The types of homology and their significance for evolutionary biology ...

J. evol.

Biol.

5: 13 24 (1992)

1010

061X;92,‘01013-12$ Tj 1992 BirkhHuser

The types of homology and their significance evolutionary biology and phylogenetics Gerhard

1.50+0.20/O Verlag. Base1

for

Haszprunar

tnstitut ,fiir Zoologie tier Unirersitiit A-6020 Innsbruck, Austria Kc~J, words:

Definition

of homology;

Innsbruck

TechnikerstruJe

25,

types of homology

Abstract This paper comments on recently revived discussion about the most adequate definition of homology. Homologues are considered as similarities of complex structures or patterns which are based on a continuity of biological information or instruction. Dependent on the level of comparison four types of homology are defined: ( 1) Iterative ( = serial = homonomy), (2) ontogenetic, (3) di- or polymorphic, and (4) supraspecific homology. The significance of all four types for evolutionary biology and phylogenetic analysis is outlined.

Introduction Scientists have recently been paying renewed attention to the homology question. This revival is the result of recent progress in developmental biology (cf. Wagner, 1986, 1989a, b; Dohle, 1989; Sander, 1989) as well as in reflexions about morphological and phylogenetic methodology and foundations concerning homology problems (Rieger and Tyler, 1979, 1985; Patterson, 1982, 1988; Sattler, 1984; Tyler 1988; Roth, 1988, 1991; Ax, 1989; Bock, 1989; Paulus, 1989; Schmitt, 1989). There are at least two sets of issues concerning homology (Roth, 1991): One is to identify what, why and how characters are conserved, the other is to identify homologues in different taxa and to reconstruct their common ancestral stage, and both aspects are fundamentally interdependent. The considerations presented herein focus on the definition of homology, the different kinds of homology and their use in evolutionary biology and phylogenetic reconstruction. 13

14 The Definition

Haszprunar

of homology

There has been some discussion recently on how best to define homology (e.g. Roth, 1988, 1991; Ax, 1989; Michaux, 1989; Wagner, 1989a, b) and I am well aware of the difficulties. The classic, predarwinian and thus non-evolutionary definition by Owen ( 1843; glossary: “Homologue: The same organ in different animals under every variety of form and function”) speaks about “animals” not about “species”. In addition, this meaning of homology was purely morphological and was not made in a phylogenetic sense (e.g. Schmitt, 1989). Therefore, the definition recently given by Ax ( 1989: title: “. . . a relational term in the comparison of species”), which restricts the use of homology to supraspecific comparison only, is not historically founded. Patterson ( 1982, 1988) proposed that “homology” should be synonymous Although every synapomorphy is a homologue and every with “apomorphy”. homologue is an apomorphy at a distinct hierarchical level. this definition is not valid, because homology concerns characters, whereas apomorphy concerns taxa. In other words, symplesiomorphies are also homologues and even a “non-character” (e.g. loss of. .) might be regarded as an apomorphy. In addition, some of Patterson’s tests result in probability degrees (see Remane, 1952, 1954; Haszprunar, 1990) yet these results are taken as a simple “yes/no” distinction to infer the homology type. Most recently, Ax (1989) wanted to restrict homology to the comparative level of species. As discussed in detail below, this does not work and I fully agree with Roth (1988: 3) that “it is obviously essential to recognize that phylogenetic and iterative homology are distinct, yet it is also important to acknowledge the conceptual and biological relationship between the two”. It will be shown that there are even some interconnecting types of homology. I prefer here a definition combining that of Osche (1973, 1982: 21): “Homologies are non-random similarities of complex structures which are based on common genetic information (in the sense of instruction)” (translation by the author from the original German) and that of Van Valen (1982: 309): “Homology . . . is a correspondence caused by a continuity of information”. The two are very similar. However. whereas Osche’s (1982) definition restricts homology to genetic information and thus to biology, the definition of Van Valen (1982) also includes continuity of information by tradition (e.g. comparison of languages, computer software, etc.). In Osche’s ( 1982) definition the restriction to “non-random” similarities should exclude similarities which are created in our mind only (cf. Riedl 1975, 1980 for (several far suns, or neuronal patterns after an reasoning), such as “asterics” accident, or a small colony of ascidians, or specific skeletal elements of sponges, holothurians, etc.). I would like to widen Osche’s “structures” to “structures or patterns”, to also include physiological (e.g. homeothermy) and neural aspects (e.g. phono- or encephalograms), or behavior (cf. Lauder, 1989; Tembrock, 1989). On the other hand, the “common genetic basis” in Osche’s definition has become problematic (cf. Roth, 1988, 1991; Wagner, 1989a, b). so I prefer Van Valen’s “continuity of information” with the restriction to biological information (e.g. also

