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Structure and Development |
2Department of Evolution, Ecology and Organismal Biology, Ohio State University, 1315 Kinnear Road, Columbus, Ohio 43212 USA; 3Botanical Institute, University of Copenhagen, Gothersgade 140, 1123 Copenhagen K, Denmark
Received for publication March 5, 2002. Accepted for publication June 4, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: anther • column • development • Epidendroideae • Orchidaceae • pollinium
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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studied pollinium development with particular reference to how different numbers are produced and examined differences among sectile pollinia (Freudenstein and Rasmussen, 1997
). Rasmussen (1985
, 1986a
) has characterized some of the variation observed in pollinium stalks. As part of a continuing study of characters relevant to phylogenetic analysis in orchids, here we investigate two characters related to anther position and shape—the relative position of the anther on the column and the orientation of pollinia within the anther.
Variation in anther position on the column has been recognized as a systematically important feature at least since the time of Bentham (1881)
. At least three states have been recognized (Dressler and Dodson, 1960
; Rasmussen, 1982
, 1986b
): erect, reflexed, and incumbent (bent forward or inflexed). The erect state is most common outside of epidendroids, while the reflexed state is known only from some Diseae (Orchidoideae; Dressler, 1993
). The incumbent state is often considered a primary defining feature of Epidendroideae (Dressler, 1981
). Given that there is variation even among taxa with incumbent anthers (i.e., the difference between vandoids and other epidendroids, the former recognized as an additional state by Rasmussen, 1986b
), as well as recent indications that one incumbent group, Vanilloideae, is only distantly related to the rest, the need to better understand this variation is clear.
The position of the pollinia within the anther (as seen in a transverse section) has had a similarly long use in orchid systematics, again known at least since the time of Bentham (1881)
, who distinguished between pollinia that are "collateral and parallel, as in Epidendroideae" and those that are "fore and aft in each pair." Dressler and Dodson (1960)
termed the latter state, known only from the epidendroids, "superposed," while Freudenstein and Rasmussen (1996)
called the former, much more widespread state, "juxtaposed." The character has been used in cladistic analyses of the family (e.g., Burns-Balogh and Funk, 1986
; Freudenstein and Rasmussen, 1999
), although essentially nothing is known about how the orientations of the pollinia are achieved. Dressler (1993)
suggested that the superposed condition arises by rotation of the thecae outward, relative to the juxtaposed condition, but as with any character that is found in a large number of taxa, there is the possibility that not all instances of the morphology arise in the same way.
In this study we analyze the morphology of fully developed anthers as well as developmental sequences from representatives of various tribes in order to discover how these states are achieved, forming the basis for homology hypotheses in these characters that will be subject to testing in phylogenetic analysis. Increasing our knowledge of the details of these character transformations also facilitates our understanding of character evolution in the family.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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For paraffin sections, bud series were fixed in FAA (formaldehyde-acetic acid-ethanol; Johansen, 1940
) for 24 h and then stored in 70% ethanol until ready for use. This material was dehydrated in an ethanol-tertiary butyl alcohol series and embedded in Paraplast (Oxford Labwork, St. Louis, Missouri, USA). Sections were cut at 8–10 µm on a rotary microtome and stained in Safranin O counterstained either with Alcian Blue or Fast Green (Sigma, St. Louis, Missouri, USA) (Joel, 1983
; Ruzin, 1999
).
Material for glycol methacrylate (GMA) sectioning was fixed in 3% glutaraldehyde in 0.1 mol/L Sørensen's phosphate buffer (using KH2PO4, pH 7.0; Ruzin, 1999
), to which a few drops of Tween (Fisher Scientific, Fair Lawn, New Jersey, USA) were added to aid in wetting the material. Columns were held under vacuum in the fixative at room temperature for 30 min, followed by 24 h at 4°C. The material was then washed twice in 0.1 mol/L phosphate buffer and twice in distilled water for at least 1 h in each wash. The tissue was then chemically dehydrated using an excess of acidified dimethoxypropane at 4°C for a minimum of 12 h (Lin, Falk, and Stocking, 1977
). This was followed by two washes in n-butanol (1 h), and three changes of glycol methacrylate monomer blend (10% polyethylene glycol [PEG] 400, 89.5% glycolmethacrylate monomer, 0.5% 2,2'-azobis [2-methylpropionitrile]) with agitation at 4°C (Feder and O'Brien, 1968
; O'Brien and McCully, 1981
). The material was stored in this last change of monomer blend in the dark at 4°C until it was embedded. Specimens were embedded in gelatin capsules with fresh GMA monomer blend and polymerized for 3 d at 48°C. Sections were cut at 3 µm with glass knives on an LKB microtome (Stockholm, Sweden) and stained with 0.5% Toluidine Blue O at pH 3.6 or 4.4 (O'Brien and McCully, 1981
).
