Walter Zimmermann and the Growth of Phylogenetic Theory

Author(s): Michael J. Donoghue and Joachim W. Kadereit

Source: Systematic Biology , Mar., 1992, Vol. 41, No. 1 (Mar., 1992), pp. 74-85
Published by: Oxford University Press for the Society of Systematic Biologists

Stable URL: http://www.jstor.com/stable/2992507

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide
range of content in a trusted digital archive. We use information technology and tools to increase productivity and
facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at
https://about.jstor.org/terms

Oxford University Press and are collaborating with JSTOR to digitize, preserve and extend
access to Systematic Biology

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 Points of View

Syst. Biol. 41(l):74-85, 1992

Walter Zimmermann and the Growth of Phylogenetic Theory

Michael J. Donoghue1 and Joachim W. Kadereit2

department of Ecology and Evolutionary Biology, University of Arizona,

Tucson, Arizona 85721, USA
Hnstitut fur Spezielle Botanik und Botanischer Garten, Johannes Gutenberg-Universitat Mainz,
Bentzelweg 7-9, 6500 Mainz, Germany

Walter Zimmermann, shown in Figurethe core of his theory. Zimmermann also

1, is well known among plant morpholo-focused attention on several basic meth?
gists for developing the "telome theory/' odological issues, especially those con?
which accounts for the derivation of lateral cerning rates of evolution and the analysis
appendages from undifferentiated axes
of what he called "character phylogeny/'
(Zimmermann, 1938, 1965). Plant system-
atists are generally aware of Zimmer-
mann's collaboration with Arthur Cron- Background

quist and Armen Takhtajan in classifying Zimmermann (1892-1980) received his

embryophytes (Cronquist et al., 1966), Ph.D.
andfrom Freiburg i. Br. in 1921, and
his "hologenetic spiral" is a familiar taught image in Tubingen, Germany, as a private
to many botanists, having been repro? lecturer (1925-1929) and professor (1929-
duced in texts such as Foster and Gifford 1980) of botany (Stafleu and Cowan, 1976).
(1974:48) and Stewart (1983:81). Although he published extensively on
Although Zimmermann was cited matters re? of interest to plant systematists (see
peatedly by Willi Hennig (1966), whoreferences re? in Zimmermann, 1965), we have
ferred to him as "one of the best of modern not attempted to summarize this entire
theoreticians of systematic work" (p. 9) and body of work nor even that portion of it
"one of the most zealous of modern ad? devoted to systematic theory. Instead, we
vocates of a consistent phylogenetic focussys?
more or less exclusively on his paper
tematics" (p. 10), his contributions of to 1931,
phy? which is his earliest and most com?
logenetic theory have been largely prehensive treatment of phylogenetic
overlooked. Here we draw attention to his analysis and seems to have influenced
seminal theoretical paper, "Arbeitsweise Hennig's thinking most directly. This pa?
der botanischen Phylogenetik und anderer per, variously modified, also formed the
Gruppierungswissenschaften" ("Methods basis of Zimmermann's contribution to
of botanical phylogenetics and other Heberer's "Die Evolution der Organis-
grouping sciences"), first published in 1931. men" (Zimmermann, 1943, 1967).
In this paper, Zimmermann clearly ex? The 1931 paper appeared in "Handbuch
pressed many of the underlying principles der biologischen Arbeitsmethoden," an
of phylogenetic systematics?ideas that ambitious series of review articles (edited
were later taken up by Hennig and formed by E. Abderhalden) that endeavored to
74

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 POINTS OF VIEW 75

summarize working m
of biological research.
parently not widely a
(both dates are cited, som
author; e.g., Hennig, 1966). Zimmer-
mann's work appeared in an unlikely po?
sition in the series, between a treatise on
the microscopy of skin capillaries of living
humans and an analysis of methods for
detecting hidden Mendelain genes for cold
pigmentation in red albino eyes, particu?
larly in rabbits. Several other contributors
to this series are more familiar to system-
atists, including A. Remane, L. Diels, and
C. Mez.
Zimmermann's paper is a comprehen?
sive account of systematic methods, which
includes extensive commentary on various
sources of evidence (e.g., comparative on? Figure 1. Walter Zimmermann, 1959, IX Inter?
togeny, plant geography, hybridization
national Botanical Congress, Montreal, Canada (pho?
experiments, and serology). We will not courtesy of Arthur Cronquist, New York Bo?
tograph
review the entire paper, as many of theGarden).
tanical
particulars are no longer of general inter?
est. Instead, we focus on issues that are
most interesting from the standpointatics, of Zimmermann's work is now primar?
phylogenetic theory as it was developed ily of historical interest.
by Hennig and as we known it today. A
Grouping Theory
more complete analysis of Zimmermann's
thought?its origins and its influence on The first section of Zimmermann's paper
later developments?would certainly (pp. be 941-970), entitled "Die Fragestellung
valuable, but this task deserves the atten? ("The problem"), is devoted to the philo
tion of historians and philosophers of sci?sophical underpinnings of systematic the?
ence. We hope, in fact, that our account ory. Although we concentrate on phylo
will stimulate a more complete analysis ofgenetic methods, we will outline briefly
Zimmermann's contributions, as well as the opening philosophical arguments, as
those of others who laid the foundations
these provide the rationale for the remain?
der of the analysis. The general structure
of modern phylogenetic theory (e.g., Plate,
1914). Unfortunately, this subject seems
of these
to arguments is also noteworthy, be
have attracted very little attention in cause
com? much the same approach is eviden
parison, for example, to the history of introductory sections of Hennig'
in the
the "modern synthesis" (e.g., Mayr(1966)
and book.
Provine, 1980). Zimmermann's discussion revolves
The passages from Zimmermann quoted around the comparison of three gen
below were translated by us. We haveways not,of grouping: special purpose (in
however, prepared a translation of the which
en? basic forms or "types" are chosen
"randomly"
tire text. Although it might be valuable to for some practical purpose),
do so, it would be a major undertaking idealistic
in (in which the "type" is an ide?
view of the length of the paper, the alized
sub? form "chosen intuitively" and need
tlety of the material, and the style ofnot correspond to anything that has actu?
writ?
ally existed), and phylogenetic (based on
ing. Furthermore, in contrast to the trans?
lation of Hennig, which stimulated the
genealogy). Phylogenetic grouping differs
fundamentally from the others in being
development of new methods in system-