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cytoplasmatic Factors). In summary I propose the following definition: “Homologies are similarities of complex structures or patterns which are caused by a continuity of biological information (in the sense of instruction)“. Thus, it is believed that homologous characters Caere based on the same biological information in the common ancestor. Of course, the information of a usually hypothetical common ancestor is not available. However. definition and the mode of inference of homology are different topics (see Remane, 1952, 1954; Roth, 1988). The definition given has essentially a phylogenetic meaning also with respect to serial homology or homonomy (Riedl, 1975, 1978; Roth, 1984, 1988, 1991; Michaux, 19X9), or heterotopy (distinct entities at different positions): There are cases where more or less individualized (Wagner, 1989a, b) homologous entities (segments, legs, etc.; see below) are based on actually different (but usually neighbouring) genes such as in Drosophila or mouse segments(e.g. Wilkinson et al., 1989; Sander. 1989). Nevertheless, calling these segments homologous, it is assumed/proposed that in an early articulate, respectively vertebrate ancestor all segments were based on one or several identical genes. I agree with Roth (1991) that cases of serial homology (and other types of homology as well; see below) might well be used to study this interrelationship of characters. Recent progress in genetics seemsto weaken this information concept. De Beer (1971) cited the case of the ~JY+XY allele of Drosophila, where modifers are able to restore the original phenotype in the absence of the wild allele at the ~I.V/CK~locus. At first glance it seemsthat a homologous character is based on actually different genes. However, on closer inspection, it becomes clear that this is not the case. What has really happened is that one allele of a quite complex epigenetic system has been replaced by another, whereas the overwhelming majority of the included genetic basis of the eye has remained unchanged. In fact, this is a very common phenomenon of evolution, and of course the (homologous) cycs of man and ape are actually based on somewhat different genes. The uniqueness of the abovementioned case lies in the fact that in the intermediate stage the whole end-product was not expressed. The same pattern is to be expected if we use bacterial mutants unable to synthesize a specific enzyme, and look carefully at the phenotypic backmutants. As outlined above, homology is defined as a phylogenetic matter.

Homology and individuality Wagner (1989b: 62) recently proposed defining the entity of homology by the criterion of individuality: “Structures from two individuals or from the same individual arc homologous if they share a set of developmental constraints, caused by locally acting self-regulatory mechanisms of organ differentiation. These structures are thus developmentally indiviualized parts of the phenotype”. This definition has been given primarily for application in evolutionary biology and comparative embryology. It mainly concerns questions where character comparison becomes meaningless (e.g. “homology” of amino acids, “homology” of the 24th segment of an annclid, etc.; cf. also Bock, 1989).