The taxonomic scheme used here follows Dressler (1993)
except where emended by Chase, Freudenstein, and Cameron (in press).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), the base of the anther where it attaches to the column (and the abscission layer), and the region of developing sporogenous tissue are important references in defining the overall shape of the anther. Another critical feature is the stomium that is present on each theca. We use the terms introrse and latrorse to refer to the shape of the anther (Fig. 2)—whether the thecae are directed with their stomia positioned adaxially (introrse) or laterally outward (latrorse). There is another anther morphology in addition to introrse and latrorse that is uncommon (and unnamed), in which the stomia are positioned laterally inward. The superposed pollinium state could in theory occur in either the latter or in a latrorse anther, while juxtaposed pollinia are associated only with an introrse anther.
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Pollinium orientation
Sobraliinae
Elleanthus pollinia exhibit an essentially juxtaposed morphology (Fig. 3), with only slight tendencies toward a superposed arrangement in that the outer anther sacs are positioned slightly lower than the inner ones. The stomium is located on the adaxial surface between the anther sacs in each theca. The anther morphology is correspondingly introrse.
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Coelogyniinae
Coelogyne, Dendrochilum, Pholidota, and Pleione differ in the degree to which their pollinia are superposed, revealing a continuum from juxtaposed to fully superposed pollinia. In transverse section, it is clear that the pollinia of Pleione are essentially juxtaposed. Those of Coelogyne (Fig. 6) and Dendrochilum (not shown here) are superposed approximately 45°. The stomium is located in the anther wall between the two pollinia of each theca, facing outward. An early developmental stage examined for Coelogyne shows the pollinia oriented at this angle as well (not shown here); the earliest developmental stages were not observed. Pholidota shows a much greater extent of superposition (Fig. 7), with the pollinia positioned at an angle of nearly 90° compared to the juxtaposed arrangement. The stomium is again located on the outer anther wall between the two pollinia. The central portion of the connective in these taxa as seen in transverse section is thickened and continuous, especially in Pholidota, where it extends approximately halfway down between the thecae. In a mature, dehisced anther, the remnant thecal walls remain connected at the center of the anther.
Vandoid epidendroids
The vandoid orchids exhibit a common anther morphology across the groups examined here. Degree of superposition is variable, with some species having pollinia that are essentially juxtaposed. The central thecal partitions typically disintegrate at maturity, as has been noted by Bentham (1881)
and Dressler (1981)
as characteristic of the vandoid orchids. At dehiscence, this results in thecal wall remnants that are attached at the lower outer side of each theca, along the thickened outer wall. Examples of this pattern include Pelatantheria (Fig. 8), Kingidium, and Ascocentrum (Vandeae; not shown), Polystachya (Polystachyeae; Fig. 9), Corallorhiza (Corallorhizinae; Fig. 10), Promenaea, and Gongora from Maxillarieae, and Eulophia (Fig. 11) and Cymbidium from Cymbidieae. In most of these, the pollinia are superposed approximately 45° with relation to the adaxial surface of the anther as seen in transverse section, with Corallorhiza exhibiting a greater degree of superposition.
