AMER. ZOOL., 40:455–460 (2000)
The Evolutionary Origin of Feathers: A Problem Demanding Interdisciplinary Communication1 PAUL F. A. MADERSON2,*AND DOMINIQUE G. HOMBERGER3,† *Department of Biology, Brooklyn College of CUNY, Brooklyn, New York 11210, and †Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803-1715
THE ORIGINS
OF
THIS SYMPOSIUM
The last contributed paper in the last session of the Division of Vertebrate Morphology on the last day of the SICB meeting in December 1995 reevaluated the longstanding problem of how feathers move (see Homberger and de Silva, 1995). Dominique Homberger’s interpretation of the involvement of the extensive cutaneous and subcutaneous fat as a hydraulic skeleton in this context was most intriguing to Gopi Menon and Paul Maderson. This adipose tissue was one of many puzzling features of sauropsid (sensu Laurin and Reisz, 1995: 180) skin that had attracted their attention during the writing of a paper on avian cutaneous water loss (see Menon et al., 1996). Two realizations emerged from considering the observations in these papers. First, available data imply that, in many aspects, avian skin resembles that of reptiles more than that of mammals. Second, there are surprising gaps in our knowledge of the structure, function, and physiology of avian skin, and the absence of critical data leaves several fundamental issues unresolved. As the three of us shared our interest in, and passion for, the functional and evolutionary morphology of the sauropsid integument, Dominique Homberger suggested that avian skin would make an ideal focus for a symposium, a theme that had never been entertained before. Over the next 15 months we contacted persons interested in joining us in an interdisciplinary analysis of the sauropsid integument built around the theme of ‘‘the evo1 From the Symposium Evolutionary Origin of Feathers presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 6–10 January 1999, at Denver, Colorado. 2 E-mail: maderson@brooklyn.cuny.edu 3 E-mail: zodhomb@lsu.edu
lutionary origin of feathers.’’ Throughout that same period, there were numerous allusions to feathered dinosaurs in the media (e.g., Browne, 1996; Arthur, 1998; Nuttall, 1998). Sinosauropteryx became the avatar of the renaissance of interest in dinosaurs on the dust cover of Currie and Padian’s (1997) Encyclopedia, and its integument was the focus of debate in the Journal of Vertebrate Paleontology (Unwin, 1998). The concomitant publication of reviews, pro and con, of Feduccia’s (1996) book on avian biology further indicated that ours was a ‘‘hot’’ topic that would continue to ‘‘fly’’ in the foreseeable future. These developments provided additional support for our idea of an interdisciplinary and integrating symposium, since we were aware of the dearth of data concerning the structure and function of the integument of extant sauropsids and were keenly interested in the many opinions expressed by paleontologists concerning the physiological, adaptive, ecological and evolutionary significance of feathers. THREE INTER-RELATED PROBLEMS: THE SYSTEMATICS OF SAUROPSIDS, THE EVOLUTION OF AVIAN FLIGHT AND THE ORIGIN OF FEATHERS From our earliest discussion, we had been aware that our symposium would have to deal with two related, yet separate issues in addition to the issue of the evolutionary origin of feathers, namely the evolutionary origin of birds and the evolutionary origin of avian flight. The three issues are inextricably linked, because both the concept of birds and the unique mechanism of avian flight are dependent on the presence of feathers. The issue of the evolutionary origin of birds is complicated by the fact that birds did not ‘‘originate’’ in the true sense of the
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word, but evolved gradually through relatively minor, selectively advantageous structural and functional modifications from a ‘‘reptilian’’ (i.e., non-avian) ancestor. This evolutionary development, however, needs to be divided into a reptilian and an avian phase by an artificial dividing line in order to classify fossil and extant taxa as either birds or reptiles. The dividing line has traditionally been defined by the presence or absence of feathers. However, feathers did most probably not spring into existence fully developed, such as contour feathers, for example, but more likely developed gradually from simpler integumentary precursors (see for example, Jones et al., 2000). Thus, as a matter of definition, the evolutionary origin of feathers is not necessarily congruent with that of birds and may have predated it. The issue of the evolutionary origin of avian flight, in turn, is complicated by the fact that the first birds (i.e., feathered vertebrates) may not necessarily have had the capacity for fully powered flight, because the earliest feathers were unlikely to have been specialized flight feathers. Thus, as a matter of definition, the evolutionary origin of avian flight is not necessarily congruent with the origins of birds or feathers and may have followed both. The issue of the evolutionary origin of feathers, finally, is complicated by the fact that the evolutionary origin of structural modifications is generally based on an interplay of two distinct mechanisms: variation arising from genetic and epigenetic processes and selection operating on the emergent phenotypic characters. Questions concerning the former mechanism lie in the domain of developmental genetics, while questions concerning the latter lie in the domain of evolutionary biology. Thus, a complete understanding of the evolutionary origin of feathers needs to be approached through at least two different research avenues that rely on different types of data and information as evidence for their analyses. Theories of feather origins, however, have generally suffered from a relatively weak database. And although it has been alluded to en passant in a variety of con-