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The main problem with this definition is that the criterion “individuality” occurs in various gradations. There is a general trend to individualize repetitive structures such as annelid segments,crustacean legs or mammalian teeth (cf. Riedl, 1975: 134), although exceptions are known (e.g. secondarily uniform teeth in cetacean mammals). Often evolution starts with a series of repeated units which are then individually modified and might finally result in (several or all) fully individualized substructures. Using the vertebrate column as an example, such trends can be well traced comparing fish or snakes, with conditions in mammals (e.g. the atlas vertebra). However, the idea behind the concept is crucial. It is indeed necessary to consider which entitites can be compared meaningfully. For practical reasons I propose the following definition: “The entity of comparison is a feature of such complexity or distinctness to enable clear identification of this structure or pattern”. In other words, the entity of comparison needs diagnostic subcharacters. For instance, it is usually not possible to identify certain nerve cells in the brain (Ax, 1989). Individual nerve cells, which can be clearly characterized by a combination of histochemical and neurophysiological methods, have been reported in euthyneuran snails,however, and have been homologized between major subtaxa (cf. Dorsett, 1986 for a recent review). The main advantage of the entity definition given herein is that the respective criteria are available for the overwhelming majority of characters. In addition, it also allows one to homologize characters which are integrated in a net-like process of differentiation. For instance, I do not seeany reason why one should not homologize the eye lens between vertebrate species,although it is involved in a cyclic induction process(Coulombre, 1965). However, I do not argue with the necessity to investigate the developmental constraints of characters. In contrast, knowledge of such constraints may be very important to estimate the possibility of change: Despite (or even because of) a high degree of complexity of a character, a dramatic change of the phenotype might be caused by a minimal change in the epigenetic system. Considering these circumstances, the inferred probability of convergence of such a change may increase.

Types

of homology

Homology depends on comparison between characters. Usually two types of homology are considered, one (called “phylogenetic” or “evolutionary”) between species,the other (called “serial”, “iterative” or “homonomy”) within individuals. If we look closer, however, at least four levels of comparison correlated with four types of homology can be distinguished (Table I). 1. Comparison between characters of THE SAME INDIVIDUAL AT THE SAME TIME: Zteratbe homology ( = normative homology = serial homology = homonomy = paralogy). Examples concern all levels of organization such as molecules of a specific protein, homologous chromosomes or mitochondria in a cell or an organism, hairs of a mammal, legs or segmentsof an arthropod, any structure represented symmetrically in an organism, etc.

for

(Uru).

of a hen

individualization

feathers paedomorphosis. progenesis, neoteny. etc

teeth

at

feathers of chicken and hen

antenna of nauplius-mandible of fiddler crab.

crab

and leg of

antenna fiddler

tentacles of polyp and hydromedusa. radular teeth of veliger-radular of adult I)

of an athecdte polyp.

heterochronic mutations

radular teeth of trochoid archaeogastropods.

tentacles hydrozoan

*) see text I) see Waren ( 1990) 2) see Robertson (1985)

importance phylogenetics

Examples

homoeotic

Mutations

mutations

same individual at the same time

Ontogenetic Homology same individual different times

types of homology

Iterative Homology, Serial H., Homonomy

of the various

Comparative level

*)

I. Comparison

Type of homology

Table

basis for speciation

white and brown of hen races

feathers

chelae of male and female of fiddler crabs.

radular teeth of male and female Tricolra variahilis (Trochoidea) 2)

tentacles of autozyoids and dactyloroids.

sexual chromosome mutations

di-/polymorphic individuals (clones) of the same species

Di-/Polymorphic Homology

teeth of different species 2)

of different species.

species

obvious

feathers

of hen and pheasant

chelae of fiddler crabchelae of lobster.

