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0 Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4
Received for publication June 8, 1999. Accepted for publication June 30, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: androecium • angiosperm • floral evolution • functional shifts • pollination • staminode • vestigial organs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Floral evolution often modifies the androecium, resulting in either stamen loss or transformation of stamen function from pollen production and presentation to alternate functions (Weberling, 1989
; Ronse Decraene and Smets, 1993, 1995
). With the loss of their defining function as producers of viable male gametophytes, stamens become staminodes. Staminodes are relatively uncommon, but widely distributed taxonomically, occurring in at least one species in 32.5% of angiosperm families and 54.4% of angiosperm genera. This latter figure largely reflects the abundance of orchid genera (>10 000 genera), most of which have staminodes; however, staminodes also occur in 
5.9% of the remaining angiosperm genera.
The fate of staminodes likely depends on whether they assume new functions. Nonfunctional staminodes arise as intermediate structures during reductive processes in the androecium. Decreases in stamen number typically involve progressive suppression of stamen development during morphogenesis (Tucker, 1988
; Ronse Decraene and Smets, 1995
) reflected by transition series in some groups. For example, among species of Bauhinia (Fabaceae) stamen number varies from ten (the ancestral state) to one, and "missing" stamens are absent or represented by stamen remnants (Endress, 1994
). Because nonfunctional staminodes probably interfere with interactions between flowers and pollen vectors, they should be lost quickly. Hence, when staminodes are largely nonfunctional, they should occur among only closely related taxa and be lost quickly from a lineage.
In contrast, functional staminodes should persist, becoming integral features of floral morphology and be represented in large lineages of taxa. Commonly implicated staminode roles include pollinator attraction through visual conspicuousness and/or provision of attractants and rewards, avoidance of self-pollination, and facilitation of pollen removal and receipt through various trigger-mechanisms. Evolutionarily, staminodes could attain functions either directly or indirectly after an intervening nonfunctional phase. Direct evolution from stamen to functional staminode likely occurs when stamens initially serve purposes in addition to pollen production and presentation (e.g., pollinator attraction). In this situation, functional constraints should favor "division of labor," which converts some stamens into staminodes specialized for the ancillary function and allows specialization of the remaining stamens on their primary role. Because of this history, staminodes that evolve directly should serve functions that stamens can also provide. In contrast, with indirect evolution, the nonfunctional phase preceding adoption of a new function allows staminodes to assume novel functions not expected of stamens. Hence, the taxonomic distribution of staminodes should reflect functional evolution and the variety of functions served by staminodes should reveal the course of that evolution.
Despite occurring widely, staminodes have not been examined synoptically, except as an incidental subject in recent reviews of androecium development by Ronse Decraene and Smets (1992, 1993, 1995)
. This lack of attention fosters an incomplete view of the morphological and functional evolution of angiosperm flowers. To rectify this deficiency, we review the incidence and proposed function of staminodes in angiosperms. To structure our study, we analyzed the possible evolutionary history of staminodes in the context of the Chase et al. (1993)
phylogeny of the angiosperms, which was inferred from the DNA sequence of most of the chloroplast rbcL gene. In particular, we focus on reductive trends in floral evolution associated with staminode origins and the role of function in the retention of staminodes in lineages.
Our interpretation of staminode evolutionary history hinges on the resolution of the Chase et al. (1993)
phylogeny, which is limited to the family level and above. Often, families comprise many species with differing androecial arrangements, and the resulting polymorphic staminode states at the family level may obscure the pattern of staminode evolution within a clade. To examine this possibility, we therefore present a more detailed analysis of staminode evolution in the Scrophulariales based on a DNA sequence analysis (compiled from Olmstead and Reeves, 1995
; Wolfe et al., 1997
; Wolfe, personal communication 1997
; Spangler and Olmstead, 1999
).
We consider staminodes only in hermaphroditic flowers. Staminodes also occur frequently in female flowers of dioecious and monoecious species (e.g. in dioecious genera of the Asteraceae: Kuijt, 1987
) due to incomplete suppression of male function. These staminodes may play important floral roles, such as the staminodes of Saurauia (Actinidiaceae), which provision pollinators with sterile pollen (Cane, 1993
). However, reduction of the entire androecium likely involves different genetic processes than partial reduction, so these staminode types warrant separate investigation.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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phylogeny of the angiosperms, although we also mention the implications of relevant deviations from this phylogeny identified by Soltis, Soltis, and Chase (1999)
. Chase et al. (1993)
constructed their phylogeny by parsimony analysis of DNA sequences for the chloroplast gene rbcL from 475 species representing all major taxonomic groups (subclasses and orders). This analysis resolved relationships within and above the order level and, in some cases, demonstrated paraphyly of families with several representatives (notably the Saxifragaceae, Grossulariaceae, and Scrophulariaceae). Soltis, Soltis, and Chase (1999)
expanded on the Chase analysis by considering both more species (560 total) and the sequences of two additional genes (the plastid gene alpB and the nuclear gene 18S). These two analyses agree on the relationships between most major clades. When relevant, we identify differences between the Chase et al. (1993)
and Soltis, Soltis, and Chase (1999)
phylogenies that bear on the interpretation of staminode evolution.
