Publications by authors named "Jun Kitano"

54 Publications

The evolutionary ecology of fatty-acid variation: Implications for consumer adaptation and diversification.

Ecol Lett 2021 Jun 10. Epub 2021 Jun 10.

Department of Fish Ecology and Evolution, Eawag, Center of Ecology, Evolution and Biochemistry, Swiss Federal Institute of Aquatic Science and Technology, Kastanienbaum, Switzerland.

The nutritional diversity of resources can affect the adaptive evolution of consumer metabolism and consumer diversification. The omega-3 long-chain polyunsaturated fatty acids eicosapentaenoic acid (EPA; 20:5n-3) and docosahexaenoic acid (DHA; 22:6n-3) have a high potential to affect consumer fitness, through their widespread effects on reproduction, growth and survival. However, few studies consider the evolution of fatty acid metabolism within an ecological context. In this review, we first document the extensive diversity in both primary producer and consumer fatty acid distributions amongst major ecosystems, between habitats and amongst species within habitats. We highlight some of the key nutritional contrasts that can shape behavioural and/or metabolic adaptation in consumers, discussing how consumers can evolve in response to the spatial, seasonal and community-level variation of resource quality. We propose a hierarchical trait-based approach for studying the evolution of consumers' metabolic networks and review the evolutionary genetic mechanisms underpinning consumer adaptation to EPA and DHA distributions. In doing so, we consider how the metabolic traits of consumers are hierarchically structured, from cell membrane function to maternal investment, and have strongly environment-dependent expression. Finally, we conclude with an outlook on how studying the metabolic adaptation of consumers within the context of nutritional landscapes can open up new opportunities for understanding evolutionary diversification.
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http://dx.doi.org/10.1111/ele.13771DOI Listing
June 2021

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

Multiple paths to the same destination: Influence of gene flow on convergent evolution.

Mol Ecol 2021 05 23;30(9):1939-1942. Epub 2021 Apr 23.

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

Elucidation of the genetic mechanisms of convergent evolution, the evolution of similar or the same phenotypes in phylogenetically independent lineages, helps predict how populations will respond to the same selective pressures. Convergent evolution can be caused by either the fixation of identical-by-descent alleles, independent mutations at the same gene, or mutations in different genes controlling the same trait. To what extent does the fixation of identical-by-descent alleles lead to convergent evolution in isolated populations where inflow of adaptive alleles from other populations is limited? In a From the Cover article in this issue of Molecular Ecology, Kemppainen et al. (2021) compared the genetic basis for the reduction of pelvic structures in three isolated freshwater populations of nine-spined stickleback (Pungitius pungitius) from Northern Europe. The authors used quantitative trait loci (QTL) mapping to reveal that the pelvic reduction in these three populations was caused by mutations at different genetic loci. In contrast to studies in three-spined stickleback (Gasterosteus aculeatus), where independently derived Pitx1 mutations were shown to be responsible for plate reduction across multiple freshwater populations, Kemppainen et al. (2021) found Pitx1 to be the candidate causative gene for only one population of P. pungitius. This study highlights the importance of genetic studies of convergent evolution, not only in the presence of gene flow but also in its absence for a better understanding of the genetic architecture of convergent evolution.
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http://dx.doi.org/10.1111/mec.15896DOI Listing
May 2021

Genome editing reveals fitness effects of a gene for sexual dichromatism in Sulawesian fishes.

Nat Commun 2021 03 1;12(1):1350. Epub 2021 Mar 1.

Ecological Genetics Laboratory, Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Shizuoka, Japan.

Sexual selection drives rapid phenotypic diversification of mating traits. However, we know little about the causative genes underlying divergence in sexually selected traits. Here, we investigate the genetic basis of male mating trait diversification in the medaka fishes (genus Oryzias) from Sulawesi, Indonesia. Using linkage mapping, transcriptome analysis, and genome editing, we identify csf1 as a causative gene for red pectoral fins that are unique to male Oryzias woworae. A cis-regulatory mutation enables androgen-induced expression of csf1 in male fins. csf1-knockout males have reduced red coloration and require longer for mating, suggesting that coloration can contribute to male reproductive success. Contrary to expectations, non-red males are more attractive to a predatory fish than are red males. Our results demonstrate that integrating genomics with genome editing enables us to identify causative genes underlying sexually selected traits and provides a new avenue for testing theories of sexual selection.
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http://dx.doi.org/10.1038/s41467-021-21697-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7921647PMC
March 2021

Multiple waves of freshwater colonization of the three-spined stickleback in the Japanese Archipelago.

