Publications by authors named "Kohta Yoshida"

22 Publications

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Tempo and mode in karyotype evolution revealed by a probabilistic model incorporating both chromosome number and morphology.

PLoS Genet 2021 Apr 16;17(4):e1009502. Epub 2021 Apr 16.

Ecological Genetics Laboratory, National Institute of Genetics, Mishima, Japan.

Karyotype, including the chromosome and arm numbers, is a fundamental genetic characteristic of all organisms and has long been used as a species-diagnostic character. Additionally, karyotype evolution plays an important role in divergent adaptation and speciation. Centric fusion and fission change chromosome numbers, whereas the intra-chromosomal movement of the centromere, such as pericentric inversion, changes arm numbers. A probabilistic model simultaneously incorporating both chromosome and arm numbers has not been established. Here, we built a probabilistic model of karyotype evolution based on the "karyograph", which treats karyotype evolution as a walk on the two-dimensional space representing the chromosome and arm numbers. This model enables analysis of the stationary distribution with a stable karyotype for any given parameter. After evaluating their performance using simulated data, we applied our model to two large taxonomic groups of fish, Eurypterygii and series Otophysi, to perform maximum likelihood estimation of the transition rates and reconstruct the evolutionary history of karyotypes. The two taxa significantly differed in the evolution of arm number. The inclusion of speciation and extinction rates demonstrated possibly high extinction rates in species with karyotypes other than the most typical karyotype in both groups. Finally, we made a model including polyploidization rates and applied it to a small plant group. Thus, the use of this probabilistic model can contribute to a better understanding of tempo and mode in karyotype evolution and its possible role in speciation and extinction.
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http://dx.doi.org/10.1371/journal.pgen.1009502DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8081341PMC
April 2021

Accumulation of Deleterious Mutations in Landlocked Threespine Stickleback Populations.

Genome Biol Evol 2020 04;12(4):479-492

Ecological Genetics Laboratory, National Institute of Genetics, Mishima, Shizuoka, Japan.

Colonization of new habitats often reduces population sizes and may result in the accumulation of deleterious mutations by genetic drift. Compared with the genomic basis for adaptation to new environments, genome-wide analysis of deleterious mutations in isolated populations remains limited. In the present study, we investigated the accumulation of deleterious mutations in five endangered freshwater populations of threespine stickleback (Gasterosteus aculeatus) in the central part of the mainland of Japan. Using whole-genome resequencing data, we first conducted phylogenomic analysis and confirmed at least two independent freshwater colonization events in the central mainland from ancestral marine ecotypes. Next, analyses of single nucleotide polymorphisms showed a substantial reduction of heterozygosity in freshwater populations compared with marine populations. Reduction in heterozygosity was more apparent at the center of each chromosome than the peripheries and on X chromosomes compared with autosomes. Third, bioinformatic analysis of deleterious mutations showed increased accumulation of putatively deleterious mutations in the landlocked freshwater populations compared with marine populations. For the majority of populations examined, the frequencies of putatively deleterious mutations were higher on X chromosomes than on autosomes. The interpopulation comparison indicated that the majority of putatively deleterious mutations may have accumulated independently. Thus, whole-genome resequencing of endangered populations can help to estimate the accumulation of deleterious mutations and inform us of which populations are the most severely endangered. Furthermore, analysis of variation among chromosomes can give insights into whether any particular chromosomes are likely to accumulate deleterious mutations.
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http://dx.doi.org/10.1093/gbe/evaa065DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7197494PMC
April 2020

Two new Species of (Nematoda: Diplogastridae) include the Gonochoristic Sister Species of .

J Nematol 2019 ;51:1-14

Department of Evolutionary Biology, Spemannstraße 37, Max Planck Institute for Developmental Biology , Tübingen , Germany.

The genus (Kreis, 1932) consists of more than 30 soil nematode species that are often found in association with scarab beetles. Three major radiations have resulted in the " species group" in America, the " species group" in Asia, and the " species group," which contains species from Europe and Asia. Phylogenetic analysis indicates that a group of three species, including the gonochorists and and the hermaphrodite , is basal to the above-mentioned radiations. Two novel species are described here: sp. n. from Taiwan and sp. n. from Japan by means of morphology, morphometrics and genome-wide transcriptome sequence analysis. Previous phylotranscriptomic analysis of the complete genus recognized sp. n. as the sister species of , and thus its importance for macro-evolutionary studies. Specifically, the gonochorist sp. n. and the hermaphrodite form a species pair that is the sister group to all other described species. sp. n. has two distinct mouth forms, supporting the notion that the mouth dimorphism is ancestral in the genus .

