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schmidt's work and place in research into development and evolution; Raff and Kaufman ... Laubichler advances the position that Hans Spe- mann (most often ...

AMER. ZOOL., 41:1049–1051 (2001)

COMMENTARY A Commentary on ‘‘Evolutionary Developmental Biology: Paradigms, Problems and Prospects.’’ Richard M. Burian, Scott F. Gilbert, Paula M. Mabee and Billie J. Swalla, editors. 2000. American Zoologist 40, pp. 711–831. The fifth issue of Volume 40 of American Zoologist, the journal of the Society for Integrative and Comparative Biology (SICB), contains 12 papers from the symposium on evolutionary developmental biology presented at the SICB annual meeting in January 2000 to inaugurate a new division that bears the same name as the symposium. The papers represent a fascinating snapshot of many of the issues embraced by ‘‘evodevo,’’ a field with ancient origins yet modern currency. One of the strongest messages emerging from these papers is the critical importance of a historical perspective in modern-day evo-devo; half the papers provide an historical framework for such ongoing problems as homology, homoplasy, the integration of genetics (especially physiological genetics) with development and evolution, analysis of growth, and the integration of environment, genes and evolution. Richard Burian sets the stage with considerations of epigenetics and preformation, the changing nature of the relationship between the terms and the disciplines of development and evolution, and the way in which present-day research is reformulating old problems and providing new paradigms. Hall’s paper discusses 1870–1970 as the first century of evolutionary embryology (often referred to as evolutionary morphology and the forerunner of evo-devo), by evaluating the contributions of Francis Balfour. Walter Garstang and Gavin de Beer to homology (especially use of developmental criteria such as germ layer of origin and anlage), to the importance of larvae and of larval evolution, and to the way in which deviation in the timing of embryonic development in ontogeny and phylogeny has persisted as an evolutionary developmental mechanism for the origin of novelties, body plans and new groups of organisms. The pivotal importance of homology emerges in this and other papers. 1 See the special issue of the International Journal of Developmental Biology devoted to The SpemannMangold Organizer: 75 Years On. edited by De Robertis and Arechaga (2001), which includes a translation ¨ ber Inby Victor Hamburger of the seminal paper. U duktion von Embryonalanlagen durch Implantation artfremder Organisatoren, published by Spemann and Mangold in 1924. 2 Although he did not like the theory, Dobzhansky (1940) thought Goldschmidt’s was the only new evolutionary theory proposed in the first 40 yr of the 20th century; Templeton (1982) outlined why we should read Goldschmidt in a review of the reissue of his Material Basis of Evolution for which Gould (1982) wrote a thoughtful introduction evaluating Goldschmidt’s work and place in research into development and evolution; Raff and Kaufman dedicated their 1983 book to Richard Goldschmidt.

Laubichler advances the position that Hans Spemann (most often remembered for the organizer, primary embryonic induction, and as the first embryologist to receive a Nobel Prize1) was a founder of the developmental approach to homology, now most associated with the work of Gavin de Beer. Laubichler elaborates on this approach, arguing that developmental processes are inherent in assessment and explanations of homology—developmental processes as homologues themselves—and for understanding of developmental mechanisms as fundamental to understanding the origin of novelties in evolution. Environmental change can elicit heritable developmental changes that are fundamental to evolutionary change. Gilbert explores this concept (genetic assimilation) in an analysis of the work of C. H. Waddington, showing how current research, especially that of Rutherford and Lindquist (1998) on the heat shock proteins Hsp83 and Hsp90, has vindicated Waddington’s approach and provided a molecular mechanism for genetic assimilation. How often genetic assimilation has been the instrument of evolutionary change remains an open question. Demonstrating the role of genetic assimilation in nature would be an important contribution to evo-devo. The bad press given to Richard Goldschmidt is slowly giving way to an appreciation of the important role he played through his own (the first) efforts to integrate genetics, development and evolution; through his pivotal influence on others;2 and through the incorporation of his ideas in other mechanisms of evolution given much more credence than those Goldschmidt himself proposed. For example, Goldschmidt’s elaboration of the concept that genes affect rates of development and developmental processes, was the basis of and is enshrined in, de Beer’s (1954) theory of heterochrony (see p. 726 in the symposium proceedings). Heterochrony—hopeful times—has had enormous influence on our understanding of the relationship between development and evolution, unlike Goldschmidt’s macromutational theories—hopeful monsters—which were based on systemic mutations. Dietrich’s symposium contribution and other recent publications (e.g., Dietrich, 2000) set Goldschmidt in his rightful place—as the first to integrate genetics, development and evolution. Emphasis on altered timing of development leads inevitably to the importance of analyses of growth in evo-devo, a topic that Gayon discusses in the context of the work of Georges Tessier and Julian Huxley on allometry. Gayon both places this work in historical context and discusses the subsequent elaboration of allometry by Gould. In another contribution to the symposium, Roth and Mercer place allometry in the context of morphometrics, a tradition that goes back to the biometrics/statistics of Pearson and Galton and to the transformational analyses of D’Arcy Thompson. Goldschmidt’s advocacy of a hierarchy of genetic units anticipated the hierarchical approach of (some) current evo-devoists; see below. Though few embraced




