Preface
"If facts of the old kind will not help us, let us seek facts of a new kind." (Batesotr, W. 1894. 'Materials for the Study of
Variation' Preface page vi)
Relationships between the processes of development and
evolution were central to biological thought in the latter half
of the nineteenth century. Accordingly, comparative morphology and embryology were at the pinnacle of the biological
sciences. By the turn of the century, though, comparative morphology had been pushed to its limits, and perhaps beyond.
Frustration set in. William Bateson described it well. Trained
in the old school, he had been investigating what light the
anatomy and development of acorn worms might throw on the
origin of the chordates. Reflecting on the outcome of this study,
he wrote "From the same facts, opposite conclusions are
drawn; facts of the same kind will take us no further. Need we
waste more effort in these vain and sophistical disputes"
(Bateson, 1894). From then on, the old comparative biology
was pushed to the sidelines. Any relationship between development and evolution remained peripheral to the major
triumphs of twentieth century biology - to the emergence of
molecular cell biology on the one hand, and to the 'modern
synthesis' in evolutionary biology, with all its subsequent ramifications and revisions, on the other.
Yet even Wilhelm Roux, champion of the experimental
approach and polemicist against the old biology, envisaged a
time when his 'developmental mechanics' might encompass
phylogenetic studies. He recognised that this endeavour would
have to be adjourned until "Entwickelungsmechanik has been
developed so far that we have gained deep insights, not only
into the mechanisms forming the individual from the germ
plasm, but also into the mechanisms that vary the germ plasm"
(Roux, 1892; by germ plasm Roux meant something close to
our 'genome'). Would Roux agree that his criteria are, at least
in some measure, fulfilled? We believe he would. This volume
charts some of the routes that are bringing new facts to bear
on these old problems.
Underpinning all discussion is the need for a secure phylogenetic framework. Unlike Bateson, we do not seek to establish
relationships by the comparative analysis of development. We
have reason to hope that, as the database for molecular phylogenetic analysis expands, the domain where phylogeny equals
mythology will shrink. We believe this, not because molecular
data are intrinsically 'better' than morphological data, but
simply because the extent of the potenti al database is so great.
Already, the systematic analysis of a very few molecular
species, notably large and small subunit ribosomal RNA, has
confirmed that these molecules conserve phylogenetic information that is useful at many taxonomic levels. However, in
their survey of thes e data, Philippe et al. (pp . 15-25) point out
just how extensive sequence data must be, even under ideal
conditions, to resolve relationships within explosive radiation
events. It will be a long while before molecular taxonomy can
approach the temporal resolution of a good stratigraphic series.
Molecular phylogenetics may resolve the relationships
between taxa - but they can never tell us what sort of beast a
stem group species was. Hypothetical archetypes are no substitute for a few good fossils - a point emphasised by Conway-
Morris (pp. 1-13), and by Coates (pp. 169-180) in his reconsiderations of tetrapod origins. Palaeontology may not often
give us a developmental series (uvenile trilobites notwithstanding) but it can constrain speculation about the end
products of ancestral developmental processes - and provide
clues to ancestral states that are no longer evident in extant
species.
There would be no need of such clues if ontogeny did recapitulate ancestral developmental stages faithfully, but even
Haeckel admitted that it does not. Modern species reflect their
phylogenetic history selectively, and even then, the reflections
are strangely distorted. In the context of vertebrate gastrulation, De Robertis et al. (pp. III -I24) show how molecular
probes can reveal the unity of pattern and process beneath the
distortions of morphology. Haeckel would be delighted.
One thing that has not been over-written or replaced during
the diversification of the metazoa is the basic tool-kit of development. Since the 1940s, we have been used to the idea that
metabolic enzymes and pathways are universal but only
recently has it become clear how extensively conserved are the
molecules that regulate development: transcription factors,
receptors and extracellular matrix molecules. As little as ten
years 4go, the idea of searching for insect homologues of such
'vertebtate' molecules as fibronectin or Myc seemed almost an
irrelevance. (All credit to those few who persevered). Now the
very idea of 'vertebrate' molecules seems a nonsense, and the
relevance of functional studies in tractable model systems is
established beyond dispute. Chothia (pp. 27 -33) utilises data
accumulating in the protein and nucleic databases to survey
this metazoan tool-kit. He concludes that life uses rather few
of the possible protein structures to generate its diversity - the
great majority of proteins may be referred to perhaps no more
than a thousand structural families.
