Abstracts
Abstracts
Alec L. Panchen
Department of Marine Sciences, University of Newcastle upon Tyne, NE1 7RU,
UK
The concept of homology is traceable
to Aristotle, but Belon’s comparison in 1555 of a human skeleton with that of
a bird expressed it overtly. Before the late 18th century, the dominant view of
the pattern of organisms was the scala
naturae—even Linnaeus with his divergent hierarchical classification did
not necessarily see the resulting taxonomic pattern as a natural phenomenon. The
divergent hierarchy, rather than the acceptance of phylogeny, was the necessary
spur to discussion of homology and the concept of analogy. Lamarck, despite his
proposal of evolution, attributed homology to his escalator naturae and analogy to convergent acquired characters.
Significantly, it was the concept of serial homology that emerged at the end of
the 18th century, although comparison between organisms became popular soon
after, and was boosted by the famous Cuvier/Geoffroy Saint-Hilaire debate of the
1830s. The concepts of homology and analogy were well understood by the pre- (or
anti-) evolutionary comparative anatomists before the general acceptance of
phylogeny, and they were defined by Owen in 1843. The acceptance of evolution
led to the idea that homology should be defined by common ancestry, and to the
confusion between definition and explanation. The term ‘homoplasy’,
introduced by Lankester in 1870, also arose from a phylogenetic explanation of
homology.
Return to contents
©1999 The Novartis Foundation
Homoplasy,
homology and the problem of ‘sameness’ in biology
David B. Wake
Museum
of Vertebrate Zoology, University of California, Berkeley, CA 94720-3160, USA
The reality of evolution requires
some concept of ‘sameness’. That which evolves changes its state to some
degree, however minute or grand, although parts remain ‘the same’. Yet
homology, our word for sameness, while universal in the sense of being
necessarily true, can only ever be partial with respect to features that change.
Determining what is equivalent to what among taxa, and from what something has
evolved, remain real problems, but the word homology is not helpful in these
problematic contexts. Hennig saw this clearly when he coined new terms with
technical meanings for phylogenetic studies. Analysis in phylogenetic
systematics remains contentious and relatively subjective, especially as new
information accumulates or as one changes one's mind about characters. This
pragmatic decision making should not be called homology assessment. Homology as
a concept anticipated evolution. Homology dates to pre-evolutionary times and
represents late 18th and early 19th century idealism. Our attempts to recycle
words in science leads to difficulty, and we should eschew giving precise modern
definitions to terms that originally arose in entirely different contexts.
Rather than continue to refine our homology concept we should focus on issues
that have high relevance to modern evolutionary biology, in particular homoplasy—derived
similarity—whose biological bases require elucidation.
Return to contents
©1999 The Novartis Foundation
Robert
L. Carroll
Redpath
Museum, McGill University, 859 Sherbrooke St. West, Montreal, Canada H3A 2K6
A stringent definition of
homology is necessary to establish phylogenetic relationships among Paleozoic
amphibians. Many derived characters exhibited by divergent clades of
Carboniferous lepospondyls resemble those achieved convergently among Cenozoic
squamates that have elongate bodies and reduced limbs, and by lineages of modern
amphibians that have undergone miniaturization. Incongruent character
distribution, poorly resolved cladograms and functionally improbable character
transformations determined by phylogenetic analysis suggest that convergence was
also common among Paleozoic amphibians with a skull length under 3#60cm,
including lepospondyls, early amniotes and the putative ancestors of modern
amphibians. For this reason, it is injudicious to equate apparent synapomorphy
(perceived common presence of a particular derived character in two putative
sister-taxa) with strict homology of phylogenetic origin. Identification of
homology by the similarity of structure, anatomical position and pattern of
development is insufficient to establish the synapomorphy of bone and limb loss
or precocial ossification of vertebral centra, which are common among small
Paleozoic amphibians. The only way in which synapomorphies can be established
definitively is through the discovery and recognition of the trait in question
in basal members of each of the clades under study, and in their immediate
common ancestors.