Many vandoid taxa, such as Eulophia, Gongora, Oncidium, and some Cymbidium, have only two pollinia, which may be variously lobed or folded. Because there are not two pollinia per theca that clearly demonstrate the superposed condition in these taxa, additional criteria must be used to ascertain the presence of the superposed state. In these cases, we can use the position of the stomium as an indication of thecal orientation. In addition, some taxa have partially fused pollinium pairs, such as Eulophia streptopetala (Fig. 11). In certain sections/planes, the pollinia appear free in each theca but are clearly fused in other sections/planes. If we use this free portion as a guide to their orientation, it is clear that they also are superposed approximately 45°, with a corresponding stomium placement between the two free pollinium ends.
Odontoglossum (Fig. 12) shows an almost juxtaposed arrangement of its two lobed pollinia. This is representative of many species in Oncidiinae. In all other respects, the anther is vandoid and undergoes early incumbency.
Anther orientation
We found considerable variation among taxa with respect to the zone(s) that experience growth as well as the timing of the growth that causes the anther to become incumbent. This variation circumscribes three groups of taxa (vanilloid, non-vandoid epidendroid, vandoid epidendroid; Table 1).
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), as well as Pogonia (Ames, 1922
).
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It is important to note that not all epidendroid anthers examined were incumbent. For example, Epidendrum imatophyllum was bent only ca. 45°, while Dendrobium secundum was fully erect (no incumbency). The failure of the anthers in these two taxa to become completely incumbent is conjectured to be related to their pollination syndrome. The floral color and morphology of both of these species suggest bird pollination, a less common pollination syndrome for this largely entomophilous family.
Vandoid epidendroids exhibit very little growth in the column zone. Growth in the basal and sporogenous zones occurs very early in ontogeny while the anther primordium is still completely undifferentiated (current study and Kurzweil, 1987a
). The bending occurs so early that we were unable to obtain material of anther primordia prior to that reorientation. The earliest, still rather undifferentiated, stages that were observable resemble the earliest stage of Cymbidium (Fig. 22), in which the anther is already incumbent. More advanced stages of Cymbidium (Figs. 23, 24), Xylobium (Fig. 25), and Polystachya (Fig. 26) show clearly an incumbent anther that results from growth toward the rostellum apex. Because of the early onset of this growth, differences in the resulting anther morphology are highly significant and yield a much differently shaped anther than that observed in the nonvandoids. Whereas in the latter the anther essentially completes development before it is reoriented into the incumbent position, in the vandoids the anther actually grows into the incumbent orientation by cell proliferation in the basal and sporogenous zones prior to and as differentiation occurs. Sporogenous tissue also experiences this growth, leading to the often curved and unequal pollinia seen in the vandoids (Figs. 23–26).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Because most orchids achieve their final thecal orientation very early in ontogeny (Freudenstein and Rasmussen, 1996
), and because of the complications of anther incumbency occurring simultaneously with thecal growth, in most cases it was not possible to observe development of thecal orientation directly. Hence, our conclusions about the nature of pollinium and thecal orientation are based largely on final anther morphology, interpreted in the context of previous studies of development of the anther (Hirmer, 1920
; Rasmussen, 1986b
; Kurzweil, 1987a
; Freudenstein and Rasmussen, 1996
).
When determining pollinium orientation, several phenomena must be considered in order to make an accurate determination. It is important that pollinium orientation be determined in anthers that have not yet dehisced because the relative positions of the pollinia may change when the pollinarium is removed. This has been noted for Polystachya in particular (Dressler, 1993
), where in some species the pollinia assume the superposed orientation only after they are removed from the anther. Obviously, in those anthers that have only two pollinia (one in each theca), arrangement of the pollinia themselves cannot be used as a determinant of orientation. In those cases, position of the stomium and direction of any pollinium lobing are the only features that provide a clue to thecal and pollinium orientation.
A consideration of previous ontogenetic data along with the present elucidation of anther structure leads to a general model for the development of the various pollinium orientations seen in the Epidendroideae (Fig. 27). The observations made by Kurzweil (1987a
, b
, 1988
, 1993
), Freudenstein and Rasmussen (1996)
, and Kocyan and Endress (2001)
indicate that the anther primordia in all currently recognized orchid subfamilies (Apostasioideae, Vanilloideae, Cypripedioideae, Orchidoideae, Epidendroideae) are flattened to triangular in earliest stages as seen in transverse section. These primordia attain their final morphology by differential growth of the thecae, which in effect results in a "rotation" or reorientation of the thecae during development, based on the observation that the stomia and pollinia (or sporogenous zones) are seen to change their relative positions. Different taxa vary greatly with respect to the degree of these changes.