The genus (Kreis, 1932) consists of more than 30 soil nematode species that are often found in association with scarab beetles. Three major radiations have resulted in the “ species group” in America, the “ species group” in Asia, and the “ species group,” which contains species from Europe and Asia. Phylogenetic analysis indicates that a group of three species, including the gonochorists and and the hermaphrodite , is basal to the above-mentioned radiations. Two novel species are described here: sp. n. from Taiwan and sp. n. from Japan by means of morphology, morphometrics and genome-wide transcriptome sequence analysis. Previous phylotranscriptomic analysis of the complete genus recognized sp. n. as the sister species of , and thus its importance for macro-evolutionary studies. Specifically, the gonochorist sp. n. and the hermaphrodite form a species pair that is the sister group to all other described species. sp. n. has two distinct mouth forms, supporting the notion that the mouth dimorphism is ancestral in the genus .
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http://dx.doi.org/10.21307/jofnem-2019-024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6930957PMC
January 2019

Two New Species of (Nematoda: Diplogastridae) from Taiwan and the Definition of the Species-Complex Sensu Stricto.

J Nematol 2018 ;50(3):355-368

Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, Spemannstraße 37, Tübingen, Germany.

Pristionchus pacificus Sommer, Carta, Kim, and Sternberg, 1996 is an important model organism in evolutionary biology that aims to integrate developmental biology and evo-devo with population genetics and ecology. Functional studies in P. pacificus are supported by a well-established phylogenetic framework of around 30 species of the genus Pristionchus that have been described in the last decade based on their entomophilic and necromenic association with scarab beetles. Biogeographically, East Asia has emerged as a hotspot of Pristionchus speciation and recent samplings have therefore focused on Islands and mainland settings in East Asia. Here, we describe in a series of three publications the results of our sampling efforts in Taiwan, Japan, and Hongkong in 2016 and 2017. We describe a total of nine new species that cover different phylogenetic species-complexes of the Pristionchus genus. In this first publication, we describe two new species, Pristionchus sikae sp. n. and Pristionchus kurosawai sp. n. that are closely related to P. pacificus . Together with five previously described species they form the " pacificus species-complex sensu stricto" that is characterized by all species forming viable, but sterile F1 hybrids indicating reproductive isolation. P. sikae sp. n. and P. kurosawai sp. n. have a gonochorist mode of reproduction and they are described using morphology, morphometrics, mating experiments, and genome-wide sequence analysis. We discuss the extreme diversification in the pacificus species-complex sensu stricto in East Asia and its potential power to study speciation processes.
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http://dx.doi.org/10.21307/jofnem-2018-019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6909367PMC
January 2018

Phylotranscriptomics of Pristionchus Nematodes Reveals Parallel Gene Loss in Six Hermaphroditic Lineages.

Curr Biol 2018 10 20;28(19):3123-3127.e5. Epub 2018 Sep 20.

Department for Evolutionary Biology, Max Planck Institute for Developmental Biology, Max-Planck-Ring 9, 72076 Tübingen, Germany. Electronic address:

Mutation and recombination are main drivers of phenotypic diversity, but the ability to create new allelic combinations is strongly dependent on the mode of reproduction. While most animals are dioecious (i.e., separated male and female sexes), in a number of evolutionary lineages females have gained the ability to self-fertilize [1, 2], with drastic consequences on effective recombination rate, genetic diversity, and the efficacy of selection [3]. In the genus Caenorhabditis, such hermaphroditic or androdioecious lineages, including C. briggsae and C. tropicalis, display a genome shrinkage relative to their dioecious sister species C. nigoni and C. brenneri, respectively [4, 5]. However, common consequences of reproductive modes on nematode genomes remain unknown, because most taxa contain single or few androdioecious species. One exception is the genus Pristionchus, with seven androdioecious species. Pristionchus worms are found in association with scarab beetles in worldwide samplings, resulting in deep taxon sampling and currently 39 culturable and available species. Here, we use phylotranscriptomics of all 39 Pristionchus species to provide a robust phylogeny based on an alignment of more than 2,000 orthologous clusters, which indicates that the seven androdioecious species represent six independent lineages. We show that gene loss is more prevalent in all hermaphroditic lineages than in dioecious relatives and that the majority of lost genes evolved recently in the Pristionchus genus. Further, we provide evidence that genes with male-biased expression are preferentially lost in hermaphroditic lineages. This supports a contribution of adaptive gene loss to shaping nematode genomes following the evolution of hermaphroditism.
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http://dx.doi.org/10.1016/j.cub.2018.07.041DOI Listing
October 2018

Functional divergence of a heterochromatin-binding protein during stickleback speciation.

