Integrative and Comparative Biology Advance Access originally published online on July 15, 2006
Integrative and Comparative Biology 2006 46(5):569-576; doi:10.1093/icb/icl017
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Zebrafish in comparative context: A symposium
* Department of Biology, Villanova University Villanova, PA 19085, USA
Department of Developmental and Cell Biology, University of California Irvine, Irvine, CA 92697, USA
Correspondence: 1E-mail: jacqueline_webb{at}mail.uri.edu
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The Symposium "Zebrafish in Comparative Context" was organized to bring together two largely separate but highly complementary research traditions in order to make developmental and genetic information about a model species (Danio rerio, the zebrafish) more accessible to the comparative biology community. The meeting focused on the relationship of this model organism to other vertebrates (particularly other fishes) using a comparative and evolutionary approach. Topics included the phylogeny of cypriniform fishes, genome evolution, the evolution of gastrulation, dentition, pigmentation, craniofacial development, and nervous system structure and function. Participants also met informally to discuss ways to facilitate collaborative projects in areas of common interest and determine priorities for the development of shared resources. Continuing interactions between comparative biologists, with their extensive body of knowledge of morphological variation among fish species, and developmental biologists and geneticists working with model species such as the zebrafish will facilitate our understanding of the evolution of developmental patterns and processes in vertebrates.
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Introduction |
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The field of developmental biology relies on a small number of animal model species (Caenorhabditis elegans, Drosophila, zebrafish, Xenopus, chick, mouse) that may be experimentally and/or genetically manipulated to reveal patterns and mechanisms of development. These model species are sufficiently similar in fundamental genetic mechanisms of development that much of this work is transferable to the analysis of human development and disease (Shin and Fishman 2002
; North and Zon 2003). The reasons for choosing a particular model species may not be apparent and often reflect more practical considerations than its phylogenetic position (Bolker 1995). However, once the momentum has been established by a growing research community (for example, Rasooly and others 2003), the resources developed for a model species can be used to address a multitude of evolutionary questions when that species is placed in a phylogenetic context (Metscher and Ahlberg 1999).
The zebrafish research community, less than a generation old, is composed of scientists trained largely in the fields of developmental genetics and functional genomics (see www.zfin.org). The primary goal of their work is to use one species (Danio rerio) to define the genetic mechanisms underlying vertebrate development, in many cases with direct application to human health (de Jong and Zon 2005; Grabher and Look 2006). This important work has revealed fundamental mechanisms of embryonic vertebrate development and basic features of the early vertebrate body plan (Schier and Talbot 2005). It has also revealed genes whose functions have been highly conserved over millions of years that can provide important insights into the development of other fishes and other vertebrates. Mutational studies in zebrafish identify candidates for genes that may have changed their expression or function over evolutionary time resulting in adaptive phenotypic change in natural contexts. Nevertheless, the majority of work on zebrafish has been on embryonic lethal mutants that cannot address most issues of phylogenetic interest.
For more than a century, ichthyologists have studied development, morphology, taxonomy, systematics, physiology, and ecology in order to understand the structural and functional diversity among fishes (>29,000+ species; see www.fishbase.org) at all levels of biological organization. There is extensive literature on the development of a wide array of fish species (reviewed by Kunz 2004) and on the field identification and morphology of fish eggs and larvae (for example, Moser and others 1984; Moser 1996; Leis and Carson-Ewart 2004; Richards 2005), many of commercial importance in traditional fisheries. There has also been a renewed emphasis on the study of the early life history of fishes in the context of fish ecology, ichthyoplankton ecology and aquaculture. Evolutionary biologists have begun to (re)turn to development to shed light on patterns and processes in evolution (Raff 1996; McNamara 1997; Hall 1999; Wilkins 2002; Carroll and others 2005) and fishes have already begun to provide an important context for such studies (for example, stickleback Cresko and others 2004; Kimmel and others 2005; blind cavefish Jeffery 2001; cichlids Albertson and others 2003, 2005).
The need for robust hypotheses of phylogenetic relationships continues to present a major challenge for analyses of evolutionary change among fishes, since they are the most speciose group of vertebrates. The systematics community uses morphological characters in adult and larval fishes, as well as molecular characters to construct phylogenetic hypotheses (for example, Stiassny and others 1996; Kocher and Stepien 1997; Stiassny and others 2004), and large-scale phylogenies based on molecular characters are becoming increasingly available (for example, Inuoe and others 2001; Miya and others 2001).