BMC Evol Biol 2020 11 3;20(1):143. Epub 2020 Nov 3.

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

Background: The three-spined stickleback (Gasterosteus aculeatus) is a remarkable system to study the genetic mechanisms underlying parallel evolution during the transition from marine to freshwater habitats. Although the majority of previous studies on the parallel evolution of sticklebacks have mainly focused on postglacial freshwater populations in the Pacific Northwest of North America and northern Europe, we recently use Japanese stickleback populations for investigating shared and unique features of adaptation and speciation between geographically distant populations. However, we currently lack a comprehensive phylogeny of the Japanese three-spined sticklebacks, despite the fact that a good phylogeny is essential for any evolutionary and ecological studies. Here, we conducted a phylogenomic analysis of the three-spined stickleback in the Japanese Archipelago.

Results: We found that freshwater colonization occurred in multiple waves, each of which may reflect different interglacial isolations. Some of the oldest freshwater populations from the central regions of the mainland of Japan (hariyo populations) were estimated to colonize freshwater approximately 170,000 years ago. The next wave of colonization likely occurred approximately 100,000 years ago. The inferred origins of several human-introduced populations showed that introduction occurred mainly from nearby habitats. We also found a new habitat of the three-spined stickleback sympatric with the Japan Sea stickleback (Gasterosteus nipponicus).

Conclusions: These Japanese stickleback systems differ from those in the Pacific Northwest of North America and northern Europe in terms of divergence time and history. Stickleback populations in the Japanese Archipelago offer valuable opportunities to study diverse evolutionary processes in historical and contemporary timescales.
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http://dx.doi.org/10.1186/s12862-020-01713-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7641863PMC
November 2020

Genome-wide patterns of divergence and introgression after secondary contact between sticklebacks.

Philos Trans R Soc Lond B Biol Sci 2020 08 13;375(1806):20190548. Epub 2020 Jul 13.

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

Speciation is a continuous process. Although it is known that differential adaptation can initiate divergence even in the face of gene flow, we know relatively little about the mechanisms driving complete reproductive isolation and the genomic patterns of divergence and introgression at the later stages of speciation. Sticklebacks contain many pairs of sympatric species differing in levels of reproductive isolation and divergence history. Nevertheless, most previous studies have focused on young species pairs. Here, we investigated two sympatric stickleback species, and , whose habitats overlap in eastern Hokkaido; these species show hybrid male sterility, suggesting that they may be at a late stage of speciation. Our demographic analysis using whole-genome sequence data showed that these species split 1.73 Ma and came into secondary contact 37 200 years ago after a period of allopatry. This long period of allopatry might have promoted the evolution of intrinsic incompatibility. Although we detected on-going gene flow and signatures of introgression, overall genomic divergence was high, with considerable heterogeneity across the genome. The heterogeneity was significantly associated with variation in recombination rate. This sympatric pair provides new avenues to investigate the late stages of the stickleback speciation continuum. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.
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http://dx.doi.org/10.1098/rstb.2019.0548DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423276PMC
August 2020

Patterns of genomic divergence and introgression between Japanese stickleback species with overlapping breeding habitats.

J Evol Biol 2021 01 8;34(1):114-127. Epub 2020 Jul 8.

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

With only a few absolute geographic barriers in marine environments, the factors maintaining reproductive isolation among marine organisms remain elusive. However, spatial structuring in breeding habitat can contribute to reproductive isolation. This is particularly important for marine organisms that migrate to use fresh- or brackish water environments to breed. The Japanese Gasterosteus stickleback species, the Pacific Ocean three-spined stickleback (G. aculeatus) and the Japan Sea stickleback (G. nipponicus) overwinter in the sea, but migrate to rivers for spawning. Although they co-occur at several locations across the Japanese islands, they are reproductively isolated. Our previous studies in Bekanbeushi River showed that the Japan Sea stickleback spawns in the estuary, while the Pacific Ocean stickleback mainly spawns further upstream in freshwater. Overall genomic divergence was very high with many interspersed regions of introgression. Here, we investigated genomic divergence and introgression between the sympatric species in the much shorter Tokotan River, where they share spawning sites. The levels of genome-wide divergence were reduced and introgression was increased, suggesting that habitat isolation substantially contributes to a reduction in gene flow. We also found that genomic regions of introgression were largely shared between the two systems. Furthermore, some regions of introgression were located near loci with a heterozygote advantage for juvenile survival. Taken together, introgression may be partially driven by adaptation in this system. Although, the two species remain clearly genetically differentiated. Regions with low recombination rates showed especially low introgression. Speciation reversal is therefore likely prevented by barriers other than habitat isolation.
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http://dx.doi.org/10.1111/jeb.13664DOI Listing
January 2021

Differences in the contributions of sex linkage and androgen regulation to sex-biased gene expression in juvenile and adult sticklebacks.

