DNA data and Orchidaceae systematics: a new phylogenetic classification

Abstract

Orchidaceae are rapidly becoming one of the best-studied families of the angiosperms in terms of infra-familial phylogenetic relationships. These studies demonstrate that several previous concepts about phylogenetic patterns were incorrect, which make all previous classifications in need of review. Therefore, in this paper we describe the emerging patterns and propose a new phylogenetic classification of Orchidaceae that accords with these newly discovered relationships. We recognise five subfamilies: Apostasioideae, Vanilloideae, Cypripedioideae, Orchidoideae and Epidendroideae, the last containing the bulk of the taxa in the family. Apostasioideae are sister to all the rest, followed successively by Vanilloideae, Cypripedioideae and the remainder of the monandrous orchids, Orchidoideae and Epidendroideae. Although only an interim classification, it should help to focus other areas of orchid research and stimulate the creation of new hypotheses that will direct orchid researchers to new questions.

Full text

Chapter 5
DNA DATA AND ORCHIDACEAE SYSTEMATICS: A NEW
PHYLOGENETIC CLASSIFICATION
Mark W. Chase
Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK.
Kenneth M. Cameron
The Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies, The New York Botanical Garden,
Bronx, New York 10458-5126, USA.
Russell L. Barrett
Kings Park and Botanic Garden, Botanic Gardens and Parks Authority, West Perth, 6005, Western Australia and
Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley 6009,
Western Australia.
John V. Freudenstein
Ohio State University Herbarium, 1315 Kinnear Road, Columbus, Ohio 43212-1157, USA.
Orchidaceae are rapidly becoming one of the best-studied families of the angiosperms in terms
of infra-familial phylogenetic relationships. These studies demonstrate that several previous
concepts about phylogenetic patterns were incorrect, which make all previous classications in
need of review. Therefore, in this paper we describe the emerging patterns and propose a new
phylogenetic classication of Orchidaceae that accords with these newly discovered relationships.
We recognise ve subfamilies: Apostasioideae, Vanilloideae, Cypripedioideae, Orchidoideae and
Epidendroideae, the last containing the bulk of the taxa in the family. Apostasioideae are sister
to all the rest, followed successively by Vanilloideae, Cypripedioideae and the remainder of the
monandrous orchids, Orchidoideae and Epidendroideae. Although only an interim classication,
it should help to focus other areas of orchid research and stimulate the creation of new hypotheses
that will direct orchid researchers to new questions.
1. Introduction
For many years, orchid classication has been based almost exclusively on features of their
gymnostemium or column (Brown, 1810; Lindley, 1840; Ptzer, 1887; Schlechter, 1926; Swartz,
1800). In the two most recent of these systems, an evolutionary progression was hypothesised
from two or three anthers in the apostasioid orchids (Apostasia and Neuwiedia) through two in the
cypripedioids (Cypripedium, Mexipedium, Paphiopedilum, Phragmipedium, and Selenipedium) to
K.W. Dixon, S.P. Kell, R.L. Barrett and P.J. Cribb (eds) 2003. Orchid Conservation. pp. 69–89.
© Natural History Publications, Kota Kinabalu, Sabah.
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one in the monandrous orchids (Epidendroideae, Orchidoideae and Spiranthoideae sensu Dressler,
1993). Within the monandrous orchids, which contain the great majority of orchid taxa, classication
has depended largely on whether pollen in the anther was loose or formed into packets of various
sorts, including hard pollinia. In the apostasioids, pollen is powdery as it is in most groups of
Asparagales (sensu Angiosperm Phylogeny Group (APG), 1998), but in all other orchids, pollen is
at least sticky and self-adherent so that it travels in packets, which is probably related to the large
number of ovules in the ovaries of most orchids. In the most highly evolved groups of epidendroid
orchids (roughly 80% of the species in the family; Dressler, 1993), pollen is rmly bound into hard
pollinia deposited as complete units in the stigmatic cavity, but in the other monandrous orchids,
there is every possible intermediate stage between free monads and hard pollinia. Most systems
have also emphasised the other structures that comprise pollinaria, such as stipes, caudicles, and
viscidia, but only a few older classications (e.g. Ptzer, 1887) have incorporated any number of
vegetative characters.
Because orchid classication has largely been based on the relative degree of organisation of
the pollinia, the distinction between Neottioideae and Epidendroideae has been highly problematic,
such that the more primitive group, Neottioideae, has been variously narrowly and broadly dened.
In Dressler’s two schemes (1981; 1993), the neottioid orchids were narrowly treated. In addition to
circumscription of the neottioids, the other major group of orchids that has been problematic is the