radular Tricnlia

tentacles athecate

atavisms

different

Supraspecific Homology

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Hawprunar

In addition to Remane’s (1952) homology criteria, such homologies might be detected by the occurrence of homoeotic mutations. i.e. doubling or multiple repetition or replacement of homologous entities in ontogeny. Such entitites might be quite complex, such as in various Drosophilrr mutants (e.g. aristopedia, tctraltera, tetraptera; cf. Riedl, 1975: 2322234 and Garcia-Bellido, 1977 for reviews). Certain casesof heteromorphosis cause similar phenomena by erroneous regeneration (cf. Riedl. 1975: 238). However, inferring homologies is a matter of probabilities (Remane, 1952; Rieger and Tyler. 1979, 1985; Haszprunar, 1990) and the presence of homoeotic mutations can also be misleading. For instance, in Drvsophiltr transitions arc also known between eyes and wings or antennae and eyes (Garcia-Bellido et al., 1979), which cannot be considered as homologous structures. 2. Comparison between characters of THE SAME INDIVIDUAL AT DIFFERENT TIMES: Ontogentic homnlog~~. For instance, quite ditrerently structured characters of the larval and the adult body are considered homologous, such as Wolf’s duct and vas deferens in vertebrates, leg of a nauplius larva compared with antenna and mandible of an adult crustacean, polyp tentacles and medusoid rhopalia in scyphozoans, etc. A specific criterion to detect ontogenetic homology is to follow the differentiation or modification of the character during ontogeny. Spontaneous paedomorphosis as a mutation has rarely been observed, yet is often considered in reconstructing phylogenies (e.g. McKinney (ed.), 1988). It should be stressed here, however, that this does not imply that all characters of a distinct ontogenetic stage are precursor homologues of the adult stage. Ontogeny is by itself a product of evolution, and many ontogenetic characters arc adaptive for the respective stage of the life-cycle (e.g. Gould, 1977; Osche 1982, Kluge, 1988; Dohle, 1989; Wolpert, 1990). The subjects might be even more complicated, however. In cases of bi- or polyphasic life-cycles the larval character might have been modified from an adult stage of an ancestor. Such a process may be assumed for the stemmata of larval insects (Paulus, 1989) which thus might be homologues with the ommatidia of the imaginal ancestor and cannot be considered as simple precursors of the ommatidia of the same individual. A similar case might be found with respect to proto- and metanephridia in larvae and adults of coelomate metazoans (for recent review cf. Ruppert and Smith, 1988 and Smith and Ruppert, 1988). Thus, ontogenetic homology concerns a distinct mode of comparison, but does not concern the exact phylogenetic process (e.g. paedomorphosis, terminal addition, etc.). The question of the ancestral version of characters, which are considered to be ontogenetically homologous, is a question of apo- or plesiomorphy (with criteria proper; cf. Hennig, 1966) but not a question of homology. 3. Comparison between characters of DIFFERENT INDIVIDUALS (OR CLONES) OF THE SAME SPECIES: Di- or polymorphic homology. This is usually done beween races (subspecies, variants. mutants), where the respective modifications of characters are often not yet fixed. In cases of (sexual) dimorphism or polymorphism such character modifications are fixed. Examples of the latter are

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clitoris and glans penis in mammals, sperm sac and sperm reservoir of male respectively pharynx of female bonelliid echiurans. or female genital organs respectively defense apparatus in fertile and infertile female hymenopteran insects. This kind of homology also includes examples like the different kinds of polyps of siphonophore Cnidaria or of bryozoan zoids. Considering asexual reproduction for the two latter cases, the comparative level is a clone, showing that there may be transition between iterative and polymorphic homology, if individuality is doubtful. Inferring this type of homology may include observation of specific mutations or determination experiments concerning either sex or polymorphism. In particular in cases of (additional) phenotypic sexual determination the results are often intermediate structures. Intersexual mutations are well known in particular in humans, where XXY-, XYY-, X0-, or similar mutants show intermediate phenotypes. A case of experimental polymorphic determination is found in bees, where normal larvae can be stimulated by food to become a queen. In the neogastropods Nucella fupillus and Ocenebra erinacea pollution of water by tributyltin (from anti-fouling paints of ships) induces imposex or sex change with all intermediate forms (Gibbs et al., 1988, 1990). 4. Comparison between characters of DIFFERENT SPECIES OR HIGHER TAXA: Supraspec$c homology. The term “phylogenetic homology” should be avoided in this case, because other types (in particular ontogenetic and bi- or polymorphic homology) are also phylogenetic. Nevertheless, supraspecific homology is the most important case in phylogenetic reconstruction. The former types are found within a species, therefore genetic exchange (or “piracy”) during the meiosis cycle can easily take place. This is usually not the case between species, although there are certain exceptions such as gene transfer by vectors or by conjugation (e.g. Syvanen, 1985; or Stachel and Zambryski, 1989). Atavistic mutations, such as the 3-digit variant in horses or the reappearance of the Drosopphih eye in a mutant of an eye-less line (see above), or neovistic mutations, such as the replacement of scales by feathers at the legs of domestic cocks or pigeons, can be used as additional criteria to homologize the respective structures. Often no clear distinction can be made between an atavistic and paedomorphic mutation, if an interphene of the species equals a metaphene of the ancestor (e.g. hairs of ape, lanugo and wolf-man).