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 76 SYSTEMATIC BIOLOGY VOL. 41

tied directly ence. He

to adopted it, therefore,
objects thatsimply as hav
existence in the world: an "axiom" or heuristic guiding principle.
Furthermore, he contended that nondual-
The ancestral form [Urform] in phylogenetics once
istic approaches,
which fail to sharply de?
existed in reality; it is objectively characterized by
limit object
the genealogical relationships, that is, by its po? and subject, give rise to pseu-
doproblems,
sition at the root [Wurzel] of the phylogenetic line of which he offered several
in question [p. 949]. examples.
Having opted for phylogenetic group?
It is in this sense that phylogenetic group?
ing, Zimmermann was careful to acknowl?
ing can be considered "objective," as edge
com? that the three methods can coexist
pared with artificial (special purpose) or
and complement one another:
subjective (idealistic).
Having characterized these three Itap?needs to be stressed that the mutual relationship
proaches, Zimmermann expressed the between
cen? the different grouping procedures con?
tral question, and his answer to it, in sists
theonly in the decision which procedure we want
following terms: to choose. In contrast to this, it is not true that
individual results (obtained from the different
Do we want to group phylogenetically, that is,grouping
fol? procedures) confirm or contradict each
lowing naturally given relationships? or do weother.
want For example, a practical grouping obviously
to group artificially? or do we want to group remains
in? practical even when it is shown to be non-
tuitively, following subjective impression? We phylogenetic
do and vice versa the existence of "sim?
not have any other possibilities. Of course, one pler"
cangrouping does not contradict the correctness
do entirely without phylogenetics. One must of abe
phylogenetic grouping [p. 975].
aware, however, that then one is forced to group
Nevertheless,
artificially, or "idealistically;" phylogenetics is the he was firm in the belief that
only procedure which groups according tothese
natu?different sorts of groups must not be
rally given relationships, the only procedure which,
confused with one another nor mixed to?
through the act of grouping, directly depicts nat?
ural relationships [pp. 949-950].
gether in a single system. This same po?
sition was adopted by Hennig (1966, e.g.,
Zimmermann's justification for prefer? p. 9), who also flatly rejected the idea that
ring phylogenetic grouping is surprisingly all but one method of grouping should be
subtle. After rejecting criticisms aimed dismissed.
at
the degree of exactness of phylogenetic It is perhaps difficult, from our present
procedures and briefly discussing the perspective,
role to appreciate the need for such
of intuition, Zimmermann at length basic
dis?philosophical arguments. However,
cussed his main argument in favor ofboth phy? Zimmermann and Hennig were
logeny. He argued that phylogenetic forced to cope with idealism, which was at
grouping assumes the separation of subject that time the dominant outlook among
and object; that is, it accepts that there are German scientists (Grene, 1958; Reif, 1986).
objects that exist in the world outside the Reaction to idealism is even more evident
in Zimmermann's writing than in Hen-
mind of the observer. In contrast, idealism
denies any such separation and thereforenig's, perhaps because some of Zimmer?
can reflect only subjective ideas. Zimmer? mann's contemporaries in plant morphol?
mann made it clear that his position, whichogy were outspoken advocates of idealism,
he referred to as "consistent [konsequent] notably Wilhelm Troll (e.g., Troll, 1940; see
dualism," was not strictly equivalent toSattler, 1964).
"realism," which entails philosophical Although idealism is now rarely de?
commitments that he clearly appreciatedfended as such, it is still evident in tax?
but preferred to sidestep. His acceptance onomy, even in the work of those who
of the existence of objects in the world wasappear to represent phylogenetic system?
motivated instead by practical concerns. Inatics. As unappealing as the prospect is to
particular, he argued that the realist/ma? most systematists, we believe that progress
terialist position has been an eminentlyin the development of systematic theory
successful approach in other areas of sci-still depends critically on attention to

