25
Cytogenetic Approach to Fish Systematics
To clarify interrelationships of fishes cytogenetically, genome size has been studied in fi
fi
shes (Hinfi
egardner and Rosen 1972: H-13; Ojima and Yamamoto 1990: O-48; Hardie and Hebert 2004: H-40;
Pie et al. 2007: P-61; Smith and Gregory 2009: S-191). However, the question of the C-value enigma
has been a puzzle for almost half a century, which suggests that a simple comparison of taxa and
their genome size may be insufficient for the study of genome evolution in fi
fi
shes. Concerning
fi
genome size, the transposable elements, the spectrum of size and frequency of small spontaneous
nucleotide insertions and deletions, and genome duplication are the important parameters in the
long-term evolution of genome size (Petrov 2001: P-5; Gregory 2005: G-22).
As inferred by gene mapping analysis, inter- and intra-chromosomal rearrangements by
Robertsonian translocation, tandem fusion, pericentric- and paracentric-inversion have occurred
in fi shes and a higher rate of chromosomal rearrangements in teleosts compared to other vertefi
brates has been hypothesized based on a comparison of the medaka genome with the zebrafish, fi
pufferfi sh, and human genomes (Ravi and Venkatesh 2008: R-117). Therefore, synthetic analyses
fi
of karyotypes, genome sizes, and DNA sequences, and stepwise study inferring the karyotype and
genome size of the latest common ancestor in monophyly from lower to higher taxa, may be necessary to clarify fi sh systematics.
fi
Recently, the early fish proto-karyotype has been studied (Jaillon et al. 2004: J-21; Naruse et al.
fi
2004: N-77; Woods et al. 2005: W-37; Kohn et al. 2006: K-141; Nakatani et al. 2007: N-75). According
to Sato and Nishida (2010: S-205), whole-genome duplication (WGD), which generates many thousands of duplicate genes, is believed to be one of the major evolutionary events that shaped the
genomes of vertebrates including fi shes and tetrapods. Interestingly, the analysis of teleost fi
fi
sh
fi
genomes has revealed that teleosts experienced an additional WGD (3R-WGD), whereas tetrapods
experienced only 1R- and 2R-WGD; exceptionally, some lineages of amphibians and reptiles have
experienced an additional WGD. The chromosomal distribution of the homologous genes can be
compared between tetrapods and teleosts by whole-genome sequence analysis, and this information can then be used to infer the karyotype of the osteichthyan ancestor. Nakatani et al. (2007:
N-75) hypothesized the following karyotype evolution model in fishes based on reconstruction of
fi
the vertebrate ancestral genome. Before the first round of WGD, the vertebrate ancestor karyotype
fi
was 2n = 20–26, and the subsequent 2R-WGD and some genome rearrangements yielded the jawed
vertebrate ancestor of 2n = 80. After the divergence of Osteichthyes and Chondrichthyes, genome
rearrangements reduced the number of chromosomes in the osteichthyan ancestor to 2n = 62.
After the divergence of ray-finned and lobe-fi
fi
nned fi
fi
shes, in the lineage of ray-fi
fi
nned fi
fi
shes
fi
(Actinopterygii), chromosome fusions reduced the number of chromosomes and produced the
teleost ancestor with 2n = 26. Subsequently, the whole-genome duplication (3R-WGD) in the
teleost ancestor doubled the number of chromosomes to 2n = 52. The number of chromosomes
in the teleost lineage has remained nearly unchanged during evolution, and the chromosome
numbers of extant teleost species peak at 2n = 48 or 50.
Cytogenetic Approach to Fish Systematics
To clarify interrelationships of fishes cytogenetically, genome size has been studied in fi
fi
shes (Hinfi
egardner and Rosen 1972: H-13; Ojima and Yamamoto 1990: O-48; Hardie and Hebert 2004: H-40;
Pie et al. 2007: P-61; Smith and Gregory 2009: S-191). However, the question of the C-value enigma
has been a puzzle for almost half a century, which suggests that a simple comparison of taxa and
their genome size may be insufficient for the study of genome evolution in fi
fi
shes. Concerning
fi
genome size, the transposable elements, the spectrum of size and frequency of small spontaneous
nucleotide insertions and deletions, and genome duplication are the important parameters in the
long-term evolution of genome size (Petrov 2001: P-5; Gregory 2005: G-22).
As inferred by gene mapping analysis, inter- and intra-chromosomal rearrangements by
Robertsonian translocation, tandem fusion, pericentric- and paracentric-inversion have occurred
in fi shes and a higher rate of chromosomal rearrangements in teleosts compared to other vertefi
brates has been hypothesized based on a comparison of the medaka genome with the zebrafish, fi
pufferfi sh, and human genomes (Ravi and Venkatesh 2008: R-117). Therefore, synthetic analyses
fi
of karyotypes, genome sizes, and DNA sequences, and stepwise study inferring the karyotype and
genome size of the latest common ancestor in monophyly from lower to higher taxa, may be necessary to clarify fi sh systematics.
fi
Recently, the early fish proto-karyotype has been studied (Jaillon et al. 2004: J-21; Naruse et al.
fi
2004: N-77; Woods et al. 2005: W-37; Kohn et al. 2006: K-141; Nakatani et al. 2007: N-75). According
to Sato and Nishida (2010: S-205), whole-genome duplication (WGD), which generates many thousands of duplicate genes, is believed to be one of the major evolutionary events that shaped the
genomes of vertebrates including fi shes and tetrapods. Interestingly, the analysis of teleost fi
fi
sh
fi
genomes has revealed that teleosts experienced an additional WGD (3R-WGD), whereas tetrapods
experienced only 1R- and 2R-WGD; exceptionally, some lineages of amphibians and reptiles have
experienced an additional WGD. The chromosomal distribution of the homologous genes can be
compared between tetrapods and teleosts by whole-genome sequence analysis, and this information can then be used to infer the karyotype of the osteichthyan ancestor. Nakatani et al. (2007:
N-75) hypothesized the following karyotype evolution model in fishes based on reconstruction of
fi
the vertebrate ancestral genome. Before the first round of WGD, the vertebrate ancestor karyotype
fi
was 2n = 20–26, and the subsequent 2R-WGD and some genome rearrangements yielded the jawed
vertebrate ancestor of 2n = 80. After the divergence of Osteichthyes and Chondrichthyes, genome
rearrangements reduced the number of chromosomes in the osteichthyan ancestor to 2n = 62.
After the divergence of ray-finned and lobe-fi
fi
nned fi
fi
shes, in the lineage of ray-fi
fi
nned fi
fi
shes
fi
(Actinopterygii), chromosome fusions reduced the number of chromosomes and produced the
teleost ancestor with 2n = 26. Subsequently, the whole-genome duplication (3R-WGD) in the
teleost ancestor doubled the number of chromosomes to 2n = 52. The number of chromosomes
in the teleost lineage has remained nearly unchanged during evolution, and the chromosome
numbers of extant teleost species peak at 2n = 48 or 50.