic origins of dioecy, we did not include the unisexual flowers of monoecious taxa in this data set. Renner and Ricklefs (1995) estimated that of the 240000 species of flowering plants, 14 620 are dioecious. A list of the dioecious genera used in their study was the starting point in assembling a list of dioecious taxa for this study. Several other comprehensive reviews (Yampolsky and Yampolsky, 1922 ; Lindsay, 1930 ; Delph et al., 1996 ; Heilbuth, 2000 ) provided additional occurrences. Descriptions of mature flower morphology were obtained from various sources including floras (e.g., Radford et al., 1968 ; Harden, 2000 ), developmental morphology texts (e.g., Payer, 1857 ; Sattler, 1973 ), and the primary literature. References to the primary literature were obtained by searching databases such as ISI Web of Science (website http://www.isiknowledge.com) and archives of several botanical journals available through JSTOR (2002). Informative descriptions of floral morphology and development could not be found in the literature for all dioecious species; however, the resulting data set includes 477 of the 994 genera that contain dioecious species and spans 36 of the 37 angiosperm orders in which dioecy occurs (Renner and Ricklefs, 1995 , website http://www.umsl.edu/biosrenn/dioecy.pdf) and is therefore likely to be a representative sample.

From the data on mature morphology, each taxon was assigned to one of the two basic types of unisexual flowers based on the presence or absence of rudiments of the gynoecium or androecium (type I = rudiments present; type II = rudiments absent). For each species, staminate and carpellate flower types were considered separately. The overall frequency of the two unisexual flower types was tabulated by hand from these data.

Using MacClade (Maddison and Maddison, 2001 ), unisexual flower types were mapped onto a composite angiosperm phylogeny (Table 1, Fig. 3; see Weiblen et al., 2000 , for a discussion of the use of composite phylogenies). This large composite phylogeny was assembled by integrating 29 published phylogenies using the framework of Soltis et al. (2000) . The phylogenies were mixed in hierarchy between family and genus level in order to best fit the taxonomic unit used by the systematists and the data collected in this study. Due to this mixture, the general term "taxon" is used to describe the taxonomic unit at branch tips. To investigate transitions between flower types, all taxa were scored for a character with the following four states: (0) no dioecy present in taxon, (1) type I flowers present in taxon, (2) type II flowers present in taxon, (3) both type I and II flowers present in taxon. Dioecious taxa with unknown flower types were scored 1/2 to indicate that the presence or absence of rudiments was not mentioned in the literature (a Microsoft Excel file containing coding and source for each taxon is available in the Supplemental Data accompanying the online version of this article). Staminate flower data and carpellate flower data were analyzed separately. The frequencies of character changes under ACCTRAN (accelerated transitions) optimization for resolving options were calculated for each tree. The ACCTRAN optimization yielded a more conservative estimate of independent origins than the DELTRAN (delayed transitions) optimization.

View larger version (25K): [in this window] [in a new window]   Fig. 3. Summary of the relationship between individual trees in the assembled angiosperm tree. Numbers refer to individual trees in Table 1

RESULTS

Frequency of unisexual flower types
Morphological data on mature flowers were obtained for 482 genera (678 species) from 124 families (Appendix, see Supplemental Data accompanying online version of this article; taxonomy based on GRIN taxonomy [Germplasm Resources Information Network {Wiersema and León, 1999 }]). Table 2 summarizes the frequency of type I and type II morphology for both staminate and carpellate flowers. Useful information for staminate flowers was more common in the literature and led in part to differing totals for staminate and carpellate flowers. Type I flowers (unisexual by abortion) are more frequent overall among dioecious species examined (Table 2). For species in which the morphology of both flower sexes was documented, staminate and carpellate flowers were typically of the same type (both type I or both type II). However, flower type differed between staminate and carpellate flowers in 57 cases (9% of species examined). For a small number of species, a single source indicated that the species produced flowers of the same gender with clear rudiments and also flowers that lacked rudiments. These are recorded as "type I and II." Species recorded as "type I or II" had conflicting reports for flowers of the same gender in the literature.

