Jun Kitano

Sex Determination: Why So Many Ways of Doing It?

Sex is universal amongst most eukaryotes, yet a remarkable diversity of sex determining mechanisms exists. We review our current understanding of how and why sex determination evolves in animals and plants.

A role for a neo-sex chromosome in stickleback speciation

Sexual antagonism, or conflict between the sexes, has been proposed as a driving force in both sex-chromosome turnover and speciation. Although closely related species often have different sex-chromosome systems, it is unknown whether sex-chromosome turnover contributes to the evolution of reproductive isolation between species. Here we show that a newly evolved sex chromosome contains genes that contribute to speciation in threespine stickleback fish (Gasterosteus aculeatus). We first identified a neo-sex chromosome system found only in one member of a sympatric species pair in Japan. We then performed genetic linkage mapping of male-specific traits important for reproductive isolation between the Japanese species pair. The neo-X chromosome contains loci for male courtship display traits that contribute to behavioural isolation, whereas the ancestral X chromosome contains loci for both behavioural isolation and hybrid male sterility. Our work not only provides strong evidence for a large X-effect on reproductive isolation in a vertebrate system, but also provides direct evidence that a young neo-X chromosome contributes to reproductive isolation between closely related species. Our data indicate that sex-chromosome turnover might have a greater role in speciation than was previously appreciated.

Adaptive Divergence in the Thyroid Hormone Signaling Pathway in the Stickleback Radiation

During adaptive radiations, animals colonize diverse environments, which requires adaptation in multiple phenotypic traits. Because hormones mediate the dynamic regulation of suites of phenotypic traits, evolutionary changes in hormonal signaling pathways might contribute to adaptation to new environments. Here we report changes in the thyroid hormone signaling pathway in stream-resident ecotypes of threespine stickleback fish (Gasterosteus aculeatus), which have repeatedly evolved from ancestral marine ecotypes. Stream-resident fish exhibit a lower plasma concentration of thyroid hormone and a lower metabolic rate, which is likely adaptive for permanent residency in small streams. The thyroid-stimulating hormone-β2 (TSHβ2) gene exhibited significantly lower mRNA expression in pituitary glands of stream-resident sticklebacks relative to marine sticklebacks. Some of the difference in TSHβ2 transcript levels can be explained by cis-regulatory differences at the TSHβ2 gene locus. Consistent with these expression differences, a strong signature of divergent natural selection was found at the TSHβ2 genomic locus. By contrast, there were no differences between the marine and stream-resident ecotypes in mRNA levels or genomic sequence in the paralogous TSHβ1 gene. Our data indicate that evolutionary changes in hormonal signaling have played an important role in the postglacial adaptive radiation of sticklebacks.

Sexual Dimorphism in the External Morphology of the Threespine Stickleback (Gasterosteus aculeatus)

Abstract Information about sexual dimorphism is essential for understanding the ecology, behavior, and life history of a species, as well as for making morphological comparisons between populations. Furthermore, in order to understand the evolution of sexual dimorphism, it is important to know whether sexual dimorphism is genetically determined or the result of phenotypic plasticity. To this end, we have characterized patterns of sexual dimorphism in the threespine stickleback (Gasterosteus aculeatus). These fish are widely distributed throughout the temperate Northern Hemisphere, and their behavior, ecology, and evolution have been extensively characterized. We first examined sexual dimorphism in morphometric and meristic characters of wild-caught threespine sticklebacks from multiple populations that demonstrate different life history strategies in order to understand general patterns of sexual dimorphism in the threespine stickleback. Next, we made several crosses by in vitro fertilization and raised them in the laboratory to investigate developmental and genetic contributions to sexual dimorphism. Morphological analysis of wild-caught breeding males and females from four North American and six Asian populations revealed that adult males have larger heads and mouths than adult females in all populations. In contrast, adult females were longer in standard length and had longer pelvic girdles than adult males in many populations. Sexual dimorphism in dorsal-spine length was variable among populations. Except for body size, sexual dimorphism in most external morphological traits was similar between wild-caught and lab-reared fish. However, sexual dimorphism was only observed after the fish became reproductively mature. These results suggest that general features of secondary sexual characters are shared across different threespine stickleback populations and that sexual dimorphism in some morphological traits may have a genetic basis.