Mol Ecol 2019 03 7;28(6):1563-1578. Epub 2018 Sep 7.

Division of Ecological Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan.

Intragenomic conflict, the conflict of interest between different genomic regions within an individual, is proposed as a mechanism driving both the rapid evolution of heterochromatin-related proteins and the establishment of intrinsic genomic incompatibility between species. Although molecular studies of laboratory model organisms have demonstrated the link between heterochromatin evolution and hybrid abnormalities, we know little about their link in natural systems. Previously, we showed that F hybrids between the Japan Sea stickleback and the Pacific Ocean stickleback show hybrid male sterility and found a region responsible for hybrid male sterility on the X chromosome, but did not identify any candidate genes. In this study, we first screened for genes rapidly evolving under positive selection during the speciation of Japanese sticklebacks to find genes possibly involved in intragenomic conflict. We found that the region responsible for hybrid male sterility contains a rapidly evolving gene encoding a heterochromatin-binding protein TRIM24B. We conducted biochemical experiments and showed that the binding affinity of TRIM24B to a heterochromatin mark found at centromeres and transposons, histone H4 lysine 20 trimethylation (H4K20me3), is reduced in the Japan Sea stickleback. In addition, mRNA expression levels of Trim24b were different between the Japan Sea and the Pacific Ocean testes. Further expression analysis of genes possibly in the TRIM24B-regulated pathway showed that some gypsy retrotransposons are overexpressed in the F hybrid testes. We, therefore, demonstrate that a heterochromatin-binding protein can evolve rapidly under positive selection and functionally diverge during stickleback speciation.
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http://dx.doi.org/10.1111/mec.14841DOI Listing
March 2019

The genomic landscape at a late stage of stickleback speciation: High genomic divergence interspersed by small localized regions of introgression.

PLoS Genet 2018 May 23;14(5):e1007358. Epub 2018 May 23.

Division of Ecological Genetics, Department of Population Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan.

Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little knowledge of the genomic signatures of divergence and introgression in older stickleback systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian Computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.
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http://dx.doi.org/10.1371/journal.pgen.1007358DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5988309PMC
May 2018

Samplings of Millipedes in Japan and Scarab Beetles in Hong Kong result in five new Species of (Nematoda: Diplogastridae).

J Nematol 2018 ;50(4):587-610

Max Planck Institute for Developmental Biology, Department of Evolutionary Biology , Spemannstraße 37, Tübingen , Germany.

The authors describe five new species of from Japan and Hongkong. Scarab beetle samplings in Hongkong identified sp. n. and sp. n., representing the first beetle-associated species from China. Surprisingly, samplings of millipedes in Japan revealed a previously unknown association of nematodes with these arthropods. Specifically, the authors found three previously known species, , , and on Japanese millipedes. In addition, the authors found three new species on millipedes, which are described as sp. n., sp. n., and , sp. n., the latter of which was also found on stag beetles. These species are most closely related to , , and and belong to the species-complex. The authors describe all species based on morphology, morphometrics, and genome-wide sequence analysis. Mating experiments indicated that all species are reproductively isolated from each other and in contrast to the species of the " species-complex " they do not form F1 hybrids.

The authors describe five new species of from Japan and Hongkong. Scarab beetle samplings in Hongkong identified sp. n. and sp. n., representing the first beetle-associated species from China. Surprisingly, samplings of millipedes in Japan revealed a previously unknown association of nematodes with these arthropods. Specifically, the authors found three previously known species, , , and on Japanese millipedes. In addition, the authors found three new species on millipedes, which are described as sp. n., sp. n., and , sp. n., the latter of which was also found on stag beetles. These species are most closely related to , , and and belong to the species-complex. The authors describe all species based on morphology, morphometrics, and genome-wide sequence analysis. Mating experiments indicated that all species are reproductively isolated from each other and in contrast to the species of the “ species-complex ” they do not form F1 hybrids.
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http://dx.doi.org/10.21307/jofnem-2018-044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6909306PMC
January 2018

Contribution of gene flow to the evolution of recombination suppression in sex chromosomes.

