Biology subjects

Ma, W.-J.

Publications and source records attributed to Ma, W.-J..

7 recordsLinked to original sources

bioRxiv2026

Non-canonical sex chromosome evolution revealed by extreme heterogeneity in homomorphic Y chromosome differentiation in the common frog

Sex chromosome evolution is often viewed as a unidirectional process in which recombination suppression expands around a sex-determining locus, leading eventually to Y-chromosome degeneration. Yet many vertebrates, including frogs, retain homomorphic sex chromosomes and polymorphic differentiation despite long-term recombination suppression, which is quite puzzling. Here, we combine pooled whole-genome resequencing, doubled-haploid YY genomes, and RNA-seq to understand the dynamics of homomorphic sex chromosome evolution in a Swiss Alpine population of the common frog, Rana temporaria, where multiple Y haplotypes coexist. We show that two fully differentiated Y haplotypes carry exceptionally large nonrecombining regions spanning [~]90% of the sex chromosome ([~]618-625 Mb), whereas semi-differentiated Y haplotype retains only a 4.64 Mb Dmrt1-linked sex-determining region, and XX males are genetically indistinguishable from XX females. The large NRRs show limited degeneration, with no evidence of gene loss, Y-linked copy decay, faster-X evolution or enrichment of sex-biased genes, and only modest repeat accumulation. Surprisingly, the coexisting Y haplotypes are neither independent sex-determining systems nor successive stages of a single degeneration trajectory. Instead, they share an ancestral Dmrt1-linked region whose X-Y divergence dates to [~]3.47-5.70 Mya, while present-day Y copies of this region remain nearly identical and the large NRRs have accumulated private mutations independently. We thus propose that the Y chromosome undergoes cyclic dynamics of differentiation: extreme heterochiasmy promotes rapid large NRRs formation, sex-reversed XY females recurrently restore X-Y recombination, gene conversion and/or rare Y-Y recombination may homogenize Y copies at the Dmrt1-linked region, and renewed male transmission drives subsequent Y-specific differentiation. The findings provide a genome-wide resolution to a central paradox in sex chromosome evolution: how sex chromosomes can experience extensive recombination suppression yet remain homomorphic and only weakly degenerated. By showing that heterochiasmy and sex reversal uncouple the physical extent, age, and degeneration of sex-linked regions, our study reframes homomorphic sex chromosomes as dynamic, repeatedly regenerated systems shaped by alternating phases of recombination suppression, restored X-Y recombination and renewed Y differentiation. Significance statementWhy many vertebrate sex chromosomes remain homomorphic despite long-term recombination suppression remains unresolved. Using whole-genome population genomics, doubled-haploid YY genomes, and transcriptomics in the common frog, we show that multiple coexisting Y haplotypes in a single pond share an old Dmrt1-linked sex-determining region but carry younger, independently differentiated Y chromosomes. This genome-wide resolution reveals that extreme heterochiasmy, where recombination is largely restricted to chromosome ends in males, can rapidly generate very large nonrecombining regions, while sex-reversed XY females can restore X-Y recombination and reduce divergence outside the Dmrt1-linked region. These opposing processes generate cyclic dynamics of Y differentiation rather than a directional path towards degeneration. Our study provides a mechanistic explanation for the persistence of co-existing multiple Y haplotypes in one population, maintenance of homomorphic sex chromosomes, and a broadly relevant framework for sex chromosome evolution in lineages with heterochiasmy and sex reversal.

evolutionary biology↗

bioRxiv2025

Gene duplication, translocation and molecular evolution of Dmrt1 and related sex-determining genes in anurans

Sex determination, the developmental process that directs embryos toward male or female fates, is controlled by master sex-determining genes whose origins and evolutionary dynamics remain poorly understood outside of a few model systems. In contrast to the highly differentiated sex chromosomes of mammals, birds, and Drosophila, most anurans (frogs and toads) maintain homomorphic sex chromosomes that exhibit a rapid turnover, even among closely related species. To uncover the mechanisms underlying the emergence of new master sex-determining genes and sex chromosome turnover, we analysed 53 published anurans and one caecilian genome (>200 Ma divergence) and available transcriptomes. We asked how often new master sex-determining genes arise by gene duplication, whether and how often gene translocation associates with sex chromosome turnover, and if new master sex-determining genes evolve under positive selection. We find that chromosome-level synteny is remarkably conserved, with only a few fusions or fissions and no evidence for translocation of four candidate master sex-determining genes (Dmrt1, Foxl2, Bod1l, Sox3). Only Dmrt1 duplicated in 3 out of 50 species (excluding tetraploid Xenopus), and it showed strong testis-biased expression in all 8 species with available gonadal expression data. While Dmrt1 has evolved under purifying selection, Dmrt1 duplicates exhibit elevated nonsynonymous substitution rates and a tendency towards positive selection. Lineage-specific amino acid changes were observed in the conserved DM domain of Dmrt1. These results demonstrate that, in anurans, master sex-determining genes arise rarely via gene duplication, and more likely evolve via allelic diversification. Sex chromosome turnover is not associated with gene translocation, and is more likely driven by mutations on genes involved in sexual developmental pathway. All candidate sex-determining genes were under strong purifying selection, with the exception of duplications which are linked to positive selection. Our results suggest future research on anuran sex determination and sex chromosome evolution should focus on identifying allelic diversification and novel mutations on genes involved in sexual developmental pathway.

evolutionary biology↗

bioRxiv2025

Cytological and preliminary genomic analysis of two Leptodactylus frog species (Anura, Leptodactylidae) with recently evolved large meiotic rings of multiple X and Y sex chromosomes