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 points of view 77

of taxa and the transformation

philosophical of individ?
questio
roz and Donoghue
ual characters: [
versus "classes" in connection with the
Within this historical phylogenetics we can distin?
species problem). As Hennig (1966:78) not?
guish two main tasks as, so to speak, far and near
ed, the systematist will have to come
aims: 1. to
taxon phyletics, and 2. character phyletics.
grips with underlying conceptualTaxon
issues,
phyletics is that branch of historical phy?
"if he is to avoid the justifiable charge of which in general can be characterized
logenetics
not knowing what he is doing or even by the
whatconstruction of phylogenetic trees of "spe?
cies" or other taxa. .. . Character phyletics ("se-
he is trying to do." mophyletics"), the study of the transformation of
individual characters, is, from a practical point of
Phylogenetic Methods
view, the basis of the whole of historical phylo?
The second part of genetics
Zimmermann's treat?[p. 984].
ment (pp. 975-1048) is entitled "Die Phy-
Zimmermann clearly appreciated that
logenetischen Methoden" ("Theanalyses
phylo?of taxon phyletics and character
genetic methods"). This section begins (as
phyletics are closely related. Hypotheses
does Hennig, 1966) with an analysis of the
about genealogical relationships among
place of systematics in biology and
taxa "are the
deduced from the assumed rela?
special tasks of biological systematics. Re?
tionships of characters" (p. 984). He con?
garding the analysis of the history of
sidered character transformation series to
organisms, Zimmermann contrasted (1)
be primary in that such ordering does not
description (which he equates with
depend on knowledge of genealogical re?
paleontology), (2) "historical phylogenet-
lationships, nor is it contradicted by such
ics," and (3) process-oriented research. The
knowledge. However, a hypothesis of
remainder of the paper is organized around
the tasks he identified with these three ar? phylogenetic relationship is necessary to
eas: to discover whether evolution oc? specify the number of originations of a trait,
instances of reversal, and so on:
curred, the historical course of phylogeny,
and the causal factors responsible for phy?
one of the most important questions of taxon phy?
logeny, respectively. This approach,logeny
which is whether and when a character might
have reversed; further in which sequence the dif?
attempted to integrate microevolutionary
ferent character transformation series followed each
process and macroevolutionary pattern,
other [p. led
985].
Reif (1986) to conclude that Zimmermann
was among a handful of GermanToworkersclarify this point, Zimmermann offered
(including B. Rensch) who formulated
two examples a (modification of the foot in
synthetic view of evolution, more the or
evolution
less of equids and reduction of
independently of English-speaking the gametophyte
biolo? in land plants) to illus?
gists (see Mayr and Provine, 1980). trate that although linear character trans?
Our discussion emphasizes methods for
formation series are often presented, taxon
discerning the course of phylogeny, phylogenies
whichare trees, and some character
was Zimmermann's primary focus. He modifications may have occurred only on
spelled out the goals of "historical phy- lateral branches.
logenetics" in the following terms: He was also careful to point out that the
process of phylogenetic character trans?
The task of historical phylogenetics is to find out formation is continuous and does not allow
"how it was." This task would be completely solved
if we could, just by description, erect a gigantic a clearcut distinction between phylogeny
phylogenetic tree of genealogical affinities for all and ontogeny. This argument foreshad?
organisms which ever existed and enter all trans? owed his "hologenetic spiral," mentioned
formations by which descendants are distin?
guished from their ancestors [pp. 981-982].
above. He also noted that for purposes of
phylogeny reconstruction we are forced to
A general theme is evident in this state? select particular stages of the life cycle for
ment and runs throughout Zimmermann's comparison. Here, Zimmermann's outlook
account, i.e., the distinction between a tree is similar to that of Hennig (1966:6), who

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 78 systematic biology vol. 41

Only one exception was briefly noted, the

"possible reticulate structure of a phylo?
/A /'"B C \
genetic tree
[Ginkgo [Magno/ie due to sexual hybridization
Apfelbaum\
between species" (p. 989).
(a) For Zimmermann, knowledge of phy?
logenetic relationships was directly con?
nected to phylogenetic grouping (see Fig.
2):

flpfetbaum)
In phylogenetically oriented systematics this rel?
ative grouping implies the positioning into the
hierarchy of systematic categories: species, genus,
family, etc. B + C, for example, might correspond
to a species, and A + B + C to a genus, or B + C
may correspond to a family, and A + B + C to an
order or class, etc. [p. 989].

In contrast to grouping, however, Zim?

