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a Department of Biological Sciences, Kent State University, Kent, Ohio 44242; and Botanical Laboratory, University of Copenhagen, Gothersgade 140,1123 Copenhagen K, Denmark
Received for publication December 18, 1997. Accepted for publication June 11, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: cladistics • classification • morphology • Orchidaceae • systematics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), are perhaps the largest family of angiosperms. They are known for their diversity of specialized pollination and ecological strategies and provide a rich system in which to study evolutionary patterns. Most systematic work on the family has been concentrated at the species level, describing the seemingly boundless variation that occurs particularly in tropical regions. This is not to say that no attention has been given to relationships at higher levels, however; for two centuries systems of classification have attempted to trace a pattern in variation above the generic level. Swartz (1800)
was the first to produce such a treatment, and he was followed by Brown (1810)
, Lindley (1840
), Pfitzer (1887)
, Schlechter (1926)
, and others. Recent systems of classification have been framed in the context of phylogenetic patterns, utilizing as much character information as possible. Such systems include those of Dressler and Dodson (1960)
, Garay (1960
, 1972a
), Vermeulen (1966)
, Brieger, Butzin, and Senghas (1970–1995)
, Dressler (1981
, 1993
), Rasmussen (1985)
, Burns-Balogh and Funk (1986)
, and Szlachetko (1995)
.
The development of the cladistic approach to data analysis has marked a shift toward a more explicit methodology in systematics. Explicitly cladistic studies of orchids were done as early as the beginning of the 1980s (Linder, 1981
; Rasmussen, 1982
), but involved only portions of the family. The first cladistic study of the family as a whole was that of Burns-Balogh and Funk (1986)
, which suffered several shortcomings. First, it was not explicit in the methods used to generate the tree shown; neither was it clear whether the tree presented was optimal, and if so, whether it was the only tree at that level of optimality. Second, the tree shown does not wholly correspond to the data matrix presented. Third, vegetative characters were excluded from the analysis. Fourth, there are significant questions about character-state recognition and interpretation, many of which were outlined by Dressler (1987)
. In spite of these problems, the study does serve as a starting point for further work. The most recent work of Dressler (1990a–c
, 1993
) does not attempt an explicit analysis of the family as a whole, or even of smaller portions, but does employ phylogenetic thinking in suggesting relationships; it brings together much information on character variation and presents clear hypotheses of relationship to be tested further. Szlachetko's (1995)
system is explicitly polythetic and therefore essentially intuitive, rejecting a cladistic approach as being too restrictive in determining the composition of groups.
Hence, until now there has been no explicit morphological cladistic analysis of Orchidaceae. We here report the results of such an analysis and believe that it is important for several reasons. First, it is a useful tool to evaluate previous systems of classification. It is relatively easy to suggest relationships of organisms based on intuition; with other alternatives having been discarded, such hypotheses tend to take on an authoritative stature that can be difficult to evaluate. An explicit analysis reveals alternative hypotheses of pattern that might not otherwise be considered. Second, it provides a concrete, explicit set of character data and codings that form a solid basis for continued systematic work, as well as allowing the evaluation of traditionally emphasized characters. As new characters are developed, they can be added to the data set and subjected to further analysis. Third, it reveals where further efforts should be focused, in two ways. Instances of missing data in the matrix reveal an obvious need for additional study. These gaps occur primarily in poorly known and rare taxa, for which focused field work might be appropriate. Regions of the tree that show poor resolution also can direct future study, since they indicate a need for additional characters or possibly more intensive character analysis and improved hypotheses of homology. Finally, such an analysis provides a morphological character set that can be combined with other (i.e., molecular) data sets. Synthesis of the varied perspectives of these data sets would be expected to yield a maximally informative pattern.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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and included additional taxa that we knew had unique character combinations. With respect to the second goal, scoring all characters for a selected set of species would have been optimal, but is impractical, because we often relied on the literature for character scoring and different species have been examined for different characters. As a compromise, we chose a generic exemplar approach, meaning that if a character state was observed in at least one species it was scored for the genus, unless it was clear that a polymorphism was present, in which case the genus was divided into more than one terminal. Hence, it is possible that there is no single species in which all of the states that we scored for a genus occur together, but at least we have limited the error to the genus level. Characters were selected by reviewing those used in previous analyses and searching for variation that had not previously been analyzed. Our only criteria for character inclusion were that the states were mutually exclusive and that they did not vary within terminals. Characters were scored to the extent possible from living and preserved specimens, based primarily on collections at AMES, C, and K. All scoring information is available on request from the authors. This information was supplemented with published observations from the literature. Details concerning character scoring and important literature sources are given in the Results (Character Analysis section). The data matrix is shown in Table 1.
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) and recent molecular analyses have shown it to be closely related to the orchids (Chase et al., 1995
). Additional outgroups would have been important if we had intended to test the monophyly of the Orchidaceae, but this was not a goal of the analysis.
The data were analyzed in two ways. The primary analysis used Wagner parsimony as implemented in NONA (Goloboff, 1993b
). The heuristic search strategy was as follows: for each of 3000 random taxon addition sequences an initial set of trees was found by one pass through the data; these trees were then subjected to TBR (tree bisection reconnection) branch swapping, keeping 20 trees whenever the current shortest length or shorter was found. This collection of trees was then subjected to further TBR branch swapping, and all shortest trees up to the set maximum of 60 000 trees were saved and a strict consensus tree was produced. The sequence of commands used was: nona; out=xxx.out; h*;p xxx.dat; pack r rs 0; h/20; na=wa h* mult*3000; h 60000; max* sv=xxxtr.out g500 sv; nels in; s/ zzz. Several additional runs were conducted using the same procedure, although sometimes keeping fewer trees, in order to more thoroughly explore the tree space.
The second analysis employed the implied weighting function of Goloboff (1993a)
, as implemented in PIWE (Goloboff, 1993b
). This weighting procedure employs a weighting or fitness function that is based on the number of steps required for each character on a particular tree. Optimal or "fittest" trees are those that maximize the fitness function when summed over all characters. The details of this analysis were the same as for the Wagner procedure, except for using 2000 random addition sequences, saving 15 shortest trees for each, and then swapping up to 30 000 fittest trees. The default constant of concavity was used (k = 3).
Jackknifing was implemented using the parsimony jackknifing program of Farris (1995)
. The data set was first modified by recoding all ordered multistate characters as binary characters. Ten thousand replications were performed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Character analysis
0. root tubers 0 = absent, 1 = present
Root tubers are thickened roots that serve as organs of perennation, producing shoots in subsequent seasons. These structures occur primarily in the Diseae, Orchideae, and Diurideae and have been studied intensively (e.g., Irmisch, 1850
; Germain de St.-Piérre, 1855
; Prillieux, 1865
; White, 1907
; Ogura, 1953
; Pridgeon and Chase, 1995
). Triphora was scored as having a true root tuber, but Pogonia and Isotria were not, even though their unthickened roots are known to produce shoots (Ames, 1922
). Nodular root thickenings are known from Apostasia (Stern and Warcup, 1994
), Tropidia (Dressler, 1981
), and possibly others, but these evidently do not produce new shoots.
1.root epidermis 0 = rhizodermis, 1 = velamen
2.exodermis 0 = unthickened, 1 = uniformly thickened, 2 = outer walls thickened
3.exodermal cell shape 0 = ±isodiametric, 1 = elongate
4.velamen cell thickenings 0 = absent, 1 = linear, 2 = circular
These characters derive primarily from the work of Porembski and Barthlott (1988)
; velamen and exodermal features were also discussed thoroughly by Pridgeon (1987)
. Instead of coding the ten Porembski and Barthlott velamen types as states for the terminals, which would necessarily have to be coded as unordered states of a single character, we chose to code component features of the variation that they describe.
5. spiranthosomes 0 = absent, 1 = present
Spiranthosomes are specialized amyloplasts known only from the spiranthoid orchids and were first described by Stern et al. (1993a)
. Most of the occurrences of spiranthosomes are taken from Stern et al. (1993a
, b
). Many of the coded absences, outside of spiranthoid orchids, are assumed, since they have not been described before from other groups.
6. growth pattern 0 = sympodial, 1 = monopodial
Most orchids follow the sympodial growth pattern common in monocots (Holttum, 1955
). Notable exceptions are Vanilla, which is a monopodial vine with elongate internodes, and members of the Vandeae, which have monopodial growth. Pfitzer (1882)
discussed this character at length.
7. thickened stem 0 = absent, 1 = present
Stem thickening may be in the form of swelling in aerial stems, as in some species of Dendrobium, corms (e.g., Aplectrum), or pseudobulbs. If the stem is notably but uniformly thickened, as in Vanilla, the taxon is not scored as having a thickened stem. Pfitzer (1882)
coded essentially the same information in his character "stems homoblastic or heteroblastic," depending on whether the stem internodes are uniform or not, but there are some differences between our scoring and his. For example, Pfitzer called the stem of Catasetum typically homoblastic, while we recognize it as a thickened stem (the upper internodes are thickened more or less uniformly).
8. number of thickened internodes 0 = several, 1 = one
This character codes variation in the number of internodes that comprise a pseudobulb. In many taxa, it is clearly one internode (e.g., Bulbophyllum), while in others (e.g., Catasetum), it can be several. Those taxa with no thickened stem are coded as unknown. Pfitzer (1887)
also used this character.
9. phyllotaxy 0 = spiral, 1 = distichous
Phyllotaxy in orchids is usually described as either spiral or distichous, with the latter supposed to be the more advanced state (Dressler and Dodson, 1960
; Dressler, 1993
). We found that in all species examined, the condition at the base of a stem, represented by the first bracts surrounding a bud, is distichous. In some taxa (e.g., Apostasia, Neuwiedia, many spiranthoids and diurids), the phyllotaxy soon shifts to more or less spiral, so that most of the leaves appear spirally arranged. In many of these, the arrangement is not strictly spiral, as was shown by Fuchs and Ziegenspeck (e.g., 1927a
, b
, c
). In other taxa (e.g., species examined of Dactylorhiza, Orchis, many epidendroids), the majority of leaves show a distichous arrangement. Even in those species with distichous leaves, the inflorescence is often spiral in floral arrangement. In some cases, even the inflorescence is distichous (e.g., Tropidia effusa, Liparis gibbosa, Phalaenopsis cornu-cervi). Hence the basic model for orchid phyllotaxy appears to be a distichous basal condition on the shoot, with a possible shift to a spiral or pseudospiral condition at some point (before inflorescence or not). We scored states according to whether a taxon had spiral (or pseudospiral) or distichous phyllotaxy on the leaf-bearing portion of the shoot.
