Is It Kingdoms or Domains
?
Confusion
& Solutions
W I L L H. B L A C K W E L L
C
onfusion has arisen, at higher levels of
classification of organisms, over two points:
1. How many kingdoms are there, i.e., which kingdoms should we recognize?
2. How do potentially larger, supra-kingdom groupings such as “domains” fit into the picture of a
tradition of kingdom-based classification?
Even if no other source is consulted, one may ascertain from the pages of The American Biology Teacher
(ABT) that there is no universal agreement on these
questions. Consider the appearance in ABT of the presentation (Margulis, 1981) of the popular five-kingdom
concept, and a recent discussion favoring a system of
three domains over the five-kingdom concept (Offner,
2001). Such papers have fostered additional discussion
in ABT (e.g., Biermann, 2001). Also, papers in ABT have
been thrown into the mix suggesting the efficacy of
WILL H. BLACKWELL is Professor Emeritus, Miami University
(Ohio), and Adjunct Professor at The University of Alabama,
Tuscaloosa, AL 35402; e-mail W60BUBBA@aol.com.
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THE AMERICAN BIOLOGY TEACHER, VOLUME 66, NO. 4, APRIL 2004
more than five kingdoms (Blackwell & Powell, 1995,
2001). The American Biology Teacher has thus been a significant forum for discussion of kingdom and suprakingdom concepts. Much additional debate is, of
course, found in other sources as well (cf. Blackwell &
Powell, 1999). The purposes of the present paper do not
include repetition of a voluminous literature on the
details of putative kingdom categories, but are:
1. to review pertinent historical points concerning
the development of kingdom and domain concepts
2. to address questions arising from previous suggestions of kingdom and domain composition
3. to discuss recent investigations into such questions, particularly the taxonomic breakup of the
heterogeneous kingdom Protista, and to suggest
additional sorts of evidence that may contribute
to our understanding of kingdom-level groupings
4. to acknowledge that future modification of classification systems will surely occur, and to consider which kingdoms should be recognized
based on present knowledge.
Brief History of Kingdom (&
Domain) Concepts
Understanding of the distinction between the animal and plant kingdoms is traceable to the science of
ancient Greece (Margulis & Schwartz, 1998). Formal
nomenclatural recognition of these two kingdoms, however, is dated from works of Linnaeus in the mid-eighteenth century (cf. Raven & Johnson, 2002). By the
mid-nineteenth century, it was recognized that not all
organisms are neatly pigeon-holed as either animals or
plants, e.g., Euglena, and a third kingdom, containing
mainly one-celled organisms was recognized. This “unicellular kingdom” was named “Protista” by Haeckel
(1866). Earlier, Hogg (1860) had conceived of a similar
kingdom “Protoctista” for organisms, unicellular or multicellular, which simply weren’t either plants or animals
(cf. Margulis & Sagan, 1985). Though roughly equivalent, Hogg’s Protoctista, interpreted to include large
multicellular algae, is viewed as somewhat broader conceptually than Haeckel’s Protista. Various authors,
including Haeckel, have recognized four kingdoms;
however, a four-kingdom concept is often associated
with Copeland (1947, 1956) who recognized: Mychota
(for bacteria, not fungi as the name would seem to
imply), Protoctista, Plantae, and Animalia. Regardless of
name choices, Copeland’s careful exposition distinguished two basic kinds of unicellular organisms: bacteria (prokaryotes) and protists (eukaryotes)—a distinction initially made by Chatton (1937). Some authors
(e.g., Dodson, 1971) felt that Protista (or Protoctista)
were not definable, and recommended a return to a system of three kingdoms (plants, animals, and prokaryotes). Authors with a yet greater reductionist bent
(Dillon, 1963) favored recognition of only a single kingdom for all of life.
The general trend, however, has been toward
acceptance of an increased number of kingdoms. The
five-kingdom approach represented a major milestone
in kingdom concepts. The inception of the five-kingdom system—Monera (bacteria or prokaryotes), a name
traceable to Haeckel, and a better name choice than
Mychota; Protista (Haeckel’s kingdom); Fungi (added by
Whittaker as a kingdom); Plantae; and Animalia—is
attributed to Whittaker (1969). This system was further
elaborated by Whittaker and Margulis (1978). Margulis
(1981) adopted the five-kingdom system, utilizing the
name Protoctista, rather than Protista. Margulis’ use of
Protoctista, consistent with Hogg (1860), was broader
than Whittaker’s use of Protista, and included red and
brown algae in addition to more “usual” protists. Since
nomenclatural priority, i.e., priority of publication or
authorship, does not often apply, in a formal sense, at
the rank of kingdom (more stringently applied at family rank, and ranks below family), either the name
Protista or Protoctista may be selected. A little known
fact (cf. Blackwell & Powell, 2001) is that Jahn & Jahn
(1949) had recognized these five kingdoms some years
earlier, as: Monera, Protista, Fungi, Metaphyta or
Embryophyta (for Plantae) and Metazoa (for Animalia);
they also recognized a sixth “kingdom,” Archetista, for
viruses. Regardless of author credit, the five-kingdom
approach dominated biology texts through the second
half of the twentieth century. The five-kingdom
approach is still used, but often with modification (e.g.,
Solomon et al., 2002); two bacterial kingdoms,
Archaebacteria and Eubacteria, are often recognized,
bringing the kingdom total to six.