To examine the evolutionary history of staminodes, we determined androecial characters (number of stamen whorls, presence/absence of staminodes), floral design (symmetry, blossom type), primary pollen vector, and proposed staminode functionality (if found) for families considered by Chase et al. (1993)
using a variety of sources. In this analysis, "staminode" refers to both "nonfunctional" and "functional" stamen remnants. Reviews of androecium development and evolution in the flowering plants by Ronse Decraene and Smets (1992, 1993, 1995)
provided most androecial characteristics, whereas Cronquist (1981)
and family synopses in various floras provided information on floral design. We determined pollen vector and staminode functioning, when possible, from family synopses, reviews of pollination biology, and results of experimental pollination studies. Information on the relative frequency of different states of the androecium are based solely on the families considered by Chase et al. (1993)
.
We coded staminode states for single-state families as 0—staminode(s) absent, 1—complete whorls of staminodes present, or 2—partial whorls of staminodes present. A partial whorl of staminodes may involve from one to many staminodes, but the number of staminodes is always less than the number of stamens in an intact whorl. To enhance resolution by limiting the number of polymorphic codings (following Maddison and Maddison, 1992
), we coded polymorphic families as 01—states 0 and 1, 02—states 0 and 2, or 012—states 0, 1 and 2. We considered the gain of a single state as one step and the loss of a single state as one step, with no penalty for retaining polymorphisms. The character states were unordered, allowing state change in any direction.
We traced the staminode character onto the Chase et al. (1993)
phylogeny using MacClade 3.0 (Maddison and Maddison, 1992
). This software reconstructs character evolution by inferring ancestral character states that imply the fewest character state changes. Results are presented in the form of a cladogram. Cladogram branches are shaded with different patterns that represent inferred ancestral character states, whereas boxes at the tip of each terminal branch display the current character states of extant taxa. Unlike extant taxa, ancestral branches cannot be assigned more than one character state. Occasionally, several possible ancestral character states are equally parsimonious and in these cases the branch is shaded with a pattern indicating its equivocal status.
We present the resulting phylogeny in five sections, corresponding to the major clades recognized by the Chase et al. (1993)
analysis. A small, inset cladogram indicates the position of the clade in the larger phylogeny. In some cases, paraphyletic families of the Chase et al. (1993)
analysis divided along tribal boundaries. In these situations, we replaced the genus name with that of the representative tribe.
We also trace the evolution of staminodes within the Scrophulariales using MacClade (Maddison and Maddison, 1992
). We use Olmstead and Reeve's (1995)
rbcL and ndhF phylogeny of the Scrophulariales, with the addition of the Cheloneae (Scrophulariaceae) as determined by Wolfe et al.'s (1997)
and A. D. Wolfe's (personal communication 1997) rbcL phylogeny. We also inset Spangler and Olmstead's (1999)
rbcL and ndhF phylogeny of the Bignoniaceae. We assigned unordered character states for extant taxa as 0—stamen absent, 1—stamen represented by small rudimentary staminode, 2—stamen represented by large staminode, and 3—stamen fertile. We considered each character state change as one step.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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exhibit reduction of entire stamen whorls (Table 1). In particular, 34.0% of monocot, 46.2% of hamamelid/ranunculid, 67.7% of rosid, and 88.7% of asterid families considered by Chase et al. (1993)
include species with an ancestral stamen whorl that has been either incompletely or completely suppressed. Some species of the Magnoliales/Laurales clade also demonstrate reduction, but the prevalence of spirally arranged flowers confounds determination of stamen loss as discussed in the consideration of the Magnoliales/Laurales.
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Stamen reduction does not necessarily involve an entire ancestral stamen whorl. Often, individual stamens within a whorl are suppressed through partial reduction of a stamen whorl. The number of stamens involved vary from one to many, although the number of reduced stamens must be less than the number of fertile stamens in the ancestral whorl. Reduction of a partial stamen whorl occurs only in more derived clades, with 19.1% of monocot, 15.4% of hamamelid/ranunculid, 34.4% of rosid, and 23.9% of asterid families having species with either an incompletely or completely reduced partial whorl(s) (Table 1). Loss of a partial whorl is strongly associated with zygomorphy (98.9% of 11 961 genera with a reduced partial whorl(s) are zygomorphic). Staminodes represent these partial whorls in 88.9% of monocot, 100% of hamamelid/ranunculid, 33.3% of rosid, and 58.8% of asterid families that include species with a reduced partial whorl(s).
Most families, except most asterids and those with few genera, demonstrate variable staminode states and androecial configurations. This suggests that the appropriate level to study staminode evolution is the subtribe or genus. However, because floral trends differ in each major clade, analysis of androecial characters in the context of the Chase et al. (1993)
phylogeny illustrates different general patterns of stamen loss, staminode formation and staminode function. Therefore, we first discuss floral trends, staminode origin, and staminode functions individually for each major clade and then consider common themes for angiosperms as a whole.
Magnoliales/Laurales
Floral trends
Two general floral types, both with or without staminodes, characterize the Magnoliales and Laurales: (1) short-lived, large, complex conspicuous flowers ("magnolids") and (2) longer lived, small, simple inconspicuous flowers ("laurids"). Beetle-pollinated magnolid-type flowers are composed of numerous, spirally arranged parts, and often include an inner whorl of large, petaloid staminodes. These flowers typify the Idiospermaceae, Calycanthaceae, Nymphaeaceae, Barclayaceae, Austrobaileyaceae, Degeneriaceae (see Fig. 1), Himantandraceae, Eupomatiaceae, and Annonaceae. Laurid-type flowers are comprised of a reduced number of cyclically arranged parts, contain inner and outer whorls of small staminodes, and are pollinated by diverse small insects. Laurid-type flowers characterize the Lauraceae (see Fig. 2), Monimiaceae, Hernandiaceae, Cabombaceae, Amborellaceae, Schisandraceae, Chloranthaceae, Canellaceae, and Myristicaceae. The Winteraceae contain flowers of both types.