10. leaf morphology 0 = flat non-plicate, 1 = plicate, 2 = conduplicate
Variation among orchid leaves is more complex than it appears at first glance. Phyllotaxy plays a part in determining mature morphology, and since this was scored as a separate character, it is important not to duplicate this information. Leaves with convolute vernation usually are spirally arranged, while conduplicate leaves have duplicate vernation. The state found in many of the terrestrial spiranthoids and orchidoids has been termed by Dressler (1990c)
"nonplicate herbaceous," and is referred to here as "flat nonplicate." It describes those leaves that are essentially flat (not conduplicate), without prominent midrib, usually fleshy in texture, and that are the result of convolute vernation. Plicate leaves may result from either convolute or duplicate vernation, and are characterized by the accordion-like pleating of the lamina. Conduplicate leaves, as coded here, are those with a single fold of the lamina at the midrib, and without any plication. There are some conduplicate plicate leaves (e.g., Sobralia), but, again, in order to avoid redundancy, these were simply scored as plicate.
11. winter leaf 0 = absent, 1 = present
Some genera of terrestrial orchids have a leaf that is produced at the end of the growing season, overwinters, is photosynthetically active when conditions are favorable, then withers at or before flowering. These are primarily members of Corallorhizinae (e.g., Aplectrum, Calypso; cf. Freudenstein, 1994
), but occasionally other species show a similar modification (e.g., some Spiranthes have overwintering leaves [F. Rasmussen, unpublished data]).
12. leaf articulation 0 = absent, 1 = present
Pfitzer (1887)
may have been the first to use this character. It has been discussed and the state noted for each orchid group by Dressler (1981)
and denotes the presence or absence of an abscission zone at the base of a leaf. As a general rule, most epiphytic orchids are articulate, while terrestrial species are not.
13. stegmata 0 = conical, 1 = spherical, 2 = absent
Most of the information on this character is from Møller and Rasmussen (1984)
. Additional scoring was derived from sources quoted in Solereder and Meyer (1930)
and from Stern et al. (1993b)
for Spiranthoideae. The character seems to be largely uniform within genera, although Dressler and Cook (1988)
found conical stegmata in Eria javanica while other members of the genus are known to have spherical stegmata. Since the outgroup (Hypoxis) does not have stegmata, the plesiomorphic state in the analysis is absence, although Apostasia and Neuwiedia, considered to be members of a basal lineage, do have conical stegmata. Because stegmata are always found in association with fibrous support tissue, absence may be due either to loss of the stegmata themselves (where sclerenchyma is present), or to the loss of sclerenchyma. Since presence of fibrous support tissue in the leaf is scored as a separate character, those taxa that have no leaf sclerenchyma were scored as unknown for the presence of stegmata.
14. leaf fiber bundles 0 = present, 1 = absent
Many orchid leaves have sclerenchyma associated with the vascular bundles, as well as independent fiber bundles, while other leaves have no sclerenchyma. Stern et al. (1993b)
used this character in their analysis of Spiranthoideae. Presence of sclerenchyma is often, but not exclusively, associated with large leaf size.
15.leaf abaxial epidermal cells 0 = straight, 1 = wavy
Lavarack (1971)
used this character in his phenetic study of Australian Orchidaceae (Diurideae), and Stern et al. (1993b)
surveyed it in the Spiranthoideae. The states are usually quite distinct, with either clearly sinuous or straight-polygonal anticlinal walls when viewed in paradermal section, (cf. Dressler, 1993
, figs. 2–6). Adaxial surface cells may also exhibit the variation, but it is most pronounced on the abaxial surface.
16.subsidiary cells 0 = present, 1 = not distinguishable
Some detailed studies of subsidiary cells in orchids have been done (Williams, 1975
, 1979
; Rasmussen, 1981
, 1987
), but not on a broad enough scale to make it possible to score the different developmental patterns for many of our terminals. Hence, we have simply scored the presence/absence of subsidiary cells that are morphologically distinct from surrounding epidermal cells, without regard to their ontogeny.
17. inflorescence position 0 = terminal, 1 = lateral
In most orchids this appears to be a relatively straightforward character, although, as discussed by Bentham (1881)
and shown by Andersen et al. (1988)
for Eria, there may be variation within a genus and the true state can be difficult to ascertain. Pfitzer (1887)
emphasized this character in his classification, delimiting the major groups Acranthae (those with terminal inflorescences) and Pleuranthae (those with lateral inflorescences).
18.floral abscission 0 = absent, 1 = present, ovarynot stalked, 2 = present, ovary stalked
Many orchids have an abscission layer at the base of the pedicel; if the flower is not pollinated, it falls from the inflorescence. As opposed to perianth abscission, floral abscission seems to occur only in a more "advanced" group, the epidendroids. Within the Pleurothallidinae there is a further specialization, in that the abscission zone is located between the pedicel and ovary, so that after the flower falls a distinct stalk remains (Dressler, 1993
; Neyland and Urbatsch, 1993
). This character was coded as ordered (equivalent to coding the stalked ovary as a distinct character).
19. perianth abscission 0 = present, 1 = absent
The perianth may abscise at the summit of the ovary. Dressler (1983)
described this feature and noted its occurrence in the "basal" orchid groups. When it does not abscise, the perianth simply decays in place.
20. calyculus 0 = absent, 1 = vanilloid, 2 = polys- tachyoid
The calyculus is a series of small bract-like structures outside of the normal perianth. Because of its resemblance to a small perianth whorl, significant evolutionary implications sometimes have been ascribed to the structure—such as Lindley's (1847)
homologizing the calyculus with an additional floral whorl and consequent reinterpretation of the inner whorls. Soon thereafter, Crüger (1849)
concluded that the calyculus is not an additional floral whorl, but Vermeulen (1966)
again saw significance in the structure. Kurzweil (1987a)
examined the development of these structures in Neobenthamia and found no relation to the perianth whorls.
In this study two types of calyculus are recognized. Epistephium and Lecanorchis, and to a lesser extent, Vanilla, have a distinct collar below the perianth (Hashimoto, 1990
; Dressler, 1993
). The type known from Neobenthamia, and also observed here (and by Kurzweil, 1987a
) in Polystachya, is different, being essentially a series of swellings on the ovary valves. A bract-like calyculus has also been reported from some species of Bulbophyllum (e.g., Lindley, 1838
; Seidenfaden, 1979
; Dressler, 1981
).
21. slipper-shaped labellum 0 = absent, 1 = present
This distinctive labellum form has the middle portion greatly expanded and the apex and distal margin pulled back toward the column, forming a hollow, shoe-like structure. This morphology is characteristic of the Cypripedioideae. Superficially similar structures occur occasionally in the Epidendroideae (e.g., Calypso), but do not include the inrolled margin that is present in cypripedioids.
22. apiculate perianth 0 = absent, 1 = present
The perianth apices of Apostasia and Neuwiedia are prolonged into distinctive tips, the result of extension of the midrib. To our knowledge this feature has not been discussed before in a phylogenetic context, although it is visible in illustrations of the flowers (e.g., de Vogel, 1969
).
23. carinate petals 0 = present, 1 = absent
Rasmussen (1982
; fig. 61d) illustrated an unusual feature in Vanilla—interlocking sepals and petals. This condition results in a keel on the abaxial surface of the petal along the midrib that occurs in several putatively basal orchid groups.
24. lip-column marginal adnation 0 = absent, 1 = present
In some vanilloid orchids the labellum is fused to the column marginally to varying degree. Other orchids have labellum–column fusion of other types, but this is not included here.
25. dorsal median stamen 0 = present, 1 = absent
26. lateral inner stamens 0 = present, 1 = absent
The homology of the functional stamens present in orchids has been discussed by Brown (1833)
, Lindley (1853)
, Darwin (1862)
, Swamy (1948)
, and Rao (1974)
. Further investigation was not undertaken here; we assume that all monandrous orchids have A1, all diandrous orchids have a1 and a2, and triandrous orchids have A1, a1, and a2. No evidence has ever been presented to substantiate Garay's (1960)
claim that two lateral stamens of the outer whorl are present in Satyrium. Occasional unusual situations, such as the presence of a third functional stamen in Phragmipedium lindenii (Atwood, 1984
) and the putatively peloric forms observed by Chen (1982)
were not included.
27. anther orientation 0 = erect, 1 = bending late, 2 = bending early
Anther bending (incumbency) during ontogeny has been discussed by Hirmer (1920)
and Dressler (1981
, 1986b
, 1993
). Although there has been some question of whether "advanced" epidendroids bend at all (Dressler, 1981
), more recent study suggests that these taxa bend very early (Dressler, 1986b
; Kurzweil, 1987a
). We distinguish between early and late bending following Kurzweil's (1987a
, p. 438) stage 2–3 distinction, relative to the time of column elongation. This character is ordered based on ontogenetic information—the erect state is more general than the incumbent state (cf. Kurzweil, 1987a
). Degree of anther bending (illustrated by Hirmer, 1920
) could also be scored, but it is essentially a continuous character, and so was not included here.
28. operculate anther 0 = absent, 1 = present
Typical lilioid anthers dehisce by slits, releasing pollen without also shedding parts of the anther wall. Some orchid anthers (Apostasioideae, Cypripedioideae, Orchidoideae, Spiranthoideae) also have essentially this type of dehiscence. Incumbent anthers usually need to be physically disturbed to allow the pollinia to be removed. In some taxa with incumbent anthers, the anther develops in tight proximity to the clinandrium; in order for pollinia to be released, the anther (sometimes called the "anther cap") must be removed. This removable type of anther is called an operculate anther and has been used as a character since the beginning of orchid taxonomy by Swartz (1800)
, Lindley (1840)
, Pfitzer (1887)
, and Reichenbach (1852)
, as well as later authors such as Dressler (1981)
.
29. Endothecial thickenings 1 0 = other, 1 = inter- mediate, 2 = type II
30. Endothecial thickenings 2 0 = other, 1 = type III/IV
Endothecial thickening morphology in orchids was surveyed by Freudenstein (1991
). Here the distinctive type II thickening is coded as one character, and the types III/IV and their intermediates are coded as a second character. State 1 in character 29 is used for those thickenings that are intermediate in morphology between types I and II. Because it is a essentially a morphocline, the character is coded as ordered.