J Evol Biol 2020 Jun 13. Epub 2020 Jun 13.

Department of Biological Sciences, Faculty of Science, Shizuoka University, Surugaku, Shizuoka, Japan.

Different evolutionary interests between males and females can lead to the evolution of sexual dimorphism. However, intersex genetic correlations due to the shared genome can constrain the evolution of sexual dimorphism, resulting in intra-locus sexual conflict. One of the mechanisms resolving this conflict is sex linkage, which allows males and females to carry different alleles on sex chromosomes. Another is a regulatory mutation causing sex-biased gene expression, which is often mediated by gonadal steroids in vertebrates. How do these two mechanisms differ in the contributions to the resolution of intra-locus sexual conflict? The magnitude of sexual conflict often varies between the juvenile and adult stages. Because gonadal steroids change in titre during development, we hypothesized that gonadal steroids play a role in sexual dimorphism expression only at certain developmental stages, whereas sex linkage is more important for sexual dimorphism expressed throughout life. Our brain transcriptome analysis of juvenile and adult threespine sticklebacks showed that the majority of genes that were sex-biased in both stages were sex-linked. The relative contribution of androgen-dependent regulation to the sex-biased transcriptome increased and that of sex linkage declined in adults compared to juveniles. The magnitude of the sex differences was greater in sex-linked genes than androgen-responsive genes, suggesting that sex linkage is more effective than androgen regulation in the production of large sex differences in gene expression. Overall, our data are consistent with the hypothesis that sex linkage is effective in resolving sexual conflict throughout life, whereas androgen-dependent regulation can contribute to temporary resolution of sexual conflict.
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http://dx.doi.org/10.1111/jeb.13662DOI Listing
June 2020

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

Diversity in reproductive seasonality in the three-spined stickleback, .

J Exp Biol 2020 02 7;223(Pt Suppl 1). Epub 2020 Feb 7.

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

The annual timing of reproduction is a key life history trait with a large effect on fitness. Populations often vary in the timing and duration of reproduction to adapt to different seasonality of ecological and environmental variables between habitats. However, little is known about the molecular genetic mechanisms underlying interpopulation variation in reproductive seasonality. Here, we demonstrate that the three-spined stickleback () is a good model for molecular genetic analysis of variations in reproductive seasonality. We first compiled data on reproductive seasons of diverse ecotypes, covering marine-anadromous, lake and stream ecotypes, of three-spined stickleback inhabiting a wide range of latitudes. Our analysis showed that both ecotype and latitude significantly contribute to variation in reproductive seasons. Stream ecotypes tend to start breeding earlier and end later than other ecotypes. Populations from lower latitudes tend to start breeding earlier than those from higher latitudes in all three ecotypes. Additionally, stream ecotypes tend to have extended breeding seasons at lower latitudes than at higher latitudes, leading to nearly year-round reproduction in the most southern stream populations. A review of recent progress in our understanding of the physiological mechanisms underlying seasonal reproduction in the three-spined stickleback indicates that photoperiod is an important external cue that stimulates and/or suppresses reproduction in this species. Taking advantage of genomic tools available for this species, the three-spined stickleback will be a good model to investigate what kinds of genes and mutations underlie variations in the physiological signalling pathways that regulate reproduction in response to photoperiod.
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http://dx.doi.org/10.1242/jeb.208975DOI Listing
February 2020

Convergent evolution of body color between sympatric freshwater fishes via different visual sensory evolution.

Ecol Evol 2019 Jun 26;9(11):6389-6398. Epub 2019 Apr 26.

Tropical Biosphere Research Center University of the Ryukyus Okinawa Japan.