Homology

types in evolutionary

biology and phylogenetics

Ax ( 1989) has recently argued in favor of the exclusive use of supraspecific homology in phylogenetic analysis. Of course, if phylogenetics is reduced to establish solely sister-group-relationships by inference of homologies by parsimony or compatibility methods, then all other types are not necessary. However, such an approach is to be criticized for two reasons: First, phylogenetics involves not only the establishment of sistergroups-interrelationships between taxa, but also a reconstruction of what happened and the respective processes.This is the fundamental interrelationship of the two homology

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aspects mentioned by Roth (1991) and also links evolutionary biology and systematics. Secondly, a simple (all selected characters given equal weight) parsimony analysis will usually fail, if the probability of change has not been estimated before the construction of the tree (cf. Neff, 1986 for a review). Such estimation involves comparative morphological research (e.g. assessment of the number of cases of known parallelism), ecological or functional considerations (estimation of selective pressure; cf. Tyler, 1988), and might also consider possible evolutionary mechanisms. In particular the last point is important, because certain evolutionary processes may change the type of homology: Iterative homologues may shift to supraspecific homologues through individualization. It is meaningful to identify and compare specific teeth between mammalian taxa for phylogenetic purposes, but it is not meaningful to do so for crocodiles or amphibians. Reconstruction of changes in the individualized pattern of mammalian teeth, however, is, at least partly, a matter of serial homology. I agree with Wagner ( 1989a, b) that supraspecific comparison is meaningful only if the respective entity has reached individuality (diagnostic subcharacters, see above). lndividuality may be reached also in bilaterally homologous characters such as the (presently unequal) left and right claw of the lobster (e.g. Govind and Pearce, 1988). Also spontaneous multiplication of characters (cf. Riedl, 197.5: 144) is at the onset a matter of serial homology (probably a homeotic mutation). However, once they become fixed, their comparison with other taxa becomes a matter of supraspecific homology. The interrelationship between ontogenetic and supraspecific homology and the reconstruction of such shifting processes has been discussed at length (e.g. Baer, 1828; Haeckel, 1866; Hertwig, 1906; De Beer, 1958; Osche, 1982; Alberch, 1985; Kluge, 1985, 1988; Kluge and Strauss, 1985; Fink, 1988; Rieppel, 1990). Recently, specific attention has been paid to the evolutionary potential of heterochronic processes and in particular of progenesis, which turned out to be a major evolutionary mechanism (e.g. Gould, 1977, 1982; Westheide, 1987; McKinney, (ed.) 1988; Raff and Wray, 1989). Also von Baer’s and Haeckel’s rules in their modified and much less rigid forms (cf. review in Osche, 1982) express such interrelationship. This is why homology analyses often include ontogenetic data. A very recent example of the importance of considering heterochrony in evolution is the discussion about the recently described enigmatic echinoderm X~loplu.u. Baker et al. ( 1986) and Rowe et al. ( 1988) proposed a new class, Concentricycloidea. for this genus because of the drastic anatomical differences between Xyloplu.~ and the other extant echinoderm classes. However, as pointed out by Smith (1988) and further supported by McEdward ( 1989) X,dop/ax and some relatives (Caymanostellidae) might be progenetic asteroids rather than representatives of a distinct echinoderm offshoot. Whereas shifting from non-fixed polymorphic homology to supraspecific homology is the most commonly assumed mode of evolution, shifting from already fixed di- or polymorphic to supraspecific homology has been rarely reported and noticed. Nevertheless, it is at least thinkable that such shifts occur in cases of mistakes/