31. basal caudicles 0 = absent, 1 = present
Caudicles are pollinium stalks that are composed of pollen and/or pollen-derived substances, as opposed to rostellar tissue (Richard, 1817
; Mansfeld, 1934
; Rasmussen, 1986a
). In epidendroid and spiranthoid orchids they are produced apically in the anther, due to the bending of the anther or the apical position of the rostellum, respectively. In orchidoids the caudicles are basal extensions of the pollinia that are held in an erect anther. Pfitzer (1887)
termed the condition where the rostellum is near the basal part of the anther basitonic (as opposed to acrotonic, in which the rostellum is near the anther apex), and considered it an important character. The diurids show intermediate states, sometimes termed pleurotonic (Mansfeld, 1954
) or mesotonic (Dressler, 1981
), but there is a continuum from acrotonic to basitonic, so this additional variation was not used here.
32. hammer stipe 0 = absent, 1 = present
A distinctive stipe with a "hammer-like" morphology was identified by Rasmussen (1986a)
in Sunipia. We found this type also in Genyorchis.
33. tegula 0 = absent, 1 = present
Rasmussen (1982)
distinguished between the tegula, a pollinium strap formed from the epidermis of the rostellum, and a hamulus, the apex of the rostellum itself. The tegula may be a multilayered epidermis or may consist solely of the rostellar cuticle, as in Doritis (Rasmussen, 1986a
).
34. pollen unit 0 = monad, 1 = tetrad
The variation in pollen unit at anther dehiscence has been a subject of study since Reichenbach (1852)
. It was described by Schill and Pfeiffer (1977)
for a large number of species; others were reported in Newton and Williams (1978)
, Ackerman and Williams (1980
, 1981
), and Hesse, Burns-Balogh, and Wolff (1989)
. Ackerman and Williams (1981)
described cases of some diurids (e.g., Caladenia) in which both states occur. Wolter and Schill (1986)
suggested that the occurrence of tetrads in orchid pollen may be a paedomorphic transformation.
35. pollen tectum 0 = reticulate, 1 = smooth
Pollen structure has been described by Williams and Broome (1976)
, Schill and Pfeiffer (1977)
, Burns-Balogh (1983)
, Hesse, Burns-Balogh, and Wolff (1989)
, Zavada (1990)
, and Schlag and Hesse (1993)
. Rather than focus on details of the tectal structure, which has not been studied in enough genera, we simply scored the appearance of the pollen grains, whether reticulate or smooth. This variation has been known since the time of Reichenbach (1852)
.
36. pollen apertures 0 = colpate/sulcate, 1 = porate, 2 = inaperturate, 3 = polyporate
The aperture state of orchid pollen was taken from Erdtman (1944
, 1952)
, Schill and Pfeiffer (1977)
, Newton and Williams (1978)
, Ackerman and Williams (1980)
, and Hesse, Burns-Balogh, and Wolff (1989)
. The majority of orchid pollen is inaperturate (Schill and Pfeiffer, 1977
), but putatively basal groups have colpate/sulcate or porate pollen (Newton and Williams, 1978
; Hesse, Burns-Balogh, and Wolff, 1989
). Some of the vanilloids (Vanilla, Epistephium, Lecanorchis) have polyaperturate pollen (Erdtman, 1944
, 1952
; Schill and Pfeiffer, 1977
; Ackerman and Williams, 1980
).
37. operculate colpus 0 = absent, 1 = present
Burns-Balogh and Funk (1986)
used this character in their analysis. It was described and illustrated by Schill (1978)
and Newton and Williams (1978)
and only appears in Apostasia and Neuwiedia.
38. massulae 0 = absent, 1 = orchidoid, 2 = epi- dendroid, 3 = arethusoid
Sectile pollinia (those with pollen subpackaged in massulae) were recognized very early in orchid taxonomy; the term "massula" was coined by Richard (1817)
. More recently, they have been shown to vary with respect to layering and regularity of massulae (Vermeulen, 1965
; Freudenstein and Rasmussen, 1997
). Orchidoid sectile pollinia have a single layer of uniform massulae, while epidendroid pollinia have variable numbers of layers of irregular massulae. Pollinia of Arethusa and Calopogon are hollow at maturity (cf. Pace, 1909
; Freudenstein and Rasmussen, 1997
), while most other orchids have solid pollinia.
39. pollinium texture 0 = granular, 1 = solid
Pollinium texture is largely a continuous character (Dressler, 1986a
), but it is possible to distinguish those pollinia that are truly coherent from those that are soft enough to be crushed easily when touched, and the character has been used to distinguish groups since Swartz (1800)
and Richard (1817)
. The structural basis for this difference has been elucidated by ultrastructural studies of pollinia (Chardard, 1958
, 1962
, 1963
, 1969
; Cocucci and Jensen, 1969
; Schill and Pfeiffer, 1977
; Wolter and Schill, 1986
; Yeung, 1987b
; Hu and Yang, 1989
; Zavada, 1990
; Pandolfi, Pacini, and Calder, 1993
). The most important difference is whether or not exine is deposited on internal pollen grains; if not, a more cohesive, calymmate pollinium results, while those that do have exine on all grains are much more friable and are termed acalymmate (van Campo and Guinet, 1961
).
40. pollinium number: 2 0 = absent, 1 = present
41. pollinium number: 8 0 = absent, 1 = longitudinal, 2 = transverse
The primary pollinium numbers in orchids are 2, 4, and 8. Other numbers are sometimes reported (e.g., in Laeliinae), depending upon whether additional small masses of pollen that sometimes are found along the caudicles are interpreted as pollinia. Four is the predominant number. It is found in the putatively basal orchid groups, as well as in outgroups (where there are four anther locules). Freudenstein and Rasmussen (1996)
found that there are at least two ways to produce eight pollinia—by longitudinal or transverse division of embryonic pollen masses.
42. pollinium orientation 0 = juxtaposed, 1 = superposed
This character refers as much to the structure of the anther as it does to the pollinia. Richard (1817)
used the Latin term superposita to describe the anthers of Calypso and Corallorhiza. Bentham (1881)
also recognized the variation, although he did not use the term "superposed." More recently, Dressler and Dodson (1960
) recognized the superposed state, where, when four, the pairs of pollinia are stacked one on another, as opposed to the juxtaposed (Freudenstein and Rasmussen, 1996
) condition, in which the pollinia are arranged side by side. We have detected two distinct ways in which the superposed state can occur—either by inward or outward "rotation" of anther thecae (Freudenstein and Rasmussen, unpublished data), but as we have not yet completed developmental study on a sufficient number of taxa, we have here coded all superposed pollinia as the same state.
43. ovary locule number 0 = one, 1 = three
Most orchids have a single ovary locule, while a very few putatively basal groups have three locules, as does the outgroup. Transverse sections of each type are shown in Atwood (1984)
and, in diagrammatic form, in Garay (1960)
.
44. stigma 0 = protruded, 1 = sunken
Variation in stigma morphology was discussed by Dressler (1981
, 1993
), Rasmussen (1982)
, and Dannenbaum, Wolter, and Schill (1989)
. In many taxa portions of one or more stigma lobes protrude, form a raised triangular or circular mass, or are of another shape (cf. Rasmussen, 1982
, fig. 73). These morphologies are also sometimes known as "convex." A sunken stigma is usually a circular depression ("concave"), which as Dressler (1993)
has suggested, appears to be specialized to receive hard pollinia (cf. Rasmussen, 1982
, fig. 73:2.1.2); this type is usually encountered in Epidendroideae.
45. stigma receptive cells 0 = various other, 1 = finger, 2 = prosenchymatic
This character derives from the work of Dannenbaum, Wolter, and Schill (1989)
. It describes the shape of the receptive cells of the stigma that are usually hidden under stigmatic secretions in living plants.
46. viscidium 0 = none, 1 = diffuse, 2 = detachable
Most orchids have some sort of adhesive associated with insect transfer of pollen masses. This may be either in the form of a glue that is transferred to the insect before it contacts pollen (diffuse), or a more elaborate cellular structure composed of rostellar tissue that is attached either directly, or via a stalk, to the pollinia (detachable). Some controversy over terminology involving the viscidium exists, with Dressler (1986a)
and Dressler and Salazar (1991)
arguing for restricting use of the term to a detachable structure, while Rasmussen (1982)
used the term more broadly to include also any secreted adhesive. Here it is used in the broad sense simply for convenience, with the two senses of the term being the states. The character is coded as ordered because all detachable viscidia also have adhesive secretion.
47. endocarpic trichomes 0 = absent, 1 = present
Endocarpic trichomes, or Schleuderhaare, were described in the 19th century and have been generally overlooked since. Blume (1848)
, Beer (1857)
, Prillieux (1857)
, and Horowitz (1901–1902)
illustrated and discussed them at some length, showing some of the variation in shape (filiform or flattened) that occurs. Pfitzer (1882)
also mentioned them. Their function has always been assumed to be in seed dispersal, and according to Malguth (1901)
their presence is correlated with epiphytism, although not all epiphytes have them and some terrestrial orchids do. More recently, Hallé (1986)
illustrated them in transverse sections of ovaries of New Caledonian taxa. A scanning electron micrograph of a hair from Pteroceras appears in Pedersen (1993)
. The only genus in which we found them outside of Epidendroideae is Prasophyllum.
48. seed laterally compressed walls 0 = absent, 1 =present
49. seed testa cell shape 0 = all isodiametric, 1 =end isodiametric, middle elongate, 2 = all elongate
50. seed striations 0 = absent, 1 = transverse/reticulate, 2 = longitudinal
51. seed intercellular spaces 0 = absent, 1 = present
52. seed wax caps 0 = absent, 1 = present
53. seed covered cell border 0 = absent, 1 = present
Seed morphology has provided a promising new set of characters for orchids (Barthlott, 1976
; Dressler, 1986b
, 1990a
, 1993
; Molvray and Kores, 1995
). Most of these characters derive from the work of Ziegler (1981)
. Much of the scoring was done from the plates in Ziegler (1981)
, Tohda (1983
, 1985
, 1986
), Chase and Pippen (1988
, 1990
), and Kurzweil (1993)
. Rather than coding seed morphology as types, such as those recognized by Ziegler (1981)
and Dressler (1993)
, we coded component features to the extent possible. Laterally compressed testa walls refer to the extremely narrow cell lumen seen in some taxa (e.g., Vandeae), resulting from the close positioning of lateral anticlinal testa walls. Some seeds have distinct variation in testa cell size depending on location—with either all cells isodiametric, the cells at both ends isodiametric and those in the center elongate, or all cells elongate. When present, striations on the sunken testa cell lumina may be either transverse/reticulate or longitudinal/parallel. Distinct spaces occur among the cells in some taxa. "Wax caps" are present at the ends of testa cell protrusions in some members of Cymbidieae (Ziegler, 1981
; Chase and Pippen, 1990
). In some seeds the abutment of adjacent testa cell walls is clearly evident, while in others the line of demarcation between them is covered by tissue from one or the other cell (a covered cell border).
