Biological journal of the Linnean So&& ( I987), 30: 9 1-98
Reconciliation of evolution and
nomenclature among the higher
taxa of protists*
PETER HEYWOOD AND LYNN J. ROTHSCHILD
Division of Biology and Medicine, Brown Universily,
Providence, RI 02912, U.S.A.
Received I October 1986, accepted for publication 9 October 1986
Existing taxonomic schemes for the protists at the highest levels are confusing owing to insensitivity
to evolutionary data, lack of stability, evolutionarily misleading terminology and multiple,
contradictory systems. We propose a system which circumvents these problems by recognizing the
largest monophyletic groups possible, and creating a nomenclature for these by appending the suffix
‘protista’ onto an already recognizable prefix: for example, euglenoprotista, cilioprotista,
chytridioprotista. This system provides a high degree of stability while also allowing for the further
clustering of these groups and inclusion of their descendant groups, such as the plants, as more
evolutionary data become available.
KEY WORDS: --Protists
-
evolution
-
taxonomy - nomenclature
-
phylogeny
-
protozoa
-
algae.
CONTENTS
Introduction: a problem of nomenclatural prejudice.
Solution: adoption of the suffix “protista” . . .
Rationale: protozoa, protoctista, primalia or protista?
Advantages of the proposed system . . . . .
References.
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97
I N l R O D U C T I O N : A PROBLEM OF NOMENCLATURAL PREJUDICE
While the intrigue with protistan evolution is rising (demonstrated by an
increasing number of meetings and societies concerned with the subject), as is
the use of protists as model systems in experimental biology (e.g. Cande &
McDonald, 1985; Cech, 1986; Preer, Preer, Rudman & Barnett, 1985; SmithSonneborn, 1983, 1985), the existing taxonomic and nomenclatural schemes for
the protists at the highest taxonomic levels are becoming increasingly
indefensible on evolutionary grounds. This situation diminishes the usefulness of
the protists for, and actually confounds, the afore-mentioned disciplines.
Taxonomy should function as an information storage/retrieval system (primarily
evolutionary information in the post-Darwinian era, with other information
‘This work is the result of equal contributions by the authors.
91
0024-4066/87/010091 +08 803.00/0
0 1987 The Linnean Society of London
92
P. HEYWOOD AND L. J. ROTHSCHILD
being a consequence of genealogy), and nomenclature should assist in retrieval.
To be of use, the system which maximizes stability without sacrificing
evolutionary sensitivity is optimal. Existing schemes for protistan taxonomy fall
far short of these ideals. In an effort to remedy these problems, we propose a
system which maximizes the philosophically optimal taxonomic scheme with
ease of conversion from existing schemes (Rothschild & Heywood, 1986). As
more evolutionary data (e.g. from molecular biology) become available, it is
hoped that this proposal will provide a base to which the taxonomy of the
remaining eukaryotes may be connected.
Taxonomy should contain genealogical information, yet protistan taxonomy
in many cases does not, in part because of our checkered knowledge regarding
the evolution of these organisms and in part because of historical misconceptions
regarding affinity. Most egregious in this latter respect is the legacy of the twokingdom system. This system recognizes plants (photosynthetic or immobile
organisms) and animals (mobile organisms), and has forced inappropriate
alignments on the protists, as pointed out since the 19th century (see Whittaker,
1969 and references cited therein.) However, in important cases these features
have been shown to be convergent (e.g. the cell wall of bacteria, plants, and
fungi), there exist mobile, photosynthetic organisms (exemplified by Euglena),
and the symbiotic origin of chloroplasts is probable (Rothschild & Heywood, in
press), consequently taxa resulting from this legacy are often indefensible from a
phylogenetic viewpoint. Another result is the artificial splitting of closely related
taxa into ‘Protozoa’ and ‘Algae’, thus placing closely related taxa under the
jurisdiction of different codes of nomenclature. Some taxa (e.g. the
dinoflagellates) are recognized by both groups of workers, and are thus treated
by both the zoological and Botanical Codes of Nomenclature (Corliss, 1983).