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phylogeny.
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). Alternatively, staminodes may have originated as a consequence of the spiral arrangement of floral primordia. In spirally arranged flowers, floral organs often transgress into each other through intermediate forms, forming carpellodes, staminodes, staminodial petals, etc. (Ronse Decraene and Smets, 1993
).
In contrast, staminodes in cyclical laurid-type flowers arise in association with stamen whorl reduction. For example, the Lauraceae illustrate a transition series in which flowers of less derived members of this family likely produced four stamen whorls, whereas in flowers of more derived taxa the innermost stamen whorl ranges from fertile stamens (Dodecadenia,—Allen, 1948
) to staminodes (Eusideroxylon,—Hutchinson, 1964
) to absent (Endiandra,—Hutchinson, 1964
; Misantheca,—Allen, 1948
). An entire whorl of staminodes is present in the related family Gomortegaceae (not considered by Chase et al. [1993]
: see Soltis, Soltis, and Chase [1999]
). Within the Lauraceae, Hernandiaceae, and Monimiaceae, paired nectaries on each side of fertile stamens have been identified as staminodes (Hutchinson, 1964
; Correll and Correll, 1982
); however, studies of flower bud development refute this interpretation (Endress, 1980
).
Staminode function
In magnolid-type flowers, staminodes function primarily to prevent self-pollination. Petaloid inner staminodes between the carpels and stamens of these protogynous, self-compatible flowers bend inward following female phase (Grant, 1950
; Faegri and van der Pijl, 1979
; Miller, 1989
; Endress, 1994
), effectively shielding the receptive stigmas. This staminode movement occurs in all magnolid-type flowers with staminodes, except the modified trap flowers of the Nymphaeaceae (Schneider, 1976
; Faegri and van der Pijl, 1979
). Flowers without inner staminodes show alternate mechanisms for deterring self-pollination, such as stigmas raised above the stamens (Magnoliaceae and Winteraceae: Friis and Endress, 1990
) and stigma abscission (Annonaceae: Endress, 1994
).
Secondary functions of inner staminodes in magnolid-type flowers include pollinator attraction through visual and olfactory signals and the provision of rewards. Contrasting coloured staminodes in the Calycanthaceae and Himantandraceae (Endress, 1984a, b
) increase perianth conspicuousness, whereas the staminodes of the Austrobaileyaceae, Eupomatiaceae, and Degeneriaceae emit scent (Endress, 1994
). Staminodes sometimes provide rewards, secreting food bodies in the Degeneriaceae (Endress, 1984b
), Calycanthaceae (Grant, 1950
), and Eupomatiaceae (Endress, 1994
).
In laurid-type flowers, staminodes attract pollinators through the provision of nectar (Woodson and Schery, 1948
; Endress, 1984b, 1986
). Although these flowers are also protogynous and self-compatible, they lack obvious mechanisms to prevent autogamy.
Monocotyledons
Floral trends
Three main floral types exist in the monocots, depending on pollination syndrome. Animal-pollinated species tend to produce flowers either singly (e.g., Colchicaceae, Trilliaceae, some Iridaceae), arranged in loose inflorescences (e.g., Amaryllidaceae, Liliaceae, Alstroemeriaceae), or condensed into dense inflorescences (e.g., Araceae, and some Pontederiaceae, Costaceae, Xanthorreaceae, Zingiberaceae) and can be split into two groups based on flower shape. Regular flowers, commonly pollinated by diverse, small insects, occur throughout animal-pollinated monocots and likely represent the ancestral condition (Dahlgren and Clifford, 1982
). Irregular flowers, with more specialized pollinators (typically bees and birds), evolved in the Commelinales-Zingiberales clade, the Orchidaceae, and the Iridaceae (Fig. 4). Wind-pollinated plants, with small, reduced flowers generally crowded into dense spikes or heads, predominate in the Poaceae-Typhaceae clade and occur independently in the Potamogetonaceae, Pandanaceae, and Arecaceae.
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Whorled staminodes originated at least four times in monocots, with three origins restricted to single families (Fig. 4). Clades with whorled staminodes tend to be derived, indicating that staminode whorls are generally not maintained and do not persist. Although the Commelinaceae–Pontederiaceae clade seems to be an exception to this conclusion, the inferred ancestral character state of whorled staminodes present and absent seems unlikely. Most Pontederiaceae have two stamen whorls (Cronquist, 1981
) and given the seeming irreversibility of stamen whorl reduction in angiosperms (discussed in the rosid section), the ancestor must also have had two stamen whorls. This argues for independent staminode origins in both families. Indeed, Faden (2000)
claimed that staminodes evolved at least five times within the Commelinaceae. Hence, whorled staminodes probably evolved more than five times within monocots.