mermann considered ranking to be largely
arbitrary: "the decision how big a group
should be called 'species,' or 'family,' etc.,
can only be guided practically, conven?
(b) tionally" (p. 990).
Zimmermann also contrasted statements
Figure 2. (a, b) Figure 172 of Zimmermann (1931: about phylogenetic relationship with those
990). Phylogenetic relationship as recency of shared about the relative advancement or deri?
ancestors (Xl, X2).
vation of taxa. To say that one taxon is
ancestral and another derived implies ei
used the word "semaphoront" for the in? ther that the former has a preponderance
dividual organism at a particular point in of ancestral features and the latter mostl
its development. derived states or that the taxon considered
ancestral branched off earlier than the de?
Phylogenetic Relationship and the
rived taxon. But these two meanings of an?
Grouping of Taxa cestral and derived need not coincide.
Zimmermann's definition of "phyloge? Zimmermann noted, for example, that t
netic relationship" is exceptionally clear. red algae are an ancient branch yet a
In reference to his Figure 172 (reproduced highly derived in terms of many individ
here as Fig. 2), he stated: ual characters.
He also considered the derivation of co?
We say that the plant or organs B and C are more
closely related to each other than with A. The com? existing taxa from one another:
mon ancestor of B and C (X2) existed more recently
than the ancestor of all three plants or organs It is only in one case that such a derivation is truly
(Xl)... . The relative age relationship of ancestors possible in a taxon phylogenetic sense: Namely
Xl and X2 is the only direct measure of phyloge? when the "derived" taxon is of phylogenetically
netic relationship [pp. 989-990]. smaller size than the ancestral taxon, i.e., when the
derived taxon is part, an independently differen?
In fact, he argued that no other represen? tiated branch, of the (purely phylogenetically de?
tation is consistent with phylogenetic limited) ancestral taxon [p. 1007].
grouping: In this case, although Zimmermann did
A statement about phylogenetic relationship which not coin the term, the "ancestral taxon"
cannot be expressed in the basic scheme of Figure would be paraphyletic (see Discussion).
172b [Fig. 2b] does not exist.. . . Whoever believes Zimmermann's concept of phylogenetic
that he cannot illustrate relationships in this basic
scheme .. . does not have a phylogenetic but an relationship, which ties it directly to re?
"idealistic" or purely systematic "relationship" in cency of common ancestry, represented a
mind [pp. 989-990]. fundamental advance, without which, as

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 POINTS OF VIEW 79

Figure 3. (a-c) Figures 174-17

the use of similarity in assess

Hennig (1966:235)
of time. This means that similarity ispoin a substitute
measure for degree of relationship only when the
sions of individual
transformation of the characters studied in the
que
and misleading."
phylogenetic lines in question Indee
took place 1. di?
duced Zimmermann's
vergently, and 2. at an equal rate. If only oneF of
taxon names)
these twoin his
preconditions book
does not apply, our phy?
mermann (1931), along with Bigelow logenetic claim "the more similar, the more closely
related" very easily leads to mistaken conclusions
(1956), were acknowledged by Hennig [pp. 995-996].
(1966:74) as sources for his definition of
monophyly. Although Zimmermann briefly dis?
cussed convergence, parallelism, and re?
Similarity versus Relationship versal as sources of difficulty in using sim?
Zimmermann's treatment of the practi? ilarity to assess relationships, his analysis
cal methods of phylogenetic research of unequal rates of evolution was especial?
begins with a discussion of the use of ly cogent. Most of his discussion revolved
similarity in assessing phylogenetic rela? around his Figures 174-176, which we have
tionships. He credited Plate (1912) with the reproduced in Figure 3. In these trees, the
recognition that similarity has often been numbers associated with the individual
substituted for relationship, in part be? branches are meant to reflect the amount
cause similarity and relationship were of change, and the difference between pairs
equated with one another prior to the ad? of taxa is shown by the brackets above.
vent of evolutionary thought. However, Zimmermann made the point that if the
Zimmermann insisted that these are sep? amount of change in different lines (from
arate properties, with relationship refer? a given ancestor to the included tips) has
ring only to recency of common ancestry. been equal, similarity will provide an ac?
Consequently, the question arises as to the curate guide to relationships (Fig. 3a).
circumstances under which the use of sim? This situation differs from that in Figure
ilarity would actually lead one astray3b,
in in which the amount of change in dif?
assessing relationships. Zimmermann's ferent lines is unequal: A, X2, and B have
answer is remarkably clear: not diverged very much from their com?
mon ancestor Xl, whereas C has under?
Degree of similarity would be an unobjectionable
gone a burst of evolution. Under these
substitute measure for the degree of phylogenetic
relationship if organisms would have becomecircumstances,
in? similarity would be mis?
leading, suggesting the false conclusion
creasingly dissimilar in proportion to the passage

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 80 SYSTEMATIC BIOLOGY VOL. 41

with some angiosperm families that evi?

Pinaceae
Caefaceae)
dently have
^notaceae generated new forms quite
rapidly. He also noted that the extent of
phenotypic change need not mirror the ex?
tent of the underlying genetic change.
Thus, the fusion of organs, which might
appear to be a major morphological change,
could be brought about by a minor genetic
shift.
Zimmermann provided a concrete ex?
(a)
ample of the possible effects of unequal
rates, referring to Mez and Ziegenspeck's
Pinaceae Magnohaceae Cdcteceae (1926) tree based on serological evidence:
Whether, as claimed by Mez and Ziegenspeck, no
protein convergence occurs is doubtful, but even
if the "specific" proteins would have evolved di?
vergently throughout, the difficulty of unequally
fast structural change remains. But when the pro?
tein differentiates fast in one phylogenetic line and
slow in another, protein differentiation is no sub?
stitute measure for phylogenetic relationship [p.
1027].
(b)
Here he referred to his Figures 180-182,
shown in our Figure 4. The serological data
appeared to suggest that Magnoliaceae are
more closely related to Pinaceae than to
Cactaceae (Fig. 4b). Zimmermann noted,
however, that it is quite likely that angio?
sperms are monophyletic (Magnoliaceae
more closely related to Cactaceae; Fig. 4a),
with rapid evolution in the line leading to
Cactaceae and relatively little evolution in
(c) the lines leading to Magnoliaceae and Pin?
aceae (Fig. 4c).
Figure 4. (a-c) Figures 180-182 of Zimmerman Hennig (1966) cited Zimmermann's cri?
(1931:1029). The effect of unequal rates of evolution tique of the serological analyses of Mez but
on the use of serological similarity in assessing re?
lationships.
not his more general observations on rates
of evolution. In fact, Hennig (1966:88) spent
rather little time on the problem of rate
that taxa A and B are more closely related inequality, citing only Bigelow (1958), who
to one another than either is to taxon C did not cite Zimmermann's earlier and
(Fig. 3c). In this case, the branch lengths
more complete analysis.
between taxa are faithfully preserved; Having specified how convergence, re
however, the tree has been rerooted versal,
along and especially unequal rates migh
the branch leading from X2 to C, suchlead similarity measures astray, what d
that
the amount of evolution in different lines Zimmermann recommend? In effect, he
becomes more nearly equal. suggested that similarity be used but used
Zimmermann recognized that unequal
cautiously:
rates of evolution could be a very real prob?
Comparison of similarity thus might be a more or
lem in practice. He believed that such dif?less useful measure for the recognition of the de?
ferences were characteristic of plant evo? gree of relationship, provided we first 1. take into
account as many characters as possible; 2. limit
lution, contrasting the "living fossil" Ginkgo

