© 2004 by The Society for Integrative and Comparative Biology
Patterns and Processes in the Evolution of Fishes: An Introduction to the Symposium1
1 Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, M5S 3G5, Canada
2 Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen's Park, Toronto, M5S 2C6, Canada
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Researchers often tend to overlook the fact that about 98% of the biosphere is made up of salt- or freshwater ecosystems. Thus it is no surprise that we normally tend to underestimate the importance and the diversity of the biota that exists in aquatic environments. In such environments several taxa have filled all types of ecological niches creating an incredible diversity in forms and shapes. One of these groups is what we call "fish." All vertebrates with the exception of the tetrapods are part of this paraphyletic association, which is characterized by a phenomenal diversity in morphology and physiology. Furthermore, because fishes generally represent the dominant component of the animal biomass, and are the top predators, in virtually every aquatic ecosystem, they are a key ecological player, and have had an extremely important role in the evolution of aquatic ecosystems during the last half billion years. Furthermore, and of greater relevance for our own species, they have played a very significant role in human history by representing a relatively accessible and abundant source of food.
Historically, many aspects of fish evolution have been neglected or less studied than tetrapods, certainly to a large extent due to the difficulty of making experimental observations in aquatic environments. Even from a purely taxonomic point of view we have to deal with a much greater uncertainty regarding the existing number of fish species compared to birds, mammals or reptiles, even though the fish taxonomic community has in the last few years made great progress thanks to a series of international initiatives, such as FISHBASE (Froese and Pauly, 2002
), checklists and taxonomic inventories. Even the phylogenetic relationships among the main fish lineages, and often within these (such as for example within the Percomorpha, the "bush at the top" of the phylogeny of teleost fishes) are still generally "cloudy." One of the major problems is the large number of taxa within the most species-rich fish clades, such as 16,000+ species of Acanthomorpha and over 6,000 species of Ostariophysi (Froese and Pauly, 2002) compared to only about 4,000 species of mammals and 9,500 species of birds. The very high incidence of homoplasy among morphological features of fish anatomy, due perhaps to the mechanical constraints imposed by a lifestyle in a fluid medium, and the still relatively limited inclusion of fossil materials in phylogenetic analyses of morphological data—this is true mostly for the higher teleosts, for more basal lineages see for example Arratia and Schultze (1999); Grande and Bemis (1998); Stiassny et al. (1996)— prevent us from obtaining a comprehensive picture of fish phylogenetic relationships using morphological data. The first large scale molecular phylogenies (with close to, or over, 100 taxa) have also appeared only very recently (Miya et al., 2003; Chen et al., 2003). These works, however, while providing support for some of the ‘historical’ clades, are also proposing sister-group relationships virtually never suggested before by comparative morphologists, such as the Zeiformes (dories and allies)-Gadiiformes (cods and hakes) clade. It is a matter of debate if some of these recent and somewhat contentious hypotheses will be corroborated by future analyses, but we believe that the appearance of these explicit molecular hypotheses is forcing comparative morphologists to critically re-evaluate some of the previous works, and will ultimately lead to a much better understanding of the phylogeny of "fishes." We hope that the progress in understanding the phylogenetic patterns of fish evolution will be fast, because it is upon this that much additional research into the processes that have shaped the history of these animals depends.
Among other disciplines the situation is similarly mixed: while some, such as functional morphology, traditionally owe much of their development to the action of fish biologists, others, such as developmental biology and genomics have historically relied on the study of other taxa. Most developmental biology textbooks published until the early 1990s do not have any example of development in fish, or barely mention a few studies in zebrafish, clearly different to the wealth of information available at the time on amphibians, reptiles and mammals.
Things, however, are changing fast. For example, the zebrafish, Danio rerio, has recently and rapidly become a model for various fields, such as neurobiology and embryology, with hundreds of researchers attending the meetings of the zebrafish conference series. Similarly, while large scale projects to sequence genomes got their start in the mid 1980s with the human genome project, most of the early work was devoted to traditional model organisms such as C. elegans, Drosophila melanogaster and Mus musculus, with little to no attention to fishes. More recently two species of teleost fishes, the pufferfish Takifugu rubripes and Tetraodon nigroviridis, have become the second and third vertebrate taxa to have their complete genome sequenced (Aparicio et al., 2002), with several other fish species such as the stickleback, Gasterosteus aculeatus, and the zebrafish also scheduled for sequencing of their complete genome. These fish genomes are proving to be key taxa in our attempts to interpret the evolution and functioning of our very genome (Hedges and Kumar, 2002). So in just a few years, fish genomics has moved from being a little developed area of research to being one of the main components in one of the most rapidly growing disciplines of biology, even though many other ichthyological disciplines (such as systematics and comparative morphology) have not yet really started to take advantage of the flow of data that these fish genome projects are now producing.