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distortion in sex-determination (e.g. Gibbs et al., 1988, 1990) or in cases of parthenogenesis (see Suomalainen et al. ( 1987) for a review). A combination of homology types is found in the case of bonelliid echiurans. The progenetic (ontogenetic,!supraspecific homology) dwarf-male (dimorphic homology) of Bondin ririnfis is superficially very similar to a turbellarian flatworm, and one might speculate about the possibility that other turbellarian-like groups might also have evolved by similar proccsscs. Though the dwarf male still has a true coelomic cavity and its protonephridia are considered as secondary structures (Schuchert, 1990; Schuchert and Rieger, 1990) detailed studies of similar casesmight result in ideas about the constraints for the origin of turbellarian-like worms (supraspecific homologies). Such constraints certainly will influence ideas on the phylogeny of the Bilatcria (e.g. Rieger, 1986). Therefore these four types of homology and their respective levels of comparison should be clearly distinguished in phylogenetic analysis. For instance, milliped segmentsmay be compared among each other (serial homology), during embryonal development (ontogenetic homology), between male and females with respect to gonopods or genital openings at certain segments (dimorphic homology), or with the segments in crustaceans or insects (supraspecific homology) (Minelli and Pcruffo, 1991; Minelli, 1991). It depends on the precise issue which level(s) of comparison are adequate.

Conclusion

The reconsiderations of some recent arguments and statements on the homology problem can be summarized as follows: ( 1) Homology is best defined as a similarity in structure or patterns caused by continuity of biological information or instruction. To make comparison meaningful, the homologue must be clearly identified by diagnostic subcharacters. (2) According to the given definition homology can be applied to all levels of organization, but different levels of comparison with respect to subject and time should be distinguished. (3) Iterative, ontogenetic, and di-/polymorphic homology may shift into supraspecihc homology through distinct evolutionary processes. Consideration of such processes may improve evolutionary biology as well as phylogenetic reconstruction.

Acknowledgements I thank my teachers. R. Riedl (University of Vienna), L. Salvini-Plawen (University of Vienna). and R. M. Rieger (University of Innsbruck) for introducing me to the homology problem. I am grateful to G. P. Wagner (University of Vienna) for several discussions on the topic. He, V. L. Roth (Duke University, Durham. USA) and an anonymous referee made some very helpful and constructive comments on an earlier version of this paper. Last but not least I thank P. Ax (University of Gdttingen, FRG). whose recent papers induced the present contribution.