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 POINTS OF VIEW 81

ourselves to large differenc

count the diversity of the
1000].

Although Zimmermann was keenly aware

of the pitfalls of using similarity to mea?
sure relationship, he did not provide a
method to avoid these problems. In par?
ticular, he did not arrive at anything like
Hennig's principle of synapomorphy. This
shortcoming is surprising in view of his
emphasis on the direction of character evo?
lution.

Character Phylogeny
Hennig's (1966:88) discussion of meth?
ods for evaluating characters as indicators
of phylogenetic relationship begins with
Figure 5. Figure 179 of Zimmermann (1931:1004).
a reference to Zimmermann's view of evo? Diagram used to illustrate the use of parsimony and
lution as the transformation of characters knowledge of related groups in assessing the direc?
from ancestors to descendants. Hennigtion of "character phylogeny."
also
credited Zimmermann with the notion of
"character phylogeny" (1966:95), withcharacters
its which today are widespread in a larger
focus on determining which character taxon generally are more primitive than characters
condition is ancestral and which is de? limited to only a small section of this taxon [p.
1003].
rived. These ideas are central to phyloge?
netic systematics. Although this method has the advantage
Zimmermann listed and discussed six of applying to the comparison of extant
methods for determining the direction organisms,
of Zimmermann recognized a dis?
character evolution. He considered occur? tinct disadvantage, namely that it requires
rence in the fossil record to be the best and at the outset some "secure knowledge of
most direct indicator; character conditionsphylogenetic relationships."
that appear earlier in the record are likelyBy way of clarifying the application of
to be primitive. Other "auxiliary methods" this criterion, Zimmermann presented an
are less well justified, including ontogeny, example that relied on his Figure 179 (our
character correlation, reduction or loss ofFig. 5). Here, taxa A, B, C, and D are cycads,
function, and "analogous conclusion" (i.e., conifers, Ranales, and composites, respec?
if character state A is "known" to give rise tively, and the character under consider?
to state B in many cases, this sequence mightation is mode of pollination. Based on the
be assumed in an unknown case). distribution of wind and insect pollination
All of these criteria had been formulated on this tree, Zimmermann concluded that
by other authors (see Stevens, 1980). How?wind pollination is ancestral in seed plants
ever, Zimmermann's sixth (unnamed) cri?(the entire group) and that a switch to in?
terion is of particular interest, as here wesect pollination occurred in the line lead?
can see the beginnings of what has since ing to angiosperms (the included group,
become known as outgroup comparisonconsisting of C + D). The alternative, that
and a clear understanding of its connectionseed plants were primitively insect polli?
to parsimony (see Watrous and Wheeler, nated and that this condition was simply
1981; Farris, 1982; Maddison et al., 1984). retained in the angiosperm line, was re?
This method is based, according to Zim? jected on the grounds that it would require
mermann, on the following "well-found? the convergent evolution of wind polli?
ed" assumption: nation in cycads, conifers, and other "gym-

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 82 SYSTEMATIC BIOLOGY VOL. 41