Although there are many examples of color evolution potentially driven by sensory drive, only few studies have examined whether distinct species inhabiting the same environments evolve similar body colors via shared sensory mechanisms. In this study, we tested whether two sympatric freshwater fish taxa, halfbeaks of the genus and ricefishes of the genus in Sulawesi Island, converge in both body color and visual sensitivity. After reconstructing the phylogeny separately for and using transcriptome-wide sequences, we demonstrated positive correlations of body redness between these two taxa across environments, even after phylogenetic corrections, which support convergent evolution. However, substantial differences were observed in the expression profiles of opsin genes in the eyes between and . Particularly, the expression levels of the long wavelength-sensitive genes were negatively correlated between the taxa, indicating that they have different visual sensitivities despite living in similar light environments. Thus, the convergence of body colorations between these two freshwater fish taxa was not accompanied by convergence in opsin sensitivities. This system presents a case in which body color convergence can occur between sympatric species via different mechanisms.
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http://dx.doi.org/10.1002/ece3.5211DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580282PMC
June 2019

A key metabolic gene for recurrent freshwater colonization and radiation in fishes.

Science 2019 05;364(6443):886-889

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

Colonization of new ecological niches has triggered large adaptive radiations. Although some lineages have made use of such opportunities, not all do so. The factors causing this variation among lineages are largely unknown. Here, we show that deficiency in docosahexaenoic acid (DHA), an essential ω-3 fatty acid, can constrain freshwater colonization by marine fishes. Our genomic analyses revealed multiple independent duplications of the fatty acid desaturase gene in stickleback lineages that subsequently colonized and radiated in freshwater habitats, but not in close relatives that failed to colonize. Transgenic manipulation of in marine stickleback increased their ability to synthesize DHA and survive on DHA-deficient diets. Multiple freshwater ray-finned fishes also show a convergent increase in copies, indicating its key role in freshwater colonization.
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http://dx.doi.org/10.1126/science.aau5656DOI Listing
May 2019

A four-questions perspective on public information use in sticklebacks (Gasterosteidae).

R Soc Open Sci 2019 Feb 20;6(2):181735. Epub 2019 Feb 20.

Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, Fife KY16 9TF, UK.

Whether learning primarily reflects general processes or species-specific challenges is a long-standing matter of dispute. Here, we present a comprehensive analysis of public information use (PI-use) in sticklebacks (Gasterosteidae). PI-use is a form of social learning by which animals are able to assess the relative quality of resources, here prey patches, by observing the behaviour of others. PI-use was highly specific with only and their closest relative showing evidence of PI-use. We saw no effects of ontogenetic experience upon PI-use in . Experiments with live demonstrators and animated fish revealed that heightened activity and feeding strikes by foraging conspecifics are important cues in the transmission of PI. Finally, PI-use was the only form of learning in which and another stickleback, differed. PI-use in sticklebacks is species-specific and may represent an 'ecological specialization' for social foraging. Whether this reflects selection on perception, attentional or cognitive processes remains to be determined.
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http://dx.doi.org/10.1098/rsos.181735DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408396PMC
February 2019

Parallel transcriptome evolution in stream threespine sticklebacks.

Dev Growth Differ 2019 Jan 4;61(1):104-113. Epub 2018 Nov 4.

Department of Biological Science, Faculty of Science, Shizuoka University, Surugaku, Shizuoka, Japan.

Natural selection can cause similar phenotypic evolution in phylogenetically independent lineages inhabiting similar environments. Compared to morphological, behavioral, and physiological traits, little is known about the parallel evolution of transcriptome. Furthermore, the relative contribution of cis- and trans-regulatory changes to parallel transcriptome evolution largely remains unclear. The threespine stickleback fish (Gasterosteus aculeatus) is a great model for studying parallel evolution because its ancestral marine populations independently colonized freshwater habitats in multiple geographical regions, resulting in independent pairs of marine and freshwater ecotypes in each region. Here, we investigated transcriptomic parallelism among the marine and stream ecotypes of Japanese and Canadian threespine sticklebacks by conducting common garden experiments and microarray analysis of the brain, which controls several physiological and behavioral traits differing between these ecotypes. We found parallel expression differences in 103 genes, including those encoding the enzymes involved in taurine synthesis and glycoprotein hydrolysis. The number of genes differentially expressed in parallel was significantly larger than the number of genes showing an antiparallel pattern (71 genes). To investigate the genetic architecture underlying transcriptome divergence, we re-analyzed the previous expression quantitative trait locus (eQTL) data and found that most eQTLs were located on the same chromosome as the transcripts, possibly in cis-regulatory regions. Furthermore, the effect sizes of the eQTLs on the same chromosomes were larger than those on different chromosomes. Thus, we found that divergence in the brain transcriptome between the ecotypes shows parallelism and is mainly caused by genetic changes occurring on the same chromosome as the target genes.
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http://dx.doi.org/10.1111/dgd.12576DOI Listing
January 2019

The Origin of a New Sex Chromosome by Introgression between Two Stickleback Fishes.