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). The introrse anther morphology was illustrated for various members of Vanilloideae, Orchidoideae, and Epidendroideae (Rasmussen, 1982
; Freudenstein and Rasmussen, 1996
), for Neuwiedia and Apostasia (Apostasioideae; Vermeulen, 1966
, Fig. 2B; Kocyan and Endress, 2001
), and Phragmipedium (Cypripedioideae; Vermeulen, 1966
, Fig. 3B). Introrse anthers characterize all orchids except those with superposed pollinia. A functional significance of the introrse morphology can be imagined for insect-pollinated orchids. The vast majority of these taxa also possess a zygomorphic floral morphology and pollinia that have an adhesive secreted by the dorsiventrally located rostellum. Directing anther dehiscence toward the center of the flower, where the insect is located, would presumably be most efficient for facilitating pollen transfer.
Superposed pollinia have only thus far been reported from Epidendroideae, although illustrations of the anther in some orchidoid genera such as Prescottia (Dressler, 1993
:35) and Gavilea (Rasmussen, 1982
:24) suggest that the morphology might also be present in these groups. The investigations here were limited to epidendroids. Sobralia is unusual in having superposed pollinia (also visible in Hirmer's [1920
] illustration of Sobralia schoenbrunnensis)—a state unknown in other "basal" epidendroid orchids. The pollinia are elongate and twisted, which is also unusual. Superposed pollinia are usually associated with a stipe (Dressler, 1981
), but there is none present in Sobralia. The position of the stomium and development of the Sobralia anther indicate that the anthers in this genus experience an "over-rotation" as opposed to the juxtaposed condition to produce the final morphology in which the pollinia are superposed. Given the unusually late stage at which this final reorientation occurs in Sobralia, it appears to be a terminal addition to the normal developmental program of the epidendroid anther. The development and structural uniqueness of the superposed pollinia in Sobralia argue for recognizing them as a state distinct from that seen in the vandoids. Although no material was available for study here, illustrations of the nonvandoid Chysis in Schill and Pfeiffer (1977)
and Sheehan and Sheehan (1994)
suggest that this genus might have a superposed morphology similar to Sobralia. Chysis is not especially closely related to Sobralia (Cameron et al., 1999
; Goldman et al., 2001
), suggesting that this state would have been derived independently in each.
The anthers in Coelogyneae vary from introrse to latrorse, with corresponding juxtaposed to superposed pollinia. Pleione, with its introrse anthers and juxtaposed pollinia, falls at the base of the tribe in the analysis of Gravendeel and de Vogel (2000)
, suggesting that juxtaposed pollinia (and introrse anthers) are the plesiomorphic state for the tribe. Coelogyne and Dendrochilum exhibit anthers that are halfway between introrse and latrorse, with their pollinia superposed at ca. 45°. The Pholidota anther is nearly completely latrorse, with fully superposed pollinia and stomia that are directed laterally. Our model of thecal orientation suggests that the superposed members of Coelogyneae achieve that state by an incomplete reorientation of the thecae with respect to the primordial state. Therefore, we consider this to be a second distinct state of superposed pollinia.
The interpretation of the anthers in the aforementioned nonvandoid groups is straightforward, in part because anther bending occurs late, meaning that the thecal orientation itself is not affected much by the bending. The nonvandoid anther develops nearly to its full extent before it becomes incumbent late in ontogeny (Rasmussen, 1986b
; Kurzweil, 1987a
). In contrast, understanding the vandoid pollinium orientation requires that the process of anther bending also be considered concurrently. Anther bending happens very early during ontogeny—simultaneously with thecal growth. This strictly vandoid phenomenon greatly affects the final anther shape and complicates observations and interpretation.