Additional kingdoms have been proposed, with
varying acceptance. The purpose of increasing the
number of kingdoms has not been, as some might suppose, to confound the readership; rather, the goal has
been to establish more phylogenetically cohesive kingdom units (cf. Campbell & Reece, 2002). A major
problem was presented by the heterogeneous nature of
kingdom Protista, composed of both related and unrelated kinds of organisms (cf. Corliss, 1984; Blackwell
& Powell, 1999, 2001). Most of the increase in kingdoms (pursuant to the five-kingdom concept) has
resulted from “dividing up” the Protista into more logical groupings (cf. Campbell & Reece, 2002). Jeffrey
(1971) proposed a seven-kingdom scenario— including
the kingdoms Rhodobiota (red algae) and
Chromobiota (brown, golden, yellow-green algae,
diatoms and Oomycetes), carved out of the Protista.
Edwards (1976) had a similar scenario, using the name
Erythrobionta instead of Rhodobiota, and
Ochrobionta instead of Chromobiota. There is no
shortage of “neologisms,” as Margulis & Sagan (1985)
pointed out. Cavalier-Smith (1981) used the name
Biliphyta for Rhodobiota, and (in 1986) Chromista for
Chromobiota. Patterson (1989) introduced the informal term “Stramenopiles” for a natural grouping (possessing tripartite, tubular flagellar hairs) within the
Chromista; the long-range effect of Patterson’s proposal has been to question the inclusion of unrelated
forms, such as Haptophytes and Cryptomonads, in the
Chromista (cf. Blackwell & Powell, 2000, 2001). The
category Stramenopiles has been set forth as a candidate kingdom, “Stramenopila,” by Campbell et al.
(1999) and Campbell & Reece (2002); it was spelled
“Straminipila” by Dick (2001). Not only the spelling of
this name, but its status as a formally proposed kingdom could bear further scrutiny. Both Protozoa and
more “primitive” Protozoa, the Archezoa, have been
suggested as kingdoms (see discussion or listing of
kingdoms in Cavalier-Smith, 1993; Corliss, 1994). The
number of kingdoms recognized has usually ranged
from seven to nine (cf. Cavalier-Smith, 1981; Blackwell
& Powell, 1999). In an extreme view, Leedale (1974)
suggested as many as 19 kingdoms.
KINGDOMS OR DOMAINS 269
There is no over-riding consensus on which kingdoms should be recognized; and, there is also the matter of domains to consider. The introduction of domains
could be said to begin with Woese’s (1981) presentation
on Archaebacteria. Woese designated three “primary
kingdoms:” Archaebacteria, Eubacteria, and Eukaryotes.
Woese contended that, in terms of ribosomes, transfer
RNAs, and membrane lipids, the two major groupings
of prokaryotes or “ bacteria” (the Archaebacteria and
the Eubacteria) are as different from each other as each
is from the eukaryotes. Nine years later Woese et al.
(1990) proposed that these most major groupings be
“elevated” to the status of “domains,” with the names:
“Archaea,” “Bacteria,” and “Eucarya.” The basis of recognition was that these three groupings represent, biochemically, the most fundamental subdivisions of cellular life. Woese apparently felt that taxonomic systems in
use were inadequate in regard to recognition of these
most basic categorical distinctions—the “primary tripartite division of the living world,” as Woese stated it.
Woese et al. (1990) thus formally proposed a “new
(higher) taxon” or systematic category, “Domain.”
Woese’s three “domains” received acceptance by biologists, with some notable exceptions (e.g., Margulis &
Schwartz, 1998). Consequently, in addition to the perpetuation of the five (or six)-kingdom concept (borne of
Jahn & Jahn, 1949; Whittaker, 1959, 1969; Margulis,
1981), the three-domain concept of Woese has also
found support in textbooks (e.g., Campbell & Reece,
2002; Raven & Johnson, 2002; Solomon et al., 2002).
However, it is often unclear how kingdoms and
domains are envisioned to interface. To hearken back to
Offner (2001) and Biermann (2001), to some this is an
either/or option. But, as I discuss, “choosing” between
kingdoms and domains may be unnecessary.
Problems Encountered with
Present Domain & Kingdom
Concepts
“Domain” is considered to be a “supra”(above or
greater than)-kingdom category. The domains outlined
by Woese (1990): Archaea, Bacteria and Eucarya, seem
straightforward; so what could be the problem? For one
thing, Woese was not the only author to propose suprakingdom categories. Jeffrey (1982) proposed two
“Superkingdoms:” Prokaryota and Eukaryota, related to
Chatton’s (1937) recognition of two basic structural
types of cells, prokaryotic and eukaryotic. Since Jeffrey’s
proposal of supra-kingdom categories preceded
Woese’s, then shouldn’t Jeffrey receive priority recognition? This is not a significant problem, since all three
kingdom-based Codes of Nomenclature—Botanical
(ICBN 2000); Zoological (ICZN 2000); and
Bacteriological (ICNB 1992)—place little emphasis on
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THE AMERICAN BIOLOGY TEACHER, VOLUME 66, NO. 4, APRIL 2004
priority when dealing with higher taxonomic ranks
such as Kingdom, Phylum (Division), or Class. This
truly becomes a moot point when dealing with alleged
categories above kingdom level, since such categories
are not recognized by the Codes.
A more salient concern is, which proposal (three
domains, Woese; or two superkingdoms, Jeffrey) is
more biologically accurate? This is a difficult question,
since cogent arguments could be made for either.