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References Alberch. P. 1985. Problems with the interpretation of developmental sequencies. Syst. Zool. 34: 46-58. Ax. I’. 1989. Homologie in der Biologie ein Relationshcgriff im Vergleich von Arten. Zool. BcitrTgc N.F. 32: 487-496. Baer. K. E. von 1828. Entwicklungsgeschichte der Thiere: Beobachtungen und Reflexionen. 264. pp. BorntrCger. Kiinigsberg (Germany). Baker, A. N.. F. W. E. Roe and H. E. S. Clark. 1986. A new class of Echinodcrmata from New Zealand. Nature, London 321: 862-8h4. Bock, W. J. 1989. The homology concept: its philosophical foundation and practical methodology. Zool. Beittige N.F. 32: 327 353. Coloumbre, A. J. 1965. The eye. Pages: 219-251 in Organogenesis. R. L. DeHaan and H. Ursprung (eds.), Holt. Rinehart and Winston, New, York. De Beer, G. R. 1958. Embryos and Ancestors. Clarcndon Press, Oxford. De Beer. G. R. 1971. Homology, an unsolved problem. London, Oxford University Press. Dohle, W. 1989. Zur Fragc dcr Homologie ontogenctischer Muster. Zoo]. BeitrPge N.F. 32: 355-389. Dorsett. D. A. 1986. Brain to cells: The neuroanatomy of selected gastropod species. Pages: 101~ 187 in The Mollusca. Vol. 9: Neurobiology and Behaviour II (A. 0. D. Willows ed.). London, Academic Press. Fink. W. L. 1988. Phylogenetic analysis and the detection of ontogenetic patterns. Pages: 71 -91 bt Heterochrony in Evolution. .4 Multidisciplinary Approach (M. L. McKinney ed.). New York & London, Plenum Press. Garcia-Bellido, A. 1977. Homoeotic and atavistic mutations in insects. Amer. Zool. 17: 613 633. Garcia-Bellido A., P. A. Lawrence and G. Morata. 1979. Compartments in animal development. Sci. Amer. 241: 102~110. Gibbs, P. E., G. W. Bryan, P. L. Pascoe and G. R. Burt. 1990. Reproductive abnormalities in female Ocrnehra erinczceu (Gastropoda) resulting from tributyltin-induced imposex. J. mar. biol. Ass. U.K. 70: 639 656. Gibbs, P. E.. P. L. Pascoe and G. R. Burt. 1988. Sex change in the female dog-whelk, Nucella lqillus. induced by tributyltin from antifouling paints. J. mar. biol. Ass. U K. 68: 715-731. Gould, S. J. 1977. Ontogeny and Phylogeny. Belknap Press, Cambridge. Mass. Gould, S. J. 1982. Change in developmental timing as a mechanism of macro-evolution. Pages: 333 -346 by Evolution and Development (J. T. Bonner ed.). Springer Verlag, Berlin. Govind. C. K. and J. Pearse. 1988. Independent development of bilaterally homologous closer muscles in lobster claws. Rio]. Bull. 175: 430~ 433. Haeckel, E. 1866. Generelle Morphologie der Organismen: Allgemeine Grundziige der organischen Formen-Wissenschaft, mechanisch begrtindet durch die von Charles Darwin reformierte Descendcnz-Theorie. Georg Reimer. Berlin. Haszprunar, G. 1991. Systematik und Wahrscheinlichkeit-die klado-evolutionire Synthese. Verh. Dtsch. Zool. Ges. (in press). Hertwig. 0. 1906. tiber die Stellung der vergleichenden Entwicklungstheorie zur vergleichenden Anatomie, zur Systematik und Descendenztheorie (Das biogenetische Grundgesetz, Palingenese und Cenogenese). Pages: 149- 180 in Handbuch der vergleichenden und experimentellen Entwicklungslehre (0. Hertwig cd.), Gustav Fischer, Jena. Kluge, A. G. 1985. Ontogeny and phylogenetic systcmatics. Cladistics 1: 13 27. Kluge, A. G. 1988. The characterization of ontogeny. Pages: 57-81 in Ontogeny and Systematics (C. J. Humphrics, ed.). Columbia University Press, New York. Kluge, A. G. and R. E. Strauss. 1985. Ontogeny and systematics. Ann. Rev. Ecol. Syst. 16: 247-268. Lauder, G. V. 1986. Homology. analogy, and the evolution of behavior. Pages: 9 40 in Evolution of Animal Behavior (M. H. Nitecki and J. A. Kitchcll, eds.). Oxford University Press, New York. McEdward. L. R. 1989. Development and evolution of a novel type of starfish larva. Am. Zool. 29( 4): I14A (abstract 509).

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The

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Received 18 July 1990; accepted 30 October 1990. Corresponding Editor: G. Wagner

of development.

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39: 109-124.