The superposed pollinium arrangement in the vandoid groups (Cymbidieae, Maxillarieae, Vandeae, Calypsoeae) arises in a largely uniform manner in all taxa examined and is similar to that observed in Coelogyneae. However, the vandoid anther is not just an anther in which the thecae have not fully reoriented (as in Coelogyneae). If we take as a starting point a flattened anther primordium with nascent thecae, it is possible to understand how the final vandoid morphology arises by considering the simultaneous effects of dorsiventral anther bending and thecal reorientation. As the thecae develop and the first sporogenous tissue forms, the anther apex and adaxial face are simultaneously growing forward and then downward (toward the rostellum). The nascent stomium would have been approximately lateral on the primordial anther; as they reorient, the thecae become turned inward to varying degrees, resulting in the differing degrees of superposition. Little reorientation results in the most strongly superposed pollinia, while greater reorientation brings the thecae closer to a juxtaposed arrangement. The layers of tissue nearest the abaxial surface of the anther grow to a greater degree than those near the adaxial face, in essence stretching the abaxial side as it bends over relative to the adaxial side. This results in the characteristic abaxial stretching of pollinia that is often observed in vandoid anthers (see Figs. 23 and 26). The stomium runs from deep within the center of the anther on each theca, across the face of each theca to its side (see Rasmussen, 1986b
, fig. 18, for a depiction of the vandoid anther). This stomial topology is consistent with the scenario for development described here, as is the location of the central thecal wall remnants. These remnants result from the drying of the central partition of each theca at maturity and are found in the center of the anther on the connective in Coelogyne and Pholidota (Figs. 6–7), but on the lower outer wall of the anther in Pelatantheria, Polystachya, and Eulophia (Figs. 8, 9, 11). We interpret these remnant-attachment points to be homologous among all of these anthers. This description of vandoid anther development is consistent with the images presented by Kurzweil (1987a)
, as well as the observations of Freudenstein and Rasmussen (1996)
of early development in introrse orchid anthers.
The pollinium/thecal position morphologies shown in the model (Fig. 27) are arranged in an ontogenetic series by degree of thecal reorientation. This model supports Dressler's (1993)
suggestion that the superposed state evolved "by a rotation of anther cells." If we assign phylogenetic polarity to this series based on our current understanding of relationships in the family (e.g., Cameron et al., 1999
; Freudenstein and Rasmussen, 1999
; Freudenstein and Chase, 2001
), it is clear that the introrse morphology is plesiomorphic within Epidendroideae, with the others being derived. Comparison of ontogenetic and phylogenetic direction suggests that the most plesiomorphic state, the introrse anther with juxtaposed pollinia, is ontogenetically one of the most derived (in terms of the amount of thecal reorientation that occurs). In contrast, the highly phylogenetically derived vandoids have latrorse anthers with superposed pollinia that experience little or no reorientation. A comparison of the directions of ontogenetic and phylogenetic series, in conjunction with what we know about the timing of anther development, suggest that contrasting heterochronic shifts may be responsible for the two different types of superposed pollinia observed here. In Sobralia, a prolongation of the growth phase of the thecae (observed here in the late development of the superposed state) suggests the pattern of hypermorphosis (Alberch et al., 1979
), while in the case of Coelogyne and the vandoids, early cessation of reorientation relative to development of the rest of the flower suggests progenesis. Orchid anthers may be the only cases for which heterochrony is described in normal anther development, because most previous conclusions of heterochrony in anther form have been based on cases of altered floral morphology associated with self-pollination (Hill, 1996
).
Anther orientation characters
The incumbent anthers in the vanilloids and in nonvandoid epidendroids have similarities in their development—each has a significant component of elongation in the upper portion of the column. Given the phylogenetic placement of these groups, this elongation must be considered a plesiomorphic feature in the Epidendroideae. Whether the column elongation in the Epidendroideae and Vanilloideae is a symplesiomorphy is not clear, because it could also have been derived independently in these two groups. This question is outside the scope of the present study.
The principal difference between incumbent anthers in these subfamilies is in the nature of the growth that occurs in the anther itself. Nonvandoid epidendroids exhibit general enlargement of the anther, but this growth is not oriented preferentially in any direction. In contrast, the vanilloid anther experiences significant growth that is periclinal to the adaxial surface of the anther, resulting in a massive proliferation of the sterile connective tissue that is an important determinant of the final position of the pollinia in this group.