Regardless, preference has generally gone to Woese’s
system in recent years, especially in terms of adoption
by textbooks. Solomon et al. (2002), who surveyed
research on this question, concluded that Archaea,
which look like Bacteria, may be even more distinct
from Bacteria (Eubacteria), biochemically, than from
Eucarya. However, not all authors reached the same
conclusion. Cavalier-Smith (1987) indicated that
sequence homology between Eubacteria and
Archaebacteria is greater than first thought; this “closer”
relationship has been supported by certain recent evidence, cf. Brinkmann & Philippe (1999).
In the alternative kingdom classification offered in
Solomon et al. (2002), attributed to Cavalier-Smith (cf.
Cavalier-Smith 1986, 2001), Prokaryota is recognized at
the kingdom level, and any systematic distinction
between Archaebacteria and Eubacteria would thus be
“below” kingdom level, i.e. subkingdoms. As we shall
see, however, Cavalier-Smith was not averse to changes
of mind on such matters. In any case, a pragmatic problem associated with the recognition of Archaea and
Bacteria as separate domains, is that the criteria of distinction are mainly biochemical, e.g., whether peptidoglycan is present in the cell wall or not. As indicated by
Solomon et al. (2002), when viewed under the microscope, Eubacteria and Archaebacteria are very similar. It
may be difficult for students to conceive that organisms,
which appear to be virtually identical, are not in the
same kingdom, perhaps not even the same domain.
The above is not to suggest that the proposed, fundamental biochemical distinctions between Archaea
and Bacteria are incorrect; there is, in fact, plenty of evidence that Woese was correct in his domain assessments. Yet, it is unquestionably easier to perceive, initially, the prokaryote/eukaryote distinction, than that of
Archaea/Bacteria. Correspondingly, several authors,
e.g., Barnes (1998), have adopted the essence of the
“superkingdom” system of Jeffrey (Prokaryota and
Eukaryota). Similarly, Cavalier-Smith (1993), in a
change of mind from his 1986 publication, recognized
as supra-kingdom categories, an “Empire” Bacteria
(prokaryotes) and an “Empire” Eukaryota. Margulis &
Schwartz (1988) had endorsed a similar distinction, but
at a “lower” rank, employing the “kingdom
Prokaryotae” (listing Monera as a synonym).
Unexpectedly, though, Margulis (1992) raised the level
of Prokaryota (and Eukaryota, for that matter) to
“Superkingdom” (or “Domain,” as she indicated in
parenthesis). Margulis & Schwartz (1998) demonstrated that supra-kingdom, kingdom, and subkingdom categories may be intercalated without difficulty.
Thus, it is frankly not clear at present whether we
should favor a system of two supra-kingdom categories
(sensu Jeffrey) or three supra-kingdom categories (sensu
Woese). Campbell & Reece (2002) held the position
that the three-domain system of Woese (1990), particularly recognition of Archaea and Bacteria, had rendered
kingdom (or superkingdom) “Monera” (Prokaryota)
“obsolete.” But, of course, this is so only if
one accepts Woese’s system of three
domains. If the distinctions between the
domains Archaea and Bacteria turn out to
be not as great as first thought, then the
broader category, Prokaryota, would seem
to be reestablished.
code of biological nomenclature (not three separate
“kingdom codes”), in which such issues as supra-kingdom taxonony may be resolved (cf. Blackwell & Powell,
1999; Blackwell, 2002). It should be mentioned here in
passing, that there are those (e.g., Hibbett & Donoghue,
1998) who would do away with all ranks (even the concept of rank), in the promotion of “rankless” classification. However, a rank-free system could cause chaos,
providing little taxonomic structure. It is improbable as
a reality. In any event, such possible changes are in the
future; so the question now is, how do we solve present
taxonomic problems concerning higher ranks? What
NABT Affiliate Members
Bearing on the above, however, is a different, quasi-legal sort of question, one of a
fundamental nomenclatural nature. Can
we, in fact, accept (in a strict, formal taxonomic sense) any domains, empires, or
super-kingdoms? I raise this issue because
there is no provision for any sort of suprakingdom category in any of the three kingdom-based codes of nomenclature (ICBN,
ICZN & ICNB). No taxonomic rank above
kingdom is officially allowed, or even mentioned, regardless of Woese’s (1990) “formal” domain proposal. Thus, any putative
category above kingdom is spurious, in a
nomenclatural sense (cf. Blackwell &
Powell, 1999). One may ask, though,
shouldn’t such ranks be permitted? My
answer would be, probably yes, with so
many authors thinking that such are needed. But, as of the present, we don’t “legally” have these categories. It may well be
part of the solution that we need to bring
biological nomenclature “up to speed” so
that it will reflect improved biological
knowledge (cf. Blackwell & Powell, 1999).
This will require nomenclature proposals
to this effect, and approval by the respective international congresses of botanical,
zoological, and bacteriological nomenclature. But, on the other hand, should the
lack of a formal, supra-kingdom nomenclature prevent us from utilizing, at least
informally, such ranks as domains? I
should think, clearly not! As far as formal
naming methodology of the future is concerned, we may eventually have a unified
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KINGDOMS OR DOMAINS 271
recent evidence do we have? What are the most reasonable taxonomic categories to recognize based on present evidence?
