Biological Journal of the Linnean Society (1990), 39: 177-191. With 1 figure
Ontogeny-a way forward for systematics, a
way backward for phylogeny
0. RIEPPEL, F.L.S.
Palaontologisches Inslitut und Museum der Universitat, Kunstlergasse 16, CH-8006
Zurich, Switzerland
In the history of biology, the term ‘evolution’ has carried a dual meaning, viz. ontogeny (the
unfolding of the germ) versus phylogeny (descent with modification). A problem in modern biology
is the question of whether it is ontogeny which creates phylogeny, or whether it is phylogeny which
moulds ontogeny. The paper explores the relationship of ontogeny to phylogeny in the context of
‘pattern cladism’. The conclusion is that the analysis of ontogeny provides a direct method for
classification (‘a way forward for systematics’), which is a logical prerequisite for a phylogenetic
interpretation of ontogenetic sequences (‘a way backward for phylogeny’). The ontogenetic process
of growth, subdivision and differentiation is related to the ‘morphogenetic tree theory’ on the basis
of Von Baer’s “laws of individual development”. This conceptual relation shows that ontogeny
creates phylogeny in an upward direction within the morphogenetic tree, whereas phylogeny (by
means of natural selection) moulds ontogeny in a downward direction. A conflict originates with the
conventions of Linnaean classification if ontogenetic divergence is proposed as a causal agent in the
origin of higher taxa. It is proposed to solve this conflict by viewing individual organisms (or
reproductive communities) not as constituents, but as representatives of higher taxa.
KEY WORDS:--0ntogeny
-
phylogenesis
-
palingenesis
-
caenogenesis - morphogenetic tree.
CONTENTS
Introduction: the meaning of evolution.
. . . . . . . . .
Recapitulation and morphogenetic hierarchy . . . . . . . .
‘The potential and its actuality: Von Baer’s laws of individual development .
Systematics and phylogeny: logic of argumentation . . . . . . .
Evolution of the morphogenetic tree
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Evolution: continuity of change
Logical subordination versus historical contingency . . . . . . .
Acknowledgements
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References
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INTRODUCTION: T H E MEANING OF EVOLUTION
The living world is one of change, or metamorphosis in the broadest meaning
of the term. Each organism is created during its ontogeny, as it develops (in
metazoans and metaphytans) from a phenotypically homogeneous primordium
(the initial developmental inhomogeneity is at the cytoplasmic and genetic level:
Levinton, 1988) to a complex heterogeneous adult according to a genetic
programme, inherited from its parents, and according to time-independent laws
0024-4066/90/020177
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Society of London
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of geometry, physics and chemistry. I n that sense there is a persistent duality of
the term ‘evolution’ in modern biology (see Bowler, 1975 for an historical
account). The original use of the term was for the ontogenetic unfolding of a
germ; the modern use implies a phylogenetic process of transformation.
Ontogeny creates structural complexity, and in so doing it translates a genetic
programme which incorporates historical information, into positional and
physico-chemical relations. Genes serve as transmitters of information from one
generation of organisms to the next, which represent (rather than constitute) an
evolving lineage (see Rieppel, 1988a: 45, and below). The dual meaning of the
term ‘evolution’ points to a reciprocal relation between ontogeny and
phylogeny:
Any change in the ‘rules of construction’, changing developmental patterns,
causes a phylogenetic change in the lineage represented by the developing
organism(s): ontogeny creates phylogeny
Each phylogenetic change affecting an evolving lineage is reflected in the
changing ontogeny of the organism(s) representing that lineage: phylogeny
creates ontogeny.
The purpose of this paper is to explore the interdependence of ontogeny and
phylogeny, and to outline its relation to systematics.
RECAPITULATION A N D MORPHOGENETIC HIERARCHY
The relation of ontogeny to systematics and phylogeny was originally
conceptualized in terms of a parallelism between the pattern of ontogenetic
differentiation and the classification of organisms in a hierarchy of types
(Rieppel, 1985); this parallelism found its causal explanation in the theory of
recapitulation, popularized by Ernst Haeckel under the heading of the
“biogenetic law”. After a period of neglect or rejection, the parallelism of
ontogeny and order in nature has been resurrected, in the framework of cladistic
theory, as a direct method for pattern analysis and phylogeny reconstruction
(Nelson, 1978; Patterson, 1982). Two modes of recapitulation have been
recognized (Lavtrup, 1978): Haeckelian recapitulation (in fact the “MeckelSerres Law”: Gould, 1977; Arthur, 1988: 30) resulting from terminal addition of
new developmental steps to an already existing ontogenetic sequence; and Von
Baerian recapitulation or deviation (Gould, 1977: 224; Arthur, 1988: 24),
resulting from divergence (and/or non-terminal addition) of developmental
pathways (see Rieppel, 1988b, for a more detailed discussion).
