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Theory in Biosciences 124 (2005) 243–253 www.elsevier.de/thbio

The history of the homology concept and the ‘‘Phylogenetisches Symposium’’ Uwe Hoßfelda,, Lennart Olssonb a

Institut fu¨r Geschichte der Medizin, Naturwissenschaft und Technik, Ernst-Haeckel-Haus, Friedrich-Schiller-Universita¨t Jena, Berggasse 7, DE- 07745 Jena, Germany b Institut fu¨r Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universita¨t Jena, Germany Received 2 August 2005; accepted 9 September 2005

Abstract The homology concept has had a long and varied history, starting out as a geometrical term in ancient Greece. Here we describe briefly how a typological use of homology to designate organs and body parts in the same position anatomically in different organisms was changed by Darwin’s theory of evolution into a phylogenetic concept. We try to indicate the diversity of opinions on how to define and test for homology that has prevailed historically, before the important books by Hennig (1950. Grundzu¨ge einer Theorie der Phylogenetischen Systematik. Deutscher Zentralverlag, Berlin) and Remane (1952. Die Grundlagen des Natu¨rlichen Systems, der Vergleichenden Anatomie und der Phylogenetik. Geest & Portig, Leipzig) brought more rigor into both the debate on homology and into the usage of the term homology among systematists. Homology as a theme has recurred repeatedly throughout the history of the ‘‘Phylogenetisches Symposium’’ and we give a very brief overview of the different aspects of homology that have been discussed at specific symposia over the last 48 years. We also honour the fact that the 2004 symposium was held in Jena by pointing to the roles played by biologists active in Jena, such as Ernst Haeckel and Carl Gegenbaur, in starting the development towards a homology concept concordant with an evolutionary world view. As historians of biology, we emphasize the importance of major treatises on homology and its history that may be little read by systematists active today, and have sometimes also Corresponding author. Tel.: +49 03641 949505; fax: +49 03641 949502.

E-mail address: [email protected] (U. Hoßfeld). 1431-7613/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.thbio.2005.09.003

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received less attention by historians of biology than they deserve. Prominent among these are the works of Dietrich Starck, who also happened to be both a student, and later a benefactor, of systematics at Jena University. r 2005 Elsevier GmbH. All rights reserved. Keywords: Analogy; Convergent evolution; History of biology; Homology; Morphology; Phylogenetisches Symposium; Zoology

Historical development of the homology concept The concept ‘‘Homology’’ was probably first used in geometry (Spemann, 1915, p. 65; Bljacher, 1965, p. 123). Homologous angles, corners, etc. were those that had the same position in congruent or similar figures. Biology started as a descriptive and comparative science, and also before researchers had invented concepts like ‘‘Bauplan’’ and ‘‘type’’, it was obvious that many organs and parts of organs in different organisms often were in the same relative position. Such parts were labelled ‘‘analogous’’. Petrus Camper may have been the first to use this expression in comparative anatomy. He used the principle of comparison and the search for ‘‘analogies’’ for example in his investigations of orangutan anatomy (Camper, 1784, 1785). The pioneering work of Camper and others was followed by more and more rigorous anatomical studies, which established comparative anatomy as a science. George Cuvier was maybe the most important figure in this development (Friedrich, 1932, pp. 31–34). Although Cuvier had described what later came to be called Baupla¨ne, and the type concept was being used, up until the middle of the 19th century the conceptual tools for describing relationships between the organs of different organisms remained unprecise (Spemann, 1915; Junker and Hoßfeld, 2001). The first to coin the concept of homology as a term for a certain type of anatomical similarity – and to contrast homology with analogy (Nowikoff, 1935) – was Richard Owen (Rupke, 1994). He wrote ‘‘The corresponding parts in different animals being thus namesakes are called [y] ‘homologues’. The term is used by logicians as synonymous with ‘homonyms’, and by geometricians as signifying ‘the sides of similar figures which are opposite to equal and corresponding angles’’’ (Owen, 1848, p. 173). Owen distinguished between three types of homology: (1) Serial homology, when morphologically similar organs or body parts placed in series in an animal are compared to each other, (2) General homology, when a part or a series of parts are compared to the general type and (3) Special homology, when two (or more) corresponding parts in two (or more) organisms are being compared (see also Haeckel, 1866, I: 313; later see Naef, 1926, p. 411; Friedrich, 1932; Voigt, 1973). In his homology definition, Owen used a strictly formal, geometrical homology concept, and denied every connection between homology and development (such as had been proposed by e.g. J. W. von Goethe and E. Geoffroy St. Hilaire). During Owen’s time, dominated as it was by idealistic morphology, the goal was to understand the anatomical structure of the individual organism and to recognise the