Reduction of partial stamen whorls occurs in taxa with specialized animal-pollinated flowers (37.8% of monocot families). Loss of some stamens within a stamen whorl is strongly associated with zygomorphy (with the exception of the Iridaceae and some actinomorphic Pontederiaceae) and thus predominates in specialized insect-pollinated plants. In these groups, staminodes generally represent the reduced partial whorl either as small rudiments (Heliconiaceae, Musaceae, and Strelitzaceae) or as large, elaborate organs (Orchidaceae, Marantaceae, Zingiberaceae, and Costaceae). Partial staminode whorls originated independently at least twice in the monocots (Fig. 4) and typify all species of the Orchidaceae and most species of the Zingiberales (except the Musaceae-Lowiaceae clade, Fig. 4: in the phylogeny of Soltis, Soltis, and Chase [1999]
the Lowiaceae is a sister family to the Strelitziaceae, rather than the Musaceae, so complete stamen loss may have occurred independently at least twice within the Zingiberales). This retention of partial whorls of staminodes within lineages indicates that they are maintained by natural selection in these groups.
Reduction of stamens within whorls also occurs in some wind-pollinated plants with only one or two fertile stamens per flower (as in some members of the Poaceae, Pandanaceae, Eriocaulaceae, Cyperaceae, Sparaginaceae, and Typhaceae). However, in contrast to animal-pollinated taxa, this reduction of the androecium resulted in complete stamen loss with no retention of staminodes.
Direct evolution of functional staminodes from functional stamens likely occurred in the Commelineae tribe of the Commelinaceae. Unlike a stamen reductive trend, the staminodes persist and function in all species as part of a pollen mimicry system (Vogel, 1978
; Faden, 1992
). Within the tribe, a transition series is evident in which lower "fodder" stamens become larger and more conspicuous and upper stamens become less conspicuous. Upper stamens remain fertile, whereas lower stamens produce smaller and fewer pollen grains (Tinantia—Simpson, Neff, and Dieringer, 1986
) until they become staminodial (Commelina). Staminodes may be rewarding (producing sterile pollen) or nonrewarding (Yeo, 1992
). At all stages of this transition series, the lower stamens (or staminodes) remain functional and hence likely evolved without an intervening nonfunctional stage.
Staminode function
Whorls of staminodes in monocots generally appear to be nonfunctional and transitional in nature, as they are rarely elaborated to take over other roles, except in the Xyridaceae (not included in the Chase et al. [1993]
analysis, aligned with the Poales by Soltis, Soltis, and Chase [1999]
). Xyris flowers contain an outer whorl of large bifid staminodes tipped with tufts of moniliform hairs (Woodson and Schery, 1944
; Kral, 1966
). These staminodes may function as secondary pollen presenters (Yeo, 1992
), but their similarity to staminodes of other pollen flowers, such as Commelina (Commelinaceae), suggests an analogous function. In Commelina, staminodes mimic larger amounts of pollen (Osche, 1983
per Endress, 1994
; Faden, 2000
) and may stimulate bees to carry out pollen-collecting movements (Vogel, 1978
).
In contrast, partial whorls of staminodes often become integrated components of monocot flower structure, as seen in the Orchidaceae and within the Zingiberales. Two lines evolved from ancestral orchids, whose flowers included only the lateral two anthers of the inner whorl and one stamen of the outer whorl and no staminodes (Burns-Balogh and Bernhardt, 1985
). In monandrous orchids the remaining anthers of the inner whorl evolved into staminodes that range from small protuberances to flared appendages on the column ("column wings") and function to direct and control pollinator movement (Burns-Balogh and Bernhardt, 1985
). In diandrous orchids the remaining outer stamen became a staminode (Abraham and Vatsala, 1981
) that forms a fully integrated component of the trap in the Cypripedioideae (Burns-Balogh and Bernhardt, 1985
). This staminode, elaborated in a variety of ways (see Braem [1988]
for staminode diversity in Paphipedilum), generally mimics attractive structures such as brood sites (Paphipedilum rothschildianum—Fig. 5, Atwood, 1985
) and nectar (Paphiopedilum villosum—Banziger, 1996
).
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analysis, but commonly aligned with the Marantaceae [Cronquist, 1981
; Kress, 1990]
or Zingiberaceae [Soltis, Soltis, and Chase, 1999]
). In the complicated lip flowers of the Cannaceae, Costaceae, and Zingiberaceae, varying numbers of petaloid staminodes form the labellum (often the most conspicuous element of the flower: Faegri and van der Pijl, 1979
; Hickey and King, 1988
) and act with the perianth as advertising organs (Maas, 1972
; Smith, 1987
). A very different flower structure exists in the bee-pollinated Marantaceae, where staminodes are involved in a trigger mechanism for explosive pollination (see Kennedy, 1978
; Rogers, 1984
; Yeo, 1992
). A petaloid (cucullate) staminode encloses the pollen-presenting style, whereas a hooded and lobed staminode orients the pollinator and braces the mechanism. When a bee touches a trigger appendage of the cucullate staminode, the style releases and contacts the pollinator, achieving both pollen removal and pollen release.
Such radical shifts in floral roles have not occurred in other monocot families, such as the remainder of the Zingiberales and some Commelinaceae with partial staminode whorls. In the Musaceae, Heliconiaceae, Strelitzaceae, and Lowiaceae (Zingiberales) pollinated by hummingbirds, bats, and flies (Cronquist, 1981
; Heywood, 1985
; Wolf and Stiles, 1989
), only one stamen of the outer whorl has been reduced, usually represented by a small staminode (absent in the Lowiaceae). This staminode may direct pollinators' tongues towards the nectaries (Endress, 1994
). The pollen flowers of the Commelineae tribe (Commelinaceae: Fig. 6) exhibit a trend towards increased anther dimorphism as part of a pollen mimicry system (Vogel, 1978
, Faden, 1992
, 2000). Lower "fodder" stamens/staminodes attract pollinators and provide (or mimic) fertile or sterile pollen, whereas the inconspicuous upper stamens place fertile pollen onto the pollinator (Vogel, 1978
; Yeo, 1992
).