Recent Evidence for Kingdom (or
Domain) Decisions & Evidence
Still Needed
Considering prokaryotic “domains,” there is, as has
been mentioned, some evidence of a closer relationship
of Archaea and Bacteria than initially suspected; additional work along the lines of that of Aravind et al.
(1998), who demonstrated gene exchange between the
two groups, might be a fruitful area of investigation.
Among eukaryotic kingdoms, the recognition of animal,
plant, and fungal kingdoms is relatively uncontroversial;
although it should be mentioned that there is a greater
relationship, based on molecular data, between animals
and fungi than might have been expected a priori (cf.
Borchiellini et al., 1998). However, it is really the recognition of “new” (ex-protistan) eukaryotic kingdoms—
pursuant to the breakup of the presumably “simplest”
eukaryotic kingdom, Protista, or more broadly,
Protoctista—that has been associated with the most
uncertainty; see discussion in Blackwell & Powell
(1995, 1999, 2001).
Formerly within the encompassing Protoctista, the
Rhodophyta (red algae) and the related “glaucophytes”
(algae containing “cyanelles” derived Cyanobacteria)
constitute a part of the consideration (cf. Margulis et al.,
1990). Together, rhodophytes and glaucophytes constitute, according to some authors, the “Biliphyta,” in reference to possession by their plastids of “bile pigments,”
phycobiliproteins, contained in small structural units,
the phycobilisomes. The often multicellular red algae
and related forms are a good case in point as to whether
or not a given major group should be recognized as a
kingdom. One need look no further than the work of
Cavalier-Smith to sense there is a debate here; CavalierSmith (1981) recognized the Biliphyta as one of possibly nine kingdoms of “superkingdom” Eukaryota. Later,
Cavalier-Smith (1987) relegated Biliphyta to a subkingdom of kingdom Plantae. And, the debate is still on.
Solomon et al. (2002) considered red algae closely
related to the plant kingdom; whereas, Campbell &
Reece (2002) positioned them as related to plants, but
somewhat more distantly. Molecular data give comparable results. Baldauf et al. (2000), based on protein data,
connected red algae and glaucophytes to the plant kingdom. Kumar & Rzhetsky (1996), using small-subunit
ribosomal RNA, also connected red algae to plants, but
much more distantly; a distant relationship was suggested as well by large-subunit rRNA sequences
(Perasso et al., 1989). Broadwater et al. (1992) had
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THE AMERICAN BIOLOGY TEACHER, VOLUME 66, NO. 4, APRIL 2004
noted that different ribosomal molecular-genetic
sequences gave conflicting results. Based on rbcL data,
some (e.g., Delaney et al., 1995) have even postulated a
plastid connection between red algae and chromophytous algae (browns, goldens, etc.). Although ultrastructural studies have taken a back seat to molecular
approaches, investigations of red algae could benefit by
a return to the examination of ultrastructure. Distinct
structures seen during mitosis, nuclear-associated
organelles (Patrone et al., 1991) known as “polar rings”
support the supposition of the unique nature of the
group (Broadwater et al., 1992). Also, the absence of
any flagellated structure or remnant of such (Gabrielson
et al., 1990; Broadwater et al., 1992) in rhodophytes,
speaks against a connection to green algae/green plants,
in which flagellated cells figured heavily in their early
evolution (Mattox & Stewart, 1984; Van den Hoek et al.,
1995, Nakayama et al., 1998).
Further work on the cytology of red algae could be
potentially enlightening; Broadwater et al. (1992)
decried the small number of workers in this specialty
field. In any event, the paper of Kumar & Rzhetsky
(1996) is particularly interesting in that a time line is
estimated, on the basis of nucleotide sequencing. Red
algae are suggested to be an ancient lineage, arising
before the separation of green algae and land plants.
This matches well with the fossil record (ancient for
putative red algae), and with the speculation (Blackwell
& Powell, 1995) that, whereas the plastids of both
Viridiplantae (green algae/green plants) and Biliphyta
(including red algae) were derived from Cyanobacteria,
these were separate events. These respective symbioses
were lineage-defining events, and a separation of green
and red algal lines (and, for that matter, the brown algal
line) has been maintained. This supposition is supported by a difference in structure of plastids, e.g., singlethylakoid lamellae, bearing phycobilisomes, in red algae
vs. granal thylakoids, lacking phycobilisomes, in green
algae and green plants (cf. Lee, 1999); chromophytes
(brown algal line) have complex plastids (surrounded
by four membranes), distinct from those of red or green
algae (cf. Blackwell & Powell, 1995). I tentatively favor
recognition of red algae (and relatives) as a separate
kingdom, Biliphyta, based on present evidence, but
additional molecular and ultrastructural studies would
be helpful for any final decision.
Other former “protistan kingdoms” (cf. Cambell &
Reece, 2002) are equally important, but are accorded
less discussion here because they have been thoroughly
discussed elsewhere. The kingdom Chromista has been
generally accepted since its intense exposition by
Cavalier-Smith (1986, 1989). The remaining question
with kingdom Chromista has been whether to recognize this grouping sensu lato, or in the more restricted
sense of “Stramenopiles”—a fundamentally heterokont
(unequally flagellate) assemblage within the original
Chromista (cf. Patterson, 1989; Blackwell & Powell,
2000). Stramenopiles are held together taxonomically,
among a number of other characters, by the synapomorphy of composite (usually three-parted) tubular,
reverse-thrusting, mastigonemes (flagellar hairs); these
“retronemes” (Cavalier-Smith, 1989) are considered
highly significant in evolution of the group. Blackwell &
Powell (2000) provided an account of features suggesting that the Stramenopile lineage (consisting of chromophyte algae; pseudofungi; and certain primitive, heterotrophic flagellates) is fundamentally monophyletic.