J Theor Biol 2017 10 3;431:25-31. Epub 2017 Aug 3.

Division of Ecological Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan. Electronic address:

Polymorphism of alleles that benefit one sex but harm the other (sexually antagonistic alleles) generates selective pressures for reduced recombination between themselves and sex-determination loci. Such polymorphism can be maintained within a population when selection coefficients are sufficiently balanced between males and females. However, if regulatory mutations restrict gene expression only to one sex, these alleles become neutral in the other sex and easily fixed within a population, removing the selective pressures for recombination suppression in sex chromosomes. When there is spatial variation in selection regimes, however, alleles that are deleterious in one sex and neutral in the other can be maintained in other neighboring populations and gene flow may continuously supply deleterious alleles. We hypothesized that this maintenance of genetic variation may promote the establishment of recombination suppression in sex chromosomes even in cases where selection is limited to one sex. Using individual-based simulations, we show that spatial variation in male-limited selection and gene flow can promote the establishment of Y-autosome fusions, a special case of recombination suppression in sex chromosomes. This can be explained by the fact that fused Y-chromosomes that capture alleles that are beneficial for local males have a higher mean fitness compared to unfused Y chromosomes in the presence of deleterious gene flow. We also simulated the case of sex-concordant selection and found that gene flow of alleles that are deleterious in both sexes did not substantially increase the establishment rates of Y-autosome fusions across the parameter space examined. This can be accounted for by the fact that foreign alleles that are deleterious in both sexes can be efficiently removed from the population compared to alleles that are neutral in females. These results indicate that how gene flow affects the establishment rates of Y-autosome fusions depends largely on selection regimes. Spatial variation in sex-specific selection and gene flow should be appreciated as a factor affecting sex chromosome evolution.
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http://dx.doi.org/10.1016/j.jtbi.2017.08.004DOI Listing
October 2017

Different contributions of local- and distant-regulatory changes to transcriptome divergence between stickleback ecotypes.

Evolution 2017 03 2;71(3):565-581. Epub 2017 Feb 2.

Division of Ecological Genetics, National Institute of Genetics, Shizuoka, Japan.

Differential gene expression can play an important role in phenotypic evolution and divergent adaptation. Although differential gene expression can be caused by both local- and distant-regulatory changes, we know little about their relative contribution to transcriptome evolution in natural populations. Here, we conducted expression quantitative trait loci (eQTL) analysis to investigate the genetic architecture underlying transcriptome divergence between marine and stream ecotypes of threespine sticklebacks (Gasterosteus aculeatus). We identified both local and distant eQTLs, some of which constitute hotspots, regions with a disproportionate number of significant eQTLs relative to the genomic background. The majority of local eQTLs including those in the hotspots caused expression changes consistent with the direction of transcriptomic divergence between ecotypes. Genome scan analysis showed that many local eQTLs overlapped with genomic regions of high differentiation. In contrast, nearly half of the distant eQTLs including those in the hotspots caused opposite expression changes, and few overlapped with regions of high differentiation, indicating that distant eQTLs may act as a constraint of transcriptome evolution. Finally, a comparison between two salinity conditions revealed that nearly half of eQTL hotspots were environment specific, suggesting that analysis of genetic architecture in multiple conditions is essential for predicting response to selection.
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http://dx.doi.org/10.1111/evo.13175DOI Listing
March 2017

Genetic basis for variation in salinity tolerance between stickleback ecotypes.

Mol Ecol 2017 Jan 27;26(1):304-319. Epub 2016 Oct 27.

Division of Ecological Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan.