These two types of recapitulation will here be related to the “morphogenetic
tree theory” proposed by Arthur ( 1988). The “morphogenetic tree” refers to the
hierarchical structure (indicating a hierarchical organization) of epigenesis, the
process of individual development as conceptualized by W. Harvey (1651; see
Harvey, 1981), K. F. Wolff (1764) and K. E. Von Baer (1828) (see Arthur, 1984
and Rieppel, 1985, 1986, for further discussion). According to the model of
epigenesis, which was conceptualized on the basis of “purely phenotypic
observations” (Arthur, 1988: 27), development proceeds from the homogeneous
to the heterogeneous, from the more general to the less general condition of form
through a process of growth (“budding”), compartmentalization and
differentiation (“individualization”). Cells, tissues, organs and organ-complexes
ONTOGENY, SYSTEMATICS AND PHYLOGENY
179
develop in a linear or branching succession, one emerging and diff’erentiating
from the other. A linear succession of developmental stages results from terminal
addition to existing ontogenetic sequences. The basic mechanism producing a
linear succession of developmental steps is simple growth which adds to what
already exists. Growth often entails differentiation (Lavtrup, 1988), in which
case a terminal step of ‘metamorphosis’ (in the broadest meaning of the term) is
added to an existing ontogenetic sequence. Because growth and concomitant
differentiation constitute the principal mechanisms of terminal addition, they
represent the principal causes of Haeckelian recapitulation.
A simple example of terminal addition is the differentiation of the jaw
adductor musculature in amniotes. Originally confined in its extent to the space
between the inner neurocranium and the outer dermatocranium (in
captorhinomorph stem-reptiles: Heaton, 1979), the musculature shows a
tendency to escape these narrow confines in a posterodorsal direction across the
otic region to what Save-Soderbergh ( 1945) called the “temporalis position”.
The posterodorsal expansion of the jaw adductor musculature, requiring
correlated changes in cranial structure, occurs convergently in such disparate
groups as some fossorial lizards (Rieppel, 1984), amphisbaenians (Rieppel,
1979a), snakes (Rieppel, 1989), chelonians (Rieppel, 1990) and synapsids
(Crompton, 1962; Barghusen, 1968). In those cases where comparative
developmental data are available (e.g. for the grass snake and the snapping
turtle, as compared to a standard lizard: Rieppel, 1987a, 1989, 1990), the
extension of the deep layers of the jaw adductor musculature to a “temporalis
position” results from hypermorphotic growth, correlated with internal
differentiation. A similar mechanism is conceivably involved in the
differentiation of the temporalis muscle during the transition from reptiles to
mammals (cf. Edgeworth, 1935).
A deviation of developmental stages results from compartmentalization and
divergent differentiation (“individualization” in Von Baer’s terms) of the
“primary morphic units” (Rieppel, 1988b: 43). The paradigmatic example is
provided by insect development, during which segmentation (resulting from a
process of budding or compartmentalization) provides the “building pieces”
(Sander, 1983: 145) for further differentiation (see also Raff & Kaufman,
1983: 25 1-26 1) . A similar, hierarchically subordinated sequence of bifurcating
determination and differentiation characterizes the developmental fate of cell
lineages such as the mouse ectoderm (Raff & Kaufman, 1983:223) or tooth
mesenchyme (Osborn, 1984: 564). The result is Von Baerian recapitulation
(Lervtrup, 1978).
Morphogenetic tree theory treats deviation-as conceptualized by Von Baer’s
laws of individual development (see below)-as “one of the most striking
generalizations about morphological evolution” (Arthur, 1988: 29) for which it
seeks to elucidate the underlying causes and mechanisms. The ontogenetic
process of growth, subdivision and differentiation can be understood in terms of
a branching “morphogenetic tree” (Arthur, 1988), a hierarchical conception of
ontogeny composed of a number of “causal links” (Arthur, 1988: 21), and
terminal “twigs”. The topology of the morphogenetic tree, a dichotomous
hierarchy of branching points, depicts the subordinated sequence of
developmental bifurcations. The notion of “developmental bifurcation” carries a
dual meaning: it captures the phenomenological (observational) description of
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the developing system in terms of a hierarchically organized process of
differentiation, but it also refers to a causal binary “decision”, committing the
transformation system to a developmental pathway (Oster el al., 1988: 868). In
its development and compartmentalization, the paraxial mesoderm provides a
series of repetitive units or building blocks (somites). These may undergo
divergent differentiation in the development of the skull and of a regionalized
vertebral column. At a lower level of structural complexity, the somite is itself
compartmentalized, with the sclerotomic cells producing chondroblasts, osteoblasts, etc. A subordinate sequence of developmental “decisions” creates the
appearance of a hierarchically organized pattern of differentiation. More
precisely: a subordinate hierarchy of developmental “decisions” is inferred
(deduced) from the observed pattern of differentiation, which is appropriately
captured by the morphogenetic tree theory (Arthur, 1988).