The problem with the kingdom Chromista is that it
includes not only Stramenopiles, but relatively incongruous groups such as Haptophytes and
Cryptomonads. A number of authors, e.g., Leipe et al.
(1994) and Daugbjerg and Andersen (1997), have
shown that Haptophytes (Prymnesiomonads) are not
closely related to other chromophyte algae.
Haptophytes, and the equally unrelated Cryptomonads,
resemble types of flagellated Protozoa (cf. Blackwell &
Powell, 2001). The preferred kingdom, for phylogenetic
coherency, is thus Stramenopila (cf. Campbell & Reece,
2002), not Chromista.
The remaining ex-protistan kingdom, Protozoa, has
rather recently reemerged from the obscurity of “submersion” within kingdom Protista (cf. Cavalier-Smith,
1993; Blackwell & Powell, 2001; Corliss, 2002). The former kingdom Protista was the ultimate “catch-all” category, for placement of unicellular eukaryotes of uncertain relationship. The smaller, but still heterogeneous,
kingdom Protozoa has replaced the Protista in this taxonomic “holding-bin” function. For example,
Haptophytes and Cryptomonads are, at present, only
loosely placed in kingdom Protozoa. All is not phylogenetically bleak, however, because the Protozoa also contain a number of related forms, such as the Alveolates:
ciliates, dinoflagellates, and apicomplexans (sporozoans), cf. Corliss (1991). Alveolates are perhaps related
to Stramenopiles (Van de Peer & De Wachter, 1997;
Sogin & Silberman, 1998), but it is probably unwise to
merge these groups at present.
The relationship of Stramenopiles (Chromista) and
Alveolates, however, holds significant potential for ultrastructural research into evolution. Recently, a residual
plastid-like structure found in the alveolate (in this case,
malarial) parasite Plamodium (Hopkins et al., 1999) has
been linked to dinoflagellate plastids and ultimately to
plastids of Chromista (Cavalier-Smith 1999); more
work is needed to elucidate these relationships.
Progress has been made in understanding relationships
of a number of groups within the Protozoa, e.g. a relationship of Euglenoids and Trypanosomes (cf. Margulis
& Sagan, 1985; Blackwell & Powell, 2001). Knowledge
of relationship of Trichomonads and Hypermastigids,
as “Parabasalids,” has also been gained (cf. Levine et al.,
1980; Blackwell & Powell, 2001). Protozoa have
reemerged as a now somewhat more phylogenetically
cohesive group than the unwieldy assemblage recognized early in the twentieth century (cf. Calkins, 1933).
In any event, new phylogenetic insights, and the new
kingdoms pared from the old Protista (Protoctista), render it unlikely that this large, hodge-podge kingdom
(Protista, or Protoctista) will continue to be recognized,
except informally.
Which Kingdoms &
Subkingdoms, or Domains,
Should Be Recognized? (Table 1)
As we have seen, the number of kingdoms recognized has varied widely although some consensus of
seven or eight kingdoms (considering both prokaryotes
and eukaryotes) has emerged in recent years (Corliss
1994, 2002; Blackwell & Powell, 1995, 1999, 2001; see
also D. Maddison, The Tree of Life, http://tolweb.org/
tree?group=Life&contgroup=). The number of suprakingdom categories, such as domains, superkingdoms
or empires, has usually been either two (Jeffrey, 1982;
Cavalier-Smith, 1993) or three (Woese, 1990).
“Domain” has been the most common supra-kingdom
designation, and, for the sake of argument, I will settle
for use of this term. But, the question remains (e.g.,
Biermann, 2001), is it domains or kingdoms?
Discussed earlier in the paper (Problems
Encountered with Present Domain & Kingdom
Concepts), there is a question as to the nomenclatural
legitimacy of the category “domain,” or of any suprakingdom category (empire, superkingdom, etc.). This,
however, has not prevented authors of articles (e.g.,
Woese, 1990) and textbooks (e.g., Campbell & Reece,
2002) from using the rank, “domain,” and, in my opinion, should not. Nonetheless, the “safest” course of
action, if one wishes to abide by present rules of biological nomenclature, is to use the largest category formally allowed by any of the nomenclatural codes, i.e., kingdom, and work down in inclusiveness from there (next,
to subkingdom, for example). This approach was adopted by Margulis and Schwartz (1988).
If we thus decide to have kingdom as our pinnacle of
ranks, the question becomes, which kingdoms do we recognize? Better stated, perhaps, which system of kingdoms
best represents the major phylogenetic lineages as we
now understand them? As indicated at various points
throughout this paper, particularly in Recent Evidence for
Kingdom (or Domain) Decision & Evidence Still Needed,
biological information recently available has taken us
beyond the initially useful five-kingdom concept, which
featured the large and admittedly heterogeneous
KINGDOMS OR DOMAINS 273
Table 1.
Four Plausible Kingdom, Kingdom/Subkingdom & Domain/Kingdom
Scenarios, Based on Current Understanding of Major Phylogenetic Lineages.
