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Genome Biol Evol
2018 Mar 01;103:742-755. doi: 10.1093/gbe/evy045.
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Divergent Evolutionary Trajectories of Two Young, Homomorphic, and Closely Related Sex Chromosome Systems.
Furman BLS
,
Evans BJ
.
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There exists extraordinary variation among species in the degree and nature of sex chromosome divergence. However, much of our knowledge about sex chromosomes is based on comparisons between deeply diverged species with different ancestral sex chromosomes, making it difficult to establish how fast and why sex chromosomes acquire variable levels of divergence. To address this problem, we studied sex chromosome evolution in two species of African clawed frog (Xenopus), both of whom acquired novel systems for sex determination from a recent common ancestor, and both of whom have female (ZW/ZZ) heterogamy. Derived sex chromosomes of one species, X. laevis, have a small region of suppressed recombination that surrounds the sex determining locus, and have remained this way for millions of years. In the other species, X. borealis, a younger sex chromosome system exists on a different pair of chromosomes, but the region of suppressed recombination surrounding an unidentified sex determining gene is vast, spanning almost half of the sex chromosomes. Differences between these sex chromosome systems are also apparent in the extent of nucleotide divergence between the sex chromosomes carried by females. Our analyses also indicate that in autosomes of both of these species, recombination during oogenesis occurs more frequently and in different genomic locations than during spermatogenesis. These results demonstrate that new sex chromosomes can assume radically different evolutionary trajectories, with far-reaching genomic consequences. They also suggest that in some instances the origin of new triggers for sex determination may be coupled with rapid evolution sex chromosomes, including recombination suppression of large genomic regions.
Fig. 1.
—Sex-linkage of SNPs on sex chromosomes of X. borealis and X. laevis. In each graph, the x-axis is the position on the sex chromosome using the coordinates of the X. laevis reference genome and the y-axis is the major daughter genotype frequency in sons and daughters (see Materials and Methods for details) with colors as defined in the key indicating whether or not a SNP is significantly associated with sex (FDR corrected P < 0.05). For each species, a diagram of a chromosome is shaded darker in the region of suppressed recombination. The inset phylogeny is from Furman and Evans (2016); DM-W is carried by female X. clivii, but its presence on chr2L has not been confirmed.
Fig. 2.
—Linkage map length (in cM) is positively correlated with the number of bp spanned by the map (based on the X. laevis genome) for maternal but not paternal linkage maps. Black “sex chr” dots indicate the linkage map of the sex chromosome of each species (chromosome 8 L in X. borealis, chromosome 2 L in X. laevis). Lines reflect linear model relationships; gray shading indicates the 95% confidence interval of this relationship. Additionally, chromosome 8S is highlighted for X. borealis, because it is the homeolog of the sex chromosome 8 L (see Results for details).
Fig. 3.
—Density plots of recombination events with respect to the relative position along chromosomes (chromosome length scaled to be between 0 and 1) in the maternal and paternal linkage maps of X. borealis and X. laevis.
Fig. 4.
—Nucleotide diversity (π) in X. borealis based on WGS data mapped to the X. laevis reference genome. (a) Median π by chromosome as measured in the six genomic categories; error bars indicate 95% CI bootstrap estimates (for further information on differences see supplementary S1.4, Supplementary Material online). The 8 L_NL category refers to the diversity measured on chromosome 8 L in the nonsex-linked region (57–120 Mb). (b) Box and whisker plot of π across six genomic categories (described in Materials and Methods); the y-axis is truncated at 0.05 for clarity. (c) Standardized nucleotide diversity of the female divided by the standardized nucleotide diversity of male in 1-Mb windows across chr8L; the completely sex-linked region is highlighted in dark purple, and the significantly sex linked region with suppressed recombination in light purple (see fig. 1).
FIG. S1.—Using sex-specific linkage maps that were generated from sets of either female or male heterozygous sites, we determined (a) parental haplotypes. (b) A haplotype from each parent could either be inherited entirely (if no recombination happened in the genotyped region), or recombined. (c) Scoring offspring haplotypes for sex specific maps of each chromosome allows for visualization and counting of the number of recombination events and identification of genotyping errors or improbable double recombination events.
FIG. S2.—SNPs from the X. borealis family heterozygous in the mother mapped to the genome of X. laevis. Sex-linkage is calculated following Goudet et al. (1996), followed by an FDR correction to account for multiple testing (significant genotypes are indicated by black dots). The gray lines in each plot represent the significance threshold of 0.05. The sex-linked marker on chr5S can be mapped to chromosome 8S and 8L when a larger amount of sequence data is used (see Results).