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phylogeny suggests at least five origins of entire staminode whorls, as that phylogeny included the staminode-bearing Circaeasteraceae and it proposed that the Sabiaceae and Proteaceae are not sister families. Members of the Ranunculaceae and Papaveraceae demonstrate reductive series from spiral polyandry and polycycly to only one whorl of fertile stamens. A small proportion of species in both families exhibit entire whorls of staminodes (Cronquist, 1981
).
Partial staminode whorls originated once in the hamamelids and the ranunculids (Fig. 7), associated with loss of a partial stamen whorl in the Sabiaceae and within the Proteaceae of the animal-pollinated hamamelids (Fig. 7). Specialized zygomorphic flowers of each group (e.g., Conospermum [Proteaceae] and Meliosma [Sabiaceae]) have only two fertile stamens from an original whorl of four or five, with the remainder represented by staminodes (Cronquist, 1981
).
Staminode function
Whorled staminodes are relatively rare, small, and most likely transitional in nature in the ranunculids, with the exception of Aquilegia (Ranunculaceae). In Aquilegia, one or two inner whorls of broad, membranous staminodes form a sheath around the ovaries (Brayshaw, 1989
). According to Brayshaw (1989)
, this sheath protects the ovaries against damage by pollinators.
In the hamamelids, partial staminode whorls form components of explosive pollination mechanisms. In Conospermum (Proteaceae), small staminodes at the base of the style hold the style back and act as triggers (Holm, 1978
). When a pollinator probing for nectar touches the staminodes, the style is released and contacts the pollinator. Following style contact, the anthers of the two fertile stamens explode and dust the pollinator with pollen. A very different mechanism (see van Beusekom, 1971
) exists in some Meliosma (Sabiaceae), in which a complex of two fertile stamens and three fleshy staminodes encircles the pistil of open flowers with the top of the style protruding. Cavities in the staminodes enclose the anthers of the fertile stamens, which dehisce before flower anthesis. When a pollinator touches the flower, the stamen filaments release, discharging pollen explosively.
Rosidae
Floral trends
Most flowers in the Rosidae produce nectar as a reward, are open and radially symmetric, and are pollinated by diverse small insects. Trends towards more specialized insect pollination occur within most families, with some members of a family typically developing irregular petals (such as Lopezia and Gaura of the Onagraceae) and becoming zygomorphic. Papilionaceous flowers, pollinated primarily by large-bodied bees, characterize the Trigoniaceae, Fabaceae, and Polygalaceae. Tubular flowers occur rarely, formed by extension and fusion of the hypanthium in Lythraceae, Punicaceae, and Combretaceae. Pollen flowers, which are pollinated primarily by pollen-collecting female bees, occur throughout the Rosidae in the Molluginaceae–Aizoaceae clade (Fig. 8) and in families such as the Tiliaceae, Paeoniaceae, Ochnaceae, Rosaceae, Fabaceae, and Datiscaceae. Regular flowers specialized for pollination by large animals occur within the Bombaceae–Dipterocarpaceae clade and the Onagraceae–Myrtaceae clade, including species pollinated by honeyeaters (some Malvaceae and Myrtaceae), bats (Bombaceae, Malvaceae, Tiliaceae), and small rodents (some Melastomataceae). Wind pollination characterizes families within most clades of the Rosid II group (Leitneriaceae, Bataceae, Haloragaceae) and occurs within the Viscaceae, Amaranthaceae, and Aceraceae. Wind pollination occurs less frequently in the derived rosids, being common in only the Reduced Rosids I group.
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). Reduction seems to involve both inner and outer whorls of stamens, but such observations are confounded by positional shifts of the stamen primordia in the developing buds of some flowers, causing the two whorls to switch positions (Ronse Decraene and Smets, 1993
).
Reduction of a stamen whorl in rosids is never reversed. Often, pollen flowers (except those with poricidal anthers as the Melastomataceae) and flowers specialized to large animal pollinators produce abundant pollen through a secondary increase of stamen number. Stamen number increases through subdivision of fertile stamen primordia (Ronse Decraene and Smets, 1992
), rather than re-initiation of suppressed stamen primordia. For example, in the Sterculiaceae, flowers have one whorl of stamens and one whorl of staminodes present or absent. In Dombeya and Guazuma, five stamen primordia of the fertile whorl have split to form 15 stamens, whereas the reduced whorl remains as five staminodes (Robyns, 1964
; Young, Schaller, and Strand, 1984
). Similar development of staminode whorls characterizes the Tiliaceae and some Myrtaceae.
Staminodes occasionally replace reduced stamen whorls. Staminode whorls evolved independently at least 14 times within the Rosidae (Figs. 8 and 9), and the Soltis, Soltis, and Chase (1999)
phylogeny, which includes the staminode-bearing Meliaceae and Corynocarpaceae, indicates two additional origins. Within the Rosidae, whorls of staminodes evolve most commonly within individual families (indicated by character states with staminodes both present and absent) and typify only small and monotypic families (Pterostemonoideae and Moringaceae: Fig 8), indicating that staminodes seldom persist. This lack of persistence probably also characterizes the Celastraceae–Parnassiaceae clade (Fig. 9), despite the equivocal ancestral character state. Whorled staminodes seem an unlikely ancestral state, given the presence of two fertile whorls in some Celastraceae and the irreversible nature of stamen whorl loss among other angiosperms. Therefore, the most parsimonious ancestral character (if the phylogeny is correct) is whorled staminodes present and absent, which does not indicate staminode persistence.