Return to contents
©1999 The Novartis Foundation
Gerd B. Müller and Stuart A. Newman*
Department of Anatomy, University of Vienna, Währingerstrasse 13, A-1090
Wien, Konrad Lorenz Institute for Evolution and Cognition Research,
Adolf-Lorenz-Gasse 2, A-3422 Altenberg, Austria, *and Department of Cell Biology
and Anatomy, New York Medical College, Valhalla, New York 10595, USA
The homology concept harbours implicit assumptions about the evolution of
morphological organization. Homologues are natural units in the construction of
organismal body plans. Their origin and maintenance should represent a key
element of a comprehensive theory of morphological evolution. Therefore, it is
necessary to understand the causation of homology and to investigate the
mechanisms underlying its origination. The study of this issue cannot be limited
to the molecular level, because there appears to exist no strict correspondence
between genetic and morphological evolution. It is argued that the establishment
of homology follows three distinct (if overlapping) steps: (a) the generation of
morphological building elements; (b) the integration of new elements into a body
plan; and (c) the autonomization of integrated construction units as
lineage-specific homologues of phenotypic evolution. In contrast with
traditional views, it is proposed that the mechanistic basis for steps (a) and
(b) is largely epigenetic, i.e. a consequence of the inherent propensities of
developmental systems under changing conditions. Step (c) transcends the
proximate mechanisms underlying the establishment of homologues and makes them
independent attractors of morphological organization at the phenotypic level.
Return to contents
©1999 The Novartis Foundation
Frietson
Galis
Institute for Evolutionary and Ecological
Sciences, University of Leiden, PO Box 9516, 230ORA Leiden, The Netherlands
Research
on expression patterns of Hox genes
has revealed a surprisingly high conservation among vertebrates. In agreement
with this conservation, a correlation has been found between the anterior limits
of expression areas of certain Hox
genes and the borders between morphological regions of the vertebral axis. These
similarities are striking and important, but also counterintuitive, unless there
are strong selection pressures to protect this conservatism. It is important to
identify the selective forces that maintain these conservative networks. These
selective forces can be due to pleiotropy or to internal selection. Discussed
are the selective factors that are involved in the evolutionary constraint on
the number of cervical vertebral numbers in mammals. Factors involved are due to
internal selection and involve susceptibility to cancer, stillbirths and
neuronal problems. It is intriguing how similar genetic networks can lead to
fundamentally different animals. Clearly the same genes are used for different
purposes. It is therefore important to try find these differences. The search
for homology between organisms, and the enthusiasm about similarities that come
with it, at times impedes the discovery of such differences. I have searched the
literature for differences within vertebrates in the functioning and expression
patterns of Hox genes during the development of the vertebral axis. The ensuing
implications for homology of structures and genes are discussed. The vertebral
column is a promising model system for the evaluation of the relationship
between homologous Hox genes and
homologous structures because of the large conservation of Hox gene expression patterns along the anterior axis. However,
extensive remodelling of the vertebrate column indicates that important changes
in the genetic basis must have taken place. A survey of the literature indicates
that the correlation between Hox gene
expression areas and vertebral regions is not such that one can predict the
borders between vertebral regions on the basis of Hox
gene expression patterns. The involvement of Hox
genes in the development of identity of vertebrae is complex and the
problems regarding the value of gene expression patterns for the determination
of anatomical homology are discussed.
Return to contents
©1999 The Novartis Foundation
Developmental basis of limb homology in
urodeles: heterochronic evidence from the primitive hynobiid family
J. R. Hinchliffe and E. I. Vorobyeva*
Institute of Biological Sciences, University of Wales, Aberystwyth, Wales,
SY23 3DA, UK, and *Institute of Ecology and Evolution, 33 Leninsky Prospect,
Moscow 117071, Russia
The vertebrate limb is a classic
example of homology, long assumed to be underpinned by a developmental
‘bauplan’ of the type proposed in the Shubin/Alberch branching and
segmenting model. In the anuran/amniote pattern skeletogenesis proceeds in a
proximodistal direction with digits forming from the posterior to the anterior.