Treatments differ in part because the criteria used to distinguish the higher
taxomonic categories in phycology (e.g. pigmentation, storage products,
flagellation, Bold & Wynne, 1985), and in protozoology (e.g. locomotory
organelles, absence or presence of photosynthesis, Lee, Hutner & Bovee, 1985)
are different, which results in contradictory schemes for the same taxa (see
Fig. 1).
Note that in zoological systems, such as that presented in Fig. 1, the grouping
together of a number of unicellular photosynthetic protists into a class implies a
closer evolutionary relationship than may actually exist. For example, the orders
Cryptomonadida, Dinoflagellida, and Volvocida differ from each other in many
ultrastructural and biochemical features (Rothschild & Heywood, 1987),
such as flagellar apparatus, nuclear structure and division, and chloroplast
structure and biochemistry. With regard to the latter point, the differences may
be due to the origin of the chloroplast from a symbiotic event involving the
acquisition of a chloroplast, or even an entire eukaryotic cell, by a host cell. For
example, it has been hypothesized that different symbiotic associations gave rise
to the Cryptomonadida (Gibbs, 1981; Roberts, Stewart & Mattox, 1981), the
Dinoflagellida (Tomas & Cox, 1973), the Euglenida (Gibbs, 1981), and the
Chlorarachnida (Hibberd & Norris, 1984). If this is indeed the case, and there is
strong evidence for it, then inclusion into a single class implies an evolutionary
relatedness which does not exist. At the same time, the separation into
Phytomastigophorea and Zoomastigophorea is a n artificial one (e.g. Honigberg,
Balamuth, Bovee et al., 1964). One effect of this is to separate artificially
PROTISTAN EVOLUTION AND NOMENCLATURE
Kingdom Animolio
93
Kingdom Plontoe
&
algal divisionst
Sub kingdom Protozoo*
Phylum Sorcomostigophoro
Division Cryptophyto
Subphylum Mostigophoro
Division Pyrrhophyto
Class Phytomostigophoreo
Order Cryptomonodido
Division Chrysophyto
Class Chrysophyceoe
Order Dinoflogellido
Euglenida
Order Chrysomonadido
Order Silicoflogellido
Division Euglenophyto
<
Order Prymnesiida <
Subclass Chrysophycidoe
Subclass Dictyochophycidoe
z Order Dictyocholes
> Class Prymnesiophyceae
::--
Order Heteromonodido <
* Class Xonthophyceoe
Order Rophidomonodido
(Class Eustigmatophyceoe)
Order Volvocido
Class Rophidophyceoe
Order Prosinomonodido
Order Chlororochnido
Class Zoomostigophorea
(Class Boci I loriophyceoe)
Division Chlorophyto
Class Chlorophyceoe
(Order Choonoflogellido)
0 rder Vol voco les
(Order Cercomonodido)
(+ 15 more orders)
(Order Proteromonodido)
Division Chlororochniophyto
(Order Retortomonodido)
(Order Oxymonodido)
(Order Diplomonodido)
(Order Hypermostigidio )
(Order Ebri ido
(Order Kinetoplostido)
Figure I . Treatment of selected flagellated protists according to conventional zoological and
botanical nomenclature. Taxa not covered by both systems are mentioned parenthetically, while
some degree of correspondence between taxa is indicated by an arrow. We have included the
Chlorarachrida since they clearly belong to the Phytomastigophorea (Hibberd & Norris, 1984).
*Classification according to Lee d al. (1985). tClassification according to Bold & Wynne (1985).
organisms which may be evolutionarily closely related: for example, there are a
number of shared ultrastructural and biochemical features between the
Euglenida and the Kinetoplastida (Delihas, Anderson, Andresini, Kaufman &
Lyman, 1981; Kumazaki, Hori & Osawa 1982; Kivic & Walne, 1984; but also
see Sogin, Elwood & Gunderson 1986), but under the current classification of
the protozoa (Levine, Corliss, Cox et al., 1980) these are separated under the
Phytomastigophorea and Zoomastigophorea, respectively.