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correspondence of structures between individual organisms, so that they could be classified into the correct group in a hierarchical system or as belonging to one of a few types (de Beer, 1971; Gould, 1977). Even after the publication of Darwin’s On the origin of species (1859), this at first changed very little. Some researchers however, tried to renew comparative morphology by incorporating Darwin’s selection theory. Ernst Haeckel published his Generelle Morphologie in 1866 with this goal in mind. This major work (2 volumes of almost 1000 pages) also shows the problems involved in this endeavour. Haeckel used the results from the earlier idealistic era in comparative morphology, but did more than that. He also transformed e.g. the idealistic ‘‘type’’ concept into the evolutionary ‘‘phylum’’ concept (Haeckel, 1866, II: 388). The idealistic type was created in a purely formal manner through the comparison of different organisms. But for the idealistic morphologist, the causal relationships between the organisms belonging to a type were irrelevant (Meister, 2005). The groups that belonged to a type could for example be polyphyletic as well as monophyletic, whereas Haeckel’s phyla were by necessity monophyletic. Therefore, there are important differences between the concepts type and phylum: one is formal and idealistic, the other causal and based on Darwin’s theory of descent (Friedrich, 1932, p. 46). Haeckel did not provide a definition of homology, but he wrote that homologous organs are ‘‘maintained by common descent’’. Analogous organs on the other hand, are ‘‘acquired by common descent’’, i.e. they evolve convergently (Haeckel, 1866, II: 411). Haeckel’s evolutionary interpretation of the homology concept had important consequences for the development of the ‘‘biogenetic law’’, often expressed as ‘‘ontogeny recapitulates phylogeny’’. The parallel between embryonic development and phylogeny was first discussed at length in 1872 in Haeckel’s Monographie der Kalkschwa¨mme, but the most comprehensive use of the biogenetic law can be found in Haeckel’s writings on the Gastraea-theory. The Gastraea is a hypothetical ‘‘Urform’’ from which all metazoans have evolved, according to Haeckel. It has left no palaeontological traces and can therefore only be seen as the gastrula stage in the development of many extant animals: From these identical gastrulae of representatives of the most different animal phyla, from poriferans to vertebrates, I conclude, according to the biogenetic law, that the animal phyla have a common descent from one unique unknown ancestor, which in essence was identical to the gastrula: Gastraea (Haeckel, 1872, 1: 467).1 With his Gastraea-theory, Haeckel thought he had proved the monophyletic origin of all multicellular animals. If the two primary germ layers really are homologous in all metazoans, as Haeckel postulated, then he had given an evolutionary explanation of this early and important embryological process, the origin of germ layers. 1

German original: Aus dieser Identita¨t der Gastrula bei Repra¨sentanten der verschiedensten ’’ Thiersta¨mme, von den Spongien bis zu den Vertebraten, schliesse ich nach dem biogenetischen Grundgesetze auf eine gemeinsame Descendenz der animalen Phylen von einer einzigen unbekannten Stammform, welche im Wesentlichen der Gastrula gleichgebildet war: Gastraea’’.