But in free-living larvae of ‘advanced’ urodeles, the pattern of
skeletogenesis is distinctly different with digits 1 and 2 and the basal commune
developing early, in an anterior/distal position. This different pattern is
cited as evidence for a diphyletic theory of tetrapod evolution. Reassessing
this problem, we analysed the pattern of early skeletogenesis of three genera (Salamandrella,
Ranodon, Onychodactylus)
of the ‘basal’ family of Hynobiids, using immunofluorescence to localize
chondroitin-6-SO4 in Salamandrella.
Here the developmental sequence was more proximodistal (intermedium preceding
basal commune; early formation of the digital arch). This pattern, also found in
direct developing urodeles such as Bolitoglossa
subpalmata, resembled that in anurans/amniotes. Uniquely amongst tetrapods,
urodeles use their developing limbs for locomotion. We attribute the unusual
pattern in ‘advanced’ urodeles to adaptive modification of the developing
limb. Differences in the pattern between ‘basic’ and ‘advanced’ urodeles
and between urodeles and anuran/amniotes are interpreted as heterochronic within
an overall single tetrapod developmental bauplan.
Return to contents
©1999 The Novartis Foundation
Larval homologies and radical
evolutionary changes in early development
Rudolf A. Raff
Indiana Molecular Biology Institute, and Department of Biology, Indiana
University, Bloomington, IN 47405, USA
Larval forms are highly conserved in evolution, and phylogeneticists have
used shared larval features to link disparate phyla. Despite long-term
conservation, early development has in some cases evolved radically. Analysis of
evolutionary change depends on identification of homologues, and this concept of
descent with modification applies to embryo cells and territories as well.
Difficulties arise because evolutionary changes in development can obscure
homologies. Even more difficult, threshold effects can yield changes in process
whereby apparently homologous features can arise from new precursors or
pathways. We have observed phenomena of this type in closely related sea urchins
that differ in developmental mode. A species developing via a complex feeding
larva and its congener, which develops directly have different embryonic cell
lineages and divergent patterns of early development, but converge on the adult
sea urchin body plan. Despite differences in embryonic developmental pathways,
conserved gene expression territories are evident, as are territories whose
homologies are in doubt. The highly derived development of the direct developer
evidently arises from an interplay of novel organization of the egg, loss of
expression of regulatory genes involved in production of feeding larval
features, and changes in site and timing of expression of a number of genes.
Return to contents
©1999 The Novartis Foundation
A research
programme for testing the biological homology concept
Günter P. Wagner
Department of Ecology and Evolutionary Biology,
Yale University, New Haven, CT 06520-8106, USA
The classical homology concept has served as a
heuristic principle for organizing the enormous wealth of information on
comparative anatomical patterns across a wide range of organisms. However, the
classical homology concept reaches its limit as knowledge of the evolutionary,
genetic and developmental processes that underlie these anatomical patterns
increases. The biological homology concept places the known anatomical patterns
into a mechanistic context and asserts that character identity is based on
common variational properties. In this chapter a research programme for testing
the biological homology concept that involves the following steps is outlined:
(1) identifying of two or more putative homologues in a clade; (2) determining
the phylogenetic distribution of the putative homologues; (3) describing the
intra- and interspecific variation patterns of each putative homologue; (4)
describing the development of each putative homologue, and determining if modes
of development and distribution of homologues are phylogenetically congruent;
and (5) providing and testing a model of how differences in modes of development
between putative homologues effect differences in variational tendencies. The
goal is to demonstrate a link between developmental and variational differences
of two homologues.