nosperm" several of the

groups central ideasZimme
(here underlying
plicitly assumed phylogenetic
that systematics. His paper of
cases of1931 in
nation in gymnosperm is among the earliest treatmentsgroups
of its kind,
within these lines): and it presaged many later developments.
In particular, some of Zimmermann's ideas
It is clear that such convergent evolu
be much more complicated appear to have been taken up more the
than or less co
lution outlined above in which the common an? directly by Hennig, especially his defini?
tion
cestor and most of the extant branches of phanero? of phylogenetic relationship. Hen-
gams are wind pollinated and only some branches
nig's methods also relied upon the dis?
have acquired insect pollination. This assumption
tinction
that wind pollination is more primitive has a high?
made by Zimmermann between
er likelihood [p. 1003]. "character phylogeny" and "taxon phylog?
eny," and he adopted many of the same
In this discussion, Zimmermann focused
strategies in responding to idealistic mor?
his attention on the basal condition in all
phology.
seed plants, and his determination wasAlthough many of the ideas expressed
based, in effect, on which assignment to
by Zimmermann found their way into
this node appeared to be most parsimoni?
Hennig's presentation, Hennig actually
ous. His assessment was based largely onseveral elements less consideration.
gave
the seed plant ("ingroup") tree rather Thus,
thanHennig more or less took for granted
on a comparison of related ("outgroup")the impact of rate inequality on the use of
taxa, and therefore it is not outgroup anal?
similarity in assessing relationship, where?
ysis. Nevertheless, precisely the same as
rea?
Zimmermann devoted considerable at?
soning?regarding nested relationships tention to this issue. Although the basic
and character optimization?underlies logic of outgroup comparison can be dis?
outgroup comparison as we know it today cerned in Zimmermann's paper, Hennig
(Maddison et al., 1984). did not cite or elaborate on this reasoning
Hennig (1966) cited Zimmermann in in his discussion of methods for establish?
connection with the use of paleontological ing the direction of character evolution.
and ontogenetic evidence but made no In view of the elements of phylogenetic
mention of him in connection with the
theory that are evident in Zimmermann's
method just discussed. He did, however, work, it is somewhat surprising that he did
briefly describe a similar method not as one
go further than he did. Zimmermann
type of correlation argument, quoting did not, for example, formulate the concept
Maslin (1952:53), who made reference to of paraphyly. Although the distinction be?
"less modified members of related groups tween monophyly and paraphyly is im?
of the same rank."
plicit in his work, it was never explicitly
The exact origins of outgroup polarity
stated. Furthermore, in practice he did not
assessment are obscure. Although it was
appear to object to the recognition of para-
not formulated as a general principle until
phyletic groups. For example, although he
quite recently, something very much like realized that the "gymnosperms" are para-
it was employed by a number of early au? phyletic (e.g., Zimmermann, 1930; with
thors (see citations in Maslin [1952] and Gnetales and Bennettitales most closely re?
Stevens [1980]; Koponen [1968] provided lated to angiosperms), he continued to rec?
an especially clear example). Regarding ognize "gymnosperms" as a distinct group,
Zimmermann's role, he obviously did notcoordinate with angiosperms in his clas?
invent outgroup analysis exactly as we sification of seed plants (e.g., Zimmer?
know it today. Rather, he understood and mann, 1930; Cronquist et al., 1966). In
clearly explained the basic elements of log?contrast, Hennig clearly distinguished
ic underlying the outgroup method. paraphyly from monophyly and insisted
that knowledge of phylogenetic relation?
Discussion
ships be strictly and accurately reflected in
As we have documented, Zimmermann classification.
presented a clear and detailed statement ofLikewise, despite his appreciation of the

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 POINTS OF VIEW 83

importance of
was not very farpolarity
reaching until he was pub?
mermann lished
did not
in English deve
(1965, 1966). Although
that only Zimmermann published
shared several papers in
derived
English (including
apomorphies) provide a short article in the
e
genetic American Naturalist in 1934 on characterIn
relationship. t
to provideversus
a taxon
method fo
phylogeny), these attracted
phylogeny?a method
virtually no attention. th
vent the evident shortco
Even with the renewed interest in phy?
ity. He suggested
logenetic systematics sinceonly Hennig's pub?
cists proceed with
lication in English, caut
little reference has been
similarity made
andto Zimmermann's contributions.
remain
drawbacks. In Zimmermann's later work Zimmermann is not cited, for example, i
(e.g., 1966), he acknowledged Hennig's
recent textbooks on phylogenetics (El
recognition that similarity might be dredge
due to and Cracraft, 1980; Nelson and
Platnick, 1981; Wiley, 1981; Ax, 1987;
the retention of plesiomorphic characters.
Even then, however, he did not seem to Brooks and McLennan, 1991) nor is he
mentioned in Dupuis's (1984) account of
fully appreciate the significance of synapo?
Hennig's ideas and their influence on tax?
morphy as a substitute for overall similar?
ity. onomic thought. This oversight may be
The concepts of paraphyly and synapo? partly a result of the fact that the first En?
morphy awaited development by Hennig, glish-speaking students of Hennig's work
who also extended the application of phy? were zoologists (e.g., Gareth Nelson, Colin
logenetic systematics to the study of such Patterson; see Hull, 1988), who may have
things as historical biogeography and the been unaware of Zimmermann's botanical
tempo of evolution. Thus, despite Zim? contributions and had little reason to in?
mermann's early and fundamental contri? vestigate his papers cited by Hennig, es?
butions, it is correct in our opinion to view pecially in view of the language barrier.
Hennig as the father of modern phyloge? May r's (1982) brief reference to Zimmer?
netic systematics, just as it is correct to con? mann implies that he was an idealistic
sider Darwin the father of evolutionary morphologist. Yet even casual inspection
theory. But Hennig's ideas did not arise de of Zimmermann's work shows, on the con?
novo or fully formed, any more than Dar? trary, that he argued consistently against
win's did (e.g., Hull, 1988). Rather, they idealism (Reif, 1986).
are best understood as part of an intellec? The botanist Koponen (1968), who ap?
tual tradition that developed in response plied cladistic methods at a very early stage
to the idealism that pervaded German sci? (to the moss family Mniaceae), cited both
ence at the time. The "discovery" of Zim? Hennig and Zimmermann for the devel?
mermann's work helps us appreciate the opment of a "cladistic-phyletic school" of
magnitude of this influence and also helps systematics. Since then, Zimmermann
tease apart the sequence of events that cul? seems to have been forgotten even by bo?
minated in Hennig's synthesis. tanical cladists, with the exception of pass?
It is remarkable how little attention has
ing references by Stevens (1980) and more
been paid to Zimmermann's contributions recently by Humphries and Chappill
to phylogenetic theory. The timing of(1988).his
early work in relation to the onset of World Another factor contributing to the ne?
War II and the associated turmoil in Ger? glect of Zimmermann's systematic theory
many (and elsewhere) may help account is that Zimmermann was apparently not a
for this neglect. Yet Hennig assimilated
very effective advocate of his own ideas
Zimmermann's work almost as soon as it about phylogeny, although he did reiterate
was possible to do so under the circum?
his systematic theory in several later pub?
lications.
stances, referring to it frequently and in Indeed, he devoted much more
very positive terms in his earlier work
of (e.g.,
his energy in later years to his interests
in plant morphology, especially in con-
1950). Of course, even Hennig's influence