94
P. HEYWOOD AND L. J. ROTHSCHILD
An additional drawback to the current systems is that they tend to understate
the differences among major groups of organisms; for example, many of the
orders of the Phytomastigophorea differ profoundly from each other in terms of
their ultrastructure, biochemistry, and evolutionary origins. This is reflected in
the higher rank assigned by botanists; for example, the euglenoids are treated as
either the class Euglenophyceae (Leedale, Schiff & Buetow, 1982) or as the
division Euglenophyta (Bold & Wynne, 1985).
If the errors of previous systems are to be avoided, two questions must be
answered: what is the evolutionary position of the kingdom Protista? and what
are the genealogical relationships among the major subgroups of protists? The
protists are eukaryotes which are predominantly unicellular or with no more
than one tissue type (Corliss, 1984), which suggests polyphyly if either the
eukaryotes were derived polyphyletically or if some unicellular forms are
secondarily reduced. Similarities in all eukaryotes (Cavalier-Smith, 1981 )
suggest a single line of descent for the nucleus and cytoplasm, and if secondarily
derived ‘protists’ are removed from the Protista, the protists become an
evolutionarily coherent group consisting of the taxa most closely related to the
common ancestor of the eukaryotes. When the prokaryotes were considered the
ancestral stock from which the protists arose, it was tempting to avoid
paraphyly by treating the eukaryotes as a subkingdom of their ancestral taxon.
However this is no longer necessary, as Darnel1 & Doolittle (1986) point out
the likelihood that the eukaryotes and prokaryotes arose from a common stock.
Relationships among taxa are not easy to discern (Rothschild & Heywood,
1987), and so rigid systems must be overhauled frequently to accommodate new
evolutionary data.
SOLUTION: ADOPTION OF THE SUFFIX “PROIISTA”
We suggest that these problems with protistan phylogenetics can be overcome
by ( 1 ) identifying the largest monophyletic groups commonly recognized and
(2) creating a nomenclature for these higher taxa out of a prefix routinely
associated with the groups and the suffix ‘protistan’ or ‘protist’ where used as an
adjectival or singular form and ‘protista’ as a plural form (Rothschild &
Heywood, 1986). A minor variant on this suggestion would be to use the suffix
‘protists’ as a more informal designation among English speakers. An example of
this approach would be to use the stem ‘eugleno’ of the organisms variously
designated Euglenida, Euglenophyceae, Euglenophyta, and Euglenozoa to form
the term ‘euglenoprotista’, where the absence of a capital letter denotes the
informal status of this system. Further examples are provided in Table 1, where
the simplicity of the proposed system is seen to be in stark contrast to the
complexities caused by attempting to reconcile existing nomenclatural systems.
The suggested abandonment of the strict Linnaean system for higher taxa is
similar to that which has recently been instituted for the prokaryotes (Stanier,
Adelberg & Ingraham, 1976).
RATIONALE: PROTOZOA, PROTOCTISTA, PRIMILIA OR PROlISTA?
It should be noted that there are several reasons that the suffix ‘protista’ was
chosen. ‘Protista’ is a commonly recognized name for the group, although when
this term was originally proposed by Haeckel (1866) the group included several
95
PROTISTAN EVOLUTION AND NOMENCLATURE
taxa which are now considered bacteria or metazoa (i.e. the Moneres and the
Spongiae) and did not include several taxa which are now recognized as protists
(i.e. the Archephyta which included chloroprotista and cyanobacteria, the
Fucoideae or the phaeoprotista, the Florideae or rhodoprotista, and the
Infusoria which included the cilioprotista) . Haeckel altered the constitution of
the Protista in subsequent publications (see Haeckel, 1878,1892), and today the
Protista is considered to include the protozoa and algae, sensu Zuto, and
sometimes several groups of unicellular fungi.