Goldschmidt’s view of hereditary units as units of development rather than units of mutation (p. 742), the recognition of genes as units of development is a fundamental contribution of evo-devo to the modern synthesis (Beurton et al., 2000; Hall, 2001; Robert et al., 2001). Goldschmidt was one of the first to attempt to incorporate developmental approaches to evolutionary change with the population/variation approach of population biology. As Dietrich discusses, from 1949 on, Goldschmidt and Sewall Wright forged an approach that few have taken up. In this symposium, only Arthur attempts to integrate evo-devo with population genetics, and this in the context of genetic and developmental polymorphisms, internal and external selective agents, and adaptation/coadaptation as explanations for the origin of developmental novelties. Arthur’s two examples—segment number in centipedes (in which the number of trunk [limbed] appendages is always odd, and total segment number always even) and coiling in gastropods—are used to test the von Baerian thesis (Arthur’s cone model) that the earlier a change occurs in ontogeny the greater its effect will be in the adult. Phylogenetic approaches inform two papers, one by Donoghue and Ree on homoplasy and developmental constraints, the other by Mabee on the utility of developmental data in phylogenetic systematics. Both approaches lament the lack of a general theory relating phylogenetic patterns of character evolution to the units or modules of developmental systems. Both go beyond the Hennigian emphasis on how developmental sequences might be used to establish the direction of character evolution (an application of Haeckel’s recapitulation that never seemed to me to be grounded in any logic, developmental or otherwise), to phylogenetics as the handmaiden to analyses of the evolution of development. Phylogeny emerges as a tool rather than a science. Donoghue and Ree provide a cogent and well-documented argument for the relationship between numbers of evolvable states and homoplasy. Mabee comes to the unexpected conclusion that teleost fish fins and tetrapod limbs may not share any homologous skeletal elements or homologous patterns of Hox gene expression. Her rationale is that fins and limbs develop from different limb elements. A more hierarchical/inclusive approach to the homology of elements of these appendages, and additional data on fin development and on patterns of Hox gene expression in Polypterus or in Polyodon are needed to test this interpretation. Bolker discusses modules and hierarchy, stressing that modules ‘‘can exist at different levels of the biological hierarchy’’ and so must be ‘‘defined with respect to a specified level, and to the processes that occur at that level’’ (p. 774). Her focus is on the nature of modules as fundamental units, illustrated chiefly by an analysis of the dorsal marginal zone of Xenopus gastrulae, which she considers as ‘‘the best-characterized morphogenetic module’’ (p. 773). I see the progress zone of tetrapod limbs, condensations and blastemata in skeletal development and regeneration, and mammalian tooth anlage as being as well characterized as the dorsal marginal zone. The last paper by Wagner, Chiu and Laubichler, resembles Arthur’s paper in that it informs the origin of