FIG. S3.—Phased parental haplotypes in X. borealis offspring for the maternal (left column) and paternal (right column) linkage groups of chromosome 8L. In the maternal haplotypes, the beginning of chromosome 8L is completely linked to sex (all daughters with the same haplotype, 0, and all sons had haplotype 1), apart from two recombination events near the end. Note, this linkage map only spans the sex- linked region (see Methods). For the paternal map, haplotypes are evenly shared between the sexes, indicating non-sex-linked inheritance of the paternal Z chromosome. In the region of the paternal Z chromosomes that is homologous to the sex-linked region of the maternal sex chromosomes, several recombination events are observed.
FIG. S4.—Median depth (DP) and genotype quality (GQ) for offspring of the X. borealis and X. laevis families for maternal heterozygous sites used in the sex linkage analysis of Fig. 1.
FIG. S5.—SNPs from the X.laevis family heterozygous in the mother mapped to the genome of X.laevis. Sex-linkage is calculated following Goudet et al. (1996), followed by an FDR correction to account for multiple testing (significant at 0.05 colored black). The gray lines in each plot represent the significance threshold of 0.05.
Adolfsson,
Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches.
2013, Pubmed
Adolfsson,
Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches.
2013,
Pubmed
Amster,
Life history effects on the molecular clock of autosomes and sex chromosomes.
2016,
Pubmed
Bachtrog,
Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration.
2013,
Pubmed
Bachtrog,
Reduced adaptation of a non-recombining neo-Y chromosome.
2002,
Pubmed
Backström,
The recombination landscape of the zebra finch Taeniopygia guttata genome.
2010,
Pubmed
Baird,
Rapid SNP discovery and genetic mapping using sequenced RAD markers.
2008,
Pubmed
Batada,
Evolution of chromosome organization driven by selection for reduced gene expression noise.
2007,
Pubmed
Bergero,
Defining regions and rearrangements of the Silene latifolia Y chromosome.
2008,
Pubmed
Bergero,
The evolution of restricted recombination in sex chromosomes.
2009,
Pubmed
Bergero,
Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes.
2007,
Pubmed
Berset-Brändli,
Extreme heterochiasmy and nascent sex chromosomes in European tree frogs.
2008,
Pubmed
Bewick,
Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus).
2011,
Pubmed
,
Xenbase
Brelsford,
High-density sex-specific linkage maps of a European tree frog (Hyla arborea) identify the sex chromosome without information on offspring sex.
2016,
Pubmed
,
Xenbase
Chain,
Duplicate gene evolution and expression in the wake of vertebrate allopolyploidization.
2008,
Pubmed
,
Xenbase
Charlesworth,
The evolution of sex chromosomes.
1991,
Pubmed
Charlesworth,
Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation.
2009,
Pubmed
Charlesworth,
Steps in the evolution of heteromorphic sex chromosomes.
2005,
Pubmed
Charlesworth,
The degeneration of Y chromosomes.
2000,
Pubmed
Coop,
An evolutionary view of human recombination.
2007,
Pubmed
Cui,
High-density linkage mapping aided by transcriptomics documents ZW sex determination system in the Chinese mitten crab Eriocheir sinensis.
2015,
Pubmed
Dufresnes,
Sex-chromosome differentiation parallels postglacial range expansion in European tree frogs (Hyla arborea).
2014,
Pubmed
Elshire,
A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.
2011,
Pubmed
Evans,
Genetics, Morphology, Advertisement Calls, and Historical Records Distinguish Six New Polyploid Species of African Clawed Frog (Xenopus, Pipidae) from West and Central Africa.
2015,
Pubmed
,
Xenbase
Evans,
Molecular Polymorphism and Divergence of Duplicated Genes in Tetraploid African Clawed Frogs (Xenopus).
2015,
Pubmed
,
Xenbase
Furman,
Sequential Turnovers of Sex Chromosomes in African Clawed Frogs (Xenopus) Suggest Some Genomic Regions Are Good at Sex Determination.
2016,
Pubmed
,
Xenbase
Goudet,
Testing differentiation in diploid populations.
1996,
Pubmed
Graves,
Sex chromosome specialization and degeneration in mammals.
2006,
Pubmed
Groenen,
A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate.
2009,
Pubmed
Hackett,
Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps.
