Elsevier

Gene

Volume 457, Issues 1–2, 1 June 2010, Pages 13-24
Gene

Intraspecific variation in the mitochondrial genome among local populations of Medaka Oryzias latipes

https://doi.org/10.1016/j.gene.2010.02.012Get rights and content

Abstract

The draft genome data of Medaka Oryzias latipes shows that it has distinct intraspecific genetic variation. To survey the genetic variations contributing to environmental adaptation, we focused on the mitochondrial DNA (mtDNA). The complete mtDNA sequences of Medaka were compared among 8 local population stocks and 4 inbred strains established from genetically divergent groups. Inbred strain HSOK, derived from the Eastern Korean group of Medaka, has a mitochondrial gene order that was distinct from other Medaka groups. Phylogenetic trees based on the mitochondrial genome sequences indicated that the mitogenome from the Shanghai stock (China) and HSOK strain were highly diverged from Japanese Medaka, and that the Japanese Medaka mitogenome was diverged into two groups; this result was fully consistent with those of the previous study using mtDNA-encode gene sequences. Among tRNA genes, the most divergent was the tRNAThr gene as reported in humans previously. The number of tandemly repeated 11 nucleotide units in the Medaka mtDNA control region (CR) varied greatly among local populations. The number of repeats was more variable in the Northern Japanese group (10–34) than in the Southern group (7–12), while two other Oryzias species, inhabiting tropical regions, had no repeats. A comprehensive comparison between the number of repeat units and meteorological data indicated that the number of repeats correlated to the index data of a cold environment and seasonal climatic change. In cold (5 °C) acclimated fish, the mRNA levels varied among mitochondria coding genes. mRNA of the cytochrome oxidase subunit I gene in some local stocks was induced by cold temperature and seemed to be correlated with the number of repeated sequences in the CR. This study revealed that the repeated sequences in the mtDNA CR might function for mtDNA gene expression and that the number of tandem repeats in Medaka mtDNA is likely related to adaptation to a harsh habitat.

Introduction

Inter- and intraspecific mitochondrial DNA (mtDNA) variation is a very useful marker to study the evolution of animals, especially in taxonomy, systematics, ecology and population biology (Avise, 1994, Avise et al., 1987, Moritz et al., 1987). mtDNA analyses based on partial nucleotide sequences usually assume that most of the variations conform to a neutral model of molecular evolution, but some experimental studies and human mitogenome data have suggested that selective forces might act upon mtDNA (Ruiz-Pesini et al., 2004, William et al., 1995). Vertebrate mtDNA codes for 13 proteins, 2 rRNA and 22 tRNA genes and includes one non-coding control region (CR). Mitochondria serve a critical function in the maintenance of cellular energy stores, thermogenesis and apoptosis (Kelly and Scarpulla, 2004). Human mtDNA variants seem to be associated with some adaptive functions such as longevity (De Benedictis et al., 1999, Ross et al., 2001, Tanaka et al., 1998) and climatic selection (Mishmar et al., 2003).

Temperature adaptation mechanisms through mtDNA-encoded genes have been analyzed in ectotherms (Doiron et al., 2002) and endotherms (Hittel and Storey, 2002, Mishmar et al., 2003). In fish, during phenotypic cold acclimation the compensatory mechanisms in mitochondrial volume density and properties are different among species (Guderley, 2004). Moreover, adjustments in the mitochondrial properties and capacities seem to be crucial in acclimating to seasonal cold and in cold adaptation of fish (Itoi et al., 2003, Lucassen et al., 2003). If selective pressures affect the survival rate of mtDNA lineages, intra-species mitogenomic differentiation of wild animals are expected to exist.

Medaka (Oryzias latipes) is a small freshwater fish distributed in East Asia that shows apparent genetic differentiation among local populations, revealed by the phylogenetic analysis using allozymes (Sakaizumi et al., 1983) and the partial mtDNA sequences (Matsuda et al., 1997, Takehana et al., 2003, Takehana et al., 2004). The populations of Medaka have been classified into 4 genetically divergent groups: the Northern Japanese, the Southern Japanese, the Eastern Korean and the China-Western Korean groups. The Northern Japanese and the Southern Japanese groups are estimated to have diverged approximately 4–18 million years ago, and the genome-wide single nucleotide polymorphism (SNP) rate (3.42%) between the two inbred strains, HNI (Northern Japanese group) and Hd-rR (Southern Japanese group), is the highest SNP rate observed in any vertebrate species reported (Kasahara et al., 2007, Setiamarga et al., 2009). Despite the accumulated genetic variation, however, these groups can mate and produce healthy, fertile offspring.