vanilloids. Their columns are much like those of the epidendroids, but vegetatively they are highly
divergent from all other orchids (Cameron and Dickison, 1998; Stern and Judd, 2000).
More recently, orchid systematists have begun the process of incorporating other categories
of morphological information into their classications (Dressler and Dodson, 1960; Garay, 1960;
1972; Vermeulen, 1966; Rasmussen, 1985; Burns-Balogh and Funk, 1986; Brieger, Butzin and
Senghas, 1995; Szlachetko, 1995), but this process has only infrequently been couched in terms
of explicitly phylogenetic studies (Freudenstein and Rasmussen, 1999). Burns-Balogh and Funk
(1986) presented their arguments in cladogram format, but no formal analysis was conducted.
Dressler (1981; 1993) also conveyed his ideas about relationships in the form of cladograms
with characters mapped onto them, but their structure was purely intuitive. The results of the
morphological analyses of Freudenstein and Rasmussen (1999) indicated that the high degree
of hierarchical structure in all previous classications of Orchidaceae was not warranted; this
assertion was grounded on the fact that their cladistic analyses of morphological data showed little
resolution at lower taxonomic levels. They did, in contrast, provide support for some of the various
subfamilial groupings recognised in most previous systems of classication, such as Apostasioideae,
Cypripedioideae, Orchidoideae and Epidendroideae.
Molecular data have come to play an increasingly important role in angiosperm classication
(Chase et al., 1993; 2000a; b; APG, 1998; Soltis, Soltis and Chase, 1999; Chase, Fay and
Savolainen, 2000; Savolainen et al., 2000; Soltis et al., 2000), and although the main focus has
been at the supra-familial level, increasingly efforts are being focused on familial classication
(Sheahan and Chase, 1996; 2000; Chase et al., 2000c; Richardson, Fay and Chase, 2000). Within
Orchidaceae, numerous DNA phylogenetic studies have now been published, ranging from the
whole family (Neyland and Urbatsch, 1993; Chase et al., 1994; Cameron et al., 1999; Molvray,
Kores and Chase, 2000; Freudenstein, Senyo and Chase, 2000a; b), subfamilies (Cox et al., 1997;
Kores et al., 1997), tribes (Cameron and Chase, 1999; Douzery et al., 1999; Kores et al., 2000;
Whitten, Williams and Chase, 2000; Goldman et al., 2001), subtribes (Chase and Palmer, 1989;
1992; 1997; Chase and Hills, 1992; Yukawa, Cameron and Chase, 1996; Pridgeon et al., 1997;
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Generic delimitation in several subtribes has also been studied. Whitten et al. (2000)
demonstrated that generic limits in Stanhopeinae accord nearly perfectly with DNA results, as was
also true in the earlier work on Catasetinae (Chase and Hills, 1992; Pridgeon and Chase, 1998),
so DNA results do not contradict previous generic schemes based on (intuitively interpreted)
morphological information in all cases. Oncidiinae (Williams et al., 2001) are a good example
in which many genera have long been thought unsatisfactorily circumscribed (Garay and Stacy,
1976; Chase, 1986; 1987), so the gross polyphyly of the two largest genera, Odontoglossum and
Oncidium, came as a surprise to no one. Our list of Oncidiinae genera in the Appendix reects some
of the recent nomenclatural changes, but many more are planned to bring generic delimitation into
the line with a strict concept of monophyly. Likewise, many changes are in store for Eulophiinae
(Cribb, Pridgeon, Norup and Chase, in prep), Maxillariinae (Whitten, Atwood et al., in prep.), and
Zygopetalinae (Whitten, Dressler, Williams et al., in prep.).
3. Conclusions
All of these changes in taxonomy will be reected in Genera Orchidacearum (Pridgeon et al., 1999;
2001; 2003). We expect the classication as outlined here to be ephemeral (hopefully for not longer
than the next ve years), but it should serve a useful interim purpose of giving other researchers
a better place to start than Dressler (1993), which in spite of its admirable qualities is out of date.
Nevertheless, we still recommend that orchid researchers continue to consult his treatment; it
contains a wealth of information and ideas, many of which are still relevant.
Orchids should be one of the premier groups of owering plants for evolutionary studies, and
the massive amounts of DNA data now accumulating are revolutionising our ideas about these
wonderful plants. Darwin’s next book after On the Origin of Species was focused on orchids, and
the reasons for this are clear: orchids should be studied more because they epitomise evolution in its
most dynamic aspect, the rapid production of an incredibly diverse array of species. The challenge
is to understand how this has come about, and so intensive study of this largest angiosperm family
is highly appropriate. We hope that this new classication of the family facilitates research on
Orchidaceae in the same manner as have Dressler’s previous classications (1981; 1993) and that it
stimulates an understanding of the urgent need to conserve these evolutionary marvels.
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