2003,
Pubmed
Hansson,
Avian genome evolution: insights from a linkage map of the blue tit (Cyanistes caeruleus).
2010,
Pubmed
Hassold,
Cytological studies of meiotic recombination in human males.
2004,
Pubmed
Hunt,
Sex matters in meiosis.
2002,
Pubmed
Ji,
A candidate recombination modifier gene for Zea mays L.
1999,
Pubmed
Johnston,
Conserved Genetic Architecture Underlying Individual Recombination Rate Variation in a Wild Population of Soay Sheep (Ovis aries).
2016,
Pubmed
Kamiya,
A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu).
2012,
Pubmed
Kawakami,
A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution.
2014,
Pubmed
Kitano,
A role for a neo-sex chromosome in stickleback speciation.
2009,
Pubmed
Lenormand,
Recombination difference between sexes: a role for haploid selection.
2005,
Pubmed
Lenormand,
The evolution of sex dimorphism in recombination.
2003,
Pubmed
Makova,
Strong male-driven evolution of DNA sequences in humans and apes.
2002,
Pubmed
Mank,
The W, X, Y and Z of sex-chromosome dosage compensation.
2009,
Pubmed
Mank,
The evolution of heterochiasmy: the role of sexual selection and sperm competition in determining sex-specific recombination rates in eutherian mammals.
2009,
Pubmed
Margarido,
OneMap: software for genetic mapping in outcrossing species.
2007,
Pubmed
Matsuda,
A New Nomenclature of Xenopus laevis Chromosomes Based on the Phylogenetic Relationship to Silurana/Xenopus tropicalis.
2015,
Pubmed
,
Xenbase
Mawaribuchi,
Sex chromosome differentiation and the W- and Z-specific loci in Xenopus laevis.
2017,
Pubmed
,
Xenbase
Natri,
Progressive recombination suppression and differentiation in recently evolved neo-sex chromosomes.
2013,
Pubmed
Nietlisbach,
A microsatellite-based linkage map for song sparrows (Melospiza melodia).
2015,
Pubmed
Olmstead,
Genotyping sex in the amphibian, Xenopus (Silurana) tropicalis, for endocrine disruptor bioassays.
2010,
Pubmed
,
Xenbase
Otto,
Resolving the paradox of sex and recombination.
2002,
Pubmed
Ottolini,
Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates.
2015,
Pubmed
Perrin,
Sex reversal: a fountain of youth for sex chromosomes?
2009,
Pubmed
Rice,
Degeneration of a nonrecombining chromosome.
1994,
Pubmed
Rice,
THE ACCUMULATION OF SEXUALLY ANTAGONISTIC GENES AS A SELECTIVE AGENT PROMOTING THE EVOLUTION OF REDUCED RECOMBINATION BETWEEN PRIMITIVE SEX CHROMOSOMES.
1987,
Pubmed
Roco,
Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis.
2015,
Pubmed
,
Xenbase
Session,
Genome evolution in the allotetraploid frog Xenopus laevis.
2016,
Pubmed
,
Xenbase
Shen,
Genomic dynamics of transposable elements in the western clawed frog (Silurana tropicalis).
2013,
Pubmed
,
Xenbase
Stöck,
Low rates of X-Y recombination, not turnovers, account for homomorphic sex chromosomes in several diploid species of Palearctic green toads (Bufo viridis subgroup).
2013,
Pubmed
Stöck,
Ever-young sex chromosomes in European tree frogs.
2011,
Pubmed
Tymowska,
Chromosome complements of the genus Xenopus.
1973,
Pubmed
,
Xenbase
Venn,
Nonhuman genetics. Strong male bias drives germline mutation in chimpanzees.
2014,
Pubmed
Vicoso,
Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution.
2013,
Pubmed
Wong,
A comprehensive linkage map of the dog genome.
2010,
Pubmed
Wright,
How to make a sex chromosome.
2016,
Pubmed
Wright,
Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation.
2017,
Pubmed
Wu,
Simultaneous maximum likelihood estimation of linkage and linkage phases in outcrossing species.
2002,
Pubmed
Yazdi,
Old but not (so) degenerated--slow evolution of largely homomorphic sex chromosomes in ratites.
2014,
Pubmed
Yoshimoto,
A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis.
2008,
Pubmed
,
Xenbase
Zhou,
Complex evolutionary trajectories of sex chromosomes across bird taxa.
2014,
Pubmed
Zickler,
A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis.
2016,
Pubmed