Terminal addition increases the length of the terminal twigs on a
morphogenetic tree and hence causes a linear sequence of transformation stages
which will be recapitulated during ontogeny in a Haeckelian pattern. Deviating
differentiation, starting from a common early primordium, induces a branching
point in the process of morphogenetic differentiation and hence increases the
number of links (i.e. of stages or pathways) in the development of complex
systems. The subordinated pattern of increasing structural heterogeneity is
recapitulated during ontogeny in a Von Baerian pattern. Other possibilities are
as follows: non-terminal addition increases the length of intermediate links; insertion
(a special case of non-terminal addition) is a means of intercalating additional
links such as larval adaptations; deletion removes previously present links, a
simple case being the loss of a terminal twig through paedomorphosis. Arthur
(1988: 21-22) gives a different classification of evolutionary changes possible for
a morphogenetic tree system.
The number of links which make up a morphogenetic tree is a measure of
complexity (or heterogeneity) of that particular organism (Arthur, 1988) in
comparison to its sister taxon (or hypothetical ancestor). The basic
constructional principle permitting an increase in complexity (heterogeneity) is
the metameric organization of the anluge, or segmentation. Growth adds to the
size and, in combination with subdivision or ‘budding’, to the number of
building blocks emerging from a primordium. Compartmentalization results in
multiplication of constituent elements of a given structure, while divergent
differentiation of segments or compartments adds the potential for structural and
functional diversification. This view links with work on functional anatomy
showing “duplication and repetition” of parts to represent an important
prerequisite for morphological diversification (Lauder, 1981: 438).
THE POTENTIAL AND ITS ACTUALITY: VON BAER’S LAWS OF INDIVIDUAL
DEVELOPMENT
“Development translates genotype into phenotype” (Raff, 1989: 5 16). T h e
genetic programme defines a “norm of reaction” and hence the developmental
potential of an organism which becomes actualized during ontogeny. The
developmental actualization (materialization) of structural complexity is
hierarchically ordered, the order being determined by terminal addition
(sequential hierarchy) or by deviation (subordinated hierarchy). Since L ~ v t r u p
ONTOGENY, SYSTEMATICS AND PHYLOGENY
181
(1978) has shown that terminal addition is nothing but a special case of
deviation (“terminal deviation”), it follows that Haeckelian recapitulation is a
special case of Von Baerian recapitulation.
Von Baer (1828: 224) formulated four “Laws of Individual Development”, of
which the third and the fourth specify the principle of divergence directed
against the Meckel-Serres-Law. The third law reads: “each embryo of a given
animal form, instead of passing through the definite form of other animals,
deviates from the latter”. The fourth law states: “therefore, an embryo of a
higher animal form never corresponds to another animal form, but only to the
latter’s embryo”.
Von Baer’s first and second laws capture the hierarchy of the epigenetic
process of morphological differentiation. According to the first law, “common
features of a more inclusive group of animals develop earlier in the embryo than
special features”, characterizing a subordinated, less inclusive group. The second
law states: “from the most general characteristics of form develop the less general
characteristics until finally the most specialized features make their appearance”.
It is important to distinguish Von Baer’s first and second laws because they
make different predictions (Patterson, 1983). The second law predicts that the
ontogenetic process of differentiation determines structural relations according to
the “principle of generality” (see next section): the less generally distributed
character develops from a more general condition of form, or, to put it in simpler
terms: ontogeny proceeds from absence to presence (Patterson, 1982). The
hierarchical pattern of epigenetic unfolding will therefore be congruent with the
hierarchy of homologies established by outgroup comparison (see below).