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Carl Gegenbaur, Haeckel’s colleague and teacher, was instrumental in creating an evolutionary morphology which was based on Darwin’s theory of evolution (Hoßfeld et al., 2003). In 1878 he demanded that ‘‘precise proof of the relationships’’ were necessary and defined: ‘‘Homology [y] can be divided into two main categories, general and special homology’’ (Gegenbaur, 1878, p. 67). Gegenbaur’s ideas on homology were influenced by his development of a theory of head metamerism in vertebrates. Based on studies of the embryos of sharks, which he took to be representative of the basal mode of head development in vertebrates, Gegenbaur homologised the different metameres in the head and tried to reconstruct the evolution of head development (Mitgutsch, 2003). This ‘‘segmentation theory of the vertebrate head’’, in which the cranial nerves were considered to be ‘‘homodynamous’’ (serially homologous) with the spinal nerves, made it possible to homologise the gill arches with hemal arches and the ribs with processes of hemal arches, etc. Thus an ordering system was built based on specific ideas about homology. This was the start of the ‘‘Gegenbaur school’’ in comparative morphology, and Gegenbaur’s approach was later developed in different directions by members of his school, some of whom were active in Jena, e.g. Max Fu¨rbringer and Friedrich Maurer (Hoßfeld and Olsson, 2003b). Ray Lankester understood that the homology concept, as it was taken over from comparative (idealistic) morphology, could not do what phylogenetic research demanded from it, i.e. express the real or hypothetical evolutionary relationships between organisms and their parts (Lankester, 1870, p. 34). Lankester also realised that typological and phylogenetic homology concepts describe different things, and suggested to call the latter ‘‘Homogeny’’. Later, a profusion of taxonomies of homologies developed. In his review, Voigt (1973, p. 33) writes that A. Meyer-Abich described five different ‘‘homologisms’’ in 1926, L. von Bertalanffy four different kinds of homology definitions in 1934, W. Thiele eight variants in 1967, and that L. Ja. Bljacher differentiated between 65 kinds of homology and analogy in 1965. This tendency towards increasing diversity was countered in the early 1950s by authors who wanted a rigorous methodological clarification of how homology should be defined and tested. Books by the entomologist Willi Hennig (1950) and the marine biologist, morphologist and anthropologist Adolf Remane (1952) were particularly important. After 1952 a large number of authors started to discuss Remane’s homology criteria, and to demand that these be used in all serious homology research (Voigt, 1973, p. 33; Remane, 1989). Remane himself used the homology criteria in comparative animal behaviour research (Remane, 1960) and thereby promoted their use in not only ethology (see e.g. Freye (1967), Wickler (1965, 1967), Meissner (1976, 1978) and Tembrock (1967, 1989)), but also in other biological disciplines, such as comparative endocrinology, for example by Gersch (1964, 1967). These examples (which can easily be multiplied) make it clear that homology has a long history as a concept of crucial importance for the biological sciences. In 1955, Adolf Remane even wrote of ‘‘morphology as homology research’’ (Remane, 1955), and in the contemporary literature homology is often described as the basis of comparative biology (e.g. Hall, 1994). To establish and analyse similarities and differences remains at the core of the comparative method.