The vandoid anther differs from the vanilloid and nonvandoid epidendroid anther in that the primary location of growth results in bending of the anther itself, as opposed to the column. In addition to the observations presented here, the vandoid morphology can be seen in Hirmer's (1920)
illustrations of Acampe, Ascocentrum, Bifrenaria, Catasetum, Lycaste, Mormolyca, Oncidium, Ornithidium, Phalaenopsis, Renanthera, Saccolabium, Trigonidium, and Zygopetalum, while the nonvandoid (column extension) morphology is clear in Bletilla.
These observations have significant implications for anther character state definition. The principal feature distinguishing vanilloid anther bending is the participation of connective expansion. This feature can be coded as a binary character—connective expanded vs. not. Although most of the vandoid orchids examined here effect bending solely by anther growth, Aerangis (examined but not shown in the present study) is an example where both anther growth and column zone elongation are involved, indicating that the features are independent. Therefore it is appropriate to code one multistate character to capture time of anther bending (none, late, early) and for coding presence vs. absence of column zone elongation.
The vandoid condition and anther transformation
The vandoid anther has been interpreted as bending or becoming incumbent very early in ontogeny (Hirmer, 1920
), which contrasts with the nonvandoid incumbency that is achieved by bending much later in development. Despite the broad scope of his study, Hirmer was unable to observe extremely young vandoid anther primordia, i.e., prior to bending. The vandoid anther has also been interpreted as erect with ventral dehiscence (Dressler, 1981
), a view that Dressler (1986)
later changed in favor of the early bending interpretation. Further evidence for early bending was provided by Kurzweil (1987a)
, who showed via scanning electron microscopy (SEM) studies that a significant difference in timing of bending exists in vandoid and nonvandoid epidendroids. Kurzweil (1987a)
also defined more precisely "early" and "late" bending, relating bending to column elongation and differentiation of lateral carpel apices. We follow Kurzweil's definition, but here combine his stages 1 and 2, such that we distinguish "early" and "late" solely with respect to the onset of column elongation.
A strong correlation exists among several anther character states in the advanced epidendroid orchids—superposed pollinia, early anther bending, and a cellular pollinium stalk (stipe) usually occur together, although not exclusively. Superposed pollinia and anther bending have been discussed thus far in detail; here we review briefly the nature of pollinium stalks because of its relevance to anther and pollinium structure and development. Pollinium stalks are common among orchids, particularly among Epidendroideae. Rasmussen (1982
, 1986a
) clarified the nature of these stalks, revealing that the most common are caudicles derived from the anther itself, usually comprising modified sporogenous tissue, sometimes with adherent anther wall (e.g., Blackman and Yeung, 1983
). Caudicles are a derived condition within the orchids as a whole and probably within Epidendroideae (Freudenstein and Rasmussen, 1999
). Most orchids that do not have caudicles still have a viscidium (nondetachable) derived from the rostellum.
The stipe, on the contrary, is a cellular structure derived from the rostellum—either the distal end (a hamulus) or the adaxial epidermis (a tegula; Rasmussen, 1982
). Orchids that have a stipe also have caudicles—it is caudicular material derived from the anther that attaches the pollinia to the proximal end of the stipe. A cellular pollinium stalk does occur outside of the vandoids, but only rarely; it is currently known only from Bulbophyllum (Rasmussen, 1985
), Sunipia (Rasmussen, 1986a
), and Tropidia (Rasmussen, 1982
) in Epidendroideae, and Aenhenrya, Hetaeria, and Zeuxine in Orchidoideae (Rasmussen, 1982
, 1986a
; Sathish Kumar and Rasmussen, 1997
). All of these are hamuli except for the tegulae found in the latter three genera (Rasmussen, 1982
). It is certainly possible that additional examples occur, perhaps in poorly known genera of Goodyerinae. As far as is known, all vandoids have a stipe, the great majority of them being a tegula (excepting some members of Calypsoinae and Corallorhizinae that have a hamulus—Corallorhiza, Cremastra, Oreorchis, Tipularia; Freudenstein, 1994
).