The first law of individual development is less general in that it predicts the
sequential development of “typical characteristics” within whole organisms
(Patterson, 1983: 25). Ontogeny recapitulates the hierarchy of types (Rieppel,
1985), i.e. the hierarchy of inclusive taxa: the embryonic mammal first passes
through a vertebrate stage, then through a tetrapod stage, etc., before its
mammalian characteristics make their appearance. Ontogeny is predicted to
recapitulate the axis of a cladogram which specifies the sequence of subordinated
taxa of decreasing inclusiveness (Fig. 1) : vertebrates originate before tetrapods
which precede the appearance of mammals. There are numerous exceptions to
Von Baer’s first law: the amnion develops prior to tetrapod characteristics
although the Amniota are subordinated to, and less inclusive than, the
Tetrapoda (Patterson, 1983). A great variety of larval adaptations and
specializations are exceptions to Von Baer’s first law as are instances of dissimilar
embryonic stages producing similar adult conditions of form. Early development
may differ radically in related organisms, a point raised by De Beer (1958)
against recapitulation, and by Raff (1989) against the morphogenetic tree
theory.
I n fact, exceptions to his first law, such as the amnion and other, embryonic or
larval adaptations, were well known to Von Baer (1828), and they forced
E. Haeckel to distinguish palingenesis (“epitomized history”: Gould, 1977: 82)
from caenogenesis (“falsified history”: Gould, 1977: 82). For Haeckel, only the
palingenetic sequence of phyletic stages was recapitulated in an incomplete and
abbreviated manner. This reading of the “biogenetic law” comes close to Von
Baer’s first law: ontogeny recapitulates the axis of the cladogram in a
palingenetic direction (see Rieppel, 1985, for a discussion, and Fig. l ) ,
0. RIEPPEL
182
I
0
inclusive
hlerarchy
of types
Terminal Taxa
Figure 1 . The relation of the palingenetic axis to the cladogram.
progressing from more inclusive groups to subordinated, less inclusive groups in
the hierarchy of types (phyletic stages of Haeckel). Caenogenesis refers to all
aberrations
of early development barred from recapitulation.
If morphogenetlc tree theory is to address the underlying causality of Von
Baer’s morphological generalizations, it must preserve the distinction of
palingenesis and caenogenesis. Arthur (1988: 68-69) noted the radical
differences of early development in vertebrates u p to gastrulation (an issue raised
by Raff, 1989: 516, in his review) and exempted this observation from
explanation by morphogenetic tree theory. Early patterns of cleavage might be
controlled by maternal gene products, that is by a separate genetic programme.
Arthur also made it clear that in organisms with complex life cycles, a single
ONTOGENY, SYSTEMATICS AND PHYLOGENY
183
morphogenetic tree will not suffice to capture the developmental complexity. His
figure 1.4 (Arthur, 1988: 10) shows a “double-tree system underlying the
development of holometabolus insects”. The divergence in early development of
sea urchins (Parks et al., 1988) or frogs (Levinton, 1988: 223-224) with direct
development, as opposed to related species passing through the typical larval
stage, is a striking example of caenogenesis caused by heterochrony. The
example of sea urchins provides evidence that caenogenetic larval stages
correspond to “developmentally distinct compartments” controlled by “distinct
programmes of gene expression” (Parks et al., 1988: 42). This not only explains
the ease with which the heterochronic loss of the larval stage is achieved in
closely related forms, but it also makes clear that complex life cycles require a
complex of genetically (at least partially) independent morphogenetic trees for
their explanation.
As a causal explanation of Von Baer’s first law, however, morphogenetic tree
theory needs to address the underlying causality of palingenetic change only,
leaving caenogenetic changes to separate explanations. I n view of the intricate
integration of the genetic programme it would appear questionable, however,
whether the underlying causality of Von Baer’s first law can be conceptualized in
terms of a simple and unidirectionally acting hierarchy of “developmental
genes” (Arthur, 1988). The integration of the underlying genetic programme,
and that of the developing structural complex, may have different patterns
(Levinton, 1988: 220). Nevertheless, some evidence will be discussed below
indicating rather tight constraints placed on the early ontogenetic determination
of palingenetic stages of transformation, reflecting a high degree of physiological
and/or functional integration. This is, after all, the reason for the existence of a
hierarchy of types, or body plans, permitting the classification of organic
diversity in a hierarchical system of natural groups.