Adaptation to different salinities can drive and maintain divergence between populations of aquatic organisms. Anadromous and stream ecotypes of threespine stickleback (Gasterosteus aculeatus) are an excellent model to explore the genetic mechanisms underlying osmoregulation divergence. Using a parapatric pair of anadromous and stream stickleback ecotypes, we employed an integrated genomic approach to identify candidate genes important for adaptation to different salinity environments. Quantitative trait loci (QTL) mapping of plasma sodium concentrations under a seawater challenge experiment identified a significant QTL on chromosome 16. To identify candidate genes within this QTL, we first conducted RNA-seq and microarray analysis on gill tissue to find ecotypic differences in gene expression that were associated with plasma Na levels. This resulted in the identification of ten candidate genes. Quantitative PCR analysis on gill tissue of additional Japanese stickleback populations revealed that the majority of the candidate genes showed parallel divergence in expression levels. Second, we conducted whole-genome sequencing and found five genes that are predicted to have functionally important amino acid substitutions. Finally, we conducted genome scan analysis and found that eight of these candidate genes were located in genomic islands of high differentiation, suggesting that they may be under divergent selection. The candidate genes included those involved in ATP synthesis and hormonal signalling, whose expression or amino acid changes may underlie the variation in salinity tolerance. Further functional molecular analysis of these genes will reveal the causative genetic and genomic changes underlying divergent adaptation.
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http://dx.doi.org/10.1111/mec.13875DOI Listing
January 2017

Accumulation of Deleterious Mutations on the Neo-Y Chromosome of Japan Sea Stickleback (Gasterosteus nipponicus).

J Hered 2017 01 10;108(1):63-68. Epub 2016 Sep 10.

From the Division of Ecological Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan (Yoshida and Kitano) and Division of Ecology and Evolutionary Biology, Tohoku University, Aramaki-aza-Aoba, Aobaku, Sendai, Miyagi 980-8578, Japan (Makino).

Degeneration of Y chromosomes is a common evolutionary path of XY sex chromosome systems. Recent genomic studies in flies and plants have revealed that even young neo-sex chromosomes with the age of a few million years show signs of Y degeneration, such as the accumulation of nonsense and frameshift mutations. However, it remains unclear whether neo-Y chromosomes also show rapid degeneration in fishes, which often have homomorphic sex chromosomes. Here, we investigated whether a neo-Y chromosome of Japan Sea stickleback (Gasterosteus nipponicus), which was formed by a Y-autosome fusion within the last 2 million years, accumulates deleterious mutations. Our previous genomic analyses did not detect excess nonsense and frameshift mutations on the Japan Sea stickleback neo-Y. In the present study, we found that the nonrecombining region of the neo-Y near the fusion end has accumulated nonsynonymous mutations altering amino acids of evolutionarily highly conserved residues. Enrichment of gene ontology terms related to protein phosphorylation and cellular protein modification process was found in the genes with potentially deleterious mutations on the neo-Y. These results suggest that the neo-Y of the Japan Sea stickleback has already accumulated mutations that may impair protein functions.
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http://dx.doi.org/10.1093/jhered/esw054DOI Listing
January 2017

Whole-genome sequencing reveals small genomic regions of introgression in an introduced crater lake population of threespine stickleback.

Ecol Evol 2016 04 2;6(7):2190-204. Epub 2016 Mar 2.

Division of Ecological Genetics Department of Population Genetics National Institute of Genetics Mishima Shizuoka Japan; Department of Genetics SOKENDAI (The Graduate University for Advanced Studies) Mishima Shizuoka Japan.

Invasive species pose a major threat to biological diversity. Although introduced populations often experience population bottlenecks, some invasive species are thought to be originated from hybridization between multiple populations or species, which can contribute to the maintenance of high genetic diversity. Recent advances in genome sequencing enable us to trace the evolutionary history of invasive species even at whole-genome level and may help to identify the history of past hybridization that may be overlooked by traditional marker-based analysis. Here, we conducted whole-genome sequencing of eight threespine stickleback (Gasterosteus aculeatus) individuals, four from a recently introduced crater lake population and four of the putative source population. We found that both populations have several small genomic regions with high genetic diversity, which resulted from introgression from a closely related species (Gasterosteus nipponicus). The sizes of the regions were too small to be detected with traditional marker-based analysis or even some reduced-representation sequencing methods. Further amplicon sequencing revealed linkage disequilibrium around an introgression site, which suggests the possibility of selective sweep at the introgression site. Thus, interspecies introgression might predate introduction and increase genetic variation in the source population. Whole-genome sequencing of even a small number of individuals can therefore provide higher resolution inference of history of introduced populations.
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http://dx.doi.org/10.1002/ece3.2047DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4782248PMC
April 2016

Genetic Architecture of the Variation in Male-Specific Ossified Processes on the Anal Fins of Japanese Medaka.

G3 (Bethesda) 2015 Oct 28;5(12):2875-84. Epub 2015 Oct 28.