texts (see references in Schultze and Trueb, 1991; Ruben, 1995; Feduccia, 1996), the problem of feather origins per se has been addressed in relatively few publications. The historical reason for this is that knowledge of all aspects of skin biology of sauropsids has lagged behind that of mammals (see chapters in Bereiter-Hahn et al., 1986). Most biologists, awed by the flood of reports on the integument of the domestic chicken in the primary literature of developmental biology (see references in Chuong, 1998), are unaware of the many unanswered questions documented by Lucas and Stettenheim (1972). Nevertheless, during the quarter century since Lucas and Stettenheim’s (1972) encyclopedic treatment of the avian integument and Regal’s (1975) attempt to discuss feather origins within an appropriately broad framework, many relevant data concerning the sauropsid integument have emerged dealing with its functional morphology, physiology, development, and fossil preservation, as well as with the molecular biology of integumentary lipids and keratins. But the very diversity of these data presents a problem, as it is difficult for biologists to keep abreast of specialized information that may be relevant to their particular research interests, but lies outside their expertise. Thus, given the continuing fragmentation of Biology along disciplinary lines, it is timely and important to create opportunities, such as a symposium, for specialists to come together to evaluate, explore, and discuss topics that may serve as focal points for new integrations and syntheses. As there is currently widespread interest in dinosaurs, and as the possibility of at least some of them having been feathered is being seriously discussed, new research into any aspect of sauropsid skin biology is timely and necessary. In this context, a symposium with a focus on feathers and, thus, on the sauropsid integument would serve an important function in bringing together the latest specialized information and arguments that need to be considered for a complete understanding of the evolutionary history of feathers, birds, and avian flight: It would provide an overview of what is presently known and act as a departing point for new
FEATHER SYMPOSIUM INTRODUCTION and fresh research projects. SICB is nowadays perhaps the only organization that can, and does, provide the means for organizing such a symposium. A BRIEF OVERVIEW OF THE CURRENT ISSUES REGARDING THE EVOLUTIONARY ORIGINS OF FEATHERS, BIRDS, AND AVIAN FLIGHT Our symposium appears to be timely for yet another reason. The last two decades, in particular, have been a time during which fundamental questions concerning the methodology of evolutionary biology have been discussed intensely. During the very same time period, for a variety of reasons, the problem of the evolutionary origin of birds has become one of the most-discussed questions in vertebrate evolutionary biology. Both topics have become entangled in recent times. The following brief, necessarily simplified and generalized review is intended to provide some clarifications of the historical and scientific issues lying at the heart of the current discussions concerning the evolutionary origin of birds, feathers, and avian flight. Further discussions and specific references can be found in Hecht et al. (1985) and in the various contributions to this symposium. Because the first fossil specimens of Archaeopteryx lithographica were discovered shortly after Darwin’s publication of The Origin of Species (1859), it was almost a given that Archaeopteryx would become a touchstone for the validity of the Theory of Evolution. Archaeopteryx was seen as a typical representative of a ‘‘missing link’’ which had been postulated by Darwin (1859) to support his prediction that certain taxa, such as birds, could have evolved from other major taxa, such as reptiles. Archaeopteryx consists of a mosaic of ancestral reptilian and derived avian characters. The latter include feathers, and it was on the basis of these that Archaeopteryx was defined as a bird. Practically also from the moment of the discovery of Archaeopteryx, which at that time was considered to be an ancestral bird, the search for its reptilian ancestor was on. Essentially from its very beginnings, this search was pursued through two different avenues. One research avenue consists mainly of