This situation stems, in our opinion, at least in part from the little interaction that has so far existed between workers in different disciplines, such as systematics, ecology, genomics, developmental biology, just to name a few. Traditionally these various categories of workers have kept working in isolation from one another, often having little interaction with other groups of investigators that may have been working on similar problems but with different approaches.
Due to our personal backgrounds (F.S., an ecosystems ecologist who later converted into a systematist, and G.Y., a geneticist who is also doing systematics and biogeography), we became keenly aware of the difficulty of interacting with people who may be interested in similar biological problems, but with a different perspective, a situation that permeates our academic environment especially in an age of extreme specialization. It was this awareness that prompted us to put together the proposal for the symposium, and to submit it to the Society for Integrative and Comparative Biology, which has made its mission to foster collaborative and integrative approaches to study the evolution of life. We believe that attempts to bring together workers from different disciplines who work on similar questions using very different approaches, and helping them to start a line of dialogue are of paramount importance, especially now that things are changing rapidly in many areas of ichthyologic research.
Fish biologists are now living in exciting times, and it is more important than ever that the exchange of information across various disciplines is fostered and encouraged. We hope to have given a small contribution to such a process with this symposium on "patterns and processes in the evolution of fishes" that took place in January 2003 during the annual meeting of SICB in Toronto, and that the collection of papers that follows, will illustrate the importance of integrative approaches.
The first series of papers deals with historical (i.e., paleontological and phylogenetic) patterns of fish evolutions. These deal with fish phylogenetics spanning across morphological methodologies (papers by Parenti and Grier, Santini and Tyler). In the second part of this issue the papers discuss evolutionary processes in areas such as development and genomics (papers by Lovejoy et al., and by Stellwag), functional morphology (paper by Westneat), and rules of assembly and structure of communities (paper by Sale).
Obviously, much still remains to be done. We are aware that this symposium is only a first step in a long journey. However, we hope that new interactions among researchers in these different fields will start to produce their first fruits in an early future.
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ACKNOWLEDGMENTS |
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The symposium on "Patterns and processes in the evolution of fishes," received financial support from the Society for Integrative and Comparative Biology, and the divisions of Systematics and Evolutionary Biology, Vertebrate Morphology, Evolutionary Developmental Biology and Ecology and Evolution of SICB, and from the Department of Zoology of the University of Toronto. A number of people helped us with various aspects of the organizations, and we especially wish to thank Donald Swiderski, program officer of DSEB, and Stacia Sower, program officer of SICB.
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FOOTNOTES |
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1 From the Symposium Patterns and Processes in the Evolution of Fishes presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
2 Author for correspondence; E-mail: gybazeta{at}zoo.utoronto.ca
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References |
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Aparicio, S., J. Chapman, E. Stupk, N. Putnam, J. M. Chia, P. Dehal, A. Christoffels, S. Rash, S. Hoon, and A. Smit.et al. 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science, 297:1301-1310.
Arratia, G., and H.-P. Schultze. 1999. Mesozoic fishes 2—systematics and fossil record. Verlag Dr. Friedrich Pfeil, München.
Chen, W.-J., C. Bonillo, and G. Lecointre. 2003. Repeatability of clades as a criterion of reliability: A case study for molecular phylogeny of Acanthomorpha (Teleostei) with larger number of taxa. Mol. Phyl. Evol, 26:262-288.[CrossRef][Web of Science][Medline]
Froese, R., and D. Pauly. 2002. FISHBASE. World Wide Web electronic publication. www.fishbase.org, version 26/12/2002.
Grande, L., and W. E. Bemis. 1998. A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. Supplement, J. Vert. Paleont, 18:1-690.
Hedges, S. B., and S. Kumar. 2002. Genomics: Vertebrate genomes compared. Science, 297:1283-1285.
Miya, M., H. Takeshima, H. Endo, N. B. Ishiguro, J. G. Inoue, T. Mukai, T. P. Satoh, M. Yamaguchi, A. Kawaguchi, K. Mabuchi, S. M. Shirai, and M. Nishida. 2003. Major patterns of higher teleostean phylogenies: A new perspective based on 100 complete mitochondrial DNA sequences. Mol. Phyl. Evol, 26:121-138.[CrossRef][Web of Science][Medline]
Stiassny, M., L. Parenti, and G. D. Johnson. 1996. Interrelationships of fishes. Academic Press, San Diego.
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