Mol Biol Evol 2019 01;36(1):28-38

Department of Integrative Biology, University of Texas, Austin, TX.

Introgression is increasingly recognized as a source of genetic diversity that fuels adaptation. Its role in the evolution of sex chromosomes, however, is not well known. Here, we confirm the hypothesis that the Y chromosome in the ninespine stickleback, Pungitius pungitius, was established by introgression from the Amur stickleback, P. sinensis. Using whole genome resequencing, we identified a large region of Chr 12 in P. pungitius that is diverged between males and females. Within but not outside of this region, several lines of evidence show that the Y chromosome of P. pungitius shares a most recent common ancestor not with the X chromosome, but with the homologous chromosome in P. sinensis. Accumulation of repetitive elements and gene expression changes on the new Y are consistent with a young sex chromosome in early stages of degeneration, but other hallmarks of Y chromosomes have not yet appeared. Our findings indicate that porous species boundaries can trigger rapid sex chromosome evolution.
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http://dx.doi.org/10.1093/molbev/msy181DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340465PMC
January 2019

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

Lateralized expression of left-right axis formation genes is shared by adult brains of lefty and righty scale-eating cichlids.

Comp Biochem Physiol Part D Genomics Proteomics 2018 12 7;28:99-106. Epub 2018 Jul 7.

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

Variation in the laterality often exists within species and can be maintained by frequency-dependent selection. Although the molecular developmental mechanisms underlying the left-right axis formation have been investigated, the genomic mechanisms underlying variation in laterality remain largely unknown. The scale-eating cichlid Perissodus microlepis in Lake Tanganyika exhibit lateralized predation; lefty individuals with the mouth opening toward the right preferentially attack on the prey's left trunk, while righty individuals with the opposite opening attacks on the right trunk. Here, we performed RNA-sequencing and subsequent confirmation with quantitative-PCR in the telencephalon, optic tectum, and hindbrain of the cichlid and identified five genes (pkd1b, ntn1b, ansn, pde6g, and rbp4l1) that were differentially expressed between the hemispheres regardless of the laterality. Surprisingly, pkd1b and ntn1b are involved in nodal and netrin signalling, respectively, which are important for left-right asymmetry formation during early embryogenesis. This result indicates that nodal- and netrin-related signals may also play important roles in the maintenance of asymmetry in adult brain. By contrast, no genes showed reversal of lateral differences between lefty and righty individuals in any brain regions examined, suggesting that laterality in the scale-eating cichlid does not simply result from inversion of the left-right asymmetry of gene expression.
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http://dx.doi.org/10.1016/j.cbd.2018.07.002DOI Listing
December 2018

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

Sex Differences in Recombination in Sticklebacks.

G3 (Bethesda) 2018 05 31;8(6):1971-1983. Epub 2018 May 31.

Department of Integrative Biology, University of Texas at Austin, Texas 78712.

Recombination often differs markedly between males and females. Here we present the first analysis of sex-specific recombination in sticklebacks. Using whole-genome sequencing of 15 crosses between and , we localized 698 crossovers with a median resolution of 2.3 kb. We also used a bioinformatic approach to infer historical sex-averaged recombination patterns for both species. Recombination is greater in females than males on all chromosomes, and overall map length is 1.64 times longer in females. The locations of crossovers differ strikingly between sexes. Crossovers cluster toward chromosome ends in males, but are distributed more evenly across chromosomes in females. Suppression of recombination near the centromeres in males causes crossovers to cluster at the ends of long arms in acrocentric chromosomes, and greatly reduces crossing over on short arms. The effect of centromeres on recombination is much weaker in females. Genomic differentiation between and is strongly correlated with recombination rate, and patterns of differentiation along chromosomes are strongly influenced by male-specific telomere and centromere effects. We found no evidence for fine-scale correlations between recombination and local gene content in either sex. We discuss hypotheses for the origin of sexual dimorphism in recombination and its consequences for sexually antagonistic selection and sex chromosome evolution.
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http://dx.doi.org/10.1534/g3.118.200166DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5982825PMC
May 2018

Impact of the huge 2011 Tohoku-oki tsunami on the phenotypes and genotypes of Japanese coastal threespine stickleback populations.