Excluded characters
A number of additional characters have been used in previous analyses, are commonly used in keys to separate major groups, or at least have been suggested to be of phylogenetic significance. Here we describe those characters and the reasons for their exclusion. In addition to those listed here, there are many characters that essentially reflect shape differences that are clearly continuous or problematic in scoring. This category includes some of the characters employed by Burns-Balogh and Funk (1986)
, such as degree of style fusion and rostellum shape.
Vessel perforation plate type
Cheadle and Kosakai (1982)
, Stern, Cheadle, and Thorsch (1993)
, and Thorsch and Stern (1997)
described the variation in perforation plates in the Orchidaceae. While most taxa have scalariform plates, Apostasia and Neuwiedia have a significant proportion of simple perforation plates. The problem is with state delimitation. An individual plant may have both simple and scalariform plates, meaning that simple perforation plates are a tendency in apostasiads, rather than a true defining feature.
Pollen tetrad shape
Reichenbach (1852)
illustrated several tetrad cell arrangements. Konta and Tsuji (1982)
and Konta and Hayakawa (1982)
recognized up to six shapes of pollen tetrads, but found that all species had more than one type of tetrad, with some having all of the recognized types. Yeung (1987a)
also discussed this variation. The rampant intra-individual polymorphism precluded use of the character.
Resting nucleus type
Tanaka (1971)
has recognized five morphological classes of interphase chromatin. He found the states to be largely distinct, with few intermediates. Additional information has been provided by Okada (1988)
, who recognized only three states, and Sera (1990)
. The character was not included here because there are still a significant number of missing data.
Sclerotic seed coat
Significance has been attributed to the fact that both Apostasia and Vanilla (as well as Selenipedium, which was not a terminal in this analysis) have a hard, black "sclerotic" seed (Swamy, 1947
). Garay (1986)
interpreted this state as a symplesiomorphy. Rübsamen (1986)
and Nishimura and Tamura (1993)
showed that in Apostasia it is the inner layer of the outer integument that becomes sclerotic, while in Vanilla it is the outer layer of outer integument (Swamy, 1947
; Krupko, Israelstam, and Martinovic, 1954
), indicating that the condition is not homologous in these taxa.
Number of vascular traces in the pedicel
Swamy (1948)
and Lavarack (1971)
discussed this character, indicating that cypripedioids and apostasioids have six vascular traces that enter the flower, while the monandrous orchids have three. Working with fresh material we found it difficult to ascertain the number. Observations made from serial sections showed three traces in Habenaria tridactyle, but six in Thelasis pygmaea, and apparently six in Appendicula hexandra. Without a careful study of this character, we chose to omit it.
Resupination
Twisting of the flower, resulting in the labellum being lowermost, is characteristic of many orchid groups. It may be achieved in either of two ways. The pedicel may be curved (but not twisted) and directed to the opposite side of the raceme, so that the subtending bract is actually at the top of the flower rather than below. This is very easily achieved in inflorescences with only one flower (many Paphiopedilum, various others), but can also be accomplished in racemes such as those of Spiranthes. Alternatively, the pedicel may be twisted 180°. In this case the subtending bract is lowermost and the flower faces the same side of the raceme. No solitary-flowered species observed here showed this type of resupination. Some taxa (e.g., Malaxis monophylla var. monophylla) have the pedicel twisted 360°, which gives a nonresupinate orientation. Arching inflorescences provide another complication in this feature since the inflorescence axis is no longer vertical; in order to maintain an orientation with the labellum lowermost, 180° of twisting may not be necessary. Dressler (1983)
imagined a flower twisting away from its subtending bract as a precursor to resupination. This feature has not been used traditionally in classification, but is a useful character in keys. It is often polymorphic in genera and can be in species (e.g., Malaxis monophylla).
Column foot
This structure is a thickening at the base of the column where the labellum is attached. Whether it is actually column or labellum tissue that is thickened is often not clear. Bentham (1881)
and Schlechter (1926)
used the character particularly within Vandeae. Garay (1972b)
discussed the ambiguity of this character and avoided it in his scheme for Vandeae. It is polymorphic within genera and difficult to homologize.
Embryogeny
The form of the suspensor in orchid embryos is a promising systematic character. Its variation has been described in most detail by Treub (1879)
, Swamy (1949)
, and Veyret (1965)
, and it is possible to describe character states (e.g., the suspensor types of Swamy [1949]
). Unfortunately, there remains a majority of taxa included here for which no information on embryogeny is available.
Auricles
A number of protrusions associated with the anther and column of monandrous orchids are known. These are often considered to be staminodes, but it is difficult to compare them without developmental information. The type seen in Orchideae, termed auricles, have been considered a defining character for the group (e.g., Dressler, 1981
). Vermeulen (1966)
believed that they are nonstaminodal. Kurzweil (1987b)
examined these structures developmentally and also concluded that they do not represent staminodes, but that they are appendages of the fertile anther. He observed other structures, which he called "basal bulges," that may represent staminodes. The auricles and basal bulges fuse late in development with the lateral margins of the median stigma lobe, making them indistinguishable in the mature flower (Kurzweil, 1987b
). Further complexity was encountered in the South African Orchideae (Kurzweil, 1991
). Because of the difficulty in distinguishing these structures and establishing their homology, we did not include the character.
Cohesion strands
Burns-Balogh and Funk (1986)
employed a character called "cohesion strands," which they found only in neottioid and spiranthoid groups. They described them as acetolysis-resistant strands that appear only when pollinia are pulled apart, suggesting that they are different from elastoviscin, which is found in many pollinia. Because no further work has been done to elucidate their nature, we chose not to include them.
Topological results
Using the search strategy outlined above, the NONA heuristic search reached the maximum tree limit set (60 000), meaning that tree swapping was incomplete. Approximately 2.5% of the replicates found the shortest tree (= 241 steps). In order to explore how thoroughly the initial set of most parsimonious trees was swapped, we selected a single tree and subjected it to extensive branch swapping. We found that 31 000 trees had been produced when we terminated the swapping, suggesting that the 60 000 trees produced may have been the result of swapping only one of the initial most parsimonious trees. The consensus would then be based on the trees found by swapping this single tree plus the remaining trees from the set of initial most parsimonious trees. In order to better explore the tree space we repeated the analysis, but with deeper branch swapping at each repetition (saving 100 trees rather than 20). Consensus of this collection of trees (without further swapping) gave almost the same tree as the first analysis, with only one group (Ceratostylis + Appendicula) that did not appear in the first consensus. We did several analyses with large numbers (2000–3000) of random addition replicates and always the consensus was nearly identical to the tree we report here (sometimes with one or two additional small groups that did not collapse), giving us confidence that we have explored to some extent the major regions of tree space.
Although as is typical with large data sets the consistency index was fairly low (0.29), the retention index was high (0.83), suggesting that even though there is a large amount of homoplasy in the data set, characters are functioning as synapomorphies to a high degree. The strict consensus topology (Fig. 1) will be the focus of discussion here, since the significance of particular branches in any single most parsimonious tree is doubtful. This tree shows only branches that appeared in all of the equally weighted analyses. Jackknife values of greater than 50% are shown on the consensus tree; not surprisingly, most values are low, between 0.50 and 0.70, although some clades have higher support. A single most parsimonious tree is also shown (Fig. 2) to show branch lengths and character distribution. The character discussion that follows is based on the consensus topology and refers only to characters that unambiguously support nodes in the consensus tree. Major clades are numbered for reference in the following discussion (see Fig 1).
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In most cases where a genus was subdivided to accommodate polymorphism, the divisions are depicted as sister taxa or at least as members of the same polytomy (e.g., Pterostylis, Thelymitra, Coelogyne). In the case of Cymbidium, the two divisions (representing subgenera Cymbidium and Jensoa) did not. In fact, Jensoa is a member of the large epidendroid polytomy, while Cymbidium is part of the vandoid clade. This is because Jensoa shows later anther bending than Cymbidium and lacks other features that place Cymbidium among the vandoids, such as two pollinia and presence of endocarpic trichomes.
The first small clade resolved at the base of the tree (clade 1) corresponds exactly to the traditionally recognized Apostasioideae. The subfamily comprises only two genera, Apostasia and Neuwiedia, both of which were included in the present analysis. The characters that unambiguously unite Apostasioideae are perianth abscission (19), extended perianth apices (22), carinate petals (23), and operculate pollen colpus (37).
The remainder of the family is united by distichous phyllotaxy (9), unilocular ovary (43), and seed testa cell size (49), although all of these characters reverse in other parts of the tree. Clade two within this group comprises the cypripedioids. Cypripedioideae (here represented by two of the 4–5 genera) are united by the slipper-shaped labellum (21), loss of the dorsal median stamen (25), type III–IV endothecial thickenings (30), and smooth pollen tectum (35). Apostasia also has lost the median stamen, but this analysis indicates that the loss was independent in this genus and Cypripedioideae, in contrast to the hypothesis of Burns-Balogh and Funk (1986)
, which united Apostasia and Cypripedioideae based on this feature.
Sister to the cypripedioids are the monandrous orchids, which are shown to be monophyletic. They are united unambiguously by polygonal leaf abaxial epidermal cells (15), loss of lateral inner stamens (26), porate pollen (36), finger-shaped or prosenchymatic stigma receptive cells (45), and presence of a viscidium (46). The polytomy formed by Epipactis, Cephalanthera, and clades 3 and 6 results in uncertainty about the state change in character 16 to indistinguishable subsidiary cells, since depending upon resolution of the polytomy, this change could be a synapomorphy for Epipactis + Cephalanthera + clade 3 or may be as shown in Fig. 2, with a reversal to distinguishable subsidiary cells uniting clade 6.