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a search among fossils to find reptiles sensu lato that would show morphological similarities to Archaeopteryx. In this approach, morphological similarity is interpreted as evidence of shared genetic information and, thus, of phylogenetic relationship. With the widespread acceptance of the cladistic, or phylogenetic, methodology of classification about three decades ago, the degrees of phenotypic similarity between extant birds and particular fossils could be established with a certain objectivity. One of the earliest practitioners of this approach for the question of avian ancestry was Thomas Huxley (1868a, b), who described the morphological similarities between certain dinosaurs and birds, and who proposed that birds might have evolved from dinosaurs. This idea was revived by John Ostrom (e.g., 1974, 1986) and has found many supporters since then, especially among biologists with an interest in vertebrate paleontology. The other research avenue towards elucidating the ancestry of birds consists mainly of a search among extant reptiles and other vertebrates to provide models for an avian ancestor, whose functional morphology, behavior, and ecology would have allowed it to have become gradually evolutionarily modified into an avian organism. This approach seeks to reconstruct the actual evolutionary history by applying known evolutionary mechanisms to create a scenario of morphological, behavioral and ecological transformations. Practitioners of this approach are aware that many phenotypic similarities may be the result of convergent evolution due to similar selective regimes and, therefore, try to discriminate between homologous and convergent similarities. Two of the earliest practitioners of this approach for the question of avian ancestry were Otto Abel (1910) and Friedrich von Huene (1914), who proposed an archosaurian ancestry for birds. Subsequently, a number of scientists with an interest in ornithology, functional morphology, or ecology have used this approach. Because the evolutionary origin of birds is so intimately connected to the evolutionary origin of feathers, scientists who deal with the question of avian ancestry almost always also deal with the evolutionary or-
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igin of feathers or with the functional and ecological reasons for the selective advantage of feathers. Among the various functions of feathers, two stand out and have been the focus of various evolutionary scenarios: Aerial locomotion and thermal insulation. The idea of a primary selective regime that favored the evolution of feathers as thermal insulators and, thus, as a precondition for the evolution of avian endothermy-homoiothermy is supported mainly, though not exclusively, by scientists who favor a terrestrial dinosaurian ancestry of birds. In contrast, the idea of a primary selective regime that favored the evolution of feathers as supporting aerial locomotion and, thus, as a precondition for avian flight is supported mainly, though not exclusively, by scientists who favor an arboreal archosaurian ancestry of birds. However, as our symposium with its sixteen contributions by representatives of various specialized research fields shows, the two avenues towards understanding avian ancestry are not necessarily mutually exclusive (for a review of the theoretical issues, see Homberger, 2000). This realization may be one of the more significant contributions of our symposium as it may prepare the ground for a less polarized discussion of the issues and for a more problem-oriented discourse focused on finding solutions. Perhaps the best approach towards finding a complete understanding of the unique historical event of the evolution of birds, feathers, and avian flight would be a combination of both approaches: A reconstruction of the evolutionary history based on known evolutionary mechanisms of morphological, behavioral and ecological change as well as a continuing search for fossil evidence for the evolutionary history of birds. IMPROVING THE DATA BASE Our symposium brings together biologists with diverse interests. The order of their papers follows the logical sequence of the platform presentations with each contribution building on those preceding it. In his overview of avian skin morphology, Peter Stettenheim emphasizes that birds are not simply ‘‘covered with feathers.’’ Walter
Bock reviews previous theories of feather origins. Such theories are placed in the context of current systematic opinion regarding the relationships of amniotes in general by Stuart Sumida and Christopher Brochu, and archosaurs-birds in particular by Peter Dodson. Both papers elucidate the value of, and controversies generated by, cladistic methodology. Aspects of developmental biology, one of the traditional sources of morphological data for considering the problem of feather evolution, is reviewed by Paul Maderson and Lorenzo Alibardi. The reviews of scale and feather keratins by Roger Sawyer and his co-workers, and of epidermal lipids and their role in controlling cutaneous water loss by Gopi Menon and Jaishri Menon, lay the foundations for discussing the functional morphology of the avian integument. Dominique Homberger and Kumudini de Silva document the anatomical basis of controlled maneuverability of feathers, which is a more complex motion than piloerection in mammals, and explore the problems associated with its role in the evolution of birds and avian flight. Their treatment puts into a broader context Blair Wolff and Glenn Walsberg’s exploration of the significance of the plumage in heat transfer, a phenomenon wherein we see the complex interaction between control of water balance