Division of Ecological Genetics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan School of Life Sciences, SOKENDAI, Mishima, Shizuoka 411-8540, Japan

Traits involved in reproduction evolve rapidly and show great diversity among closely related species. However, the genetic mechanisms that underlie the diversification of courtship traits are mostly unknown. Japanese medaka fishes (Oryzias latipes) use anal fins to attract females and to grasp females during courtship; the males have longer anal fins with male-specific ossified papillary processes on the fin rays. However, anal fin morphology varies between populations: the southern populations tend to have longer anal fins and more processes than the northern populations. In the present study, we conducted quantitative trait locus (QTL) mapping to investigate the genetic architecture underlying the variation in the number of papillary processes of Japanese medaka fish and compared the QTL with previously identified QTL controlling anal fin length. First, we found that only a few QTL were shared between anal fin length and papillary process number. Second, we found that the numbers of papillary processes on different fin rays often were controlled by different QTL. Finally, we produced another independent cross and found that some QTL were repeatable between the two crosses, whereas others were specific to only one cross. These results suggest that variation in the number of papillary processes is polygenic and controlled by QTL that are distinct from those controlling anal fin length. Thus, different courtship traits in Japanese medaka share a small number of QTL and have the potential for independent evolution.
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http://dx.doi.org/10.1534/g3.115.021956DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4683658PMC
October 2015

A microsatellite-based genetic linkage map and putative sex-determining genomic regions in Lake Victoria cichlids.

Gene 2015 Apr 30;560(2):156-64. Epub 2015 Jan 30.

Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan; Foundation for Advancement of International Science, Tsukuba 305-0821, Japan; Department of Life Sciences, National Cheng Kung University, Tainan 701, Taiwan. Electronic address:

Cichlid fishes in East Africa have undergone extensive adaptive radiation, which has led to spectacular diversity in their morphology and ecology. To date, genetic linkage maps have been constructed for several tilapias (riverine), Astatotilapia burtoni (Lake Tanganyika), and hybrid lines of Lake Malawi cichlids to facilitate genome-wide comparative analyses. In the present study, we constructed a genetic linkage map of the hybrid line of Lake Victoria cichlids, so that maps of cichlids from all the major areas of East Africa will be available. The genetic linkage map shown here is derived from the F2 progeny of an interspecific cross between Haplochromis chilotes and Haplochromis sauvagei and is based on 184 microsatellite and two single-nucleotide polymorphism (SNP) markers. Most of the microsatellite markers used in the present study were originally designed for other genetic linkage maps, allowing us to directly compare each linkage group (LG) among different cichlid groups. We found 25 LGs, the total length of which was 1133.2cM with an average marker spacing of about 6.09cM. Our subsequent linkage mapping analysis identified two putative sex-determining loci in cichlids. Interestingly, one of these two loci is located on cichlid LG5, on which the female heterogametic ZW locus and several quantitative trait loci (QTLs) related to adaptive evolution have been reported in Lake Malawi cichlids. We also found that V1R1 and V1R2, candidate genes for the fish pheromone receptor, are located very close to the recently detected sex-determining locus on cichlid LG5. The genetic linkage map study presented here may provide a valuable foundation for studying the chromosomal evolution of East African cichlids and the possible role of sex chromosomes in generating their genomic diversity.
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http://dx.doi.org/10.1016/j.gene.2015.01.057DOI Listing
April 2015

Ontogenetic stage-specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations.

Mol Ecol 2014 Nov 13;23(21):5258-75. Epub 2014 Oct 13.

Ecological Genetics Laboratory, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan.

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age-specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex-specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex- and age-specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.
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http://dx.doi.org/10.1111/mec.12933DOI Listing
November 2014

Sex chromosome turnover contributes to genomic divergence between incipient stickleback species.

PLoS Genet 2014 Mar 13;10(3):e1004223. Epub 2014 Mar 13.

Ecological Genetics Laboratory, National Institute of Genetics, Shizuoka, Japan; PRESTO, Japan Science and Technology Agency, Saitama, Japan.