Within a few years, genome projects will provide a complete
inventory
of
these proteins
for a usefully
diverse set of
reference species. Such sequences alone will be no sure guide
to structure or function, but, without doubt, one striking lesson
from these inventories will be the extent to which we are
indeed one flesh, mite and man and lowly woffn. Yes, there
will be new genes - mostly made by recombining old domains
(Engel et a1., pp. 35-42); duplication of old genes will be rife
(Holland et al.,pp. I25-I33; Ruddle et al.,pp. 155-161); some
old molecules will be seen to have acquired wholly new
functions (the lens crystallins are a good case in point (Piatogorsky and Wistow, 1989)). Even so, as we see tt at present,
the history of life since the Cambrian has been dominated by
the elaboration of regulatory mechanisms that exploit a
common set of genes.
How have these regulatory mechanisms evolved? We cannot
yet see 'the big picture'. Are the same cell types specified by
homologous regulatory molecules in different phyla? How
conserved is the molecular basis for induction, lateral inhibition or neurogenesis? Several papers in this volume provide
glimpses of conserved developmental mechanisms - the
hedgehog and TGFB family signalling molecules used in
analogous ways in vertebrates and invertebrates (Fietz et a1.,
pp. 43-51; Hogan et a1., pp. 53-60); transcription factors that
seem to specify the same organs in vertebrates and invertebrates - heart, eyes, - despite the most diverse morphology
(Manak and Scott, pp. 6l-ll). Are we seeing homologous
mechanisms? If so, at what level does the homology lie? Will
downstream and upstream regulatory networks be conserved,
or are there constrained steps in cellular differentiation
(cytotypic stages?) just as there are during embryogenesis,
above and below which regulatory networks are more fluid?
There is a new world of evolutionary biology here.
The 'new facts' of molecular biology pertain not just to
molecular phylogeny and cell biology, but to the questions of
organismal form - Bauplan; zootype. The Hox genes provide
the outstanding example. The linear deployment of Hox genes
along the anteroposterior axis of nematodes, insects and
chordates provides a strong argument to establish the primitive
homology of this axis in all bilateria (Ruddle et a1., pp. 15516l; Manak and Scott, pp. 6l-17). The expression of the same
genes in echinoderms, in molluscs, even in Cnidaria, now
provides a criterion to assess how the body axes of these groups
relate to those of other triploblasts. Analogous data may yet
place Geoffrey St Hilaire's classic conjecture (1822) concerning the relation of vertebrate and insect dorsoventral axes in
the realm of testable hypothesis.
More immediately, the same Hox genes are being used as
molecular labels to indicate homology between specific body
regions - between insects and crustaceans (Akam et al., pp.
209-215); between cephalochordates and vertebrates (Holland
et al. , 1992), even between phyla (Morgan and Tabin, pp. 181186). It remains to be seen whether this 'internal representation' of the genes will reveal relationships where comparative
morphology has failed. Whether or not it succeeds, the com-
parison must provide some indication of the mechanisms
underlying morphological change, for the Hox genes and their
like are not just passive labels, but tools that sculpt morphology.
This direct link with mechanism is perhaps the
most
important characteristic of the 'new facts'. In the past, evolu-
tionary change has been analysed by comparing, not the
of development, but the static forms generated by
processes
it is becoming possible to
compare the processes themselves, at the cellular level (Wray
and Bely, pp.97-106; Sommer et al.,pp. 85-95) as well as the
these processes. Increasingly,
molecular (Patel, pp. 20I-207; Tautz et aI., pp. 193-199;
Morgan and Tabin, pp. 181-186). Only when we understand
the process of development can we begin to map the relationship between genetic change and morphological effect. It is a
commonplace of developmental genetics that minimal genetic
change can lead to the most dramatic morphological effect (a
single base substitution in the bicoid gene of Drosophila can
reverse the axes and symmetry of the embryo (Frohnhofer and
Niisslein-Volhard, 1986; Struhl et al., 1989)). What we do not
yet know is the genetic complexity of observed transitions in
evolutionary history of heterochronic changes in rates of
growth, of duplications or suppression in segmentation, or
inventions of morphological novelty. Papers in this volume
provide glimpses of understanding. How did the complex and
beautiful patterns on the wings of a butterfly arise - and how
have evolutionary pressures moulded them for immediate
adaptation? Nijhout (pp. 225-233) sketches, in a formal model,
the outlines of a common mechanism that can generate the
apparent complexity; Carroll (pp. 2Il -223) raises the hope that
genes we already know, identified in Drosophila, may provide
the material basis for part of this complexity.
We do not fully understand butterfly wings, insect segments
or vertebrate limbs. Far from it. But we can now pose questions
that address the diversity of life in geological time and species
space, with some hope of finding answers that are neither
trivial nor obvious: answers that go some way towards illuminating that obscure sector on the Venn diagram where genetics,
evolution and development intersect.
M. A., P. H., G. W., August 1994
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