SYSTEMATICS AND PHYLOGENY: LOGIC OF ARGUMENTATION
Epigenesis is a model of development with hierarchical subordination of. steps
of metamorphosis or differentiation by growth, subdivision and subsequent
individualization of compartments. As formalized by Von Baer’s second law of
individual development, this hierarchy of epigenetic development parallels the
subordinated classification of organic diversity in a hierarchy of types and
subtypes (Rieppel, 1985). More general precede less general conditions of form
during ontogeny, a phenomenon that corresponds to the subordinated
classification of organisms on the priniciple of generality (Nelson, 1978, 1985;
Patterson, 1982, 1983). The principle of generality has been concisely formulated
by W. P. Maddison (quoted in de Queiroz, 1985: 283), and it states: “character x
is more general than charactery if and only if all organisms possessingy (at some
stage in ontogeny) also possess x and in addition some organisms possessing x do
not possess$’. This principle not only forms the basis for the method of outgroup
comparison (an indirect method of pattern reconstruction: Nelson, 1985), but it
also conforms to Von Baer’s second law (Patterson, 1983). As long as the second
law holds (and it remains unrefuted for vertebrates: Patterson, 1983), the
developmental hierarchy is a direct method for classification (Nelson, 1 9 8 5 ) p a
way forward for systematics. The analysis of the epigenetic hierarchy is an
empirical clue to the construction of rational classification. A corollary is that the
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morphogenetic tree mirrors the cladogram. The causal explanation for that
parallelism of ontogeny and classification is the theory of recapitulation.
Classification on the principle of generality corresponds to the method of
logical subordination (Rieppel, 1987b, 1988a, b), producing a time-independent
hierarchy of types. In this context, the hierarchy of types is not idealistic, but
rather a logical concept, indicating congruence of diagnostic characteristics in a
subordinated hierarchical pattern (Rieppel, 1985). Congruence of characters
(Patterson, 1982) a measure of stability and of information content of the
corresponding classification, reflects regularity in character distribution, which
calls for a causal explanation: why should characters fall into a hierarchical
pattern? The causal explanation for the hierarchy of types is provided by
evolutionary theory: Darwin explained the unity of type by unity of descent
(Brady, 1985). Congruence of characters provides evidence of common ancestry.
Descent with modification implies no logical necessity, but addresses historical
contingency. Descent with modification is not observable; it must be inferred
from observed regularity of character distribution. It follows that pattern
reconstruction has precedence over evolutionary explanation both in terms of
logical stringency and of empirical content (Brady, 1985). Observed regularity of
pattern must precede its explanation by a theory of phylogenetic process: every
hypothesis of descent depends on observed similarity; every hypothesis of descent
must be framed within a hypothesis of relationship. Evolutionary explanation
looks back on pattern reconstruction. This relation between pattern
reconstruction and evolutionary theory is the reason why ontogeny is a way
forward for systematics and a way backward for phylogeny. Epigenetic
development, proceeding from the more general to the less general condition of
form, is an observational (empirical) clue to the axis of the cladogram specifying
ever less inclusive levels of generality (Fig. 1); hypotheses of descent with
modification proceed along the axis of the cladogram to ever higher levels of
inclusiveness to find the shared evolutionary roots of organismic diversity.
This complementary relation of ontogeny to systematics and phylogeny is
highlighted by the continuing argument against the use of ontogeny in
systematics. The ontogenetic method is rejected because it cannot test for
paedomorphosis (Rieppel, 197913; Kluge, 1985, 1988). Paedomorphosis removes
“twigs” from the morphogenetic tree, by retardation of somatic development
(neoteny), by delayed onset of embryonic development (post-displacement) or
by precocious attainment of sexual maturity (progenesis) (Gould, 1977). A
paedomorphic organism is likely to be inserted a t an incorrect level of
inclusiveness on the axis of the cladogram, which results in its erroneous
classification. Paedomorphosis can be treated as an instance of character
incongruence which requires, for its detection, a robust hypothesis of relationship
based on independent evidence (i.e. congruence of independent characters).
Outgroup comparison is proposed as the standard alternative to the ontogenetic
method, but outgroup comparison is not only as prone to character
incongruence as ontogeny; it also requires, in addition, a hypothesis of higher
level relationship which specifies the outgroup (sister group) of the group under
investigation.
The crux of the debate lies in a failure to distinguish arguments about pattern
reconstruction from those about phylogeny. Classification is based on observed
regularity of character distribution, and it can be obtained by ontogeny (direct
ONTOGENY, SYSTEMATICS AND PHYLOGENY
185
method) or by outgroup comparison (indirect method). The hierarchy of types
capturing character congruence is explained by the theory of descent with
modification, and its parallelism to the ontogenetic process of differentiation is
explained by the theory of recapitulation. However, both methods, ontogeny as
much as outgroup comparisons, are likely to reveal some character
incongruence-a hindrance to classification which is causally explained either by
convergence or by paedomorphosis (convergence may result from
paedomorphosis). I t is only logical that the ontogenetic method cannot test for
paedomorphosis, because it is an empirical way forward not for phylogeny, but
for systematics. Once an economic (parsimonious) classification has been
established, it is possible to look back at the hierarchical pattern of order to see
which instances of incongruence it reveals, and to ask how these might be
explained. Paedomorphosis might be the answer.