Sci Rep 2018 01 26;8(1):1684. Epub 2018 Jan 26.

Gifu-keizai University, Kitakata 5-50, Ogaki, Gifu, 503-8550, Japan.

On March 11, 2011, a large earthquake occurred, causing a tsunami which struck the Pacific coast of northeast Japan. We investigated the ecological and genetic effects of the large tsunami on the threespine stickleback (genus Gasterosteus) populations in Otsuchi Town, which was one of the most severely damaged areas after the tsunami. Our environmental surveys showed that spring water may have contributed to the habitat recovery. Morphological analysis of the stickleback before and after the tsunami showed morphological shifts in the gill raker number, which is a foraging trait. Genetic analyses revealed that the allelic richness of one population was maintained after the tsunami, whereas that of another decreased in 2012 and then started to recover in 2013. Additionally, we found that the large tsunami and ground subsidence created new spring water-fed pools with sticklebacks, suggesting that the tsunami brought sticklebacks into these pools. Genetic analysis of this population showed that this population might be derived from hybridization between freshwater Gasterosteus aculeatus and anadromous G. nipponicus. Overall, our data indicate that tsunamis can influence morphologies and genetic structures of freshwater fishes. Furthermore, spring water may play important roles in the maintenance and creation of fish habitats, faced with environmental disturbance.
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http://dx.doi.org/10.1038/s41598-018-20075-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5785970PMC
January 2018

Phylogenomics reveals habitat-associated body shape divergence in Oryzias woworae species group (Teleostei: Adrianichthyidae).

Mol Phylogenet Evol 2018 01 9;118:194-203. Epub 2017 Oct 9.

Tropical Biosphere Research Center, University of the Ryukyus, Okinawa 903-0213, Japan. Electronic address:

The Oryzias woworae species group, composed of O. asinua, O. wolasi, and O. woworae, is widely distributed in southeastern Sulawesi, an island in the Indo-Australian Archipelago. Deep-elongated body shape divergence is evident among these three species to the extent that it is used as a species-diagnostic character. These fishes inhabit a variety of habitats, ranging from upper streams to ponds, suggesting that the body shape divergence among the three species may reflect adaptation to local environments. First, our geometric morphometrics among eight local populations of this species group revealed that the three species cannot be separated by body shape and that riverine populations had more elongated bodies and longer caudal parts than lacustrine populations. Second, their phylogenetic relationships did not support the presence of three species; phylogenies using mitochondrial DNA and genomic data obtained from RNA-Seq revealed that the eight populations could not be sorted into three different clades representing three described species. Third, phylogenetic corrections of body shape variations and ancestral state reconstruction of body shapes demonstrated that body shape divergence between riverine and lacustrine populations persisted even if the phylogenies were considered and that body shape evolved rapidly irrespective of phylogeny. Sexual dimorphism in body shape was also evident, but the degree of dimorphism did not significantly differ between riverine and lacustrine populations after phylogenetic corrections, suggesting that sexual selection may not substantially contribute to geographical variations in body shape. Overall, these results indicate that the deep-elongated body shape divergence of the O. woworae species group evolved locally in response to habitat environments, such as water currents, and that a thorough taxonomic reexamination of the O. woworae species group may be necessary.
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http://dx.doi.org/10.1016/j.ympev.2017.10.005DOI Listing
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

Toward conservation of genetic and phenotypic diversity in Japanese sticklebacks.

Genes Genet Syst 2016 Oct 10;91(2):77-84. Epub 2016 Jun 10.

Division of Ecological Genetics, National Institute of Genetics.