The monandrous clade comprises two large clades (3 and 6), as well as Epipactis and Cephalanthera. The latter two genera, along with Listera (here at the base of clade 3) have been difficult to place in phylogenetic classifications because they share few known apomorphies with other groups. They are often placed together in Neottieae (sensu Dressler, 1993
) and are in some ways transitional between epidendroids and orchidoids, which is reflected by their position in this analysis. Cephalanthera, for example, shares floral abscission (18) and prosenchymatic stigma cells (45) with epidendroids, but does not have other key epidendroid features such as anther incumbency (27; see below).
Listera is sister to a large group of terrestrial orchids that have been placed in subfamilies Orchidoideae and Spiranthoideae and is united with them primarily by the nonplicate ("fleshy") leaf (10) and the absence of sclerenchyma bundles in the leaves (14). The Orchidoideae/Spiranthoideae group (excluding Listera) is defined by spiral phyllotaxy (9), polygonal epidermal cells (15), and intercellular spaces in the testa (51). The lower branches of this clade (i.e., Pterostylis, Chloraea, Cryptostylis, Diuris, Prasophyllum, Thelymitra, Acianthus, Caladenia) comprise genera usually placed in Diurideae; this collection of genera is clearly not monophyletic based on these data. From within this group are derived two distinct assemblages that are often recognized at the tribal level or higher. Clade 4 comprises those genera usually placed in Spiranthoideae, united by spiranthosomes (5), distinguishable subsidiary cells (16), and Type III/IV endothecial thickenings (30). The consensus tree shows no resolution within this group.
The other distinct group includes those genera usually placed in the Orchideae and Diseae, here comprising clade 5. They are united by basal caudicles (31) and massulae (38). Again, there is little structure within this clade, except for a group of genera that are sister to Disperis and that are united by the Type II endothecial thickenings.
The remaining clade of the polytomy (number 6) suggests some new ideas about relationships and confirms some older ones. These taxa are united by presence of a distinct velamen (1), and at least in some optimizations, by presence of floral abscission (18), and prosenchymatic stigma cells (45). One of its daughter clades is Tropidia and the other is the epidendroids in the broad sense, meaning that Tropidia is sister to the epidendroid + vanilloid orchids.
The epidendroid + vanilloid clade is defined by an anther that bends late in development (27) and covered cell borders in the seed testa (53; reverses in the core Vanilleae). The vanilloid orchids (clade 7) have long been problematic as to placement in the family—again due to a lack of clear synapomorphies that unite them with other groups. They are well defined, here consisting of members of Pogoniinae (Pogonia), Palmorchideae (Palmorchis), and a core Vanilleae (Vanilla + Lecanorchis + Epistephium). The core Vanilleae are united by absence of stegmata (13), straight-walled abaxial epidermal leaf cells (15), presence of a calyculus (20), fusion of column to labellum margins (24), and a reversal to absence of the covered testa cell wall border (53). This core group is united with Pogonia and Palmorchis by carinate petals (23), and pollen in monads (34). Pogonia is united with the core based on the "flat, nonplicate" leaf (10) and presence of perianth abscission (19). Note that some of these character states (carinate petals, pollen monads, and perianth abscission) are otherwise distinctly plesiomorphic in the tree, appearing only in the apostasioids and relatives.
Sister to the vanilloids is a group containing several "proto-epidendroids" and what may be called the "true" epidendroids. They are united by a thickened stem (7), abaxial leaf epidermal cells with straight walls (15), type III-IV endothecial thickenings (30), and inaperturate pollen (36). The "proto" genera are unresolved here and are members of three tribes in Dressler's (1993)
system; two of them, Gastrodia and Epipogium, are leafless, while Nervilia has a single leaf. Like the vanilloids, their placement often has been uncertain.
Clade 8 corresponds largely with what may be called the "true" Epidendroideae. Although some other genera, including members of Neottieae and Vanilleae, are sometimes included in Epidendroideae, they are often alternatively considered to be part of the "neottioid" orchids (see Discussion). The members of clade 8 have generally been associated as a subfamily or equivalent unit and are united by an operculate anther (28) and a concave stigma (44). These genera correspond largely to the Epidendroideae + Vandoideae of Dressler (1981)
and Burns-Balogh and Funk (1986)
, and the Epidendroideae of most other recent authors (Dressler, 1993
; Szlachetko, 1995
). The most striking feature of this clade is that a large portion of it shows no resolution; the only groups revealed are small ones, namely, Coelogyne + Dendrobium, and Bulbophyllum + Sunipia + Genyorchis. Examination of the character distribution among these genera reveals that the lack of resolution is not due to a lack of character variation (see the single most parsimonious tree shown, Fig. 2), but rather a high degree of homoplasy, such that many alternate patterns are possible.
One conspicuous exception to the lack of resolution within clade 8 is clade 9. This group is clearly marked only by the presence of a tegula (33), and corresponds to the "vandoid" orchids, often treated as an informal group, but recognized as a subfamily by Dressler (1981)
. The vandoids also share superposed pollinia (42) and detachable viscidium (46), but these characters appear in a few nonvandoid epidendroids as well, so that depending upon the resolution, these characters might be plotted at the vandoid node or at a slightly less or more inclusive node. Among the vandoids, three other notable small groups are resolved. Neobenthamia + Polystachya are united by the polystachyoid calyculus, and Phalaenopsis + Acampe + Aerangis + Angraecum, representatives of the Old World tribe Vandeae, are united by distinctively shaped root exodermal cells (3) and monopodial habit (6). Cymbidium subgenus Cymbidium forms a small clade with Catasetum, Thecostele, and Acriopsis, based on shared possession of longitudinal seed striations (50) and seed testa wax caps (52).
The implied weighting analysis also reached the set tree limit—30 000 trees with fitness = 335.9. Its consensus tree (Fig. 3) is more resolved than the equally weighted consensus tree, particularly within the Epidendroideae. The Apostasioideae and Cypripedioideae are shown to be monophyletic. Here, in contrast to the equally weighted analysis, the Spiranthoideae and Orchidoideae (neither including Cryptostylis) are both monophyletic groups. Each of these has a unique character to support it—spiranthosomes for the Spiranthoideae and root tubers for the Orchidoideae. The Orchidoideae are sister to Cryptostylis + Neottieae (Epipactis, Cephalanthera, Listera + Epidendroideae, but based only on the absence of distinct subsidiary cells, which soon reverses in the tree (at the node above Tropidia). Epipactis, Cephalanthera, and Listera are united with the epidendroid + vanilloid clades, based mainly on vegetative characters—epidermal cell shape, phyllotaxy, and leaf morphology. As in the equally weighted tree, Tropidia is sister group to epidendroids + vanilloids, and vanilloids are sister to epidendroids. There are some differences in the epidendroid groups, however. Gastrodia, Nervilia, and Epipogium form a monophyletic group, based primarily on the presence of their unique sectile pollinia.
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) are united by the winter leaf. Several members of the Epidendreae form a monophyletic group, with the New World taxa (Arpophyllum, Epidendrum, Cattleya, Schomburgkia, Meiracyllium, and Chysis) forming a clade that is closely related to the Old World Agrostophyllum and Appendicula. Isochilus, Pleurothallis and Restrepia are also New World members of Dressler's Epidendreae, but show relationships to members of the other main epidendroid clade. The latter two, both members of the commonly recognized group Pleurothallidinae, are united in this analysis by the distinctive stalked ovary. Instead of Coelogyne and Dendrobium appearing as a distinct group, here they are members of a clade that also includes the vandoids. Surprisingly, there is less resolution among the vandoids in the implied weighting analysis than with equal weighting, as evidenced by a polytomy comprising several individual genera as well as four groups of genera. Both Cymbidium subg. Jensoa (Jensoa in the matrix) and Cymbidium subg. Cymbidium (Cymbidium in the matrix) are vandoids in this topology, and Polystachya + Neobenthamia are sister to the Vandeae, based on seed structure (48). Lockhartia and Oncidium, usually placed near one another in classifications (Oncidiinae: Dressler, 1993
), are here part of the vandoid polytomy, allowing for a possible closer relationship than in the equally weighted analysis, where they are several nodes apart. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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; Brown, 1810
; Lindley, 1840
)—of course many fewer species were known at that time. Subsequent systems have been more elaborate, employing more hierarchic levels and thereby implying that there is character support for this structure. These include Bentham (1881)
, Reichenbach (1884)
, Pfitzer (1987
, 1888–1889
), Schlechter (1926)
, Mansfeld (1937)
, Dressler and Dodson (1960)
, Vermeulen (1966)
, Dressler (1981)
, Rasmussen (1985)
, Burns-Balogh and Funk (1986)
, Dressler (1993)
, and Szlachetko (1995)
. Garay (1960)
recognized subfamilies, but did not produce a detailed classification system. Because most of these systems have not included explicit character analysis, it is often not clear which characters really support recognition of a particular group; the central problem is that intuitive classifications usually focus on different "key" characters in different parts of the family, meaning that it is often difficult to assess how characters interact over the family as a whole. In a cladistic framework, character support (or lack thereof) for groups is obvious, and it was with the purpose of evaluating support for morphological hypotheses of relationship that this study was undertaken.
As with many cladistic analyses of large groups based on morphological data, most groups are not supported by very many characters, simply because the ratio of characters to taxa is small. Examination of one of the most parsimonious trees from the equally weighted analysis (Fig. 2) reveals nodes with from one to six characters supporting them, with many of these being homoplastic changes. Since there are few enough character changes per branch that they can be shown, support indices such as bootstrapping (Felsenstein, 1985
), Bremer support (Bremer, 1988
), and jackknifing (Farris et al., 1996
) are less important for an analysis such as this than for most molecular analyses. However, we did implement Farris' (1995)
jackknife procedure on the data set for a more quantitative assessment of relative branch support. The results are not surprising, since those clades that appear in the strict consensus tree and are supported by several characters are the ones that receive greater jackknife support. Two small clades, Calypso + Tipularia and Restrepia + Pleurothallis, received jackknife support of over 50% but do not appear in the strict consensus tree, while other clades that have weaker jackknife support do appear in the consensus tree. This might at first seem unusual, but simply reflects the different operation of strict consensus and character resampling.