Some researchers investigating the developmental genetics and functional morphology of fishes now seek to understand the molecular mechanisms underlying the evolution of form. Zebrafish work is uncovering the molecular basis for the development of specific actinopterygian and teleost features (for example, rayed fins, kinetic skulls, swim bladders), which will allow an assessment of their importance in the development and evolution of form among other cyprinids, cypriniforms, otophysans, teleosts, and fish species in general. However, given the different ultimate goals of the zebrafish and comparative biology communities (use of a model system to determine the genetic control of development in humans versus elucidation of patterns of evolution in structure and function, respectively) there have been very few opportunities for these communities to share their common understanding of the analysis of form and function in the context of development and evolution.
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The symposium |
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The symposium "Zebrafish in Comparative Context" was held on 5 and 6 January 2006 in Orlando, Florida, at the annual meeting of the Society for Integrative and Comparative Biology. The goal of the symposium was to address two questions: (1) how can a model species for developmental biology (that is, zebrafish) provide conceptual and methodological contexts for asking fundamental questions in comparative and evolutionary biology (a devo
evo approach) and (2) how can a comparative (phylogenetic) approach allow the formulation of hypotheses concerning evolution of mechanisms of vertebrate development that can be tested in a well-established model species such as zebrafish (an evo devo approach)? Thus, the symposium represented an important first step in making the vast amount of developmental and genetic information about the zebrafish model system more accessible to the comparative biology community and it served as a forum for discussing the relationship of a model organism to other fishes and other vertebrates using a comparative/evolutionary approach.
The zebrafish, D. rerio (the zebra danio) is a minnow, a member of the Family Cyprinidae and a member of the Otophysi, a group that represents 25% of all living fishes and 75% of all freshwater fishes. A well-defined phylogeny that illustrates the evolutionary relationships among related taxa is needed to determine the polarity of change in form, and by extension, the evolution of patterns and mechanisms of development among fishes. Recent comparative studies have led to a change in the taxonomy and phylogenetic placement of the zebrafish, with its genus (formerly Brachydanio) re-assigned to Danio, as sister group to Devario (Meyer and others 1993). With additional sequences from nearly 1000 cypriniform species, including D. rerio, Richard Mayden (Saint Louis University) has rejected this hypothesis of relationships and has hypothesized that Danio is in a sister clade to a clade including Chela, Microrasboras, Devario, and Inlecypris. He is building an online resource for information on the diversity and phylogeny of cypriniform fishes, through the NSF-funded Cypriniform Tree of Life Project (CToL; www.cypriniformes.org). Paula Mabee (University of South Dakota), another member of the CToL project, emphasized how the resources generated by the CToL initiative that will become an important means of sharing information between the zebrafish and comparative biology communities.
Once a robust phylogenetic tree is established, patterns of change in evolutionary time may be determined by mapping well-defined characters on that tree. Mark Cooper (University of Washington) described variation in gastrulation movements among different basal actinopterygian (ray-finned) fishes (for example, sturgeon and bowfin) that reveal how the process of gastrulation has evolved. Non-teleost fishes demonstrate a pattern in which the yolk cleaves, similar to that in amphibians, while the teleost mode of gastrulation in which the yolk remains uncleaved appears to be more derived. The large number of nuclei in the yolk syncytial layer, characteristic of zebrafish and its relatives, are likely an evolutionary remnant of the vegetal blastomeres of basal actinopterygian fishes (for example, sturgeon bichir bowfin Dean 1895; D'Amico and Cooper 2001). David Stock (University of Colorado) pointed out that while zebrafish and other cypriniform fishes lack oral teeth but develop pharyngeal teeth, the ancestral condition, as inferred from a phylogenetic out-group comparison, is the presence of both oral and pharyngeal teeth (Stock 2001). His laboratory has identified several changes in gene expression associated with loss of oral teeth in cypriniform fishes and is attempting to determine whether these are the consequence of one or multiple upstream genetic changes. The latter result would be consistent with a hypothesis that the loss of oral teeth was a constraint on the subsequent evolution of cypriniform feeding modes.