EVOLUTION OF T H E MORPHOGENETIC T R E E
Epigenesis reveals the evolution of the morphogenetic tree in the original sense
of the word, meaning its unfolding during the morphogenetic timescale. This
hierarchically structured process of unfolding mirrors the subordinated
classification of organisms, which is explained by evolution. In this context,
however, the term evolution changes its meaning to descent with modification
during the phylogenetic timescale. T h e dual meaning of the term ‘evolution’
thus provides a potential bridge linking the morphogenetic tree to the
phylogenetic tree. An organism is created through evolution (ontogeny) as a
representative of an evolving (phylogenetic) lineage.
There are two ways of looking at the hierarchy of ontogenetic development:
from the ‘bottom up’ (proceeding from more inclusive to ever less inclusive levels
of generality), or from the ‘top down’ (from less to more inclusive hierarchical
levels). From the causal explanation of order in nature through the theory of
evolution it follows that ontogeny creates phylogeny from ‘bottom up’, whereas
phylogeny moulds ontogeny from ‘top down’.
Ontogeny is a creative process: it creates complexity following a genetic
programme, which is historically contingent, and epigenetic factors, which are
time-independent (such as geometrical relations and physico-chemical laws).
Phylogeny is likewise a creative process: it creates structural diversity through
selection and adaptation. The sources of evolutionary modification are twofold:
any change in the developmental programme changes the rules of construction
of biological systems. Because each organism is also a representative of an
evolving lineage, any change in its rules of construction has an effect on the
phylogeny of the respective lineage, provided the change comes to characterize a
reproductive community: ontogeny creates phylogeny. The converse holds true
for adaptive modifications of biological structures, caused by natural selection
operating on reproductive communities. Because every biological structure must
evolve (unfold) through ontogeny, any adaptive modification of structure must
become fixed in the ontogeny of the representatives of a phylogenetic lineage if
this adaptation is to be propagated from one generation to the next. Phylogeny
creates ontogeny.
Ontogeny reveals a hierarchically organized process of morphogenesis.
Organisms created through this process fall into a parallel hierarchy of groups
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under groups: to the extent that the jirst law of Von Baer holds, ontogeny
recapitulates the (palingenetic) axis of the cladogram in an orderly pattern
(Fig. 1). The axis of the cladogram determines the hierarchy of inclusive taxa,
proceeding from more inclusive to less inclusive levels. Any change in the rules of
construction of an organism (as a representative of a phylogenetic lineage)
induces a bifurcation on the axis of the cladogram. The bifurcation is introduced
at a higher level of inclusiveness the earlier the ontogenetic stage of the deviating
differentiation. If ontogeny creates phylogeny, it must follow that ontogeny
creates phylogeny along the axis of the cladogram, that is proceeding from more
inclusive to less inclusive levels of the genealogical hierarchy. In Linnaean terms,
evolution through ontogenetic deviation proceeds from phylum to class, to order,
to family, to genus, to species. Ontogeny is the cause of discontinuity in
macroevolution, with the potential to cause major changes within relatively
short periods of time.
T h e reverse holds true for phylogeny (evolution) as a process of adaptation
through natural selection which affects the terminal taxa on the cladogram, that
is, the reproductive communities (terminal taxa under creation sensu Lmtrup,
1977: 49-50). It acts from top to bottom within the morphogenetic hierarchy,
from less to more inclusive levels in the genealogical hierarchy: in Linnaean
terms, successive changes in evolving populations add up to the formation of
species, of genera, of families, of orders, of classes, of phyla, etc. Adaptation
through natural selection is the cause of continuous microevolution, which may
add up to macroevolutionary effects through geological time.
An empirical measure of the respective importance of the two mechanisms of
evolutionary change is provided by character incongruence, which increases
along the axis of the cladogram towards lesser levels of inclusiveness. More
inclusive taxa such as metazoan phyla, classes or orders are usually very stable
groups, characterized by a high degree of character congruence. Incongruence
increases dramatically in the analysis of less inclusive groups such as genera,
species or populations. One might view this relation as a function of extinction
over time, but in view of the notorious absence of fossil intermediates (Valentine
& Erwin, 1987), it seems more reasonable to view character congruence as a
measure of integration of biological structures, resulting from the functional and/
or physiological correlation of their constituent elements. T h e corollary is that
developmental constraints increase with increasing inclusiveness of hierarchical
levels, or, to put it in other words: early ontogenetic stages, specifying topological
relations of major body plans at high levels of inclusiveness along the
palingenetic axis (Fig. l ) , will rarely if ever tolerate major perturbations. The
stability of classifications at more inclusive levels is explained by the
conservativeness of early developmental sequences, deriving from their causal
interdependence (Alberch, 1985). Conversely, greater character incongruence at
less inclusive levels of the genealogical hierarchy indicates a greater adaptive
plasticity of structures as well as of developmental mechanisms during late
ontogenetic stages. This observation is in accordance with the (theoretical) call
for a hierarchical compartmentalization or partitioning of the genome
(Valentine, 1986; Bonner, 1988) controlling development, with mutations
affecting early developmental stages having greater phenotypical consequences
as compared to mutations affecting later stages (Arthur, 1984).