The geographical distribution area of Medaka is wide, ranging from the subarctic (ex. northernmost Japan) to the subtropical zones (southernmost Japan and China). Several studies have suggested that climate may create genetic difference among populations of this species. Iwamatsu (1997) reported that the range of the highest survival temperature in Medaka and related species is narrow (from 41 to 42 °C), whereas the lowest survival temperature is considerably broader (from 0 to 10 °C). Hirayama et al. (2006) demonstrated that at low temperatures, inter-group variations in the cell proliferation rate also exist. It was shown that cell lines derived from the Northern Japanese and Eastern Korean groups could proliferate at lower temperatures than those from the Southern Japanese group and the Medaka-related species O. celebensis, which inhabits a tropical zone. In addition, the inter- and intra-population variations in thermal reaction norms for the growth rate of the Northern Japanese group at different temperatures were determined, including the individual growth rates during the juvenile stage within 12 latitudinal populations of the Northern Japanese group in a temperature controlled (28 °C) environment (Yamahira et al., 2007, Yamahira and Takeshi, 2008). The results suggested that natural selection in high latitudes favors individuals that grow faster within a shorter growing season to individuals that have longer growing seasons. Moreover, Matsumoto et al. (2009) indicated that some of the SNPs for several genes with apparent orthology between Medaka and humans show signals of positive selection in Medaka. Thus, Medaka (Oryzias species) is an ideal model animal to how higher latitude poikilotherms have acquired a greater capacity for temperature acclimation at a genetic level.

In this study, we compared 12 complete and nearly complete mtDNA sequences of Medaka from different local populations. The molecular evolutionary rate, phylogenetic utility, and nonsynonymous/synonymous substitution rates of each mitochondrial gene were assessed. We also compared CR of 36 Medakas, including 30 local populations, 4 inbred strains and 2 other Oryzias species, to find any features of environmental adaptation in Medaka populations.

Section snippets

Medaka fish

The local Medaka (O. latipes, Japanese killifish) populations, inbred strains and Medaka-related species used in this study are summarized in Fig. 1 and Table 1. The local stocks, which were collected from local sites have been maintained for many generations as closed colonies in Graduate School of Frontier Sciences, the University of Tokyo (Mitani et al., 2006, Shima et al., 1985). O. curvinotus and O. luzonensis were obtained from the National Biological Resource Project (NBRP). A portion of

Mitochondrial genome organization

The newly determined complete light (L)-strand nucleotide sequences of the Niigata stock, HNI, KAGA and Hd-rR strains, and the nearly complete sequences (except for a portion of the CR) of the other 6 stocks and the HSOK strain have been registered in DDBJ/EMBL/GenBank under the accession nos. AP008938–AP008948AP008938AP008939AP008940AP008941AP008942AP008943AP008944AP008945AP008946AP008947AP008948. The genomic content of 11 of 12 Medaka mitogenomes including AP004421, contained two rRNA, 22

Intraspecific variation in the mitochondrial gene order

The mitochondrion plays a critical role in the maintenance of cellular energy stores, thermogenesis, and apoptosis. In this study, the complete mitogenome sequences of 8 Medaka stocks and 4 inbred strains were compared. A local duplication was found between the ND3 and ND4 genes in the mtDNA of the HSOK strain, but the duplicated genes had lost all function. The arrangement of the pseudogenes between the COIII and ND4 gene region can be explained by a single duplication event of the segment tRNA

Acknowledgments

We would like to express our sincere thanks to Dr. G.N. Somero, Stanford University, USA, for critical reading of the manuscript. Thanks are also due to Drs. Y. Ishikawa (National Institute of Radiological Sciences) and N. Shibata (Shinshu University) for kindly providing inbred Medaka strains and foreign species, respectively. We are grateful to Mr. Y. Hashiguchi (Ocean Research Institute, The University of Tokyo) for providing valuable technical advice concerning the computational analysis.

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    Present address: Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan.

    2

    Present address: Faculty of Regional Studies, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan.

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