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WIREs Dev Biol
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Goldfish morphology as a model for evolutionary developmental biology

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Morphological variation of the goldfish is known to have been established by artificial selection for ornamental purposes during the domestication process. Chinese texts that date to the Song dynasty contain descriptions of goldfish breeding for ornamental purposes, indicating that the practice originated over one thousand years ago. Such a well‐documented goldfish breeding process, combined with the phylogenetic and embryological proximities of this species with zebrafish, would appear to make the morphologically diverse goldfish strains suitable models for evolutionary developmental (evodevo) studies. However, few modern evodevo studies of goldfish have been conducted. In this review, we provide an overview of the historical background of goldfish breeding, and the differences between this teleost and zebrafish from an evolutionary perspective. We also summarize recent progress in the field of molecular developmental genetics, with a particular focus on the twin‐tail goldfish morphology. Furthermore, we discuss unanswered questions relating to the evolution of the genome, developmental robustness, and morphologies in the goldfish lineage, with the goal of blazing a path toward an evodevo study paradigm using this teleost species as a new model species. WIREs Dev Biol 2016, 5:272–295. doi: 10.1002/wdev.224 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan Comparative Development and Evolution > Model Systems Comparative Development and Evolution > Evolutionary Novelties
Variation of goldfish strains. (a–i) Dorsal views of nine different goldfish strains: (a) the single fin Wakin; (b) duplicated caudal fin Wakin; (c) Ryukin; (d) Oranda; (e) Redcap Oranda; (f) telescope (the ‘black moutan’ strain); (g) telescope (butterfly tail); (h) red‐color telescope; and (i) Ranchu (Reprinted with permission from Ref . Copyright 2014). (j) Illustration of Matsui's genealogical diagram. The name of each strain is based on Ref . Solid and dotted lines indicate spontaneous mutation and hybridization of different strains, respectively.
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Schematic representation of the relationship between genetic polymorphisms and developmental robustness. Arrows indicate the direction of changes in genetic polymorphisms and developmental robustness. Circles represent the populations [white: before the change; gray: after the change(s)]. (a) Increased genetic polymorphisms under low developmental robustness. This enables polymorphic phenotypes to become the subject of selection. This condition can be generated by additional mutations and/or hybridization between different strains or species. (b) Decreased genetic polymorphisms under low developmental robustness. If the genetic polymorphisms remain, the population depicted as a gray circle can still exhibit polymorphic phenotypes. This condition can be caused by bottlenecks and inbreeding. (c) Reduced robustness while retaining genetic polymorphisms. The genetic polymorphisms can manifest as phenotypic polymorphisms, as observed in the research on Hsp90 of Drosophila. (d) Simultaneous reduction of robustness and genetic polymorphisms (light to dark gray circles), preceded by an increase of genetic polymorphisms (white to light gray circles). (e) Increased genetic polymorphisms (light to dark gray circles), preceded by a reduction of robustness and genetic polymorphisms (white to light gray circles).
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Increase in described goldfish strains from the early to late 20th century. The number of strains is based on the study by Smartt.
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Gene regulatory network of DV‐patterning‐related genes. (a) Zebrafish DV‐patterning‐related genes and their regulatory relationship. (Reprinted with permission from Ref . Copyright 2011 Annual Review) (b) Hypothetical goldfish DV‐patterning‐related genes. Hypothetical paralogous genes are indicated by single (′) and double (″) primes.
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Contrast between zebrafish mutagenesis and goldfish breeding. (a–d) The screening and maintenance process for zebrafish mutants. (e–g) Establishment of goldfish mutant strains. The vertical and horizontal axes of each graph indicate the individual number and phenotype of the populations, respectively. (a, e) Wild‐type populations show a narrow distribution of the phenotype. (b, f) Distribution patterns of the wild‐type, heterozygous, and mutant homozygous population in early generations. Arrowheads indicate mutated phenotypes. Black arrowheads indicate the most preferred mutated phenotypes for breeders. Horizontal arrows indicate selective pressures. This scheme is described under the assumptions that the + allele is dominant to the − allele, (+/+) and (+/−) populations show narrow and identical distributions, and the population consisting of −/− individuals shows a polymorphic phenotype. (c, g) The distribution patterns after screening. The screening of homozygous mutants with morphological features tends to remove individuals with low penetrance of the phenotype (asterisks in b and c). (d, g) The distribution patterns after long‐term repeated selections. (d) The distribution patterns of the zebrafish mutant populations tend to show the same distribution patterns with former generations (c). (g) During goldfish breeding, the most preferred mutated traits in each generation (black arrowheads in g and h) tend to be selected and finally fixed in the population. If the morphological feature in question has high commercial value, stabilizing selection makes the distribution pattern narrow.
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Schematic representation of gene expression patterns in wild‐type and dino zebrafish, and wild‐type and twin‐tail goldfish strains. Olive, light green, green, red, and blue regions represent areas positive for zebrafish chordin, chdAwt, chdB, ventral markers (eve1, sizzled, and bmp4), and krox20, respectively. Asterisks indicate areas of krox20 expression in twin‐tail goldfish and dino zebrafish. (Reprinted with permission from Ref . Copyright 2014).
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Rescue phenotype of twin‐tail goldfish. (a, b) Control twin‐tail goldfish larval individuals. (c–g) Twin‐tail goldfish individuals injected at the one‐cell zygote stage with chdAwt mRNA. The magnified views of caudal regions in (b) and (d) correspond to the asterisked specimens in (a) and (c), respectively. (e) Lateral view of juvenile. (f) Alcian blue‐ and alizarin red‐stained specimen. (g) Magnified view of the caudal region of (f). Scale bars: 5mm (e, f), 1 mm (a, c, g), 100 µm (b, d). (Reprinted with permission from Ref . Copyright 2014 Nature Publishing Group).
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Schematic representation of backcross analysis of the twin‐tail phenotypes. The number in bold indicates the number of exceptional wildtype individuals (E127X/E127X), suggesting low penetrance. (Reprinted with permission from Ref . Copyright 2014).
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Zebrafish and goldfish chordin genes. (a) Schematic representation of the Chordin amino acid sequences of zebrafish and goldfish. Colored boxes indicate cysteine‐rich domains. Arrowheads indicate the mutated sites. (b) Chordin gene alleles possessed by zebrafish dino mutants and twin‐tail goldfish strains.
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Anatomy of the caudal skeleton of twin‐tail goldfish as described by Watase. (a) Drawings of transverse sections at the caudal level in different goldfish specimens with variations in twin‐tail morphology. Black colored ovals indicate skeletal elements. (b) Drawings of transverse sections at the anal fin level in single (left) and bifurcated anal fin (right) goldfish specimens.
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Phylogenetic relationships between goldfish, common carp, and 10 representative ray fin fish species in which whole genome sequences are available are described based on Refs ; Fugu, Cichlid, Medaka, and Stickleback are collectively grouped as Percomorpha. Evolutionary events and their dating in the lineages of goldfish, common carp, and zebrafish are based on Refs (circles and squares). CE and MYA indicate Common Era and million years ago, respectively. The branch lengths were drawn arbitrarily and do not reflect evolutionary time. Previously reported divergence times (MYA) of each node are indicated in italics.
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