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), but loss through stamen fusion occurs in some taxa (Cucurbitaceae: Ronse Decraene and Smets, 1995
). Reduction of partial stamen whorls is strongly associated with zygomorphy (82% of species with partial stamen loss are zygomorphic compared to 0% of species with intact stamen whorls) and specialized entomophilous pollination syndromes. The Rosidae demonstrate the complete spectrum of stamen reduction, from flowers with staminodes producing sterile pollen (Anacardium—Freitas and Paxton, 1996
), or flowers with unstable androecia and variable numbers of fertile stamens and staminodes, as in Pelargonium (Geraniaceae: McDonald and Van der Walt, 1992
) and caesalpinioid Fabaceae (Hokche and Ramirez, 1990
; Tucker, 1998
), to flowers that have completely lost reduced stamens (the Bretschneideraceae–Tropaeolaceae clade, Polygalaceae, and papilionaceous Fabaceae).
Partial staminode whorls evolved independently at least eight times within the rosids (Figs. 8 and 9), and the Soltis, Soltis, and Chase (1999)
phylogeny, which includes the staminode-bearing Frankeniaceae (allied with the Droseraceae-Plumbaginaceae clade), indicates an additional origin. Within the Rosids, partial whorls of staminodes typically evolve within families, and they typify only small families, such as the Trigoniaceae and Vochysiaceae (Fig. 9).
Staminode function
Whorls of staminodes seem transitional in most rosid groups, being small and unelaborated, but occasionally they are secondarily modified to take over other diverse roles. In some cases, staminodes signal pollinators as part of the perianth, as in the contrasting colored staminodes of several Linum species (Linaceae: Heywood, 1985
). Staminodes also attract pollinators by mimicking rewarding structures. For example, in the pollen flowers of Sparmannia (Tiliaceae) an outer whorl of moniliform and bright yellow staminodes mimic large amounts of pollen (Vogel, 1978
). Alternatively, in the Parnassiaceae the shiny, multifid, and gland-tipped staminodes resemble nectaries (Muller, 1883
; Knuth, 1908
; Richards, 1986
) and emit scent (Proctor and Yeo, 1972
). Some staminodes provide rewards. In the Corynocarpaceae (Hemsley, 1903
) and Ochnaceae (Cronquist, 1981
) staminodes secrete nectar, with those of the Ochnaceae forming a brightly colored intrastaminal nectary. The staminodes of some beetle-pollinated Verticordia species may present pollen secondarily, receiving pollen from the fertile stamens before flower anthesis (Holm, 1978
; Yeo, 1992
). Staminode movements in the slightly protandrous Theobroma (Fig. 10), Herrania, and Dombeya of the Sterculiaceae prevent selfing by mediating insect movement within the flower (Posnette, 1950
; Cuatrecasas, 1964
; Sampayan, 1966
; and Entwistle, 1972
). During male phase, staminodes closely surround the style (Young et al., 1987
) and pollinating midges enter the flower from vertical petal ligules, which act as a landing site (Young, 1984
; Young, Schaller, and Strand, 1984
) and exit without contacting the style. The staminodes flare outwards from the style during female phase and petal ligules reflex to a horizontal position (Young et al., 1987
). Pollinators then land on the staminodes, crawl down between the staminodes and the style, and exit the flower through the petal ligules (Young, 1984
; Young, Schaller, and Strand, 1984
). Staminode whorls may also enclose and protect the ovaries as in some Ochnaceae in which an inner whorl of fused staminodes forms a tube surrounding the ovaries (Cronquist, 1981
). In many bird-pollinated, feather flowers (Verticordia and Darwinia of the Myrtaceae), staminodes prevent nectar robbing by bending inwards (sometimes along with fertile stamens) to cover the nectary disk (Yeo, 1992
).
|
; Plitmann, Raven, and Breedlove, 1973
; Heywood, 1985
). Anacardium flowers have one fertile stamen surrounded by shorter staminodes. According to Freitas and Paxton (1996)
, these staminodes provide sterile pollen as a reward to pollinating insects.
|
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), and Napoleonaea in the Lecythidaceae, which is allied with the Asterid III clade, especially the Sapotaceae (Morton et al., 1997
; Soltis, Soltis, and Chase, 1999
). Four of these origins are limited to single families. Staminodes occur in only a small proportion of species comprising these families (except Theophrastaceae). These staminodes are generally small and rudimentary (e.g., Salmolus, Primulaceae; Kupicha [1983]
: Myrsine africana, Myrsinaceae; P. Caris, Katholieke Universiteit Leuven, personal communication), but the corollas of Sideroxylon (Sapotaceae), Jacquinia (Theophrastaceae; Fig. 14) and Napoleonaea (Lecythidaceae) include large petaloid staminodes.
|
; Prance, 1976
; Mori, Prance, and Bolten, 1978
). In the Asterid I clade, staminodes persist after partial reduction of the stamen whorl in only in a few Solanaceae (Eichler, 1875
; Murray, 1945
; Mair, 1977
) and species in the Scrophulariales with bilabiate flowers (Fig. 13).