Several years before Haeckel, Richard Owen pointed out the necessity for
another kingdom of organisms to include the “. . . numerous beings, mostly of
minute size and retaining the form of nucleated cells, which manifest the
common organic characters, but without the distinctive superadditions of true
plants or animals.” (Owen, 1859). Owen dubbed this kingdom the “Protozoa”,
or “first life or living thing” (Owen, 1859; 1860; 1861). However, we agree with
Hogg (1860) that the adoption of Owen’s term with his usage would be
inappropriate and cause confusion since the common translation of “protozoa”
is ‘first or primitive animal’. Hogg (1860) suggested instead that the additional
kingdom be called the Regnum Primigenum, which would include the
“Protoctista”, that is the “Protophyta” and “Protozoa”. I t is unclear from this
work whether Hogg intended to include the sponges in the Regnum
Primigenum, although this seems to be a reasonable interpretation since Hogg
objected to their designation as “Amorphozoa” and instead proposed the term
“Amorphoctista”, or ‘amorphous beings’. Secondly, many authors at the time of
Haeckel included the sponges in the “Protozoa” (see, for example, the entry
“Protozoa” in the glossary prepared by W. S. Dallas for the 6th edition of The
Origin of Species, Darwin, 1872), and so it is possible that Hogg intended to
subsume the sponges under this group.
Table 1. Effects of the proposed system on taxa previously assigned to the algae,
selected protozoa, and ‘lower fungi’
Proposed term
Common name
Botanical name
chloroprotista
Green algae
Division Chlorophyta
euglenoprotista
chlorarachnioprotist a
cryptoprotista
chrysoprotista
xanthoprotista
haptoprotista*
bacillarioprotista
raphidoprotista
dinoprotista
eustigmatoprotista
acrasioprotista
Euglenoids
Division Euglenophyta
Division Chlorarachniophyta
Division Cryptophyta
Class Chrysophyceae
Class Xanthophyceae
Class Haptophyceae
Class Bacillariophyceae
Class Raphidophyceae
Division Dinophyta
Class Eustigmatophyceae
Class Acrasiomycetes
myxoprotista
chytridioprotista
ooprotista
cilioprotista
Cryptomonads
Golden-brown algae
Yellow-green algae
Haptophytes
Diatoms
Raphidophytes
Dinoflagellates
Eustigmatophytes
Cellular slime molds
Acellular slime molds
Chytrids
Ciliates
Class Myxomycetes
Class Chytridiomycetes
Class Oomycetes
Zoological name
various subgroups of the
phytoflagellates
Order Euglenida; Euglenozoa
subgroup of subphylum Sarcodina
Order Cryptomonadida
Order Chrysomonadida
Order Heteromonadida
Order Prymnesiida
Order Raphidomonadida
Order Dinoflagellida
Order Dictyosteliida and
subclass Guttulinia
Subclass Myxogastria
Phylum Ciliophora
*We have chosen to designate these organisms as ‘haptoprotista’ rather than ‘prymnesioprotista’ to avoid typifying a
higher taxon on the basis of one of its members.
96
P. HEYWOOD AND L. J. ROTHSCHILD
In a work that has rarely been mentioned in recent debates, Wilson & Cassin
(1863) also proposed the formation of an additional kingdom to accommodate
organisms that are not clearly animals or plants, but are of “cellular structure
only”. However, we do not wish to adopt the “Kingdom Primalia” of Wilson &
Cassin (1863) because it is neither coincident with current conceptions of the
group (for example, it includes lichens and sponges) and it would not be widely
understood. Furthermore, the most likely suffix to be derived from “Primalia”
would have clear animalian, and thus prejudicial, connotations.
It is apparent that none of the earlier proposed terms were likely to have been
defined originally in a way that is identical with our current conceptions of the
kingdom. Therefore priority need not be considered in choosing a name for the
kingdom. Anyway, the codes of nomenclature do not apply to taxa over the
familial level. Rather, ‘protista’ is here used because, in contrast to ‘protoctista’,
it is short and euphonious, its meaning is clear, and it has been the term used by
the vast majority of scholars for over a century.