These features—early anther bending, superposed pollinia, stipe—along with other features, such as the presence of lateral inflorescences, form the basis for what is called the "vandoid" morphology. This suite of characters has at times been used to define taxa, even at the level of subfamily (Vandoideae or its equivalent; Bentham, 1881
; Dressler, 1981
). At other times, it has been recognized as a morphological suite that has evolved more than once (e.g., Dressler, 1986
, 1993
). In the current state of orchid phylogenetic work it remains unclear exactly how many times the suite has arisen because of a continuing lack of resolution among many clades in the "advanced" Epidendroideae (Freudenstein et al., 2001
)—anywhere from one to four times is our best estimate based on well-supported topologies, depending on the relationship among the following putatively monophyletic vandoid groups: Calypsoinae, Corallorhizinae, Vandeae + Polystachyeae, and Cymbidieae + Maxillarieae. Regardless of the exact number of times that the suite has evolved, the correlation remains striking. No nonvandoids exhibit early anther bending, so it is perhaps the defining character for the assemblage. Outside of vandoid orchids, superposed pollinia occur in Epidendroideae only in Coelogyneae and Sobralia (possibly Chysis). These groups have a late-bending anther and only caudicles, if any pollinium stalk, rather than a stipe.
In seeking to understand the relationship among these characters, it is crucial to consider the physical adjacency of the rostellum and anther in the context of timing of anther development. Epidendroids that have caudicles rely on an insect visitor to contact the viscidium, picking up adhesive and then touching the caudicles, affixing them to the insect's body. The physical coordination of anther and rostellum during ontogeny cannot be critical, because the anther does not bend to come into contact with the rostellum until shortly before anthesis. However, with the vandoid pollinarium, which represents an intimate physical connection between the anther and rostellum via the stipe and caudicles, it is likely that a longer period of codevelopment between rostellum and anther would be necessary. This would be facilitated by drawing the time of anther bending earlier into the developmental sequence.
Timing of anther bending is therefore a critical factor in determining the morphology of the upper portion of the column, including the anther. It is clear that anther bending in vandoids is accelerated relative to other floral events (Rasmussen, 1986b
; Kurzweil, 1987a
; present results) and compared to nonvandoids. Indeed, Rasmussen (1986b)
depicted the difference in relative timing of anther growth and inflexion graphically for vandoid and nonvandoid epidendroids. However, due to the different mechanism of bending in vandoids as opposed to nonvandoids, it cannot be interpreted as only a heterochronic shift.
What significance might the superposed condition have in the vandoids? Mechanically, it would seem to be easier to attach the stipe to four pollinia if their apices come together at a single point, rather than along an extended line. The superposed condition facilitates this by stacking the pairs of pollinia one on another, as opposed to the juxtaposed condition, in which the pollinia are aligned in a single row.
If the stipe is a key to precision pollinium placement on insects, and therefore to pollinator specialization, and if the vandoid floral morphology allows for efficient construction and deployment of this pollinium delivery device, it would not be surprising to find that such an important character suite has in fact evolved more than once. Although there are occasional examples of loss of the stipe in cleistogamous flowers (e.g., Corallorhiza odontorhiza; Freudenstein, 1994
), the stipe and associated vandoid features may well be examples of key apomorphies that have led to success (in terms of numbers of species) in the Epidendroideae.
It is clear that understanding the phenomena of anther bending and pollinium placement in those orchids that undergo these processes (the vanilloids, vandoids, and remaining epidendroids) is crucial to the understanding and elucidation of their phylogenetic relationships. With the development of these successful suites of characters, among others, the epidendroids (comprising 80% of the family) apparently experienced an explosive species radiation. Reconstructing the pattern of this explosion has been difficult in the extreme. A clearer understanding of some of the characters that fueled this radiation will facilitate teasing apart the relationships of these still highly unresolved groups.
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FOOTNOTES |
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4 Author for reprint requests (freudenstein.1{at}osu.edu
)
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LITERATURE CITED |
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