HAECKEL AND THE VERTEBRATE ARCHETYPE

A recent paper by Michael Richardson and his colleagues
(1997) has corrected a major misunderstanding among developmental biologists and
evolutionary biologists which can be traced back to Ernst Haeckel. Haeckel
(1874) had claimed that members of all vertebrate classes pass through an
identical evolutionarily conserved "phylotypic" stage. Until this new paper
appeared, it was assumed that Haeckel was correct and that there was a
particular stage of development that was identical to all vertebrates. Only
later in development would specific differences appear. Interestingly, there was
some discussion as to what exactly this stage was (Richardson , 1995). This
conserved stage was sometimes considered the neurula stage (Wolpert, 1991), the
"pharyngula" stage (characterized by the branchial arches; Ballard, 1981), the
tailbud stage (Slack et al., 1993), or the stages between those of headfold and
tailbud (Duboule, 1994). Figure 1 shows one of Haeckel's representation of
vertebrate embryology. The top row shows that all the vertebrate embryos (no
matter what path they took to reach this stage) have a stage where they appear
almost identical.

FIGURE 1. Haeckel's 1874 version of vertebrate embryonic development. The
top row shows an early stage common to all groups, the second row shows a middle
stage of development, and the bottom row shows a late stage embryo. Groups from
left to right are: fish, salamander, turtle, chicken, pig, cow, rabbit, and
human. (Adapted from Gilbert, 1997.)

But Haeckel's drawings are wrong. Photographing actual
embryos at these stages, Richardson and colleagues show that Haeckel's drawings
are oversimplified to the point of obscuring important differences between
classes of vertebrates. The Richardson et al. paper does not dispute that there
is a highly conserved embryonic stage among the vertebrate classes. Indeed, at
the late tailbud stage, vertebrate embryos of most all classes possess "somites,
neural tube, optic anlagen, notochord, and pharyngeal pouches." However, these
authors do criticise the notion that this stage is nearly identical in all
species and that differences beteen the classes can be resolved only after
subsequent development. Rather, they discover significant differences between
groups. Size is one distinctive marker. The scorpion fish embryo is 700 microns
long at the tailbud stage, while the mudpuppy salamander measures some 9
millimeters. Heterochrony is another problem. In some species of direct
developing frogs, and in monotreme mammals, limb buds are already present at the
tailbud stage, whereas in other species, these are not seen until significantly
later. Birds are characterized by their prominent mesencephalon. Whereas most
amniote embryos have a heart by this stage, the zebrafish does not. (Teleosts
such as zebrafish are even the exception to the rule mentioned above. They
eventually possess a notochord, somites, pharyngeal pouches, etc., but they do
not have the pharyngeal pouches until after the tailbud stage). Some of
these differences are depicted in Figures 2 and 3.

FIGURE 2. Selected embryos shown at the "phylotypic" stage. (A) Sea
lamprey (jawless cyclostome fish, Petroyzon) with nearly identical pharyngeal
pouches and heart that is caudal to the pharynx; (B) electric ray (cartilagenous
chondrichthes fish, Torpedo) with nearly identical pharyngeal pouches and
a pronounced hindbrain/midbrain flexure; (C) sterlet (bony Osteichthyes fish,
Acipenser) where the pharyngeal pouches have not yet formed; (D) frog
(direct -developing anuran amphibian Eleutherodactylus) which has
hindlimb buds at the tailbud stage and only two pairs of aortic arches; (E) pond
turtle (chelonian reptile, Emys) where there is no craniocaudal rotation
(torsion) to the embryo, whereas the same stage of the chick (avian) embryo (F)
shows pronounced torsion; (G) brush-tailed possum (marsupial mammal,
Trichosurus) where there is (in contrast to the cartilagenous fishes)
large maxillary and mandibular processes. In ther cat (eutherian mammal,
Felis) there is a similar size difference between the anterior and
posterior pouches, although their appearance differs from that of the
marsupials. (After Richardson, 1997.)

FIGURE 3.
Photographs of a fish, amphibian, reptile, mammal, and bird embryo at the
"phylotypic" stage. Photographs courtesy of M. Richardson.

Interestingly, this knowledge appears to be "old hat"
among German biologists. Haeckel's drawings were not trusted (see Goldschmidt,
1956), and Haeckel was accused of scientific fraud by a university court in
Jena, where he worked and by other embryologists, as well (see Hamblin, 1997;
Richardson et al., 1997b). Yet, the idea that early vertebrate embryos are
essentially identical has survived. I think there were two reasons for the
survival. First, Haeckels' illustration was reproduced in Romanes'
(1901) Darwin and After Darwin. From here, the illustration entered Anglophone biology,
"sanitized" from Haeckel. Second, the picture can be used (as it has been in
several developmental biology books, including my own [Gilbert, 1997, p. 254])
to illustrate von Baer's principles rather than Haeckel's biogenetic law. K. E.
von Baer had noted that the general features of a large group of animals appear
earlier in the embryo than do the specialized features. Indeed, von Baer
wrote:

"The embryo of the mammal, bird, lizard, and snake and
probably also the turtle, are in their early stages so uncommonly similar to
one another that one can distinguish them only according to their size. I
posess two small embryos in spirits of wine, embryos whose name I neglected to
note down, and I am now in no position to determine the classes to which they
belong. They could be lizards, small birds, or even very young
mammals."