Except for category emphasis, each presentation (A-D) below conveys essentially the same information. To render Woese’s domains (C) compatible with
codes of nomenclature, C may be converted to kingdom/subkingdom levels
(D). The concern over domains versus kingdoms may be unnecessary; kingdoms and domains are readily interfaced, regardless of precise spelling or suffix selected. The category of domain (or empire, or superkingdom) is, however, not recognized by nomenclatural codes. But, utilization of subcategories, as
allowed by codes, permits ample groupings (ranks) with which to represent
the depth of variation in nature.
A. Kingdom Archaebacteria
B. Kingdom Monera (Prokaryota)
Kingdom Eubacteria
Subkingdom Archaebacteria
Kingdom Protozoa
Subkingdom Eubacteria
Kingdom Stramenopila
Kingdom Protozoa
Kingdom Biliphyta
Kingdom Stramenopila
Kingdom Plantae
Kingdom Biliphyta
Kingdom Fungi
Kingdom Plantae
Kingdom Animalia
Kingdom Fungi
Kingdom Animalia
C. Domain Archaea
D. Kingdom Archaebacteria
Domain Bacteria
Kingdom Eubacteria
Domain Eucarya
Kingdom Eukaryota
Kingdom Protozoa
Subkingdom Protozoa
Kingdom Stramenopila
Subkingdom Stramenopila
Kindgom Biliphyta
Subkingdom Biliphyta
Kingdom Plantae
Subkingdom Plantae
Kingdom Fungi
Subkingdom Fungi
Kingdom Animalia
Subkingdom Animalia
A. Eight kingdom approach, after Blackwell and Powell (1999, 2001).
B. Seven kingdom, two subkingdom scenario, after Blackwell and Powell
(1995), and Margulis and Schwartz (1988) as regards “Monera” and its
“subkingdoms.”
C. Three domains, six kingdoms; modified from Woese (1990), Blackwell and
Powell (1999), and Campbell and Reece (2002).
D. Presentation C, converted to kingdom/subkingdom levels: three kingdoms,
six subkingdoms.
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THE AMERICAN BIOLOGY TEACHER, VOLUME 66, NO. 4, APRIL 2004
kingdom
Protista
(or
Protoctista), to a situation in
which several kingdoms
(Protozoa, Stramenopila or
Chromista, and Biliphyta)
have been split out of this
former mega-kingdom. If we
wished to recognize a
straight system of kingdoms, eight in total, without
subkingdoms, then the listing in Table IA, might be
appropriate. Table 1B represents basically the same system, but one in which seven
kingdoms are recognized,
and Archaebacteria and
Eubacteria are considered
subkingdoms of prokaryotes (compare Margulis &
Schwartz,
1988,
with
Blackwell & Powell, 1995).
If we wish, however, to
establish (regardless of rules
of nomenclature) a system
utilizing domains, i.e. following a Woesian paradigm,
then Table 1C conveys basically the same information
as IA, but employs Archaea,
Bacteria and Eucarya as
domains; under eukaryotes,
in this system, there would
thus be six kingdoms.
Margulis & Schwartz
(1998) unnecessarily concluded that use of domains
mandated a substantial
increase in kingdom number.
To the contrary, one may
extrapolate a relatively simple system of domains and
kingdoms, such as we outline
(Table IC), from the presentation in Campbell and Reece
(2002). At a minimum, it is
obvious that domains and
kingdoms may be readily
interfaced, if this is deemed
desirable. In Table ID, we
observe the same system as
IC, converted to the kingdom/subkingdom level. I do
not know of the existence of
ID per se in other publications, but it is a system that
could be defended based on our present knowledge,
and it is in compliance with the rules of nomenclature.
Perhaps of the systems discussed herein, ID is presently
the best compromise.
References
Aravind, L., Tatusov, R.L., Wolf, Y.I., Walker, D.R. & Koonin,
E.V. (1998). Evidence for massive gene exchange between
archaeal and bacterial hyperthermophiles. Trends in
Genetics, 14, 442-444.
Baldauf, S.L., Roger, A.J., Wink-Siefert, I. & Doolittle, W.F.
(2000). A kingdom-level phylogeny of eukaryotes based
on combined protein data. Science, 290, 972-977.
Cavalier-Smith, T. (1987). The origin of eukaryote and archaebacterial cells. Annals of the New York Academy of Sciences,
503, 17-54.
Cavalier-Smith, T. (1989). The kingdom Chromista. In J. C.
Green et al. (Eds.), The Chromophyte Algae: Problems and
Perspectives (pp. 381-407). Oxford: Clarendon.
Cavalier-Smith, T. (1993). Kingdom Protozoa and its 18 phyla.
Microbiological Reviews, 57, 953-994.
Cavalier-Smith, T. (1999). Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate,
and sporozoan plastid origins and the eukaryote family
tree. Journal of Eukaryotic Microbiology, 46, 347-366.
Cavalier-Smith, T. (2001). What are fungi? In D.J. McLaughlin
et al. (Eds.), The Mycota, VIIA (pp. 3-37). Berlin: Springer.
Barnes, R.S.K. (Ed.). (1998). The Diversity of Living Organisms.
Oxford, UK: Blackwell.
Chatton, E. (1937). Titres et Travaux Scientifiques (1906-1937).
Sete, France: Sottano.
Biermann, C.A. (2001). Three domains? The American Biology
Teacher, 63, 392.
Copeland, H.F. (1947). Progress report on basic classification.
American Naturalist, 81, 340-361.
Blackwell, W.H. (2002). One-hundred-year code déjà vu?