The conclusion is that the rapid or sudden appearance of a new type of
ONTOGENY, SYSTEMATICS AND PHYLOGENY
187
construction through early ontogenetic deviation is a possible but rare event
(Arthur, 1988: 72). That it is possible is documented by the rapid appearance of
a great variety of metazoan bauplans during the Paleozoic which cannot be
satisfactorily explained by a simple addition of microevolutionary events to
macroevolutionary effects; that it is a rare event is documented by the fact that
no new metazoan phyla have originated since the Paleozoic (Valentine & Erwin,
1987). Erwin & Valentine (1984: 5483; see also Arthur, 1988: 83) suggest that
there were less canalized developmental systems and more empty ecospace
during early phases of metazoan evolution.
EVOLUTION: CONTINUITY OF CHANGE
Science is about causes and effects. Regular phenomena justify the hypothesis
of underlying causality; hypothetical knowledge of causality permits (under the
assumption of uniformity in nature) prediction of regular phenomena. A
(metatheoretical) prerequisite for successful prediction is continuity of causes.
Discontinuity of causes is not the object of rational investigation.
Microevolutionary theory, postulating gradual accumulation of numerous
small changes under the guiding action of natural selection, is built on the
principle of continuity. Macroevolutionary change, effected through ontogenetic
deviation, postulates discontinuity of appearance but not of causes. The cause
leading to a bifurcation in developmental pathways may be continuous (as in the
threshold model, documented for the development of the eye in cave-fishes of the
genus Astyanax by Wilkens: 1988), but the resulting morphology may be
discontinuous.
As ontogenetic divergence provides a cause for discontinuous phenotypic
change along the axis of the cladogram, it can be stated (in Linnaean terms) that
macroevolution proceeds from the creation of phyla to classes, to orders, etc.
Such wording, based on the (debatable) convention that a Linnaean category be
assigned to each node in the cladogram, has created semantic difficulties,
culminating in the outright denial of macroevolutionary change (Willmann,
1988). The misunderstanding, specifically addressed by Lovtrup ( 1979), has its
roots in failure to distinguish clearly between pattern and process. Systematics
deals with patterns of order in nature, evolutionary change is the result of a
causal process. Another important distinction is between the cladogram,
indicating the genealogical hierarchy of monophyletic taxa, and Linnaean
classification, assigning taxa to conventional categories. If the pattern of order in
nature finds its causal explanation in the process of evolution, then the axis of the
cladogram indicates the palingenetic direction of phylogenetic change
(mammals arise after the origin of amniotes, amniotes arise after the origin of
tetrapods, tetrapods arise after the origin of gnathostomes; gnathostomes arise
after the origin of vertebrates, etc.). The causal explanation of the cladogram
adds the notion of descent with modification, that is explanation transforms the
cladogram from a time-independent system of logical subordination to a
temporalized representation of the process of phylogeny. The cladogram
becomes an abstract version of the phylogenetic tree (X-tree: Patterson, 1983),
which grows in the course of evolution. If ontogenetic deviation induces a
bifurcation in the growing tree, this happens in a representative of a terminal
taxon, that is in an evolving population. As stated in the previous section,
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ontogeny creates phylogeny only if changes of constructional rules come to
characterize an evolving population.
With continued evolution, a dichotomy will appear to be inserted lower down
on the ever growing axis of the temporalized cladogram. T h e discontinuity of
appearance caused by ontogenetic deviation will become the reason for the (a
posteriori) assignment of a Linnaean category to this node in the tree. T h e earlier
the ontogenetic deviation, the greater will be the morphological distance to the
sister taxon, and the higher is the categorical rank assigned to this level of
bifurcation. Convention creates the illusion that a phylum gives rise to a class,
when a phylogenetic viewpoint requires that a representative of a more inclusive
taxon, member of a terminal taxon in the distant geological past, has given rise
to a representative of a less inclusive, subordinated taxon. Surely, a ‘vertebrate’
cannot be the actual ancestor of a ‘tetrapod’--but the ancestral tetrapod must
have been a vertebrate animal (Schoch, 1986)! T h e unit of the genealogical
hierarchy is the monophyletic taxon. The unit of the process of evolution on the
other hand is the reproductive community, or the evolving lineage (in the case of
asexual organisms). As stated in the introduction, organisms as members of
evolving populations represent taxa of the genealogical hierarchy (by shared
homologies), they do not constitute them.