Darwin quoted this (it was Thomas Huxley's translation)
although he misattributed the story to Agassiz rather than to von Baer (see
Richards, 1992 for an analysis). The notion of development proposed by von Baer
is still used as a general approximation of certain developmental phenomena.
Certainly, the early embryos of certain vertebrate classes are very similar (for
instance, the chick and mouse twenty-somite embryos), and the processes of
somitogenesis, limb formation, axis generation, etc. are probably conserved
throughout the vertebrate groups).

Similarities and differences

What the Richardson et al. paper tells us is that we have
to be attentive to the differences as well as to the similarities. A bird embryo
is not the same as a mammalian embryo. We should not assume identity, even at a
stage where all vertebrate embryos seem to pass. The Richardson et al. paper can
be read as a critique of the recent priority of similarities over
differences.

The concept of homology enables one to celebrate the
differences or the similarities between two structures. Whether one emphasizes
the similarities between our forelimb and a bird's wing or the differences
between them depends on what you are describing. Comparative anatomy--with its
Aristotelian and Cuverian interest in relating structure to function--usually
emphasizes the differences. Morphology--with its Platonic and Geoffroyan
interest in the underlying unities of structure--usually focuses on the
similarities.

As Joseph Needham noted, embryology has swung between
these two poles during different stages of its morphogenesis. In the late 1800s,
the morphological tradition prevailed, and the similarities between
developmental stages in different organisms constituted some of the best
evidence for classification (see Nyhart, 1995; Bowler, 1996). Thus, the
discovery of the Nauplius stage of the barnacle showed that it was a modified
crustacean, and the notochord-containing tadpole of the tunicate demonstrated
its affinities with the chordates. However, after the 1920s, embryology was no
longer a major support for evolutionary biology, and the comparative anatomy
tradition came to predominate. Until the 1980s, embryology was extremely
descriptive. Each organ was seen to develop differently from any other organ,
and each species was seen to develop differently from any other species. Indeed,
embryology was defined (by one of its practitioners, E. G. Conklin) as a
"lawless science" because generalities could not be made from the observations
of animal development. When embryology underwent its anagenic transition to
become developmental biology, the similarities among organisms were again
emphasized. The similarities were now posited on the molecular rather than the
morphological or cell lineage level. The 1990s has seen a remarkable celebration
of the similarity of molecular processes throughout the animal kingdom.
Homologous genes abound (the Hox genes, fringe , tinman, and Pax6 being seen to specify the anterior-posterior axis, the limb, the
heart, and the eye, respectively, of organisms as diverse as insects and flies).
Even signalling pathways are seen as being homologous both within a developing
organism and between organisms. Thus, the neural tube in vertebrates and insects
are seen as being formed through the same interactions of the "same" proteins,
even though one neural tube is dorsal and the other ventral. The Richardson et
al paper reminds us that despite these similarities, differences are also
important, especially if one is thinking in terms of the relationships between
development and evolution.

The Richardson et al paper is a also plea for comparative
anatomy and less reliance on "model systems." This critique of model systems
echoes a recent plea from Leo Buss, Rudy Raff, Jessica Bolker, and James Hanken
who observe that model systems converge on several factors (see Bolker and Raff,
1997; Hanken, 1993): they all can develop in the laboratory and are thus
relatively free of environmental factors effecting their morphogenesis; they are
all organisms which segregate their germ line extremely early; they develop
rapidly, are small as adults, and they have short generation times.

The Richardson et al. paper does a great service to
developmental biology. As they mention, there is renewed interest in
evolutionary developmental biology, and in view of the conservation of
developmental mechanisms, we need to re-examine the extent of variation in
vertebrate embryos. There is more variation than had been assumed, and these
variations foreshadow important differences in the adult bodies. This is
important because we need to know how conservative the early embryonic stages
actually are.

References:

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maps of vertebrates. Amer. Zool. 21: 391 - 399.

Bolker, J. A. and Raff, R. A. 1997. J. N. I. H. Res. 9: 35 -
39.

Bowler, P. J. 1996. Life's
Splendid Drama. U. of Chicago Press,
Chicago.

Duboule. D. 1994. Temporal colinearity and the
phylogenetic progression: a basis for the stability of the vertebrate Bauplan
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142.

Gilbert, S. F. 1997. Developmental Biology. Fifth ed.
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Gould, S. J. 1977. Ontogeny
and Phylogeny. Belknap Press, Cambridge,
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Richardson, M. K. 1995. Heterochrony and the phylotypic
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Richardson, M. K., Hanken, J., Gooneratne, M. J. Pieau,
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Richardson, M. K., Hanken, J., Selwood, L., Wright, G.
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Romanes, G. J. 1901. Darwin
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Slack, J. M. W., Holland, P. W. H., and Graham, C. F.
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Wolpert, L. 1991. The
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