|
phylogeny and variable staminode states within families obscure the evolution and persistence of staminodes within the order. A more detailed phylogeny of the Scrophulariales reveals the varying representation of the fifth stamen throughout the group (Fig. 15). In most cases, the staminode is small and rudimentary but a large, elaborate staminode has evolved independently in flowers of the Cheloneae tribe (Scrophulariaceae) and Jacaranda (Bignoniaceae). Continued stamen loss occurs in many Lamiaceae and Scrophulariaceae through reduction of one of the two stamen pairs (Cronquist, 1981
), and in some species of Lamiaceae by further reduction of one theca of each anther (Cantino, 1992
). In scattered genera throughout the Scrophulariales apparent reversion to actinomorphy has been accompanied by restoration of the suppressed stamen (see Fig. 15) such as Verbascum (Scrophulariaceae), Oroxylum (Bignoniaceae), and Verbena (Verbenaceae). These independent reversions, along with staminode re-appearance in derived taxa (Scrophulariaceae II, Fig. 15) from ancestors with complete loss of the fifth stamen, suggest that partial reduction of stamen whorls is reversible. Such reversion is possible because genes controlling initial stages of stamen development persist. For example, in Antirrhinum (Kampny and Canne-Hilliker, 1988
) and Digitalis (Singh, 1979
), species that do not produce staminodes, the primordium of the fifth stamen forms during early ontogeny but is subsequently suppressed. Interestingly, Endress' (1999)
phylogenetic analysis revealed that reversion was less prevalent among derived taxa in the Scrophulariales than among basal taxa, indicating that genetic control of the fifth stamen degraded during the diversification of this order.
|
; Dandy, 1967
). In the Lecythidaceae, staminodes either form a showy corona, which replaces the function of the perianth (Napoleonaea: Weberling, 1989
), or they contribute to the androecial hood of only nectar-producing species in which the hood typically restricts floral access to only large-bodied, long-tongued bees (Couratari, Eschweilera, Lecythis: Prance, 1976
; Mori, Prance, and Bolten, 1978
). Finally, the single staminode of bee-pollinated Cheloneae (Fig. 16) and Jacaranda has been ascribed diverse functions, including serving as a nectar guide (Delpino, 1868–1875), a lever mechanism that promotes pollen exchange with pollinators (Torchio, 1974
; Walker-Larsen and Harder, unpublished data), a barrier mechanism to prevent nectar robbing (Straw, 1956
), and a purchase for alighting pollinators (Pennell, 1948
). Of these proposed mechanisms, experimental evidence favors the lever and barrier mechanisms, which both promote pollen exchange with pollinators (Walker-Larsen and Harder, unpublished data). In contrast, the staminode is apparently functionless in derived, bird-pollinated species of the Cheloneae (Walker-Larsen and Harder, unpublished data).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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), Lauraceae (Allen, 1948
; Hutchinson, 1964
), and many rosid families (e.g., Sterculiaceae: Robyns, 1964
; Crassulaceae: Cronquist, 1981
; Zygophyllaceae: Ronse Decraene and Smets, 1995
). The number and arrangement of staminodes directly reflect patterns of stamen loss, i.e., reduction of entire or partial stamen whorls.
In animal-pollinated plants, reduction of entire stamen whorls usually involves actinomorphic flowers pollinated by diverse small insects with more than one whorl of fertile stamens (Stebbins, 1974
; Ronse Decraene and Smets, 1993, 1995
). Reallocation of resources to more, smaller flowers and/or adaptations that increase efficiency of pollen dispersal likely prompt reduced pollen production per flower through stamen loss. These adaptations include pollen packaging and pollen-dispensing mechanisms that limit pollen removal by individual pollinators but maximize pollen dispersal (reviewed by Harder and Thomson, 1989
), and more precise contact between pollinators and pollen presenters (including anthers) or pollinators and stigmas. Both adaptations increase the proportions of pollen grains delivered to stigmas.
Reduction of partial stamen whorls accompanies the development of zygomorphy (Stebbins, 1974
; Ronse Decraene and Smets, 1995
; Endress, 1999
) and specialization towards pollination by particular pollinators. Zygomorphic flowers control pollinator entry, enhancing the precision of pollen placement (Richards, 1986
) often through repositioning of stamens (Stebbins, 1974
). Loss of stamens during the evolution of zygomorphy likely reflects the increased efficiency of pollen transfer (Faegri and van der Pijl, 1979
; Richards, 1986
) and developmental constraints. In the Scrophulariales and Zingiberales, which have zygomorphic flowers with one whorl of stamens, anthers of fertile stamens have been repositioned to the top of the corolla tube and loss of one stamen has resulted. In the Scrophulariales, reversion to radially symmetric flowers with an entire whorl of stamens occurs independently in several lines (Verbena [Verbenaceae], Oroxylum [Bignoniaceae], Verbascum [Scrophulariaceae]), and peloric mutants of usually zygomorphic species also lose stamen suppression (as in Antirrhinum mutants lacking cyc and dich genes: Coen, 1996
; Luo et al., 1996
). These results indicate close links in the genetic control of zygomorphy and suppression of partial stamen whorls.