Return to contents
©1999 The Novartis Foundation
Homology and homoplasy: the retention of
genetic programmes
Axel Meyer
Department of Biology, University of
Konstanz, 78457 Konstanz, Germany
Homology describes the inevitable
evolutionary phenomenon that the similarity of structures among different
organisms is due to the commonality of their descent. This continuity of
information is maintained in evolutionary lineages in terms of genes and
developmental mechanisms and will retain ‘sameness’ and retard, funnel and
direct evolutionary diversification. Analogous ‘sameness’ is said to be due
to independent, convergent evolution, and also involves similarity of function;
the latter is not a necessary condition for structures to be identified as
homologous. Here, I suggest that the biological basis for these seemingly
disparate kinds of ‘sameness’ in evolution may in some, or even most,
instances not be all that different and may be based on the same principle—the
long evolutionary retention of genes, gene interactions and developmental
mechanisms. Evolution might recycle and re-recruit similar mechanisms repeatedly
during its course, and it often makes do with what is already available to it
rather than to newly evolve or reinvent many gene interactions and developmental
mechanisms repeatedly. Apparently there is no, or only a negligible, ‘genomic
cost’ or even a selective advantage to maintaining genes and developmental
mechanisms for long evolutionary periods of time, even if they are not
continuously used in all members along an evolutionary line. Therefore, the
biological basis of both homologous traits (those that are evolutionarily always
expressed) and homoplasious traits (those that are not always ‘on’, but are
‘re-awakened’ during evolution) might not be so different, and the
distinction between homology and some forms of homoplasy may be somewhat
artificial.
Return to contents
©1999 The Novartis Foundation
Homology in the nervous system: of
characters, embryology and levels of analysis
Georg F. Striedter
Department of Psychobiology and Center for the Neurobiology of Learning and
Memory, University of California at Irvine, Irvine, CA 92697, USA
The establishment of homologies is
critically dependent upon the process of character identification. Valid
characters must reliably appear in many individuals and be delimitable from
other characters. They are not defined by any essential attributes, but rather
by the formation of distinct clusters in a multidimensional morphospace.
Features in two or more species can be considered possible homologues only if
they are identifiable as the same character, for it would be nonsensical to
homologize them as different characters. In order to confirm that a character is
indeed homologous between species, one must examine its phylogenetic
distribution to determine that it is unlikely to have evolved several times
independently in the taxa being compared. This method of homologue
identification can be applied to embryonic as well as adult characters and to
characters at various levels of organization, including cell types and cellular
aggregates. Difficulties arise, however, when one attempts to link the homology
of adult characters to that of their embryonic precursors, or the homology of
cellular aggregates to that of their constituent cell types. These efforts are
misguided because different characters cannot be homologized to each other (as
different characters). This perspective suggests that many neural characters may
lack homologues, and therefore be truly novel, in other taxa.
Return to contents
©1999 The Novartis Foundation
Natural history and behavioural homology
Harry W. Greene
Museum of Vertebrate Zoology and Department of Integrative Biology,
University of California, Berkeley, CA 94720-3101, USA
Although similarities and differences among animals have long inspired
ethologists, three misconceptions haunt the literature on behavioural evolution:
the absence of ‘ethofossils’ seriously hampers detection of behavioural
homology; behaviour is more variable and subject to experiential modification
than morphology; and behaviour is especially subject to convergence. As a
backdrop to address these issues, I briefly survey parental care by amniotes and
antipredator mechanisms in non-avian reptiles. Although those behaviours remain
inadequately sampled taxonomically, they clearly vary at several cladistic
levels; they are conservative across some major groups, innovative within
subclades, and exhibit apparent homoplasy among and within groups. These
behavioural examples also illustrate contextual influences on the expression of
traits, as well as how behavioural context can shape other aspects of
development. Enhanced understanding of behavioural evolution will follow from
greater emphasis on how developmental context, including behaviour itself,
shapes phenotypes; from integration of data for fossil and recent organisms; and
from much denser ethological sampling among taxa. Phylogenetic analyses of
behavioural similarity should in turn provide exciting insights into the
evolutionary roles of behavioural shifts and constraints, as well as inform our
aesthetic appreciation for the richness of nature.