Although the ensemble consistency index in the equally weighted analysis is relatively low, it is not unusually low for the size of the data matrix (cf. Sanderson and Donoghue, 1989
). In spite of the high level of homoplasy, there is considerable structure in the consensus tree; this indicates that the effects of homoplasy (alternative branching patterns) are confined to specific areas of the trees. Additionally, the retention index is high (0.85), showing that the characters are functioning as synapomorphies to a high degree—most convergences and reversals are serving to unite taxa.
The resolution in (especially) the equally weighted tree has a distinct pattern—major groups of genera, equivalent to subfamilial groups, are clearly delimited, but groups within these (e.g., tribes and groups of tribes) are often poorly or not at all resolved. Not only are groups at the approximate rank of subfamily delimited, but the composition of these groups is remarkably similar to that in many previous classifications. This suggests that intuitive classifications of the past often have placed weight on "good" characters at these higher levels—unique apomorphies or sets of apomorphies that tend to unite large groups of genera—or at least that some of these major groups are phenetically quite distinct from each other, with particularly striking differences (such as erect vs. incumbent anther). Uniquely changing characters usually provide at least some of the support for these clades; although other, homoplastic characters may also occur at these nodes, without the unique apomorphies these clades have much less chance of appearing in the consensus tree. This is also true in the weighted analysis, where those characters that change only once are strongly favored. The lack of resolution at lower levels suggests that the detailed classifications at the tribal level are not well supported by morphological evidence in most cases and that at this level intuitive approaches may be drawing conclusions beyond the ability of the data.
Taxon relationships
Although the pattern of relationships may be clear in a cladistic analysis, there is often little agreement on how this pattern should be translated into a classification. The problem of the rank to assign a particular group is especially evident; even with agreement on a pattern, personal taste seems to dictate how finely the classification should be divided, how many groups at a particular rank should be recognized, etc. Without a robust pattern on which to base orchid classification, the situation has been even more difficult. For example, Dressler (1993)
recognized five subfamilies and ~23 tribes for the family, while Szlachetko (1995)
recognized ten subfamilies and 47 tribes (dividing the family into three families). Clearly, confidence in particular groups varies, depending upon branch support and comparison of data sets. As there are no rules for assigning rank to taxa, we can only follow a guideline of striving for an internally consistent system, hopefully one that will disturb the stability of past nomenclature as little as necessary.
The Apostasioideae are a relatively uncontroversial group; nearly every recent orchid treatment (Garay, 1960
; Dressler, 1981
, 1993
; Rasmussen, 1985
; Szlachetko, 1995
) has recognized this taxon at some level, either subfamily or family, as comprising Apostasia and Neuwiedia. Very few have separated the genera—Burns-Balogh and Funk (1986)
recognized Apostasioideae and Neuwiedioideae, concluding that the former was more closely related to Cypripedioideae than to the latter, based on their shared loss of the dorsal median stamen. Dahlgren (1989)
recognized two families, Apostasiaceae and Neuwiediaceae, concluding that there are no apomorphies that unite the genera. Judd, Stern, and Cheadle (1993)
and Stern, Cheadle, and Thorsch (1993)
concluded that the genera are closely related and described synapomorphies that unite them. In the present analysis, a new character was discovered that unites Apostasia and Neuwiedia – apiculate perianth parts. The other unique synapomorphy that they share is the operculate colpus (Schill, 1978
; Newton and Williams, 1978
). Some characters that appear on this branch (carinate petals, perianth abscission) also characterize other putatively "primitive" groups and appear elsewhere on the tree. The relative paucity of apomorphies explains the widely held view that the apostasioids are a "primitive" orchid group (e.g., Garay, 1960
; Dressler, 1981
, 1993
; Burns-Balogh and Funk, 1986
)—in fact they are in many salient ways transitional between a putative lilioid relative such as Hypoxis and the monandrous orchids, especially in functional stamen number, but also in their low degree of floral fusion and zygomorphy. The apostasioids are sister to the remainder of the orchids, a finding also reported by Judd, Stern, and Cheadle (1993)
.
The Cypripedioideae are a similarly straightforward subfamily. All recent systems of classification have recognized the group, easily identified by the slipper-shaped labellum, sometimes at the level of family (Rasmussen, 1985
; Dahlgren, 1989
). The endothecial thickenings (classified as type III) resemble those of the epidendroids more than they do those of the other basal groups, but this is shown to be a parallelism. Since Apostasia and Neuwiedia form a well-defined group in our analysis, it is most parsimonious to explain evolution of the diandrous morphology as parallel loss of the median stamen in Apostasia and Cypripedioideae—i.e., diandry has evolved twice in the orchids by loss of the median stamen, A1, rather than once (uniting Apostasia and Cypripedioids), as suggested by Burns-Balogh and Funk (1986)
. As only two genera (of 4–5 total) were included here, there is no indication of structure within the subfamily; Albert (1994)
produced a detailed analysis of relationships at this level.
The Cypripedioideae are sister to the remaining orchids, all of which are monandrous. This is contrary to the pattern obtained by Neyland and Urbatsch (1995
, 1996a
, b
), who found that Cypripedium fell among the monandrous taxa they examined (between Habenaria and the other monandrous taxa). Dressler and Chase (1995)
also suggested that the monandrous orchids may not be monophyletic, but it was the Vanilleae that fell between apostasioids and cypripedioids based on rbcL sequence information; further rbcL study by Kores et al. (1997)
was unable to resolve this issue.
The many genera of monandrous orchids have been subdivided in different ways, as reflected in the names used under different recent classifications—Neottioideae, Ophrydoideae, and Kerosphaeroideae (Garay, 1960
); Orchidoideae, Spiranthoideae, Epidendroideae, and Vandoideae (Dressler, 1981
); Orchidoideae, Spiranthoideae, and Epidendroideae (Dressler, 1993
); Thelymitroideae, Orchidoideae, Tropidioideae, Spiranthoideae, Neottioideae, Vanilloideae, Epidendroideae, and Vandoideae (Szlachetko, 1995
). The term "neottioid" is often used to describe those monandrous genera that share a number of plesiomorphic features, including soft pollinia and erect anthers. They are primarily terrestrial, and usually have soft, fleshy leaves. The assemblage has been taxonomically recognized in different ways, usually as two or three subfamilies. With respect to the topology in Fig. 1, the neottioid orchids, in the broad sense, comprise all monandrous orchids excluding clades 5 and 8. Clearly, this is not a monophyletic group when taken as a whole, as recognized by most recent analyses (Rasmussen, 1982
; Burns-Balogh and Funk, 1986
, etc.).
The equally weighted consensus tree (Fig. 1) has a polytomy at the base of the monandrous orchids consisting of four clades: the genera Epipactis and Cephalanthera, and the clades including Listera and Tropidia, respectively. Dressler (1993)
defined the tribe Neottieae to include Listera, Epipactis, and Cephalanthera based on plicate leaves and lack of subsidiary cells. Neither of the present analyses gives evidence that the tribe is monophyletic, since even if in a particular most parsimonious tree Epipactis and Cephalanthera were part of the Listera clade, there would be no feature that Listera, Epipactis, and Cephalanthera share uniquely. This is in contrast to rbcL data, which suggest that the genera do form a group (Kores et al., 1997
). Plicate leaves are shown to be a plesiomorphy at this level in the equally weighted analysis, as are lack of subsidiary cells. These genera have neither clearly epidendroid nor orchidoid features and appear to be basal members of one or the other (or both) of these clades (clade 3 or clade 6). They are more clearly associated with the epidendroids in the implied weighting analysis, as they are the molecular analysis of Kores et al. (1997)
. Dressler (1981)
placed the Neottieae in the Orchidoideae, and later (1993) placed it at the base of the Epidendroideae; Rasmussen (1985)
associated it with spiranthoids (see below), and Szlachetko (1995)
combined the genera with Diceratostele (not included in this analysis because of incomplete data) to form a separate subfamily at the base of the epidendroid clade.
Listera appears in the equally weighted analysis at the base of a clade that contains the majority (in terms of species) of neottioid orchids. This clade comprises the Orchidoideae and Spiranthoideae. Although not always recognized at the subfamily level or with exactly the same composition, major elements of both of these groups have appeared in most classifications. For example, almost all authors agree that the groups called by Dressler (1993)
Orchideae and Diseae together form a distinct group, as they do in these analyses (clade 5 in Fig. 1), sharing basal caudicles and sectile pollinia. Some (e.g., Burns-Balogh and Funk, 1986
; Szlachetko, 1995
) restrict the circumscription of this subfamily to these groups. Other authors (Dressler, 1981
, 1993
; Rasmussen, 1985
) have included additional groups in the Orchidoideae, namely those genera that fall into Dressler's (1993)
Diurideae. The Diurideae comprise Southern Hemisphere species that have largely granular (rarely sectile) pollinia, a rostellum near the middle or toward the apex of the anther, and root tubers (with few exceptions; shared with Orchideae and Diseae). In Fig. 1, the diurids comprise all the members of clade 3 excluding Listera, clades 4 and 5, and Triphora. Clearly, here they are a paraphyletic group, as some of them are more closely related to the Orchideae + Diseae, while others may be most closely related to the spiranthoids (clade 4). Burns-Balogh and Funk (1986)
also showed the diurids (defined in this way) to be paraphyletic. The pattern was inconclusive in Kores et al. (1997)
. Szlachetko (1995)
concluded that the diurids do form a group, although it was unclear which character could unite them; he showed them grouped with "true" orchidoids and spiranthoids by the presence of fleshy leaves—this character is also an apomorphy uniting these groups (+ Listera) in the present analysis. Root tubers have traditionally been an important character in defining the Orchidoideae in the broad sense, although not every species has them (Dressler, 1981
; Pridgeon and Chase, 1995
). The pattern observed here suggests that either tubers have been derived independently in different orchidoid groups, or if they were present in the common ancestor of all orchidoids, that they have been lost in some lineages, including the spiranthoids.