Sex chromosomes turn over rapidly in some taxonomic groups, where closely related species have different sex chromosomes. Although there are many examples of sex chromosome turnover, we know little about the functional roles of sex chromosome turnover in phenotypic diversification and genomic evolution. The sympatric pair of Japanese threespine stickleback (Gasterosteus aculeatus) provides an excellent system to address these questions: the Japan Sea species has a neo-sex chromosome system resulting from a fusion between an ancestral Y chromosome and an autosome, while the sympatric Pacific Ocean species has a simple XY sex chromosome system. Furthermore, previous quantitative trait locus (QTL) mapping demonstrated that the Japan Sea neo-X chromosome contributes to phenotypic divergence and reproductive isolation between these sympatric species. To investigate the genomic basis for the accumulation of genes important for speciation on the neo-X chromosome, we conducted whole genome sequencing of males and females of both the Japan Sea and the Pacific Ocean species. No substantial degeneration has yet occurred on the neo-Y chromosome, but the nucleotide sequence of the neo-X and the neo-Y has started to diverge, particularly at regions near the fusion. The neo-sex chromosomes also harbor an excess of genes with sex-biased expression. Furthermore, genes on the neo-X chromosome showed higher non-synonymous substitution rates than autosomal genes in the Japan Sea lineage. Genomic regions of higher sequence divergence between species, genes with divergent expression between species, and QTL for inter-species phenotypic differences were found not only at the regions near the fusion site, but also at other regions along the neo-X chromosome. Neo-sex chromosomes can therefore accumulate substitutions causing species differences even in the absence of substantial neo-Y degeneration.
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http://dx.doi.org/10.1371/journal.pgen.1004223DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3953013PMC
March 2014

Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks.

Curr Biol 2013 Oct 12;23(19):1884-8. Epub 2013 Sep 12.

Divisions of Human Biology and Basic Sciences, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109, USA.

Although descriptions of striking diversity in animal behavior are plentiful, little is known about the mechanisms by which behaviors change and evolve between groups. To fully understand behavioral evolution, it will be necessary to identify the genetic mechanisms that mediate behavioral change in a natural context. Genetic analysis of behavior can also reveal associations between behavior and morphological or neural phenotypes, providing insight into the proximate mechanisms that control behavior. Relatively few studies to date have successfully identified genes or genomic regions that contribute to behavioral variation among natural populations or species, particularly in vertebrates. Here, we apply genetic approaches to dissect a complex social behavior that has long fascinated biologists, schooling behavior. We performed quantitative trait locus (QTL) analysis of schooling in an F2 intercross between strongly schooling marine and weakly schooling benthic sticklebacks (Gasterosteus aculeatus) and found that distinct genetic modules control different aspects of schooling behavior. Two key components of the behavior, tendency to school and body position when schooling, are uncorrelated in hybrids and map to different genomic regions. Our results further point to a genetic link between one behavioral component, schooling position, and variation in the neurosensory lateral line.
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http://dx.doi.org/10.1016/j.cub.2013.07.058DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3828509PMC
October 2013

RNA sequencing reveals small RNAs differentially expressed between incipient Japanese threespine sticklebacks.

BMC Genomics 2013 Apr 2;14:214. Epub 2013 Apr 2.

Ecological Genetics Laboratory, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, Japan.

Background: Non-coding small RNAs, ranging from 20 to 30 nucleotides in length, mediate the regulation of gene expression and play important roles in many biological processes. One class of small RNAs, microRNAs (miRNAs), are highly conserved across taxa and mediate the regulation of the chromatin state and the post-transcriptional regulation of messenger RNA (mRNA). Another class of small RNAs is the Piwi-interacting RNAs, which play important roles in the silencing of transposons and other functional genes. Although the biological functions of the different small RNAs have been elucidated in several laboratory animals, little is known regarding naturally occurring variation in small RNA transcriptomes among closely related species.

Results: We employed next-generation sequencing technology to compare the expression profiles of brain small RNAs between sympatric species of the Japanese threespine stickleback (Gasterosteus aculeatus). We identified several small RNAs that were differentially expressed between sympatric Pacific Ocean and Japan Sea sticklebacks. Potential targets of several small RNAs were identified as repetitive sequences. Female-biased miRNA expression from the old X chromosome was also observed, and it was attributed to the degeneration of the Y chromosome.

Conclusions: Our results suggest that expression patterns of small RNA can differ between incipient species and may be a potential mechanism underlying differential mRNA expression and transposon activity.
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http://dx.doi.org/10.1186/1471-2164-14-214DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3637797PMC
April 2013

The contribution of female meiotic drive to the evolution of neo-sex chromosomes.

Evolution 2012 Oct 21;66(10):3198-208. Epub 2012 May 21.

Ecological Genetics Laboratory, Center for Frontier Research, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan.