Genetic control of the loss of entire vs. partial stamen whorls differs. Loss of stamen whorls seems irreversible, as secondary stamen increases (common to many Rosidae families) involve the division of fertile stamen primordia, not re-appearance of previously reduced whorls (Ronse Decraene and Smets, 1992
). In contrast, reduction of partial stamen whorls appears evolutionarily plastic. For example, apparent reversion to actinomorphy has occurred in many taxa scattered throughout the Scrophulariales and is always accompanied by restoration of the suppressed stamen.
This difference in genetic control may explain why staminodes seem to arise more frequently from reduction of a partial stamen whorl than from reduction of an entire whorl. In particular, staminodes occur in 50.8% of families with evidence of reduction of a partial stamen whorl, but in only 14.5% of families that exhibit some reduction of an entire stamen whorl. After loss of an entire stamen whorl, limited opportunity for the modification of nonfunctional staminode whorls exists, given the permanence of stamen loss. In contrast, the evolutionary flexibility of partial staminode whorls might allow repeated opportunistic involvement of staminodes in floral function. Certainly, this appears to be the case for the Scrophulariales, as taxa with staminodes (Cheloneae) have developed from taxa characterized by staminode loss (Fig. 15). Alternatively, the higher incidence of partial staminode whorls may be related to the relatively recent evolutionary development of zygomorphy, resulting in a higher incidence of nonfunctional stamen remnants.
A strong association between stamen reduction and staminode formation, evidenced by transition series from functional stamens to remnant staminodes to functional staminodes in many lineages (e.g., Sterculiaceae, Scrophulariales, Lecythidaceae) argues for indirect evolution of most functional staminodes. We proposed that indirect evolution of staminodes affords greater flexibility of function than direct evolution by allowing staminodes to take over roles not performed by stamens. This pattern is illustrated by the frequent involvement of staminodes in both preventing self-pollination and explosive pollination. Common mechanisms preventing self-pollination involve the separation of pollen and stigma presentation, either in time (dichogamy: reviewed by Lloyd and Webb, 1986
), or in space (herkogamy: reviewed by Webb and Lloyd, 1986
). In contrast, staminodes prevent self-pollination through movements that shield receptive stigmas during pollen presentation. Clearly, fertile stamens could not play such a role.
Similarly, mechanisms for explosive pollination (although rare in flowering plants in general) commonly employ staminodes, but not stamens, to hold back the stamens and/or style in untripped flowers, and act as triggers for their release. The diverse mechanisms generally involve large, conspicuous staminode(s) that enclose the stamens and/or style (Marantaceae—Kennedy, 1978
; Rogers, 1984
; Yeo, 1992
; Meliosma [Sabiaceae]—van Beusekom, 1971
; Lopezieae [Onagraceae]—Eyde and Morgan, 1973
; Plitmann, Raven, and Breedlove, 1973
; Heywood, 1985
: but see Conospermum [Proteaceae]—Holm, 1978
). In flowers without staminodes, such as Chamaepericlymenum (Cornaceae; Mosquin, 1985
), sunbird-pollinated Loranthaceae (Feehan, 1985
), Hyptis (Lamiaceae; Brantjes and De Vos, 1981
; Keller and Armbruster, 1989
), Kalmia (Ericaceae: Henshaw, 1915
) and some Fabaceae (Medicago, Genista, Ulex, and Sarothamnus—Arroyo, 1981
; Proctor and Yeo, 1992
), the corolla encloses the stamens and/or style and acts as a trigger. Rarely, tension is provided by the exploding organ itself, as in Stylidium (Stylidiaceae—Erbar, 1992
). In these flowers, the bent region of the column (comprising anthers and stigmas) is strongly reinforced by layers of thick-walled cells, which produce a rapid movement of the column after contact by a pollinator (Findlay and Findlay, 1975
).
Although most functional staminodes appear to have evolved indirectly from stamen remnants, functional staminodes can evolve directly from functional stamens, as illustrated by the Commelinaceae. In the tribe Commelineae, the direct evolution of fertile stamens to sterile "fodder" stamens has occurred as part of a pollen mimicry system (Vogel, 1978
). In this case, the ancestral stamen functions of pollinator attraction and pollen presentation have been divided between staminodes and fertile stamens. This case supports our earlier proposal that functional staminodes that evolve directly from fertile stamens do not perform novel functions.
The persistence of functional staminodes within a lineage likely relates to the number of roles they perform. Single-function staminodes could be lost rapidly during floral diversification, should shifts in pollination render such staminodes nonfunctional. In contrast, a multifunctional staminode is less likely to become nonfunctional and subsequently lost. Indeed, multifunctional staminodes characterize groups such as the Magnoliales/Laurales, some Zingiberales, and Orchidaceae, for which staminodes have become integral components of flower structure.
Functional staminodes evolve either directly from fertile stamens or indirectly from nonfunctional stamen remnants. Most functional staminodes evolved indirectly from nonfunctional stamen remnants. The diverse functioning of these staminodes, even among closely related lineages such as the Sterculiaceae and Tiliaceae, suggests that modification of stamen remnants can provide an evolutionary "quick fix" for functional problems specific to different pollination mechanisms. The prevalence of reductive trends in stamen number throughout the angiosperms suggests that nonfunctional stamen remnants arise frequently. Presumably, modification of a nonfunctional structure would involve fewer constraints than modification of a multifunctional floral organ. As a result, evolution of staminodes could occur more quickly and show greater flexibility than that of other floral structures. However, the transitional nature of remnant staminodes creates only a brief opportunity for evolutionary modification. That modification of such transitional structures has occurred regularly reflects the rapid evolution of angiosperm flowers.
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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