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 84 SYSTEMATIC BIOLOGY VOL. 41

nection with the Grene, M. 1958. Two evolutionary theories.

development ofBr. J. th
Philos. Sci. 9:110-127, 185-193.
theory (e.g., numerous publications
Hennig, W. 1950. Grundzuge einer Theorie der phy-
satilla-, see references in Zimmermann,
logenetischen Systematik. Deutscher Zentralver?
1965). This case might support Hull's ar? lag, Berlin.
gument (1988:365-367) that in the absence Hennig, W. 1965. Phylogenetic systematics. Annu.
of a certain amount of advocacy for one's Rev. Entomol. 10:97-116.
own ideas, one may well become an un?Hennig, W. 1966. Phylogenetic systematics. Univ.
Illinois Press, Urbana.
appreciated precursor of other more asser?
Hull, D. L. 1988. Science as a process. An evolu?
tive scientists.
tionary account of the social and conceptual de?
Walter Zimmermann was an extraordi? velopment of science. Univ. Chicago Press, Chi?
narily thoughtful individual, whose con?
cago.
Humphries, C. J., and J. A. Chappill. 1988. System?
tributions to systematic and evolutionaryatics as science: A response to Cronquist. Bot. Rev.
theory never attracted the recognition they
54:129-144.

deserve. We hope that by highlighting

Koponen, T. 1968. Generic revision of Mniaceae Mitt.
Zimmermann's contributions to phyloge?(Bryophyta). Ann. Bot. Fenn. 5:117-151.
Maddison, W. P., M. J. Donoghue, and D. R. Mad?
netic theory more attention will be paid
dison. 1984. Outgroup analysis and parsimony.
not only to his work but to the social and
Syst. Zool. 33:83-103.
conceptual history of phylogenetic system?
Maslin, T. P. 1952. Morphological criteria of phy-
atics. letic relationships. Syst. Zool. 1:49-70.
Mayr, E. 1982. The growth of biological thought.
Acknowledgments Harvard Univ. Press, Cambridge, Massachusetts.
Mayr, E., and W. Provine (eds.). 1980. The evolu?
We are grateful to Ken Sytsma and the Botany
tionaryDe?
synthesis. Harvard Univ. Press, Cambridge,
partment of the University of Wisconsin Massachusetts.
for their
hospitality during our residence in Madison.
Mez, M.J.D.
C., and H. Ziegenspeck. 1926. Der Konigsber-
was supported by a grant from the National gerScience
serodiagnostische Stammbaum. Bot. Arch. 13:
Foundation (BSR-8822658), and J.W.K. was483.a Heisen?
berg Scholar, funded by the German Research Foun?
Nelson, G., and N. Platnick. 1981. Systematics and
dation (DFG). We also thank Jim Doyle, Olivier Riep-
biogeography. Cladistics and vicariance. Columbia
pel, and Peter Stevens for helpful discussion.
Univ. Press, New York.
Plate, L. 1912. Deszendenztheorie. Pages 897-950
in Handworterbuch der Naturwissenschaften. 1.
REFERENCES
Aufl. Bd. 2. G. Fischer, Jena, Germany.
Ax, P. 1987. The phylogenetic system: The system?Plate, L. 1914. Prinzipien der Systematik mit be-
ization of organisms on the basis of their phylo? sonderer Berucksichtigung des Systems der Tiere.
genesis. John Wiley & Sons, New York. Kultur der Gegenwart 4(3):92-164.
Bigelow, R. S. 1956. Monophyletic classification and Reif, W.-E. 1986. Evolutionary theory in German
evolution. Syst. Zool. 5:145-146. paleontology. Pages 173-204 in Dimensions of Dar?
Bigelow, R. S. 1958. Classification and phylogeny. winism (M. Grene, ed.). Cambridge Univ. Press,
Syst. Zool. 7:49-59. Cambridge, England.
Brooks, D., and D. Mclennan. 1991. Phylogeny, Sattler, R. 1964. Methodological problems in tax?
ecology, and behavior. A research program in com? onomy. Syst. Zool. 13:19-27.
parative biology. Univ. Chicago Press, Chicago. Stafleu, F. A., and R. S. Cowan. 1976. Taxonomic
Cronquist, A., A. Takhtajan, and W. Zimmermann. literature: A selective guide to botanical publica?
1966. On the higher taxa of Embryobionta. Taxon tions and collections with dates, commentaries and
15:129-134. types, 2nd edition. Regnum Vegetabile, Volume 94.
de Queiroz, K., and M. J. Donoghue. 1988. Phy?
Bohn, Scheltema and Holkema, Utrecht, The Neth?
logenetic systematics and the species problem.erlands.
Cla?
distics 4:317-338. Stevens, P. F. 1980. Evolutionary polarity of char?
Dupuis, C. 1984. Willi Hennig's impact on taxonom?
acter states. Annu. Rev. Ecol. Syst. 11:333-358.
ic thought. Annu. Rev. Ecol. Syst. 15:1-24. Stewart, W.N. 1983. Paleobotany and the evolution
Eldredge, N., and J. Cracraft. 1980. Phylogenetic
of plants. Cambridge Univ. Press, Cambridge, En?
patterns and the evolutionary process. Columbia
gland.
Univ. Press, New York. Troll, W. 1940. Phylogenetische oder idealistische
Farris, J. S. 1982. Outgroups and parsimony. Syst. Morphologic? Eine Berichtigung. Bot. Arch. 40.
Zool. 31:328-334. Watrous, L. E., and Q. D. Wheeler. 1981. The out?
Foster, A. S., and E. M. Gifford. 1974. Comparative
group comparison method of character analysis.
morphology of vascular plants, 2nd edition. Syst.
W. H. Zool. 30:1-11.
Freeman, San Francisco. Wiley, E. O. 1981. Phylogenetics. The theory and