Dramatic changes in the craniofacial skeleton have occurred at major transitions in vertebrate and teleost evolution, and a phylogenetic approach and the analysis of a particularly rich collection of craniofacial mutants in zebrafish have begun to provide insights into the evolution of craniofacial development. Most cranial cartilage and bone is derived embryonically from the neural crest, and Tom Schilling (University of California at Irvine) has used mutant analysis to uncover novel regulators of neural crest migration and survival, which appear to have important roles in skeletal patterning (Knight and Schilling 2006). Chuck Kimmel (University of Oregon) has focused on mandibular patterning and has shown that secreted signals pattern skeletal elements along its dorsal–ventral axis. Kimmel showed that other teleost taxa differ from zebrafish in their skeletal morphology, including the number and arrangement of branchiostegal rays, thus providing some interesting comparisons with a diversity of both extant and extinct fish taxa. The mapping of morphological variants in stickleback populations has revealed prime candidates for genes evolved to control these phenotypic traits and that have been identified in embryonic zebrafish mutants (Kimmel and others 2005). Luz Patricia Hernandez (George Washington University) showed how cranial skeletal elements involved in feeding, and crucial to premaxillary protrusion during ontogeny (Hernandez 2000), vary among members of the order Cypriniformes, thus highlighting a functional morphological approach to developmental issues (Hernandez and others 2002).
Studies of the development of the nervous system have laid the groundwork for comparisons of both structure and function among species. The transparency of zebrafish embryos allows different neuronal cell types to be labeled in living embryos and monitored with single-cell patch-clamping methods. Joe Fetcho (Cornell University) described how his lab uses transgenic zebrafish to label a subset of interneurons within the spinal cord and has shown that they play a role in gating the responses of motor-neuron targets that function in locomotion (Masino and Fetcho 2005). This experimental approach provides an opportunity for the study of related species that demonstrate different behaviors (for example swimming and feeding). Vertebrates are bilaterally symmetrical in most respects with several notable exceptions along the left–right (L–R) axis. Marnie Halpern (Carnegie Institution) described L–R asymmetries in the zebrafish brain that affect a highly conserved neural projection from the diencephalon to the midbrain. Molecular and neuroanatomical asymmetries in the epithalamus involve the parapineal, a left-positioned accessory to the pineal organ, and bilateral habenular nuclei (Gamse and others 2003). Disruption of this asymmetry affects the pattern of habenular projections onto its midbrain target (Gamse and others 2005). Although the functional significance of this asymmetry remains to be determined, it is preserved in other fish species that show dramatic bilateral asymmetry, such as flatfishes (Y. S. Kuan and M. E. Halpern, unpublished data).
Methods for the analysis of zebrafish development were largely developed for embryonic stages and early post-hatching stages (to 
5 days post-fertilization). The analysis of later stages of postembryonic development is more challenging because larvae are larger and no longer transparent. However, they also demonstrate more complex morphologies, which define species differences, and are thus important for studies of evolutionary change. Jackie Webb (Villanova University) showed that the postembryonic morphology of lateral line canal neuromasts of zebrafish are morphologically distinct from those of most other teleosts (Webb and Shirey 2003). This observation demonstrates how a model species is not necessarily representative of the larger taxon to which it belongs and requires us to reframe our understanding of the spectrum of morphological variation found in the lateral line system among fishes. She also illustrated how recent work on the genetic control of early patterning of the lateral line (for example, Lopez-Schier and others 2004; Grant and others 2005) may shed light not only on patterning among embryos and larvae of other species (Pichon and Ghysen 2004), but also on interspecific variation in neuromast number and its relationship to lateral line scale meristics in adult fishes. David Parichy (University of Washington) discussed his work that uses genetic, molecular, and cellular approaches to identify the genes and cellular processes underlying pigment-pattern formation and species differences in pigment patterns (Parichy and Turner 2003a,b; Quigley and others 2004, 2005). He has demonstrated important roles for stem-cell-derived pigment cells, and interactions among different pigment-cell classes, in generating the diversity of pigment patterns among Danio species.