Return to contents
©1999 The Novartis Foundation
Evolutionary
dissociations between homologous genes and homologous structures
Gregory A. Wray
Department
of Ecology and Evolution, State University of New York, Stony Brook, NY
11794-5425, USA
Phenotype is encoded in the genome in
an indirect manner: each morphological structure is the product of many
interacting genes, and most regulatory genes have several distinct developmental
roles and phenotypic consequences. The lack of a simple and consistent
relationship between homologous genes and structures has important implications
for understanding correlations between evolutionary changes at different levels
of biological organization. Data from a variety of organisms is beginning to
provide intriguing glimpses of the complex evolutionary relationship between
genotype and phenotype. Much attention has been devoted to remarkably conserved
relationships between homologous genes and structures. However, there is
increasing evidence that several kinds of evolutionary dissociations can evolve
between genotype and phenotype, some of which are quite unexpected. The
existence of these dissocations limits the degree to which it is possible make
inferences about the homology of structures based solely on the expression of
homologous genes.
Return to contents
©1999 The Novartis Foundation
Establishing homology criteria for
regulatory gene networks: prospects and challenges
Ehab Abouheif
Department of Ecology and Evolution, State University of New York at Stony
Brook, Stony Brook, NY 11794-5245, USA
One of the most remarkable
discoveries to emerge from the field of developmental genetics is the
observation that many regulatory genes and segments of their interactive
networks (pathways) appear to have been conserved in several metazoan phyla.
Determining whether these conserved regulatory networks are homologous, i.e.
derived from an equivalent network in the most recent common ancestor, is
critical to understanding comparisons between model system studies, and the
evolution of metazoan body plans. To this end, I outline some of the
evolutionary properties of regulatory networks, and propose both similarity and
phylogenetic criteria that can be used to test the hypothesis that two
regulatory networks are homologous. Furthermore, I propose that genetic networks
can be treated as a distinct level of biological organization, and can be
analysed together with other hierarchical levels, such as genes, embryonic
origins and morphological structures, in a comparative framework. Examples from
the literature, particularly the genetic regulatory networks involved in
patterning arthropod and vertebrate limbs, are examined using the proposed
criteria and hierarchical approach.
Return to contents
©1999 The Novartis Foundation
The effect of gene duplication on homology
Peter W. H. Holland
School of Animal and Microbial Sciences, The University of Reading,
Whiteknights, Reading RG6 6AJ, UK
Genes related by gene duplication
within an organism's evolutionary lineage are termed paralogues; genes related
by speciation are orthologues. It is generally agreed that orthologous genes
must be compared when using DNA sequences to reconstruct the evolutionary
history of organisms. There is an important exception: information from
paralogous genes can reveal the root position of a phylogenetic tree. The
duplicated rDNA genes of arrow worms provide an example. Gene duplication is
also relevant when comparing gene expression between taxa; for example, when
trying to identify homologous roles of genes. When gene duplication occurred
after lineage divergence, single orthologues no longer exist, and comparison is
complicated. This is a particular problem when comparing roles of vertebrate and
invertebrate genes. Amphioxus and ascidian genes can be useful in such
situations, since they diverged before extensive gene duplication in the
vertebrate lineage. Using Otx and Pax
as examples, I show how examination of amphioxus or ascidian genes reveals
patterns of gene divergence after duplication, assisting the identification of
homologous gene functions. Given the problems of comparing duplicated genes
between species, the time is ripe for the introduction of additional terminology
to elaborate on the concepts of paralogy and orthology.
Return to contents
©1999 The Novartis Foundation