Margulis & Sagan ( 1985) have independently suggested the suffix “protista”,
but have not provided a detailed rationale for this. Moreover, they have
restricted this term to some plastidic phyla (e.g. the Cryptoprotista and the
Chloroprotista) and to some protists which have been variously assigned to the
protozoa or aquatic fungi (e.g. the Ooprotista and the Chytridioprotista.) I n
their scheme the aplastidic phyla of protists (i.e. the ‘Protozoa’) bear a variety of
suffixes as, for example, in the Caryoblastae, the Actinopoda, the Foraminifera
and the Choanomastigota. Curiously, the euglenoprotists and the dinoprotists,
which have both plastidic and aplastidic members (and which therefore are
often variously claimed to be unicellular algae or protozoa), are listed under the
plastidic phyla, but are termed Euglenida and Dinomastigota, respectively. This
treatment is all the more inconsistent in view of the fact that Table 1 in
Margulis & Sagan (1985) also contains the Cryptoprotista which also have both
plastidic and aplastidic members and whose chloroplasts, like those of the
euglenoprotists and the dinoprotists, probably arose by a symbiotic event
(Gibbs, 1981).
These usages seem inconsistent to us, and therefore we suggest that the
uniform ending ‘protista’ or ‘protist’ be applied to all protistan higher taxa.
Again, we emphasize that this is an informal designation (cf. the use of capital
letters by Margulis & Sagan, 1985) and that it can be applied to any higher
taxon (and not just phyla as in the scheme of Margulis & Sagan, 1985).
ADVANTAGES OF THE PROPOSED SYSTEM
The system which we propose has several advantages over existing ones. It is
conservative since it co-opts existing nomenclature, but it is flexible enough to
accommodate the results of future evolutionary research; for example, by
allowing two or more groups to be clustered together or by including their
descendant taxa. The proposed suffix circumvents nomenclatural prejudice by
avoiding conflicts such as whether taxa are ‘little animals’ or ‘little plants’. It
also avoids the issue of whether individual taxa should be assigned the status of a
division, class or order, and therefore circumvents debate over such matters as
whether the cilioprotista belong to a lower taxon than the euglenoprotista. The
dilemma of how to treat taxonomic categories in different phyla has been
PROTISTAN EVOLUTION AND NOMENCLATURE
97
discussed in great detail previously (e.g. Van Valen, 1973). Consequently we
shall not explore it further except to note that there is much greater similarity
among the orders of the class Mammalia than there is among the orders of the
class Phytomastigophorea. Furthermore, ‘protista’ indicates protistan
organization, an advantage which is not conferred by a universal suffix such as
‘biont’ or certainly by the more traditional zoological, botanical, and
mycological suffixes. Note also that the proposed system avoids the pitfalls of the
existing taxonomic system which separate into different kingdoms unicellular
forms and their multicellular descendants. Thus, the order Volvocida is
separated from the multicellular green algae and plants, and the nomenclature
used gives no indication of the relationship between the two.
Many (but not all) phylogeneticists have pointed out the desirability of
eliminating paraphyly. If the reduction (elimination?) of paraphyly is desired,
the current approach of searching for the ancestors of the ‘higher’ organisms is
inappropriate, and often relegates groups which are not of direct ancestry to the
‘*important’ groups to taxonomic oblivion. Greater evolutionary precision in
phylogenetics, especially among the diverse protistan taxa, would be gained by
using the reverse approach; that is, identifying the largest monophyletic groups
possible among the protists and then including the other protists and protistan
descendants as subtaxa of the stem protistan group. In practice, this might
prove to demote the Plantae as a formal kingdom taxon to a subgroup of the
chloroprotists, although informally the concept ‘plant’ would admittedly remain
extremely useful and botanical nomenclature could be retained. Likewise, if the
‘higher’ fungi prove to be descendants of the rhodoprotists (Demoulin, 1974),
these taxa would be placed as subgroups of their parental taxon. Finally, many
workers have suggested that the kingdom Animalia is polyphyletic. For
example, Barnes (1984) thinks it probable that the sponges, Cnidaria and
Ctenophora, and Platyhelminthes represent three separate phylogenetic lineages
having three separate origins from the Protista. Our system allows this
information to be incorporated in a taxonomic system in a form which is easy to
retrieve, and thus it is hoped that ultimately this system will provide a
taxonomy which will be used as a base on which to build an overall scheme for
eukaryote phylogeny.
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