The sequencing of the genome of several fish species (Table 1) has followed the footsteps of the Human Genome Project. While most of these genomic resources were developed to determine how fish models might aid in the investigation of the genetics of developmental mechanisms in humans, they now provide the basis for the study of genome evolution, the evolution of gene function, and the genetic basis for evolutionary change in phenotype. It is thought that at least 1 whole-genome duplication occurred at or near the origin of vertebrates (Dehai and Boore 2005) and that another occurred around 370 million years ago in the common ancestor of teleost fishes. John Postlethwait (University of Oregon) spearheaded the early efforts to describe this "pre-teleost" duplication and demonstrated its consequences for gene families in zebrafish (Amores and others 1998; Postlethwait and others 1998, 1999). He addressed how duplication of the Sox9 gene, for instance, appears to have resulted in the evolution of distinct but overlapping functions of these genes in neural crest and skeletal development. The Postlethwait laboratory also has begun to address similar issues of gene evolution using sticklebacks and the larvacean Oikipleura (a pelagic urochordate, Bassham and Postlethwait 2005; Canestro and others 2005). Tom Schilling discussed gene duplication in the context of the tfap2 gene family and its roles in neural crest evolution (Knight and others 2005). David Stock used the occurrence of similar changes in the expression of recently duplicated Dlx paralogs in association with cypriniform tooth loss to hypothesize that both were consequences of the evolution of a common upstream regulator. This is supported by transgenic analysis of zebrafish Dlx regulatory regions in the blind cavefish, Astyanax mexicanus (Jackman and Stock 2005).
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Populations of the three-spined stickleback (Gasterosteus aculeatus) and assemblages of cichlid species (Family Cichlidae) have undergone rapid evolutionary change in the past few million years with dramatic changes in morphology. These processes provide an opportunity to study microevolution and the genetics underlying changes in phenotypic traits through the mapping of quantitative trait loci (QTL). Tom Kocher (University of New Hampshire) described a linkage map for cichlids, represented by Tilapia spp. (Katagiri and others 2005
; Lee and others 2005), which will allow the mapping of QTLs in cichlids. His group has already mapped traits determining functionally important aspects of the jaw skeleton using QTL analysis in related East African cichlid species (Labeotropheus fuelleborni, Metriaclima zebra; Albertson and others 2005). An important step will be to integrate these studies, with those in sticklebacks (Cresko and others 2004; Shapiro and others 2004; Colosimo and others 2005; Kimmel and others 2005), and the identification of candidate genes in zebrafish to reveal the genes underlying the QTLs.
Mutations that arise spontaneously in natural populations are the raw material for natural selection. While genetically defined laboratory strains of zebrafish have been the focus of intensive study, wild zebrafish populations are relatively inaccessible in the field and have not been well studied. Amy McCune (Cornell University) discussed the potential of using spontaneous mutants from wild-caught zebrafish for developmental genetic studies. Her work has shown that wild-caught fish demonstrate the same frequency of spontaneous mutants as does those from induced mutagenesis screens (McCune and others 2002, 2004). Mutants causing loss of the swim bladder, for instance, are commonly found in screens of both induced and spontaneous mutations, but they are also interesting because the swim bladder has been lost evolutionarily in representatives of nearly 20% of the living families of fishes (McCune and Carlson 2004). Natural variation among populations within fish species and among closely related fish species are currently the focus of work in several laboratories. Natural variation in the number and morphology of lateral plates among populations of the three-spined stickleback has become an important system for the study of microevolution (Cresko and others 2004; Colosimo and others 2005). Pigmentation patterns among Danio species (McClure and McCune 2003; Parichy 2003; Quigley and others 2004, 2005) and among species of Lake Malawi cichlids (Streelman and others 2003; Kocher 2005) have proven to be rich systems to study the relationship of genotype and phenotype in evolution.
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Symposium speakers and participants in complementary contributed paper sessions met informally to discuss the development of shared resources and ways in which to facilitate collaborative projects in areas of common interest.
The Parichy lab (http://protist.biology.washington.edu/dparichy/) is compiling a normal table of postembryonic development for zebrafish and is breeding several Danio species, which are available to investigators interested in doing comparative studies. Access to living embryos of basal teleosts (for example, osteoglossomorph) and non-teleosts (for example, sturgeon, Amia) at different developmental stages is critical for comparative studies of major features of development (for example, gastrulation), as well as the analysis of the history of genome duplications. It was suggested that continued communication of the zebrafish community with the ichthyology community (http://www.asih.org), particularly the larval fish community (for example, Early Life History Section, American Fisheries Society, http://www2.ncsu.edu/elhs/index.html), should allow the identification of such resources. CToL participants (www.cypriniformes.org) can facilitate acquisition of developmental stages of various cypriniform species and Rick Mayden (PI, CToL project) can provide access to the CToL database to those who wish to use its resources. The examination of natural variation in the wild, and its potential usefulness for studying developmental processes, especially in a microevolutionary context, is fundamental to our understanding of evolution. However, remarkably little is known about the natural history and natural variation of zebrafish in the wild. Amy McCune, Dave Parichy, and Ray Engeszer (University of Washington) have experience with the collection and shipping of fishes from India and they articulated the need to develop strategies to obtain research funds to address the nature of variation in the wild given its critical implications for both developmental and evolutionary processes.
