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What Is Metamorphosis? C Integrative and Comparative Biology Advance Access published June 6, 2006 1of7 What is metamorphosis? C. D. Bishop,* D. F. Erezyilmaz,y T. Flatt,z C. D. Georgiou,§ M. G. Hadfield,* A. Heyland,¶,** J. Hodin,1,yy M. W. Jacobs,y,** S. A. Maslakova,** A. Pires,zz A. M. Reitzel,§§ S. Santagata,**,¶¶ K. Tanakay and J. H. Youson*** *Kewalo Marine Laboratory, University of Hawaii, Honolulu, HI, USA; yDepartment of Biology, University of Washington, Seattle, WA, USA; zDepartment of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island, USA; §Biology Department, University of Patras, Patras, Greece; ¶Whitney Laboratory for Marine Biosciences, University of Florida, St Augustine, FL, USA; **Friday Harbor Laboratories, University of Washington, Friday Harbor, WA, USA; yyHopkins Marine Station, Stanford University, Pacific Grove, CA, USA; zzDepartment of Biology, Dickinson College, Carlisle, PA, USA; §§Department of Biology, Boston University, Boston, MA, USA; ¶¶Smithsonian Marine Station, Fort Pierce, FL, USA; ***Department of Zoology, University of Toronto, Toronto, ON, Canada Synopsis Metamorphosis (Gr. meta- “change” þ morphe “form”) as a biological process is generally attributed to a subset of animals: most famously insects and amphibians, but some fish and many marine invertebrates as well. We held a symposium at the 2006 Society for Integrative and Comparative Biology (SICB) annual meeting in Orlando, FL (USA) to discuss metamorphosis in a comparative context. Specifically, we considered the possibility that the term “metamorphosis” could be rightly applied to non-animals as well, including fungi, flowering plants, and some marine algae. Clearly, the answer depends upon how metamorphosis is defined. As we participants differed (sometimes quite substantially) in how we defined the term, we decided to present each of our conceptions of metamorphosis in 1 place, rather than attempting to agree on a single consensus definition. Herein we have gathered together our various definitions of metamorphosis, and offer an analysis that highlights some of the main similarities and differences among them. We present this article not only as an introduction to this symposium volume, but also as a reference tool that can be used by others interested in metamorphosis. Ultimately, we hope that this article—and the volume as a whole—will represent a springboard for further investigations into the surprisingly deep mechanistic similarities among independently evolved life cycle transitions across kingdoms. Introduction Metamorphosis is an inherently integrative concept, transitions across taxa, do we see any superficial with relevance to developmental biology, ecology, and/or deep parallels in the underlying signaling sys- life history evolution, physiology, cell biology, and tems that regulate these disparate life-cycle transitions? even conservation biology. Although most people are Why has metamorphosis apparently evolved repeatedly in agreement about a general conception that meta- in the history of multicellular life? The various articles morphosis represents a transformation of some sort in this volume represent an attempt to frame answers (think caterpillar to butterfly), there is little agreement to these questions, if not to address them specifically. on the specifics. In early January 2006, we gathered Still, it is clear that the diversity of views of metamor- in Orlando, FL (USA) to discuss metamorphosis in phosis is arguably comparable in scope to the diversity a comparative context. Our goal was to address— of organisms that undergo such life-cycle transitions. through platform talks, contributed articles, posters, Therefore, we did not intend, nor did we produce, and organized and informal discussions, as well as a consensus answers to the questions we posed above. Web site forum—the following questions: What is It has been suggested (see Michael Hadfield’s defini- metamorphosis? Is it specific to animals, or can the tion, below) that the meaning of the term term be rightly applied to life-cycle transitions “metamorphosis” should be defined before proceeding in non-animal groups? When comparing indepen- to use it. In that spirit, we here present our various dently evolved metamorphic (or metamorphic-like) views on metamorphosis, in many cases influenced in From the symposium “Metamorphosis: A Multikingdom Approach” presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida. 1 E-mail: [email protected]. All authors contributed equally and are listed alphabetically by surname. Integrative and Comparative Biology, pp. 1–7 doi:10.1093/icb/icl004 Ó The Author 2006. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 2of7 Table 1 Summary of the various conceptions of metamorphosis presented here Usually pre- Transition Major Change in Change Pre metamorphic reproductive is generally Is plant Habitat morphological adaptive in feeding stage is post- to reproductive hormone- flowering Author shift change landscape Rapid mode embryonic stage transition regulated metamorphic? Cory Bishop X X X Yes Deniz Erezyilmaz X 1 X X X Yes Thomas Flatt X X X X X X No Christos Georgiou X X X Yes Michael Hadfield X X X X X No Andreas Heyland X X X X X X X No Jason Hodin X X X X X X X Yes Molly Jacobs X X X Xa Xa Xa No Svetlana Maslakova X X X X X No Tony Pires X X3 XX No Adam Reitzel X X X X X No Scott Santagata X X4 XX No Kohtaro Tanaka X X X X Yes5 John Youson X X X X X X X No6 “X” indicates that the author considers the feature in question (see column headings) to be a key element of (that is, a proposition that is generally true about) metamorphosis. Blanks indicate that those features are not considered by the author to be integral to metamorphosis. As a way of addressing the applicability of metamorphosis across kingdoms, each author responded to the following question: “Is the vegetative to flower transition in angiosperms an example of metamorphosis?” (last column). 1Deniz Erezyilmaz supports the idea that metamorphosis represents a shift from an adaptive peak to another, without involving a change in the adaptive landscape itself. 2Molly Jacobs notes that 3 of the features selected—rapid transition, change in feeding mode, and that the pre-metamorphic stage is post-embryonic—are often but not always true of metamorphoses across taxa. 3Tony Pires notes that the change in adaptive landscape is more accurately described as the selective pressure driving the evolution of metamorphosis rather than a feature of metamorphosis sensu stricto. 4Scott Santagata notes that major morphological changes can also occur gradually in a series of smaller steps from the “larval” stage to the juvenile form. This can still be considered a type of metamorphosis and not direct development as long as there is a change in adaptive landscape between stages. 5Kohtaro Tanaka notes that plant flowering should be considered metamorphic (or metamorphic-like), even though it does not involve habitat shifts, and morphological changes occur C. D. Bishop only in parts of individual plants. Given their lack of mobility and the way they develop, this is the only way plants can carry out the type of change analogous to metamorphosis in animals. 6John Youson notes that flowering in angiosperms does share some similarities with animal metamorphosis. et al. What is metamorphosis? 3of7 their specifics by our attendance at the 2006 symposium. different the 2 forms should be to constitute a meta- By way of summary, we present a table (Table 1) indi- morphosis seems to be a matter of degree. Insects, for cating the common and unique aspects of these various instance, utilize one of 3 different life history strategies. definitions. Our hope is that this collection of thoughts, Holometabolous insects such as flies and moths have in combination with the other symposium articles in complete metamorphosis, while hemimetabolous this volume, will not only provide useful tools for other insects, such as crickets and grasshoppers merely researchers with similar interests, but also point the way gain functional wings and genitalia at the final molt. to a detailed research program, integrative both disci- This latter group also includes more “radical” hemi- plinarily and taxonomically, to investigate the impor- metabolous insects such as the dragonflies; although tance of key transitions in organismal life cycles. their larval forms are aquatic, their overall develop- ment more closely resembles that of other hemimeta- Definitions bolous insects. Ametabolous insects such as the firebrat, are truly direct developers, with the adult dis- Cory Bishop tinguished only by size and genitalia. Similar to most Metamorphosis, loosely conceived, is a component of entomologists, I consider insects of the monophyletic organismal ontogeny. In considering this symposium, Holometabola to be truly metamorphic. However, the I think it is appropriate to transcend arbitrary or exclu- field of insect physiology has shown that the same sive definitions of metamorphosis based on: (1) the machinery that is used during complete metamorpho- extent of specific and overt changes in morphology sis of flies and moths is also used to produce the poly- or ecological parameters and (2) larval type. Thus, morphisms and heteromorphoses of hemimetabolous I define metamorphosis, in the broadest sense, as a insects. Therefore, on a fundamental level, the differ- transition between vegetative and sexually reproductive ence between these broad groups of insects is the extent multicellular stages of a life history. This definition to which this “metamorphosis machinery” is deployed. serves to describe a process by which post-embryonic In my opinion, we can make more meaningful descrip- life cycle phases that are not sexually reproductive, but tions of metamorphosis by comparing the activity of whose existence is selected to increase reproductive this shared machinery between the 2 groups. success, make a transition into a form or stage that is reproductive, within a single life cycle.
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