The equally weighted analysis suggests that the spiranthoid orchids (clade 4) have been derived from the diurids. Dressler (1981
, 1993
), Burns-Balogh and Funk (1986
; also including some diurids) and Szlachetko (1995)
recognized the former genera as a distinct subfamily, while Garay (1960)
, Rasmussen (1985)
, and most earlier authors included them in the Neottioideae (or comparable group). Our analyses suggest that they are a monophyletic group only if Tropidia is not included (see below), although no structure within the group is evident. A subset of spiranthoids, the Goodyerinae, are characterized by sectile pollinia but do not form a group within the spiranthoids here, indicating that one or more of Goodyera, Ludisia, and Zeuxine must be united with other spiranthoids in at least some trees. The implied weighting analysis places the spiranthoids as sister to the rest of the monandrous orchids, and hence outside of the diurid group; the implication of this pattern is that the root tuber may be a unique apomorphy for the diurids + orchidoids in the narrow sense. As yet, no empirical morphological evidence has been presented to support either character transformation. Pridgeon and Chase (1995)
detected no significant differences among tubers that would suggest that some are not homologous to others, and their pattern analysis was not conclusive with respect to relationships among diurids and spiranthoids. The rbcL analysis of Kores et al. (1997)
places the spiranthoids among the orchidoids, but their relationship to the diurids is uncertain.
One unusual hypothesis suggested by the present analyses is the placement of Triphora well within the diurids. Triphora is another taxon of questionable relationship, often placed in a vanilloid soft-pollinium group (Pfitzer, 1887
, Schlechter, 1926
; Dressler and Dodson, 1960
; Dressler, 1993
; Szlachetko, 1995
), or left as a taxon of uncertain affinities (Dressler, 1981
). Triphora fell within the orchidoids here because it shares with them an erect anther, endothecial thickenings that are intermediate between types I and II, apparently fleshy leaves, lack of subsidiary cells, and root tubers. Triphora seems to share little morphologically with the epidendroids. Placement among the orchidoids disagrees with evidence from rbcL, which places Triphora near Nervilia and Diceratostele, at the base of the epidendroids (K. Cameron, Guilford College, personal communication). If Triphora does belong with the epidendroids, it means that a suite of orchidoid characters has evolved independently.
Vegetative characters were excluded from the analysis of Burns-Balogh and Funk (1986)
, but were found to be very important in the current analysis and have been employed in most classifications since Pfitzer (1887)
. These characters comprise 31% of the current data set and provide a suite of characters that may not be under the same selective forces as floral characters. Because orchids are so specialized for insect pollination, floral characters are presumably under high selective pressures and may be expected sometimes to show convergence and nonindependence. It is therefore crucial to have characters that will provide tests for and reveal homoplasy in floral features. The vegetative characters serve that function in this data set. A good example of this effect is placement of Tropidia. Tropidia and Corymborkis (Tropidieae) are two small tropical genera that are usually allied with the spiranthoids based on floral morphology (e.g., Lindley, 1840
; Pfitzer, 1887
; Schlechter, 1926
; Dressler, 1981
, 1986
, 1993
; Burns-Balogh and Funk, 1986
), as they share with them an erect anther with apical viscidium, and sectile pollinia (in Goodyerinae). In the present analyses, Tropidia does not fall among the spiranthoids, but is sister to the very speciose clade that includes the epidendroids. The characters that place it are root velamen, distichous plicate leaves, presence of leaf sclerenchyma and subsidiary cells—all vegetative characters. This suggests that the spiranthoid floral morphology has been derived in parallel in Tropidia and in the spiranthoids. Stern et al. (1993b)
also concluded that Tropidia is more closely related to taxa such as Palmorchis and Diceratostele than to spiranthoids, based largely on vegetative characters, and this hypothesis now has support from rbcL sequence as well (Kores et al., 1997
). Recently, Szlachetko (1995)
recognized Tropidia + Corymborkis as a distinct subfamily (Tropidioideae), but did not indicate whether the group was more closely related to spiranthoid-orchidoids or epidendroids. We suggest that it is the overlooking of the importance of vegetative features that has precluded recognizing a close relationship between the Tropidieae and epidendroids in the past.
Tropidia is sister to the vanilloids (clade 7) and epidendroids. The core vanilloid group consists of Vanilla, Epistephium, and Lecanorchis, supported by three unique synapomorphies—lip marginally fused with column, presence of a calyculus, and polyporate pollen—among other synapomorphies. Vanilla and Epistephium have long been associated, but the leafless Lecanorchis has sometimes been placed in a different subtribe (Bentham, 1881
; Dressler, 1981
). In our tree, the core vanilloids are closely related to Pogonia and Palmorchis, which have often been associated with Vanilla (especially Pogonia; Pfitzer, 1887
; Schlechter, 1926
; Dressler and Dodson, 1960
; Garay, 1986
), although Dressler (1993)
listed Pogoniinae among the "primitive orchids of uncertain classification." Schlechter (1926)
saw a closer relationship between Palmorchis and Tropidia than between the former and Vanilla. Pogonia shares perianth abscission and nonplicate leaf with the core vanilloids, here appearing as apomorphies. In fact, the rbcL data of Kores et al. (1997)
also support a very close association between these groups. Their data do not support a close relationship between Palmorchis and the vanilloids, however, placing Palmorchis as sister to the Neottieae. Palmorchis is united with the vanilloids here on the basis of carinate petals and smooth, monad pollen.
The vanilloids are an unusual mixture of plesiomorphic and apomorphic states; the lack of clear synapomorphies uniting them with another group accounts for the traditional difficulties with their placement. Most authors have either placed them in a soft-pollinium neottioid group (Bentham, 1881
; Pfitzer, 1887
; Schlechter, 1926
; Garay, 1960
) or associated them with the epidendroid orchids (Dressler and Dodson, 1960
; Dressler, 1981
, 1993
; Burns-Balogh and Funk, 1986
; Szlachetko, 1995
) because of the emphasis placed on the incumbent anther. On the one hand, the vanilloids share a single, incumbent anther and floral abscission (at least the core vanilloids), characters that would unite them with the epidendroids. Yet they also are characterized by perianth abscission, monad pollen, and carinate petals, states found otherwise only among the apostasioids and other "basal" taxa. In this analysis, the latter are suggested to be reversals in the vanilloids. Not all evidence would unite vanilloids and epidendroids, however; the preliminary rbcL tree in Dressler and Chase (1995)
showed the vanilloids to be most closely related to cypripedioids + other monandrous orchids. The more detailed analysis in Kores et al. (1997)
is equivocal on this point, although more recent molecular data suggest that they are the first clade in the monandrous orchids (P. Kores and M. Chase, Royal Botanic Gardens, Kew; Freudenstein, unpublished data). With many morphological characters there is hope that more detailed study, often of ontogeny, will reveal additional information to refine homology hypotheses. An example of where this would be useful is the single stamen of vanilloids and epidendroids. If indeed reduction to a single stamen from three had occurred more than once, it is unlikely that there will be empirical evidence to suggest it, since it is a loss character. Hence, unless additional morphological characters are uncovered that can strengthen the morphological tree, we will be dependent on molecular data to address this question.
The remainder of the tree comprises those groups known as the epidendroid orchids. At the base of this clade, an assemblage of largely leafless (excepting Nervilia) genera with sectile pollinia (the "gastrodioids") forms a polytomy with the rest of the subfamily. These genera often have been included in the neottioid group, but some authors (Dressler, 1981
, 1993
; Burns-Balogh and Funk, 1986
) include them in the epidendroids because they share epidendroid features, in particular the incumbent anther. The implied weighting analysis unites the genera based on the epidendroid sectile pollinia, suggesting that this sectile pollinium morphology, distinct from that seen in orchidoids, may indeed be a homologous feature among these taxa.
The "true" epidendroids comprise clade 8, which contains the majority of species in the family. Some of the traditional characters for the subfamily define this clade and others support the gastrodioids + "true" epidendroids, meaning that the subfamily is not quite as sharply defined as is sometimes suggested. These characters include incumbent anther, thickened stems, sunken stigma, articulated leaves, operculate anther, and firm pollinia. The most striking feature of the equally weighted cladogram is how little resolution there is among most epidendroids—the great majority form a polytomy, with only one subclade of significant size. It may seem surprising that there so little resolution within the Epidendroideae as opposed to the other subfamilies, given that there is more variation among the characters used within the Epidendroideae than any other group. Still, there are relatively few variable characters for the size of the group, and they show a large amount of homoplasy in this subfamily. Nonetheless, most previous classifications have a highly developed tribal and subtribal classification within the Epidendroideae. Our results suggest that such classifications must rely on intuitive weighting of particular characters in order to achieve this structure. This emphasis on selected characters is sometimes evident in the descriptions of particular higher taxa, but the distributions of some characters can be difficult to ascertain on a family-wide basis since often not all taxa are described uniformly and completely.
Some small epidendroid groups are resolved, however, and in some cases correspond to previously recognized taxa. Bulbophyllum is united with Sunipia and Genyorchis in both analyses by several characters, (e.g., thickened root exodermis, pseudobulbs of a single node, and lateral inflorescence), none of which is unique to this group. Dressler (1981)
placed the three genera in separate subtribes—Bulbophyllum (Bulbophyllinae), Sunipia (Sunipiinae) (both of these in the Epidendroideae: Epidendreae), and Genyorchis (Genyorchidinae; Vandoideae: Cymbidieae). More recently, Dressler (1993)
united these genera in the Bulbophyllinae, while Szlachetko (1995)
maintained the three genera in separate subtribes in the Dendrobieae. Our analysis would argue for a very close relationship among them; maintaining separate subtribes simply to emphasize their autapomorphies is not worthwhile. Dendrobium and Coelogyne are united in the equally weighted analysis by, among other characters, seed testa striations. These genera are not usually considered particularly closely related, although the similarity in seed morphology has been noted (Ziegler, 1981
; Dressler, 1993
). Preliminary molecular data (Cameron, Freudenstein, and Chase, unpublished data) do not place them close together.
Some groups resolved only in the implied weighting analysis are similar to traditionally recognized taxa. Two possibilities exist for this correlation—either the groups are real, and implied weighting is giving us increased resolving power over equal weighting, or the analysis is misled by mistaken homology assessments in the same way that previous authors have been. Only additional data will be able to distinguish these possibilities. Two examples are Aplectrum + Calypso + Tipularia, and Arethusa + Calopogon. The first of these is recognized by Dressler (1993
) as part of the Calypsoeae, and was shown by Freudenstein (1994)
to form a closely knit group. The latter was suggested by Freudenstein and Rasmussen (1997)
to be closely related especially on the basis of pollinium structure, although they have at times been placed in separate subtribes (Dressler, 1993
). Another case is the close relationship among Arpophyllum, Epidendrum, Cattleya, Schomburgkia, Meiracyllium and Chysis, supporting Dressler's (1993
) Epidendreae (similar groups have often been recognized). Separation of the Old World and New World taxa was suggested by Dressler and is also supported here. Some taxa that fall into Dressler's Epidendreae (Pleurothallis, Restrepia, Isochilus) appear here in the other, larger, epidendroid clade among largely Old World members of the tribe (Eria, Thelasis, Ceratostylis), so it is clear that there are limits to the correspondence.