and thermoregulation. Concepts from these papers are critical to an understanding of the evolution of endothermy, and how its presence or absence might reasonably be assessed in extinct forms. John Ruben and Terry Jones evaluate these problems from a paleontological viewpoint, while Warren Porter and his colleagues offer a physiological-ecological perspective. Against this background, Alan Brush explores the form of a ‘‘proto-feather’’— whatever its inferred, primary functional role may have been. A review of inferred locomotory behaviors of dinosaurs, large and small, by James Farlow and his colleagues, permits Nicholas Geist and Alan Feduccia to compare such behaviors with those observable in extant, volant, tetrapod species. Following an analysis of the aerodynamic constraints on integumentary form by Sam Tarsitano and his colleagues, Larry Martin and Steve Czerkas evaluate the form
FEATHER SYMPOSIUM INTRODUCTION of integumentary remains in recently described fossils. The accommodation of many speakers into the program necessitated restricting questions to a formal discussion period that was recorded on tape. The transcribed text forms the basis of the multi-authored report of the views expressed during the discussion. We are particularly pleased to include extensive comments by Phil Currie. We had two further goals in confining discussion of conflicting interpretations and views to this final report. The first is that the published proceedings would be seen not merely as a loose collection of papers, but as a whole expressing a unity of purpose and style— though not of opinion—and would, thus, provide a balanced view of the relevant issues. The second is to spotlight specific, definable issues that will be the focus of future research. POSSIBLE FUTURE DIRECTIONS OF RESEARCH From our vantage points as symposium organizers and editors, we can identify several areas and questions from which relevant new data could emerge in the future. Within paleontology, we venture to recommend three items: (1) the long-ignored ‘‘basal archosaur’’ Longisquama (Sharov, 1972) needs to be re-evaluated; (2) techniques for the specific identification of feather keratins in fossil specimens (see Davis and Briggs, 1995) should be applied in general to provide clear criteria for the identification of fossil feather-like structures; and (3) the basic structure of the avian and reptilian integument needs to be kept in mind by paleontologists trying to interpret fossil skin specimens. Within developmental biology and genetics we point to the following three problems demanding attention: (1) the relationship between the hexagonal spacing so often seen in embryonic primordia (Chuong, 1998) and the essentially rhomboid arrangements of feather follicles defined by feather muscles (Lucas and Stettenheim, 1972); (2) the embryonic and evolutionary development of the smooth, autonomically innervated feather muscles and the striated, somatically innervated cutaneous musculature; and (3) the question whether cell death, sensu apopto-
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sis, actually ‘‘carve out’’ the barbs and barb ridges during feather development, or whether the reports of the molecular identification of genes responsible for cell death (Chuong, 1998) merely reflect fundamental characteristics of keratinocyte differentiation. Finally, within functional morphology, three recommendations can be made: (1) aerodynamic studies on birds should include species that use flap-bounding flight; (2) future studies on the locomotion of reptiles should include species that jump ballistically; and (3) the notion that ‘‘everything is already known in anatomy’’ needs to be revised and replaced by a more enlightened understanding of the unending frontier in science. ACKNOWLEDGMENTS Many colleagues, in addition to our symposium participants, offered advice and ideas during the planning of our Symposium. The SICB staff, especially Ms. Wilma Salvatore, dealt most efficiently with logistical matters. Funding to support the Symposium came from NSF (Grant # IBN-9807168), from Alan Kohn, President of SICB, from John Wourms, Chair of the Division of Developmental and Cell Biology, and from Peter Wainwright, Chair of the Division of Vertebrate Morphology. We thank all for their much-appreciated contributions. REFERENCES Abel, O. 1911. Die Vorfahren der Vo¨gel und ihre Lebensweise. Verh. k.-k. zool.-bot. Ges. Wien 61 (7/ 8):144–191. Arthur, C. 1998. Dinosaurs got feathers to stay warm. The Independent, London, January 8th:14. Bereiter-Hahn, J., A. G. Matoltsy, and K. S. Richards. 1986. Biology of the Integument, Vol. 2, Vertebrates. Springer-Verlag, Berlin and New York. Browne, M. W. 1996. Feathery fossil hints dinosaurbird link. New York Times October 19th:1, 7. Chuong, C.-M. 1998. Molecular basis of epithelial appendage morphogenesis. R. G. Landes Company, Austin, Texas. Currie, P. J. and K. Padian. 1997. The encyclopedia of dinosaurs. Academic Press, San Diego. Darwin, C. 1859. The origin of species. John Murray, London. Davis, P. G. and D. E. G. Briggs. 1995. Fossilization of feathers. Geology 23:783–786. Feduccia, A. 1996. The origin and evolution of birds. Yale University Press, New Haven, Connecticut. Hecht, M. K., J. H. Ostrom, G. Viohl, and P. Wellnho-
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