evolutionary innovations, and Bolker’s paper in that it informs the hierarchical approach in evo-devo (or developmental evolution, as Wagner et al., prefer to call the field). Wagner et al., include change in the level of selection as a category of evolutionary innovations and raise the important caution that developmental mechanisms continue to evolve after a character has originated. What value is there then, they ask, in analysis of developmental mechanisms in highly derived taxa when seeking the origins of the character? Like Mabee, they use the fin-limb transition to illustrate character definitions. They search in basal taxa for the origin of the novelty that is the tetrapod limb—the mesopodium/acropodium components of the autopod (the wrist/ankle elements 1 digits)—arguing that derived autopodial elements of more recent taxa are less informative, perhaps even uninformative, concerning the origin of the novel feature. If Mabee is describing the evolution of developmental mechanisms after the origin of the characters, and not mechanisms associated with the origin of the characters, then her conclusions of non-homology of skeletal elements may be premature. Again we see, as in so many of the papers presented, that assessment of homology is crucially important when interpreting patterns of evolution and when identifying the developmental mechanisms underlying character evolution. The symposium and resulting papers provide an informative overview of paradigms, problems and prospects in evo-devo. The historical approach shows how echoes of the past become rallying cries for the future. A consequence of the historical approach, however, is that the papers contain little on genes or on molecular approaches to evo-devo, Mabee and Wagner et al., being exceptions. However, if read in conjunction with three other SICB symposia also published in American Zoologist (Martindale and Swalla, 1998; McHugh and Hylanch, 1998; Olsson and Hall, 1999), the reader will see why evo-devo is such an exciting field of contemporary biology and how evo-devo or eco-evo-devo promises to integrate genetics, development, ecology and evolution, completing the task begun by de Beer, Goldschmidt, Waddington and the other developmental evolutionists who pioneered the field. REFERENCES Beurton, P. J., R. Falk, and H.-J. Rheinberger. (eds.) 2000. The concept of the gene in development and evolution: Historical and epistemological perspectives. Cambridge University Press, Cambridge. de Beer, G. R. 1954. Embryos and ancestors. Rev. ed. Clarendon Press, Oxford. De Robertis, E. and J. Arechaga. (eds.) 2001. ‘‘The Spemann-Mangold Organizer’’ 75 Years On. Int. J. Devel. Biol. Special Issue 45(1):1–378. Dietrich, M. R. 2000. From gene to genetic hierarchy: Richard Goldschmidt and the problem of the gene. In P. J. Beurton, R. Falk, and H.-J. Rheinberger (eds.), The concept of the gene in development and evolution: Historical and epistemological perspectives, pp. 91–114. Cambridge University Press, Cambridge.

COMMENTARY Dobzhansky, Th. 1940. Catastrophism versus evolutionism. Science 92:356–348. Gould, S. J. 1982. Introduction to reissue of The Material Basis of Evolution by Richard Goldschmidt, Pp. xiii–xlii. Yale University Press, New Haven and London. Hall, B. K. 2001. The gene is not dead, merely orphaned and seeking a home. Evol. Devel. 3:225– 228. Martindale, M. O. and B. J. Swalla. (eds.) 1998. The evolution of development: Patterns and process. A symposium. Amer. Zool. 38:591–684. McHugh, D. and K. Hylanch. (eds.) 1998. Evolutionary relationships of metazoan phyla: Advances, problems, and approaches. Amer. Zool. 38:813– 988. Olsson, L. and B. K. Hall. (eds.) 1999. Development and evolutionary perspectives on major transformations in body organization. A symposium. Amer. Zool. 39:612–694.


Raff, R. A. and T. C. Kaufman. 1983. Embryos, genes and evolution: The developmental-genetic basis of evolutionary change. Macmillan, New York. Robert, J. R., B. K. Hall, and W. M. Olson. 2001. Bridging the gap between developmental systems theory and evolutionary developmental biology. BioEssays 23:954–962. Rutherford, S. L. and S. Lindquist. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336–342. ¨ ber Indukiton Spemann, H. and H. Mangold. 1924. U von Embryonalanlagen durch Implantation artfremder Organisatoren. Wilhelm Roux’ Arch. Entwicklungsmech, Organ 100:599–638. Templeton. A. R. 1982. Why read Goldschmidt? Paleobiology 8:474–481. BRIAN K. HALL Department of Biology Dalhousie University Halifax NS Canada B3H 4J1 E-mail: [email protected]