Turnover of sex chromosomes and speciation in fishes

Closely related species of fishes often have different sex chromosome systems. Such rapid turnover of sex chromosomes can occur by several mechanisms, including fusions between an existing sex chromosome and an autosome. These fusions can result in a multiple sex chromosome system, where a species has both an ancestral and a neo-sex chromosome. Although this type of multiple sex chromosome system has been found in many fishes, little is known about the mechanisms that select for the formation of neo-sex chromosomes, or the role of neo-sex chromosomes in phenotypic evolution and speciation. The identification of closely related, sympatric species pairs in which one species has a multiple sex chromosome system and the other has a simple sex chromosome system provides an opportunity to study sex chromosome turnover. Recently, we found that a population of threespine stickleback (Gasterosteus aculeatus) from Japan has an X1X2Y multiple sex chromosome system resulting from a fusion between the ancestral Y chromosome and an autosome, while a sympatric threespine stickleback population has a simple XY sex chromosome system. Furthermore, we demonstrated that the neo-X chromosome (X2) plays an important role in phenotypic divergence and reproductive isolation between these sympatric stickleback species pairs. Here, we review multiple sex chromosome systems in fishes, as well as recent advances in our understanding of the evolutionary role of sex chromosome turnover in stickleback speciation.

Tree of Sex: A database of sexual systems

The vast majority of eukaryotic organisms reproduce sexually, yet the nature of the sexual system and the mechanism of sex determination often vary remarkably, even among closely related species. Some species of animals and plants change sex across their lifespan, some contain hermaphrodites as well as males and females, some determine sex with highly differentiated chromosomes, while others determine sex according to their environment. Testing evolutionary hypotheses regarding the causes and consequences of this diversity requires interspecific data placed in a phylogenetic context. Such comparative studies have been hampered by the lack of accessible data listing sexual systems and sex determination mechanisms across the eukaryotic tree of life. Here, we describe a database developed to facilitate access to sexual system and sex chromosome information, with data on sexual systems from 11,038 plant, 705 fish, 173 amphibian, 593 non-avian reptilian, 195 avian, 479 mammalian, and 11,556 invertebrate species.

Hyperpolarization-activated, cyclic nucleotide-gated HCN2 cation channel forms a protein assembly with multiple neuronal scaffold proteins in distinct modes of protein–protein interaction

Hyperpolarization‐activated cation currents, termed Ih, are non‐uniformly distributed along dendritic arbors with current density increasing with increasing distance from the soma. The non‐uniform distribution of Ih currents contributes to normalization of location‐dependent variability in temporal integration of synaptic input, but the molecular basis for the graded HCN distribution remains to be investigated. The hyperpolarization‐activated, cyclic nucleotide‐gated cation channels (HCNs) underlie Ih currents and consist of four members (HCN1‐HCN4) of the gene family in mammals. In this investigation, we report that HCN2 forms a protein assembly with tamalin, S‐SCAM and Mint2 scaffold proteins, using several different approaches including immunoprecipitation of rat brain and heterologously expressing cell extracts and glutathione S‐transferase pull‐down assays. The PDZ domain of tamalin interacts with HCN2 at both the PDZ‐binding motif and the internal carboxy‐terminal tail of HCN2, whereas binding of the PDZ domain of S‐SCAM occurs at the cyclic nucleotide‐binding domain (CNBD) and the CNBD‐downstream sequence of the carboxy‐terminal tail of HCN2. A protein assembly between HCN2 and Mint2 is formed by the interaction of the munc18‐interacting domain of Mint2 with the CNBD‐downstream sequence of HCN2. The results demonstrate that HCN2 forms a protein complex with multiple neuronal scaffold proteins in distinct modes of protein–protein interaction.

Sex Chromosome Turnover Contributes to Genomic Divergence between Incipient Stickleback Species

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.

Y Fuse? Sex Chromosome Fusions in Fishes and Reptiles

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.

THE CONTRIBUTION OF FEMALE MEIOTIC DRIVE TO THE EVOLUTION OF NEO-SEX CHROMOSOMES

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 XY1Y2 sex chromosome system is more prevalent in species with karyotypes of more biarmed chromosomes, whereas the X1X2Y 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 (XY1Y2 sex chromosome system) will be also favored by female meiotic drive. In contrast, in species with more acrocentric chromosomes, Y‐autosome fusions (X1X2Y 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.