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In fact this fundamental concept – homology – is as old as comparative morphology itself. Buffon, Vicq D’Azyr, Petrus Camper and others established homologies without using this term. In 1825, Geoffroy St. Hilaire used the label ‘‘homologous’’ for the first time, when he wrote: ‘‘when the development of organs is analogous, they are called homologous’’ (Schmitt, 2004) The basic criterion for establishing homologies was the position in the Bauplan or type. The type only exists in the realm of ideas, but using the type concept made a short but exact description of morphological regularities within larger taxonomic groups possible. In idealistic morphology parts that have the same position in the type are called homologous, regardless of their function or descent (Meister, 2005). The dissemination and acceptance of at least parts of Darwin’s theory of evolution in the second half of the 19th century made it necessary to redefine the homology concept as a historical concept suitable for integration into evolutionary (rather than idealistic) morphology. The difficulties involved in creating a clear new definition of homology made some biologists return to a typological homology concept, and reject a phylogenetic one. The zoologist Adolf Naef (1926, 1927) can serve as an example, and his typological homology concept (or similar versions of it) was accepted by for example Hans Driesch, Wilhelm Lubosch and Adolf Meyer-Abich. Partly as a reaction to this, a strictly genetic formulation of the homology concept was developed by the evolutionary morphologists Victor Franz and Nikolai A. Sewertzoff (Hoßfeld and Olsson, 2003a; Levit et al., 2004). Hans Bo¨ker’s program for a ‘‘comparative biological anatomy’’ in the 1920s and 1930s also could have contributed to a clarification of the homology concept as an evolutionary concept, but had only limited success (Hoßfeld, 2002). At roughly the same time as these developments among German biologists, the zoologist Mikhail M. Nowikoff, working in Prague, developed a table in which he collected ‘‘all categories of correspondences of organs or organisms’’ (Nowikoff, 1935, p. 392). Nowikoff divides the organisms, whose characters are to be compared, into those with and without common descent. It can be argued that all organisms have a common descent, but Nowikoff means relatively unrelated organisms when he uses the label ‘‘not common descent’’. Characters are divided into primary and secondary. Secondary characters have arisen independently in different organisms and are secondary also in a historical sense, they are relatively new. Primary characters are fundamental to the functioning of the organism and belong to its ‘‘Bauplan’’. This leads to a differentiation between four different kinds of characters, two of which are the familiar homology and analogy, whereas the remaining two, homomorphy and homoiology, are less familiar. Nowikoff uses homology only for primary characters in organisms with common descent. Secondary characters in organisms with common descent are called homoiologies, following a suggestion by Plate (1922), to use this term to designate characters in related organisms, where these characters have arisen independently. Nowikoff gives as examples the beaks of birds and turtles, and the compound eyes in different arthropods. Nowikoff’s homomorphy is a relationship between characters in unrelated organisms, when the characters are of a ‘‘truly morphological nature’’. Their similarity can for example be explained by simple physical laws and regularities. Nowikoff’s examples are the tendency for soft

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organisms without a skeleton or a shell to form rounded structures, or the tendency for hexagonal forms to appear in closely packed structures, regardless of the type of organism. Nowikoff’s suggestion had limited success, however (Hermann and Kleisner, 2005) (Table 1). Fifteen years after Nowikoff’s work, the vertebrate morphologist Dietrich Starck at the University of Frankfurt am Main published an important investigation into the historical metamorphoses of the homology concept (Starck, 1950). Here Starck argued that in order to become more integrative and synthetic (also in terms of the homology concept), evolutionary morphology must take into account results from other fields of biology, in particular evolutionary biology in the form of the ‘‘Modern Synthesis’’ (Starck, 1950, p. 967). Starck’s study is, together with Friedrich’s,1932 and Voigt’s, 1973 paper, the most comprehensive investigation into the historical development of the homology concept, at least in the German literature. Based on the work of Friedrich and Starck, five different meanings had been given to the term homology until the middle of the 20th century: 1. Typological homology: Parts are homologous, which have the same positional relationships in the Bauplan, independent of form and descent; 2. Typological-ontogenetic homology: Embryonic development is used to establish the typological relationship; 3. Phylogenetic homology: The same as Lancester’s ‘‘Homogeny’’; Organs are homologous, which have common descent, i.e. have been inherited from a common ancestor; 4. Developmental homology: Referring to Ludwig von Bertalanffy’s work; Organs are homologous, which develop under comparable organizing relationships. This interpretation of homology necessarily includes 1–3; 5. Genetic or molecular biological homology: Parts are homologous, which result from homologous mutations in homologous genes. A genetic relationship is not necessary. Nowikoff’s ‘‘Homomorphies’’ belong here. Unfortunately, all these studies (by Friedrich, Starck, Voigt) are hardly known, and not cited, in the recent literature in English on the topic (e.g., Abouheif, 1997; Dickinson, 1995; Hall, 1994; Laubichler, 2000; Mu¨ller and Wagner, 1996; Panchen, 1999; Raff, 1996; Rieppel, 1994; Roth, 1988; Wagner, 1995; Wake, 2003). This is partly because of the language barrier, but also because the traditions in the history of morphology and embryology are different in different countries. Another important factor is that large parts of this history remain to be written. Table 1. English version of the table in Nowikoff (1935, p. 392) Organisms with:

Primary characters

Secondary characters

Common descent Not common descent

Homology Homomorphy

Homoiology Isomorphy or Analogy

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Homology and the ‘‘Phylogenetisches Symposium’’ In November 1957, at the initiative of Adolf Remane, Curt Kosswig and Wolf Herre, a small group of zoologists and anatomists met in Hamburg. They all knew each other and the idea was to discuss problems of common interest in contemporary research. At this meeting the focus was on genetics and evolution. Later, it is reported that: ‘‘The impulses that emerged from this unconstrained discussion held in a spirit of mutual trust were seen as being so valuable, that problems in modern systematics were discussed in Kiel in February 1958 and problems relating to evolutionary trends in Gießen in November 1958’’ (Zoologischer Anzeiger 162, issue 7–8, p. 187, 1959, our translation). This was the birth of the ‘‘Phylogenetisches Symposium’’. The 46th ‘‘Phylogenetisches Symposium’’ was convened in Jena from November 19 to 21 in 2004, and had particular aspects of homology as its theme. This places this meeting in a tradition that permeates the entire history of the ‘‘Phylogenetisches Symposium’’ (Kraus, 1984; Kraus and Hoßfeld, 1998). One earlier symposium (in 1988) had homology as its main theme, and in several others some of the lectures treated different aspects of the homology problem. In 1961, for example, discussions of the ‘‘head problem’’ led to an emphasis on serial homology. Bearing in mind that we might have missed lectures that were in fact about homology in a more or less indirect way (as are many aspects of comparative studies) we have made the following compilation of symposia and lecture titles (translated by us) related to homology. We abstain from commenting on the contents and from making comparisons. This would have required a much longer paper, or indeed a book, to do the subject full justice. We hope that our first foray into this material can inspire further research.

Fifth Symposium, Frankfurt a. M., November 26–27, 1960 Parallel evolution and phylogeny Published in Zool. Anz. 166 (9/12), 1961 C. Kosswig, Hamburg: On so-called homologous genes; A. Remane, Kiel: Thoughts about the problems: homology and analogy, preadaptation and parallelisms; Discussion with contributions by D. Starck, F. Seidel, F. Anders, H. Hofer, J. Ka¨lin, G. Niethammer, G. Osche und G. von Wahlert.

Seventh Symposium, Hamburg, December 1–2, 1961 Problems of the metamery of the head Published in Zool. Anz. 170 (11/12), 1963 D. Starck, Frankfurt a. M.: The metamery of the vertebrate head;

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R. Siewing, Kiel: On the problem of arthropod head segmentation; S. L. Tuxen, Copenhagen, Denmark: Presumed external signs of a head segmentation in the arthropods; A. Remane, Kiel: On the possibilities to homologise connective structures (muscles, blood-vessels, nerves) and cavities; A. Remane, Kiel: On metamery, metamerisms and metamerisation in vertebrates. Discussion with contributions by J. Ka¨lin, K. von Haffner, R. Siewing, R. Riedl, H. – J. Mu¨ller, D. Starck.