Sex chromosomes undergo rapid turnover in certain taxonomic groups. One of the mechanisms of sex chromosome turnover involves fusions between sex chromosomes and autosomes. Sexual antagonism, heterozygote advantage, and genetic drift have been proposed as the drivers for the fixation of this evolutionary event. However, all empirical patterns of the prevalence of multiple sex chromosome systems across different taxa cannot be simply explained by these three mechanisms. In this study, we propose that female meiotic drive may contribute to the evolution of neo-sex chromosomes. The results of this study showed that in mammals, the XY(1) Y(2) sex chromosome system is more prevalent in species with karyotypes of more biarmed chromosomes, whereas the X(1) X(2) Y sex chromosome system is more prevalent in species with predominantly acrocentric chromosomes. In species where biarmed chromosomes are favored by female meiotic drive, X-autosome fusions (XY(1) Y(2) sex chromosome system) will be also favored by female meiotic drive. In contrast, in species with more acrocentric chromosomes, Y-autosome fusions (X(1) X(2) Y sex chromosome system) will be favored just because of the biased mutation rate toward chromosomal fusions. Further consideration should be given to female meiotic drive as a mechanism in the fixation of neo-sex chromosomes.
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http://dx.doi.org/10.1111/j.1558-5646.2012.01681.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3494977PMC
October 2012

B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes.

PLoS Genet 2011 Aug 18;7(8):e1002203. Epub 2011 Aug 18.

Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan.

The endemic cichlid fishes in Lake Victoria are a model system for speciation through adaptive radiation. Although the evolution of the sex-determination system may also play a role in speciation, little is known about the sex-determination system of Lake Victoria cichlids. To understand the evolution of the sex-determination system in these fish, we performed cytogenetic analysis in 11 cichlid species from Lake Victoria. B chromosomes, which are present in addition to standard chromosomes, were found at a high prevalence rate (85%) in these cichlids. In one species, B chromosomes were female-specific. Cross-breeding using females with and without the B chromosomes demonstrated that the presence of the B chromosomes leads to a female-biased sex ratio in this species. Although B chromosomes were believed to be selfish genetic elements with little effect on phenotype and to lack protein-coding genes, the present study provides evidence that B chromosomes have a functional effect on female sex determination. FISH analysis using a BAC clone containing B chromosome DNA suggested that the B chromosomes are derived from sex chromosomes. Determination of the nucleotide sequences of this clone (104.5 kb) revealed the presence of several protein-coding genes in the B chromosome, suggesting that B chromosomes have the potential to contain functional genes. Because some sex chromosomes in amphibians and arthropods are thought to be derived from B chromosomes, the B chromosomes in Lake Victoria cichlids may represent an evolutionary transition toward the generation of sex chromosomes.
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http://dx.doi.org/10.1371/journal.pgen.1002203DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3158035PMC
August 2011

Heritable differences in schooling behavior among threespine stickleback populations revealed by a novel assay.

PLoS One 2011 Mar 25;6(3):e18316. Epub 2011 Mar 25.

Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America.

Identifying the proximate and ultimate mechanisms of social behavior remains a major goal of behavioral biology. In particular, the complex social interactions mediating schooling behavior have long fascinated biologists, leading to theoretical and empirical investigations that have focused on schooling as a group-level phenomenon. However, methods to examine the behavior of individual fish within a school are needed in order to investigate the mechanisms that underlie both the performance and the evolution of schooling behavior. We have developed a technique to quantify the schooling behavior of an individual in standardized but easily manipulated social circumstances. Using our model school assay, we show that threespine sticklebacks (Gasterosteus aculeatus) from alternative habitats differ in behavior when tested in identical social circumstances. Not only do marine sticklebacks show increased association with the model school relative to freshwater benthic sticklebacks, they also display a greater degree of parallel swimming with the models. Taken together, these data indicate that marine sticklebacks exhibit a stronger tendency to school than benthic sticklebacks. We demonstrate that these population-level differences in schooling tendency are heritable and are shared by individuals within a population even when they have experienced mixed-population housing conditions. Finally, we begin to explore the stimuli that elicit schooling behavior in these populations. Our data suggest that the difference in schooling tendency between marine and benthic sticklebacks is accompanied by differential preferences for social vs. non-social and moving vs. stationary shelter options. Our study thus provides novel insights into the evolution of schooling behavior, as well as a new experimental approach to investigate the genetic and neural mechanisms that underlie this complex social behavior.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0018316PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3064674PMC
March 2011