LOGICAL SUBORDINAI‘ION VERSUS HISTORICAL CONTINGENCY
Pattern reconstruction is based on the logical subordination of homologies
(Rieppel, 1988a). Homologies do not represent parts of material and genetic
identity between individual organisms; they represent an abstract (Nelson, 1970)
relation of (topographic) similarity of relative invariance, characterizing a static
hierarchy of types (Rieppel, 1985). T h e hierarchy of homologies, and with it the
hierarchy of types, must be abstracted from the dynamic, ever evolving (in both
senses of the word) individual organism (Alberch, 1985; De Queiroz, 1985).
Homologies stand to the hierarchy of types in the relation of the more general to
the less general. The hierarchy of types thus corresponds to a subordinate
hierarchy of logical classes. Only if we have evidence for order in nature,
expressed in a classification based on invariant characters, is it possible to ask for
the underlying causality. Only if we have identified discontinuous groups as
potential ancestors and descendants is it possible to bridge the discontinuity by a
hypothesis of continuous transformation. Every hypothesis of descent requires a
hypothesis of relationship based on recorded similarity (homology).
The regularity of character distribution, depicted by the time-independent
cladogram, finds its causal explanation in the theory of evolution. Pattern
reconstruction provides phylogeny with a direction; the theory of evolution
provides a causal explanation for order in nature. However, the theory of
evolution addresses a historically contingent process, not the logical
subordination of characters. Explained by the theory of evolution, types become
monophyletic taxa bestowed with historical reality, homologies become evidence
for common descent (Rieppel, 1988a). T h e problem is to bridge the gap between
logical subordination in pattern reconstruction and historical contingency in the
evolutionary process.
The problem seems to disappear if monophyletic taxa are granted the
ontological status of individuals (see Patterson, 1988, for a discussion), integrated
ONTOGENY, SYSTEMAIICS AND PHYLOGENY
189
units of evolution at high hierarchical levels with organisms as their parts.
Organisms would constitute monophyletic taxa. Consider the individual organism
as paradigma for individuality: it shows that organs stand to the organism in the
relation of the part to the whole. Homologies, however, stand to the hierarchy of
types in the relation of the general (more general) to the specialized (less
general). The gulf between logical subordination and historical contingency does
not appear to be bridged. Furthermore, evolution occurs in terminal taxa, that is
in reproductive communities (or evolving lineages in the case of asexual
organisms), not in inclusive taxa of higher rank.
The problems might be solved if it is admitted that organisms, participants in
a reproductive community (in an evolving lineage) represent rather than constitute
monophyletic taxa: they represent these taxa by virtue of the homologies which
they share. The statement that an ancestral vertebrate has given rise to a
tetrapod animal would appear quite reasonable if an answer can be found as to
how the Vertebrata are represented in an individual organism which, embedded
in its reproductive community, gives rise to another individual organism
representing the Tetrapoda. If the type were an idealistic concept, the conclusion
would be that organisms represent taxa in a purely idealistic sense: homologies
would be nothing more but mental abstractions. If the type were taken as real,
this would imply material and genetic identity of homologies. A more promising
approach is to view the type as a logical concept, and to ask how homology, an
abstract relation of topographical similarity, is represented in the organism. The
answer is that similarity (homology) results from ontogenetic rules of
construction. The epigenetic process of development is one of unfolding, of
growth, compartmentalization and differentiation. Organs or their rudiments
develop one from the other, a process which determines relations of topological
similarity. Rules of construction are the material base for the relation of
homology. The relation of homology is an abstract concept, providing access to
the hierarchy of types and with it to the hierarchy of taxa. These taxa are
represented in individual organisms by shared rules of construction. If the rules
of construction of a limb bud change, a vertebrate can give rise to a tetrapod.
Ontogeny has created phylogeny.
ACKNOWLEDGEMENTS
I thank Drs W. Arthur, S. Blackmore, T. Burgin, R. D. Martin, G. Nelson
and C. Patterson, who all read an earlier draft of this paper, for offering many
helpful criticisms and suggestions.
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