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms
 1992 POINTS OF VIEW 85

practice of Zimmermann, W. 1943. Die Methoden der syst

phylogenetic Phylo?
Sons, New York. genetic Pages 20-56 in Die Evolution der Organis-
Zimmermann, W. 1930. Die Phylogenie der Pflan-men (G. Heberer, ed.). 1. Aufl. G. Fischer, Jena,
zen. G. Fischer, Jena, Germany. Germany.
Zimmermann, W. 1931 (1937). Arbeitsweise der bo- Zimmermann, W. 1965. Die Telomtheorie. Fort-
tanischen Phylogenetik und anderer Gruppie- schrifte der Evolutionsforschung, Band I. G. Fi?
rungswissenschaften. Pages 941-1053 in Handbuch scher, Stuttgart, Germany.
der biologischen Arbeitsmethoden (E. Abderhal- Zimmermann, W. 1966. Phanetische und phyloge-
den, ed.). Abt. 3, 2, Teil 9. Urban & Schwarzenberg, netische Verwandtschaft. Phyton 11:145-163.
Berlin. Zimmermann, W. 1967. Methoden der Evolutions-
Zimmermann, W. 1934. Research on phylogeny ofwissenschaft [=Phylogenetik]. Pages 61-160 in Die
species and of single characters. Am. Nat. 68:381-Evolution der Organismen (G. Heberer, ed.). 3. Aufl.
384. G. Fischer, Stuttgart, Germany.
Zimmermann, W. 1938. Die Telomtheorie. Biologe
7:385-391. Received 3 July 1991; accepted ll December 1991

Syst. Biol. 41(l):85-88, 1992

A Review of Estimates of Nonreciprocity in

Immunological Studies
Craig Guyer

Department of Zoology and Wildlife Science, Auburn University,

Auburn, Alabama 36849, USA

Biochemical data are useful for inferring

from B to A. If this requirement were met
phylogenetic relationships. Albumin im?
consistently, then there could be a massive
reduction
munology represents one such type of data. in workload because analyses
With this method, the relative degree
couldofbe performed with one-way com?
antigen-antibody reactions is usedparisons
to es? (e.g., only the distance from A to
timate the immunological distance be? be needed because this would be
B would
tween pairs of taxa. Because the reaction
an accurate estimate of the distance from
B to A).
strength is linearly related to the number
of amino acid replacements (MaxsonMany
andstudies have demonstrated that
Maxson, 1986), this method is touted to be
reciprocity is rarely achieved. The only
appropriate for phylogenetic distance
model designed to explain nonreciprocity
analyses (following the criteria ofexplicitly
Farris is that of Faith (1985). According
[1972]). If other assumptions are met, this
to this model, nonreciprocity results from
method can be used to estimate divergence
the fact that antibodies to species A are
times and divergence patterns (Wilson et by a host organism, usually a
generated
al., 1977). rabbit. A perfect antibody would recognize
The utility of albumin immunological
all antigenic sites in albumin proteins from
data depends upon conformation to A.
the as?
However, because rabbits can share an?
sumptions of the triangle inequality tigenic sites with species A, some sites may
(Sneath and Sokal, 1973). One assumptionnot be recognized by the antibody. There?
is that the data generated are reciprocal, fore, the measurable distance between spe?
i.e., the distance estimated from taxon A cies A and some other taxon (species B) is
to taxon B is the same as that estimated typically less than the total distance be-

This content downloaded from

179.217.140.163 on Wed, 20 Apr 2022 04:06:44 UTC
All use subject to https://about.jstor.org/terms