Taxon, 51, 151-154.
Copeland, H.F. (1956). The Classification of Lower Organisms.
California: Pacific Books.
Blackwell, W.H. & Powell, M.J. (1995). Where have all the
algae gone, or, how many kingdoms are there? The
American Biology Teacher, 57, 160-167.
Corliss, J.O. (1984). The kingdom Protista and its 45 phyla.
BioSystems, 17, 87-126.
Blackwell, W.H. & Powell, M.J. (1999). Reconciling kingdoms
with codes of nomenclature: Is it necessary? Systematic
Biology, 48, 406-412.
Blackwell, W.H. & Powell, M.J. (2000). A review of group filiation of Stramenopiles, additional approaches to the
question. Evolutionary Theory, 12, 49-88.
Blackwell, W.H. & Powell, M.J. (2001). The Protozoa, a kingdom by default? The American Biology Teacher, 63, 483490.
Borchiellini, C., Boury-Esnault, N., Vacelet, J. & Le Parco, Y.
(1998). Phylogenetic analysis of the HSp70 sequences
reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Molecular
Biology and Evolution, 15, 647-655.
Brinkmann, H. & Philippe, H. (1999). Archaea sister group of
bacteria? Indications from tree reconstruction artifacts in
ancient phylogenies. Molecular Biology and Evolution, 16,
817-825.
Broadwater, S.T., Scott, J.L. & Garbary, D.J. (1992).
Cytoskeleton and mitotic spindle in red algae. In D.
Menzel (Ed.), The Cytoskeleton of the Algae (pp. 93-112).
Boca Raton, Florida: CRC Press.
Calkins, G.N. (1933). The Biology of the Protozoa, 2nd Ed.
Philadelphia: Lea and Febiger.
Campbell, N.A. & Reece, J.B. (2002). Biology, 6th Ed. San
Francisco: Benjamin Cummings.
Campbell, N.A., Reece, J.B. & Mitchell, L.G. (1999). Biology,
5th Ed. San Francisco: Benjamin Cummings.
Corliss, J.O. (1991). Introduction to the Protozoa. Microscopic
Anatomy of Invertebrates, 1, 1-12.
Corliss, J.O. (1994). The place of the protists in the microbial
world. U.S. Federation for Culture Collections, Newsletter,
24(3), 1-6.
Corliss, J.O. (2002). Biodiversity and biocomplexity of the
protists and an overview of their significant roles in maintenance of our biosphere. Acta Protozoologica, 41, 199-219.
Daugbjerg, N. & Andersen, R.A. (1997). Phylogenetic analyses
of the rbcL sequences from haptophytes and heterokont
algae suggest their chloroplasts are unrelated. Molecular
Biology and Evolution, 14, 1242-1251.
Delaney, T.P., Hardison, L.K. & Cattolico, R.A. (1995).
Evolution of plastid genomes: Inferences from discordant
molecular phylogenies. In C.D. Sandgren et al. (Eds.),
Chrysophyte Algae: Ecology, Phylogeny and Development
(pp. 22-45). Cambridge, UK: Cambridge Univ. Press.
Dick, M.W. (2001). Straminipilous Fungi. Dordrecht,
Netherlands: Kluwer.
Dillon, L.S. (1963). A reclassification of the major groups of
organisms based upon comparative cytology. Systematic
Zoology, 12, 71-82.
Dodson, E.O. (1971). The kingdoms of organisms. Systematic
Zoology, 20, 265-281.
Edwards, P. (1976). A classification of plants into higher taxa
based on cytological and biochemical criteria. Taxon, 25,
529-542.
Cavalier-Smith, T. (1981). Eukaryote kingdoms: Seven or
nine? BioSystems, 14, 461-481.
Gabrielson, P.W., Garbary, D.J., Sommerfeld, M.R., Townsend,
R.A. & Tyler, P.L. (1990). Phylum Rhodophyta. In L.
Margulis et al. (Eds.), Handbook of Protoctista (pp.102111). Boston: Jones & Bartlett.
Cavalier-Smith, T. (1986). The kingdom Chromista: Origin and
systematics. Progress in Phycological Research, 4, 309-347.
Haeckel, E. (1866). Generelle Morphologie der Organismen.
Berlin: Reimer.
KINGDOMS OR DOMAINS 275
Hibbett, D.S. & Donoghue, M.J. (1998). Integrating phylogenetic analysis and classification in fungi. Mycologia, 90,
347-356.
Hogg, J. (1860). On the distinctions of a plant and an animal,
and on a fourth kingdom of nature. Edinburgh New
Philosophical Journal, n.s., 12, 216-225.
Hopkins, J., Fowler, R., Krishna, S., Wilson, I., Mitchell, G. &
Bannister, L. (1999). The plastid in Plasmodium falciparum asexual blood stages: A three-dimensional ultrastructural analysis. Protist, 150, 283-295.
ICBN (2000). International Code of Botanical Nomenclature.
(adopted by 16th International Botanical Congress, St.
Louis, Mo.). Konigstein, Germany: Koeltz Scientific
Books.
ICNB. (1992). International Code of Nomenclature of Bacteria
(1990 revision). Washington, DC: American Society for
Microbiology.
ICZN. (2000). International Code of Zoological Nomenclature,
4th Ed. London: International Trust for Zoological
Nomenclature.
Jahn, T.L. & Jahn, F.F. (1949). How to Know the Protozoa.