View larger version (21K): [in this window] [in a new window]   Fig. 4. Unisexual flower type mapped onto a phylogeny of Asparagales (adapted from Soltis et al., 2000 , fig. 3 ). Asparagus, Behnia, and Ruscus with type I flowers are nested within a clade otherwise characterized by hermaphroditic flowers (pathway 1)

View larger version (40K): [in this window] [in a new window]   Fig. 6. Unisexual flower type mapped onto a phylogeny of Restionaceae (adapted from Eldenas and Linder, 2000 ). Ischyrolepis with type II flowers is nested among genera with type I flowers (pathway 3)

Extensive research on the sexual diversification of flowering plants has shown that dioecy is homoplastic at multiple levels. Dioecy has evolved numerous times; it may arise under a diverse set of selective forces and also via several distinct evolutionary pathways (e.g., Charlesworth and Charlesworth, 1978b ; Bawa, 1980 ; Freeman et al., 1980 ; Thomson and Barrett, 1981 ; Brunet and Charlesworth, 1995 ; Barrett, 2002 ; Delph, 2003 ). We show that the evolution of dioecy also ultimately involves morphological convergence resulting from multiple types of developmental transitions to unisexual flowers.

Developmental evolution
The distribution of flower types among angiosperm lineages suggests that evolutionary transitions from hermaphroditic to unisexual flowers have occurred via three of the four possible pathways of developmental modification (see Fig. 2): (1) hermaphroditic flowers to type I flowers (unisexual by abortion; e.g., Fig. 4), (2) hermaphroditic flowers to type II flowers (unisexual from inception; e.g., Fig. 5), and (3) hermaphroditic flowers to type I unisexual flowers to type II unisexual flowers (e.g., Fig. 6). The morphological category "type II flowers" (unisexual from inception) results from two of these patterns of developmental evolution. Further consideration of taxa with type II flowers, however, suggests that at least four possible homoplastic origins of type II morphology can be recognized (summarized in Fig. 7). For convenience of discussion, these four types of origins are referred to as "indirect" (essentially pathway 3 in Fig. 2), and three types of "direct" (encompassed by pathway 2 in Fig. 2): direct–early mutation, direct–homeosis, and direct–extinction.

View larger version (15K): [in this window] [in a new window]   Fig. 5. Unisexual flower type mapped onto a phylogeny of Austrobaileyales (adapted from Qiu et al., 2000 ). Schisandra and Kadsura with type II flowers are nested with a clade characterized by hermaphroditic flowers (pathway 2)

View larger version (26K): [in this window] [in a new window]   Fig. 7. Developmental transitions leading from an hermaphroditic flower to a unisexual flower. Black = functional carpels; white = functional stamens; hatched = vestigial organs

Indirect origins of type II flowers were relatively rare in the data set; however, numerous genera and families contained species with type I flowers and species with type II flowers (see Appendix). Our ability to identify transitions between these flower types was hampered by the lack of species-level phylogenetic analyses for these groups. Further testing of hypotheses for indirect origins of type II unisexual flowers, and of heterochrony, requires more detailed (preferably species-level) phylogenies of those clades with mixed unisexual flower types and thorough developmental analyses of key species within those clades.

In addition to indirect origins via type I intermediates, taxa with type II flowers (unisexual from inception) also have been derived within hermaphroditic lineages (e.g., Fig. 5). Three alternative scenarios for the direct developmental evolution of type II flowers from hermaphroditic flowers can be proposed. The first two include the instantaneous loss of reproductive organs coincident with the origin of unisexuality either by homeosis (the transformation of one organ type into a different organ type [Baum and Donoghue, 2002 ]; direct–homeosis) or through absence of initiation (direct–early mutation). A homeotic origin of unisexuality would result from the conversion of stamens into carpels and vice versa (Fig. 7). Evidence for the origin of unisexuality via homeosis requires an accounting of the number and position of all reproductive organs in the ancestral hermaphroditic state and in the derived unisexual state. For example, if carpellate flowers arose by homeosis, the ancestral bisexual flowers may have five stamens and five carpels, whereas carpellate flowers of the dioecious species would have no stamens and 10 carpels. The "carpellization of stamens" has been described for Carica papaya (Storey, 1969 ). The putative bisexual ancestral state includes five or 10 stamens (in one or two whorls, respectively) and five carpels. In dioecious C. papaya, carpellate flowers have 10 carpels in two whorls and lack any additional whorl of staminode structures. The author concluded that the stamens in the carpellate flower "have become transmuted into sterile carpels comprising part of the pistillate flower pistil and have lost their identity as stamens" (p. 494). In Arabidopsis thaliana, loci that may play a role in homeotic transformations have been identified. For example, the SUPERMAN gene has a role in establishing the boundary between stamens and carpels. In superman mutants "stamen primordia proliferate inwards at the expense of carpel primordia" (Smyth, 2001 , p. R84). The converse also has been found in other mutants of the B function genes (i.e., the ABC model of flower development, Coen and Meyerowitz, 1991 ; see Ainsworth, 2000 , for discussion of MADS-box genes in dioecious plants). These mutants are effectively female with homeotic transformations of stamens to carpels (Schwarz-Sommer et al., 1990 ).