The one clade (number 9 in Fig. 1) of significant size resolved within the epidendroids in both analyses reflects a significant pattern of variation that is often recognized, comprising the orchids with superposed pollinia, lateral inflorescences, and stipe, often known as the "vandoid" orchids. Lindley (1840)
, Pfitzer (1887)
, and Schlechter (1926)
, the latter two of which put primary emphasis on inflorescence position, grouped these genera along with some others that would currently be called nonvandoid, in their Vandeae and Pleuranthae, respectively. Bentham's (1881)
Vandeae is most like the group recognized by Dressler (1981)
as subfamily Vandoideae. Another character that led Dressler to segregate these taxa was the position of the anther. Dressler (1981)
interpreted the vandoid anther as erect and ventrally dehiscing in these species, and the nonvandoid epidendroid anther as incumbent. Hirmer (1920)
, Rasmussen (1986b)
, and Kurzweil (1987a)
showed that the vandoid anther is in fact incumbent, but that it bends very early in development. Hence, there is a difference between the epidendroid and vandoid anthers, although it is not just as Dressler had originally interpreted it. Even so, Dressler (1986b)
subsequently concluded that these taxa do not form a natural assemblage and that the vandoid morphology had evolved several times from epidendroid ancestors. Dressler is not alone among recent authors in recognizing this subfamily, as Burns-Balogh and Funk (1986)
and Szlachetko (1995)
did as well.
Although the three primary vandoid characters can be optimized at the node below Govenia, each of these characters also occurs in other taxa among the epidendroids. In fact, Calypso has all three of these characters, (and other members of Calypsoeae [Aplectrum and Tipularia] have two). Interestingly, even in the weighted analysis Calypso does not form part of the vandoid clade, suggesting that it shares alternate synapomorphies with other epidendroid taxa. Recent molecular data suggest that Dressler (1986a)
was correct in asserting that the vandoid morphology has evolved multiple times (Freudenstein and Chase, unpublished data). Of the three characters, two (superposed pollinia and stipe) are directly involved in pollination. If it is true that the character suite has evolved more than once, it is perhaps not surprising that this is not revealed in the morphological tree, since parsimony seeks agreement in character patterns. Correlated changes, such as are seen in independent evolution of adaptive complexes, may well appear as synapomorphies in data sets with relatively few characters, since it is unlikely that there will be enough other characters to support alternate topologies. This will lead to an underestimation of the number of times that the suite has evolved in both the equally weighted and implied weighting analyses.
Among the vandoids a few groups stand out. Catasetum + Cymbidium subgenus Cymbidium + Thecostele + Acriopsis are united by seed characters that were described by Chase and Pippen (1990)
, although the pattern of relationships among these genera differs somewhat here from that obtained in their study. Both Dressler (1993)
and Szlachetko (1995)
recognized a fairly close relationship among these genera. A sister group relationship between Acriopsis and Thecostele is suggested here based on what is shown to be a reversion to the juxtaposed pollinium arrangement from superposed. These genera are still often maintained in separate subtribes (Dressler, 1993
: Szlachetko, 1995
).
The long-recognized relationship among the monopodial Vandeae is strongly supported here, with Phalaenopsis + Acampe + Aerangis + Angraeum having two unambiguous synapomorphies uniting them and strong jackknife support. The monopodial habit thus appears to have evolved only twice (Vandeae and Vanilla) among the orchids included in this study.
Members of the Maxillarieae (Dressler, 1993
) are distributed through the vandoid clade. In the weighted analysis, Stanhopea is near the base of the clade, while others, such as Telipogon, are much more nested in the tree. A distinct group in both analyses is Xylobium + Lycaste + Zygopetalum, united by plicate leaves, but apart from Stanhopea, which also has plicate leaves, because of differences in pollinium number and seed morphology. Polystachya and Neobenthamia are united by the unique polystachyoid calyculus; they comprise the Polystachyinae of Dressler (1993)
and other authors.
Dichaea and Lockhartia are united in the equally weighted consenus, based on lack of leaf articulation. In fact, some species of Dichaea do have articulate leaves (Dressler, 1981
). Lockhartia is usually placed in Oncidiinae, but is modified vegetatively from other members of that subtribe, having distichous imbricate leaves instead of pseudobulbs. These vegetative differences account for the separation of Lockhartia and Oncidium on the cladogram. The imbricate leaf morphology may well be associated with the nonarticulate condition, so this relationship needs to be scrutinized carefully.
Stamen evolution
This analysis supports some previous suppositions about character evolution in orchids. Unfortunately, there is not enough resolution in some parts of the tree (Epidendroideae) or strong branch support overall to make many confident assertions about character transformation. Dressler and Dodson (1960)
provided a table of general trends within the family, and notwithstanding occasional reversals, of those that can be evaluated here all are in agreement with the character transformations from our tree except perhaps for phyllotaxy, and this is because phyllotaxy is a more complex character than previously has been perceived (see discussion under the character description).
One character of particular significance in orchid taxonomy is stamen number, which has received some attention in the literature recently. Stamen number defines some major orchid groups—Apostasioideae, Cypripedioideae ("Diandrae"), and the remainder of orchids ("Monandrae"). The variation seen in number of functional stamens has led to speculation about the evolution of the androecium. The identity of the functional stamens, relative to those present in a putative liliaceous ancestor, was worked out by Brown (1833)
, Darwin (1862)
, Swamy (1948)
, and Rao (1974)
. Remnants of some stamens, now nonfunctional, are believed to exist in some groups as ancillary structures on the gynostemium (Kurzweil, 1987a
, b
, 1988
). Burns-Balogh and Funk (1986)
concluded that the diandrous condition, seen in Apostasia and the cypripedioids, evolved once, and was therefore a synapomorphy uniting these taxa (see above). Neyland and Urbatsch (1996a)
discussed evolution of stamen characters based on an analysis of molecular data; they did not address how many times diandry has arisen, but did reach the following conclusions: (1) diandry in cypripedioids is apomorphic and was likely derived from a monandrous state, and (2) it is not clear whether the triandry seen in Neuwiedia is a plesiomorphy or an apomorphy. Their conclusions depend on both the topology of their tree and the method they used to code stamen characters. The topology may be questioned because of the extremely poor sampling employed in the analysis (one species per subfamily), but more relevant here is the character coding. Results of the present study and an analysis of their coding allow us to consider the evolution of stamen number.
What are the ways in which stamen number morphologies could be treated as characters? One possibility, employed by Neyland and Urbatsch (1996a)
and Burns-Balogh and Funk (1986)
, is to code each number—six (in outgroups), three, two, or one functional stamens—as a state of a single multistate character, unordered in the case of Neyland and Urbatsch (1996a)
, and ordering not specified by Burns-Balogh and Funk (1986)
. Another possibility is to code the presence/absence of particular stamens or groups of stamens as individual binary characters, as done here. Hence, presence/absence of A1 is one character, and presence/absence of a1 and a2 (taken together since they do not vary individually) is another. We would argue that this latter coding preserves more of the hierarchical information present in the characters, since the number states are not mutually exclusive with respect to the stamens that are present (i.e., A1 is present in both apostasioids and the monandrous orchids). The result of such coding in our analysis is that the transformations in stamen number are seen to be loss characters rather than transformations between unrelated states.
With respect to ancestral states, there is no clear evidence either in the present study or in the molecular study of Neyland and Urbatsch (1996a)
to support their notions that the diandrous orchids evolved from a monandrous ancestor or that three functional stamens might be an autapomorphy for Neuwiedia. If we plot the two stamen characters as we have coded them (plus a character to accommodate the A2, A3, and a3 stamens present in Hypoxis, but not in orchids) on our equally weighted consensus tree (Figs. 4–5), it is clear that the most parsimonious optimization (Fig. 4) requires a loss of stamen A1 in the diandrous lineage, and of stamens a1 and a2 in the monandrous lineage. This suggests that the ancestor to both the diandrous and monandrous lineages had three stamens. Similarly, we can plot the stamen characters as we have coded them on the tree in Neyland and Urbatsch (1996a
; Fig. 2) and find two equally parsimonious optimizations for these states (Figs. 6–7). In one (Fig. 6), the two lateral stamens are lost in the main lineage and then regained in Cypripedium, where the median stamen is also lost (three steps—indicating a monandrous ancestor for Cypripedium). In the other (Fig. 7), the two lateral stamens are lost in Habenaria and independently in the group comprising the other monandrous orchids, while the median stamen is lost in Cypripedium (three steps—indicating a triandrous ancestor for Cypripedium). Thus while a monandrous ancestor for Cypripedium is a possibility, it is equally likely that the ancestor was triandrous. The former would require loss of the lateral stamens followed by regain of the lateral stamens and loss of the median stamens in the Cypripedium lineage, while the latter would entail only stamen losses. Although loss would seem more likely, it is difficult to argue the probabilities of either scenario, leaving the ancestral state optimization ambiguous. In both our tree and that of Neyland and Urbatsch (1996a)
, plotting the stamen characters as we have coded them indicates that the ancestor of the triandrous orchids had at least three stamens, because outgroups to the family (lilioid monocots such as Hypoxis) have at least A1, a1, and a2. Hence, triandry cannot be an autapomorphy for Neuwiedia, since triandry is a plesiomorphy within the Orchidaceae; assuming that the ancestor to Apostasia and Neuwiedia had only two stamens is not parsimonious (Fig. 5). The possibility that triandry is an autapomorphy for Neuwiedia is only apparent when stamen number states are erroneously coded as an unordered series, leading to more uncertainty than is actually present in the data (cf. Neyland and Urbatsch, 1996a
; Fig. 3). The presence or absence of stamens A2, A3, and a1 was not included as a character in our study because we were not testing the monophyly of the family, for which a number of other nonorchid taxa should be included. However, it is clear that loss of these stamens may be considered a synapomorphy for the Orchidaceae, since no orchids have them.
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FOOTNOTES |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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