Dubuque, IA: William C. Brown.
Jeffrey, C. (1971). Thallophytes and kingdoms—a critique. Kew
Bulletin, 25, 291-299.
Jeffrey, C. (1982). Kingdoms, codes and classification. Kew
Bulletin, 37, 403-416.
Kumar, S. & Rzhetsky, A. (1996). Evolutionary relationships
of eukarytotic kingdoms. Journal of Molecular Evolution,
42, 183-193.
Lee, R.E. (1999). Phycology, 3rd Ed. Cambridge, UK:
Cambridge University Press.
Leedale, G.F. (1974). How many are the kingdoms of organisms? Taxon, 23, 261-270.
Leipe, D.D., Wainright, P.O., Gunderson, J.H., Porter, D.,
Patterson, D.J., Valois, F., Himmerich, S. & Sogin, M.L.
(1994). The stramenopiles from a molecular perspective:
16S-like rRNA sequences from Labyrinthuloides minuta
and Cafeteria roenbergensis. Phycologia, 33, 369-77.
Levine, N.D. et al. (1980). A newly revised classification of the
Protozoa. Journal of Protozoology, 27, 37-58.
Madison, D.R., The Tree of Life Web Project: A Collaborative
Internet Project Containing Information about Phylogeny and
Biodiversity. Retrieved February 7, 2004. Available online
at http://tolweborg/tree?group=Life_on_Earth&cont
group= .
Margulis, L. (1981). How many kingdoms? Current views of
biological classification. The American Biology Teacher, 43,
482-489.
Margulis, L. (1992). Biodiversity: Molecular biological domains,
symbiosis and kingdom origins. BioSystems, 27, 39-51.
Margulis, L, Corliss, J.O., Melkonian, M. & Chapman, D.J.
(Eds.). (1990). Handbook of Protoctista. Boston: Jones and
Bartlett.
Margulis, L, & Sagan, D. (1985). Order amidst animalcules:
276
THE AMERICAN BIOLOGY TEACHER, VOLUME 66, NO. 4, APRIL 2004
The Protoctista kingdom and its undulipodiated cells.
BioSystems, 18, 141-147.
Margulis, L. & Schwartz, K.V. (1988). Five Kingdoms: An
Illustrated Guide to the Phyla of Life on Earth, 2nd Ed. New
York: Freeman.
Margulis, L. & Schwartz, K.V. (1998). Five Kingdoms: An
Illustrated Guide to the Phyla of Life on Earth, 3rd Ed. New
York: Freeman.
Mattox, K.R. & Stewart, K.D. (1984). Classification of the
green algae: A concept based on comparative cytology. In
D.E.G. Irvine & D.M. John (Eds.), Systematics of the Green
Algae (pp. 29-72). London & Orlando: Academic Press.
Nakayama, T., Marin, B., Kranz, H.D., Surek, B., Huss, V.A.R.,
Inouye, I. & Melkonian, M. (1998). The basal position of
scaly green flagellates among the green algae
(Chlorophyta) is revealed by analyses of nuclear-encoded
SSU rRNA sequences, Protist, 149, 367-380.
Offner, S. (2001). A universal phylogenetic tree. The American
Biology Teacher, 63, 164-170.
Patrone, L.M., Broadwater, S.T. & Scott, J.L. (1991).
Ultrastructure of vegetative and dividing cells of the unicellular red algae Rhodella violacea and Rhodella maculata.
Journal of Phycology, 27, 742-753.
Patterson, D.H. (1989). Stramenopiles: Chromophytes from a
protistan perspective. In J.C. Green et al. (Eds.), The
Chromophyte Algae: Problems and Perspectives (pp. 357379). Oxford: Clarendon.
Perasso, R., Baroin, A., Qu, L.H., Bachellerie, J.P. & Adoutte, A.
(1989). Origin of the algae. Nature, 339, 142-144.
Raven, P.H. & Johnson, G.B. (2002). Biology, 6th Ed. Boston:
McGraw-Hill.
Sogin, M.L. & Silberman, J.D. (1998). Evolution of the protists
and protistan parasites from the perspective of molecular
systematics. International Journal of Parasitology, 28, 11-20.
Soloman, E.P., Berg, L.R. & Martin, D.W. (2002). Biology, 6th
Ed. Australia: Brooks/Cole.
Van de Peer, Y. & De Wachter, R. (1997). Evolutionary relationships among the eukaryotic crown taxa taking in
account site-to-site rate variation in 18S rRNA. Journal of
Molecular Evolution, 45, 619-30.
Van den Hoek, C., Mann, D.G. & Jahns, H.M. (1995). Algae:
An Introduction to Phycology. Cambridge, UK: Cambridge
University Press.
Whittaker, R.H. (1959). On the broad classification of organisms. The Quarterly Review of Biology, 34, 210-226.
Whittaker, R.H. (1969), New concepts of kingdoms of organisms. Science, 163, 150-160.
Whittaker, R.H. & Margulis, L. (1978). Protist classification
and the kingdoms or organisms. Biosystems, 10, 3-18.
Woese, C.R. (1981). Archaebacteria. Scientific American,
244(6), 98-122.
Woese, C.R., Kandler, O. & Wheelis, M.L. (1990). Towards a
natural system of organisms: Proposal for the domains
Archaea, Bacteria, and Eucarya. Proceedings of the National
Academy of Science, USA, 87, 4576-4579.