Type II flowers may also arise directly from hermaphroditic flowers via mutations in the process involved in organ initiation (direct–early mutation; Fig. 7). In contrast to a homeotic origin, the identity of the organs is not altered; rather, they are entirely absent. In this case, the number of functional organs in the androecium and gynoecium of unisexual flowers would not be increased relative to the ancestral state. The genus Lomandra (Lomandraceae) provides a possible example. Lomandra is comprised entirely of dioecious species with type II female flowers (Payer, 1857 ; Watson and Dallwitz, 1992 ). Chase et al. (1995) place Lomandra sister to the hermaphroditic genus Sowerbaea (Lomandraceae). The flowers of Sowerbaea have 3–6 stamens and three carpels. The female flowers of Lomandra have three carpels as well. Because carpel number remains the same, the stamens were most likely lost rather than transformed during the transition to unisexuality.

The third possible scenario that would result in the apparent "direct" evolution of type II flowers involves extinction of taxa (direct–extinction). In this case, type II flowers arise in the manner described for indirect origins, that is via a type I intermediate; however, there is subsequent extinction of type I taxa from the clade. The distribution of flower types within a phylogeny would (erroneously) indicate a direct transition from hermaphroditic to unisexual flowers, whereas the actual developmental evolution required multiple steps. This scenario might be expected for those lineages in which the origin of dioecy is relatively ancient or in which extinction rates are particularly high.

Developmental and phylogenetic analyses of additional dioecious taxa are needed to fully assess these hypotheses for the homoplastic origins of type II unisexual flowers. Nevertheless, it is clear that although unisexual flowers that lack rudiments of the nonfunctional organs share a common morphology, they should not be considered as a single type. This "type II morphology" is the result of convergence via several distinct evolutionary developmental transitions. Similarly, exploration of the development of unisexual flowers that bear rudiments of nonfunctional organs (type I flowers) is likely to show that this is not a single type either. Termination of androecial or gynoecial development could occur at many different stages and by diverse mechanisms (Ainsworth, 2000 ; Mitchell, 2003 ), all of which would result in a unisexual flower with type I morphology.

Recognition of multiple developmental origins of unisexual flowers may further refine investigations of the origins of dioecy and evolutionary dynamics within dioecious lineages. For example, does the rarity of the indirect origin of type II flowers (unisexual from inception; pathway 3 in Figs. 2, 7) suggest that nonfunctional reproductive organs are maintained by natural selection, perhaps by requirements for pollinator recognition (e.g., Ågren and Schemske, 1991 ; Vamosi and Otto, 2002 )? Are particular developmental transitions associated with particular pathways for the origin of dioecy? Because gynodioecy typically evolves via cytoplasmic male sterility loci (Saumitou-Laprade et al., 1994 ) that disrupt stamen development post-initiation (Goldberg et al., 1993 ), the presence of type I staminate flowers (bearing rudimentary stamens) in a dioecious taxon might suggest that the evolution of separate sexes occurred via a gynodioecious intermediate.

Conclusions
The historically typological approach to categorization of unisexual flowers has masked evolutionary dynamics and transitions among "types." Rather than sorting unisexual flowers into mutually exclusive types (Fig. 1), the morphology of unisexual flowers can be viewed as the result of modifications within a multifaceted developmental framework (Fig. 7). Loss of reproductive organ function can occur via diverse mechanisms and at any point in the developmental continuum, from organ inception to maturation.

Our analysis has focused on morphology and developmental transitions from hermaphroditic to unisexual flowers. The evolution of flower development, however, occurs within the context of organismal history. For example, the different pathways for the evolution of dioecy invoke the origin of unisexual flowers at different stages (Webb, 1999 ). When dioecy evolves via gynodioecy, the evolution of unisexual flowers is coincident with the evolution of unisexual individuals (females). In contrast, an origin via monoecy involves the origin of unisexual flowers prior to the separation of sexes. Future work should attempt to integrate information about floral morphology and development into analyses of particular pathways of the evolution of dioecy.

FOOTNOTES

¹ The authors thank William (Ned) Friedman, Tom Ranker, Jill Miller, Larry Hufford, and Steven Vamosi for comments on earlier drafts of this manuscript. P. K. D. was supported by National Science Foundation DEB 9982489, and C. H. M. is grateful for support from the Department of Ecology and Evolutionary Biology at the University of Colorado.

² Author for correspondence (e-mail: pamela.diggle{at}colorado.edu )

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