Stickleback fishes have been established as a leading model system for studying the genetic mechanisms that underlie naturally occurring phenotypic diversification. Because of the tremendous diversification achieved by stickleback species in various environments, different geographical populations have unique phenotypes and genotypes, which provide us with unique opportunities for evolutionary genetic research. Among sticklebacks, Japanese species have several unique characteristics that have not been found in other populations. The sympatric marine threespine stickleback species Gasterosteus aculeatus and G. nipponicus (Japan Sea stickleback) are a good system for speciation research. Gasterosteus nipponicus also has several unique characteristics, such as neo-sex chromosomes and courtship behaviors, that differ from those of G. aculeatus. Several freshwater populations derived from G. aculeatus (Hariyo threespine stickleback) inhabit spring-fed ponds and streams in central Honshu and exhibit year-round reproduction, which has never been observed in other stickleback populations. Four species of ninespine stickleback, including Pungitius tymensis and the freshwater, brackish water and Omono types of the P. pungitius-P. sinensis complex, are also excellent model systems for speciation research. Anthropogenic alteration of environments, however, has exposed several Japanese stickleback populations to the risk of extinction and has actually led to extinction of several populations and species. Pungitius kaibarae, which is endemic to East Asia, used to inhabit Kyoto and Hyogo prefectures, but is now extinct. Causes of extinction include depletion of spring water, landfill of habitats, and construction of river-mouth weirs. Here, we review the importance of Japanese sticklebacks as genetic resources, the status of several endangered stickleback populations and species, and the factors putting these populations at risk.
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http://dx.doi.org/10.1266/ggs.15-00082DOI Listing
October 2016

The intricate relationship between sexually antagonistic selection and the evolution of sex chromosome fusions.

J Theor Biol 2016 09 31;404:97-108. Epub 2016 May 31.

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

Sex chromosomes are among the most evolutionarily labile features in some groups of animals. One of the mechanisms causing structural changes of sex chromosomes is fusion with an autosome. A recent study showed that the establishment rates of Y chromosome-autosome fusions are much higher than those of other fusions (i.e., X-autosome, W-autosome, and Z-autosome fusions) in fishes and reptiles. Although sexually antagonistic selection may be one of the most important driving forces of sex chromosome-autosome fusions, a previous theoretical analysis showed that sexually antagonistic selection alone cannot explain the excess of Y-autosome fusions in these taxa. This previous analysis, however, is based on the assumption that sexually antagonistic selection is symmetric, sexually antagonistic alleles are maintained only by selection-drift balance (i.e., no supply of mutation), and only one type of fusion arises within a population. Here, we removed these assumptions and made an individual-based model to simulate the establishment of sex chromosome-autosome fusions. Our simulations showed that the highest establishment rate of Y-autosome fusion can be achieved when the fusion captures a rare male-beneficial allele, if the recurrent mutation rates are high enough to maintain the polymorphism of alleles with asymmetric, sexually antagonistic effects. Our results demonstrate that sexually antagonistic selection can influence the dynamics of sex chromosome structural changes, but the type of fusion that becomes the most common depends on fusion rates, recurrent mutation rates, and selection regimes. Because the evolutionary fate of sex chromosome-autosome fusions is highly parameter-sensitive, further attempts to empirically measure these parameters in natural populations are essential for a better understanding of the roles of sexually antagonistic selection in sex chromosome evolution.
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http://dx.doi.org/10.1016/j.jtbi.2016.05.036DOI Listing
September 2016

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

Y fuse? Sex chromosome fusions in fishes and reptiles.

PLoS Genet 2015 May 20;11(5):e1005237. Epub 2015 May 20.

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

Chromosomal fusion plays a recurring role in the evolution of adaptations and reproductive isolation among species, yet little is known of the evolutionary drivers of chromosomal fusions. Because sex chromosomes (X and Y in male heterogametic systems, Z and W in female heterogametic systems) differ in their selective, mutational, and demographic environments, those differences provide a unique opportunity to dissect the evolutionary forces that drive chromosomal fusions. We estimate the rate at which fusions between sex chromosomes and autosomes become established across the phylogenies of both fishes and squamate reptiles. Both the incidence among extant species and the establishment rate of Y-autosome fusions is much higher than for X-autosome, Z-autosome, or W-autosome fusions. Using population genetic models, we show that this pattern cannot be reconciled with many standard explanations for the spread of fusions. In particular, direct selection acting on fusions or sexually antagonistic selection cannot, on their own, account for the predominance of Y-autosome fusions. The most plausible explanation for the observed data seems to be (a) that fusions are slightly deleterious, and (b) that the mutation rate is male-biased or the reproductive sex ratio is female-biased. We identify other combinations of evolutionary forces that might in principle account for the data although they appear less likely. Our results shed light on the processes that drive structural changes throughout the genome.
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http://dx.doi.org/10.1371/journal.pgen.1005237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4439076PMC
May 2015