It was suggested that future sequencing efforts, which would complement ongoing efforts to sequence the Danio genome (http://www.ncbi.nlm.nih.gov/genome/guide/zebrafish/ and http://www.sanger.ac.uk/Projects/D_rerio/) should focus on an acanthomorph teleost, perhaps a cichlid, since no representative of this speciose taxon has been sequenced. The international Cichlid Genome Consortium, organized by Tom Kocher, is promoting the sequencing of the tilapia genome (http://hcgs.unh.edu/cichlid/). He also suggested that a 1x coverage of the genomes of 5 or more closely related species within the Cypriniformes or Acanthomorpha, rather than construction of finer maps for individual species, would allow the reconstruction of the genome of their common ancestor. This would allow an assessment of genetic variation among species, facilitate annotation of genomic data, and provide insights into the evolution of gene function.
Broadening the spectrum of analyses of developmental mechanisms beyond zebrafish embryos to include those structures that develop during the postembryonic period as well as other species requires modified methodologies. Participants pointed out that several books (for example, Zebrafish, Nusslein-Volhard and Dahm 2002; Methods in Cell Biology, Detrich and others 2004a,b) provide useful protocols for gene expression studies. In addition, some individual labs have posted protocols on their web sites, which can be used for gene expression studies in postembryonic fishes (for example, http://protist.biology.washington.edu/dparichy/). The Zebrafish International Network is building databases of zebrafish anatomy (wild type) and patterns of gene expression (http://zfin.org/zirc/home/stckctr.php), which can be used as the basis for comparative studies, at least at early stages. Paula Mabee stressed the value of the integration of the ZFIN and CToL (http://www.cypriniformes.org) databases through the construction of a comprehensive ontology that clearly defines developmental stages and morphological features in zebrafish. Such efforts will facilitate comparative studies of developmental patterns and mechanisms. Mark Cooper's DVD distribution project (Cooper and others 2004; www.depts.washington.edu/fishscop/) facilitates the distribution of images in very large files that cannot be moved easily via internet downloads or e-mail. Finally, the organizers indicated that the symposium website will be maintained as a resource including links to all participant labs and fish genome resources (http://www.sicb.org/meetings/2006/symposia/zebrafish/).
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Research communities evolve as new questions arise and new tools are developed. However, they may remain isolated from one another as the result of differences in methodological approaches and the proximate and ultimate goals of their work. The symposium "Zebrafish in Comparative Context" demonstrated how communication between 2 research communities with a common interest in fishes (the comparative biology and zebrafish research communities) can spawn new collaborations and foster the enrichment of research efforts. Periodically, we must come together to facilitate discussions between morphologists and geneticists, systematists and developmental biologists, and ichthyologists and neurobiologists, in order to take a truly integrative approach to fundamental biological questions. However, is also clear that web-based bioinformatic resources (for example, phylogenetic databases, gene expression image archives and whole-genome sequences) will be critical for integrative research efforts that seek to determine how morphological and genetic variation among individuals and among species result in patterns and mechanisms of evolutionary change.
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Acknowledgements |
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The authors thank all the participants of the symposium and associated contributed papers sessions for their valuable contributions and for comments on earlier drafts of this manuscript. The symposium was funded by the Society for Integrative and Comparative Biology and the American Microscopical Society, as well as by a National Institutes of Health R-13 grant (#HD-52411 to T.F.S., PI). The authors thank Eduardo Rosa-Molinar for obtaining a grant from Aquatic Habitats, Inc. for support of the symposium and associated activities. The American Association of Anatomists (www.anatomy.org) provided a Research Meeting Outreach Grant (to J.F.W.) for support of graduate students and post-docs presenting contributed papers in sessions complementary to the symposium. Invited symposium papers are being published as a special issue of Journalof Experimental Zoology—Molecular Development and Evolution.
Conflict of interest: None declared.
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2Present address: Deptartment of Biological Sciences, University of Rhode Island, Kingston, RI 02881
From the symposium "Zebrafish in Comparative Context" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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