17th Symposium, Frankfurt a. M., December 2–3, 1972 Analogy, convergence and parallelisms G. Osche, Freiburg: On the problems and importance of analogy research; J. Wiedmann, Tu¨bingen: Homologies, analogies and iterations in ammonites; O. Kraus, Hamburg: Correspondences in net building in different spider groups: parallelisms or homologous specialisations?; C. Kosswig, Hamburg: Analogy, convergence and parallelisms from a genetic point of view.

31st Symposium, Freiburg, November 25–27, 1988 Homology Published in Zool. Beitr. N.F. 32 (3), 1989 ed. by W. Dohle, G. Weigmann & I. Zerbst-Boroffka; K. Sander, Freiburg: Introductory remarks: Homology and ontogenesis; W. J. Bock, New York, USA: The homology concept: Its philosophical foundation and practical methodology; W. Dohle, Berlin: On the problem of homology of ontogenetic structures; J. Jacob, Hamburg: Valuation and results of chemical methods for problems of zoological systematics; G. Tembrock, Berlin: Homologies in ethology; H.F. Paulus, Freiburg: Homology in ultrastructural research: The Bolwig-organ of higher Diptera and its homology with stemmata and ommatidia of an ancestral mandibulate facetted eye; K. Bachmann, Amsterdam: Homology in Plants; P. Ax, Go¨ttingen: Homology in biology – a relational term in the comparison of species; J. Remane, Neuchatel: The development of the homology-concept since Adolf Remane; M. Schmitt, Freiburg: The homology concept in morphology and phylogenetics; G. Osche, Freiburg: summary and discussion.

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37th Symposium, Bonn, 25–26 November 1995 Molecular versus non-molecular charfacters in phylogenetics Published in M. Schmitt ed.: Phylogenetik und Moleku¨le, Edition Archaea, Gelsenkirchen 1998. J. W. Wa¨gele, Bielefeld: Homologies, apomorphies and ground patterns in molecular systematics. Discussion led by R. Willmann (Go¨ttingen). From the list above, it is clear that homology has been discussed over the last 48 years from many different aspects at the ‘‘Phylogenetisches Symposium’’. Some themes recur, however. These include the relationship between development, evolution and homology; the theme also of the 2004 meeting at Jena University. Other topics which have persisted throughout the history of the ‘‘Phylogenetisches Symposium’’ are (molecular) genetics and homology, homology in behavioural studies, serial homology (often in connection with the ‘‘head problem’’ in vertebrates and arthropods), homology and homoplasy (convergent and parallel evolution), and of course discussions focussed on the philosophical foundations of homology. We would like to end our short historical comparison by quoting Dietrich Starck: ‘‘It seems essential to me, that rigid models and hypotheses must be overcome and that the factual material must be constantly reanalysed. Morphogenesis is a dynamic process and can only be interpreted, when the living course of events is understood as such and not just replaced by a static model’’2 (Starck, 1963, p. 425). Even today, this statement retains much of its topicality for the history of homology research, and for analyses of the relationship between development, evolution and homology.

Acknowledgements We thank Wolfgang Dohle, Berlin for constructive criticism on an earlier version of this paper. Our research on the history of evolutionary biology is supported by the DFG (Ho 2143/5-2) to Uwe Hoßfeld. The manuscript was finished while LO was a visiting fellow at the Konrad-Lorenz-Institut for Evolution and Cognition in Altenberg, Austria. LO wishes to thank the Friedrich-Schiller-Universita¨t Jena for granting him a sabbatical leave in the summer semester of 2005.

References Abouheif, E., 1997. Developmental genetics and homology: a hierarchical approach. Trends Ecol. Evol. 12, 405–408. 2

German original: Wesentlich erscheint mir, daß starre Schemata und Hypothesen u¨berwunden werden ’’ und das Tatsachenmaterial immer wieder neu durchdacht wird. Morphogenese ist dynamisches Geschehen und kann nur gedeutet werden, wenn der lebendige Vorgang als solcher erfaßt und nicht nur als statisches Schema ersetzt wird’’.

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