A few species have evolved multiple sex chromosome systems with more than two Xs or Ys. These involve sex chromosome-autosome translocations (sometimes called fusions as very small heterochromatic arms may be deleted), creating neo-sex chromosome systems. Among vertebrates, frogs (Anura) have the highest known number of such translocation systems. This study within the genus Leptodactylus, investigated the two species L. pentadactylus (LPE) and L. paraensis (LPA), in which large ring multivalents are seen in male meiosis, indicating translocations involving the sex chromosomes. Four other species studied do not have such rings, but they share characteristics making rearrangements less likely to be eliminated. To start understanding the formation of multivalents, we used genomic and cytogenetic methods to investigate repetitive DNA sequences, including satellite DNAs, rDNAs, and telomeric sequences, and conducted comparative genomic hybridization (CGH). The LPE genome includes a large number of satDNA families, and in situ mapping of several satDNAs individually identified eight of the ten chromosomes in its multivalent. In LPA, morphological similarities indicate that several chromosomes are shared by the multivalents of both species, and a candidate ancestral sex chromosome pair could be identified. In situ mapping in LPE suggests recent satDNA accumulation in the subtelomeric regions, which differ from those in the outgroup species, contrary to the expectation that the translocations create sex-linkage in the pericentromeric regions.

evolutionary biology↗

bioRxiv2022

Hoisted with his own petard: how sex-ratio meiotic drive in Drosophila affinis creates resistance alleles that limit its spread

Meiotic drivers are selfish genetic elements that tinker with gametogenesis to bias their own transmission into the next generation of offspring. Such tinkering can have significant consequences on gametogenesis and end up hampering the spread of the driver. In Drosophila affinis, sex-ratio meiotic drive is caused by an X-linked complex that, when in males with a susceptible Y chromosome, results in broods that are typically more than 95% female. Interestingly, D. affinis males lacking a Y chromosome (XO) are fertile and males with the meiotic drive X and no Y produce only sons - effectively reversing the sex-ratio effect. Here, we show that meiotic drive dramatically increases the rate of nondisjunction of the Y chromosome (at least 750X), meaning that the driver is creating resistant alleles through the process of driving. We then model how the O might influence the spread, dynamics and equilibrium of the sex-ratio X chromosome. We find that the O can prevent the spread or reduce the equilibrium frequency of the sex-ratio X chromosome and it can even lead to oscillations in frequency. Finally, with reasonable parameters, the O is unlikely to lead to the loss of the Y chromosome, but we discuss how it might lead to sex-chromosome turnover indirectly.

evolutionary biology↗

bioRxiv2020

A single QTL with large effect is associated with female functional virginity in an asexual parasitoid wasp

During the transition from sexual to asexual reproduction, a suite of reproduction-related sexual traits become superfluous, and may be selected against if costly. Female functional virginity refers to asexual females resisting to mate or not fertilizing eggs after mating. These traits appear to be among the first that evolve during the gradual transition from sexual to asexual reproduction. The genetic basis of female functional virginity remains elusive. Previously, we reported that female functional virginity segregates as a single recessive locus in the asexual parasitoid wasp Asobara japonica. Here, we investigate the genetic basis of this trait by quantitative trait loci (QTL) mapping and candidate gene analyses. Consistent with the segregation of phenotypes, a single QTL of large effect was found spanning over 4.23 Mb and comprising at least 131 protein-coding genes, of which 15 featured sex-biased expression in the related sexual Asobara tabida. We speculate that two of these 15 genes may be of particular interest: CD151 antigen and nuclear pore complex protein Nup50. Overall, our results are consistent with a single gene or a cluster of linked genes underlying rapid evolution of female functional virginity in the transition to asexuality. Once a mutation for rejection to mate has swept through a population, the region comprising the gene(s) does not get smaller due to lack of recombination in asexuals.

evolutionary biology↗

bioRxiv2019

Y-chromosome haplotypes of varying differentiation to the X are not associated with male fitness in common frogs

The canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (non-recombinant Y haplotypes) coexist with both XY{degrees} males with proto-Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex-determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study shows no effect of sex-chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY{degrees} and XX males. Sexual dimorphism in common frogs seems to result from the differential expression of autosomal genes rather than sex-linked SA genes. Among-male variance in sex-chromosome differentiation is better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X-Y recombination in XY females), independent of sex-linked SA genes.\n\nImpact Summary\n\nHumans, like other mammals, present highly differentiated sex chromosomes, with a large, gene-rich X chromosome contrasting with a small, gene-poor Y chromosome. This differentiation results from a process that started approximately 160 Mya, when the Y first stopped recombining with the X. How and why this happened, however, remain controversial. According to the canonical model, the process was initiated by sexually antagonistic selection; namely, selection on the proto-Y chromosome for alleles that were beneficial to males but detrimental to females. The arrest of XY recombination then allowed such alleles to be only transmitted to sons, not to daughters. Although appealing and elegant, this model can no longer be tested in mammals, as it requires a sex-chromosome system at an incipient stage of evolution. Here we focus on a frog that displays within-population polymorphism is sex-chromosome differentiation, where XY males with differentiated chromosomes coexist with XX males lacking Y chromosomes. We find no effect of sex-chromosome differentiation on male phenotype or mating success, opposing expectations from the standard model. Sex linked genes do not seem to have a disproportionate effect on sexual dimorphism. From our results, sexually antagonistic genes show no association with sex-chromosome differentiation in frogs, which calls for alternative models of sex-chromosome evolution.

evolutionary biology↗

bioRxiv2019

Differential gene expression is associated with degeneration of mating-type chromosomes in the absence of sexual antagonism

In animals and plants, differential expression of genes on sex chromosomes is widespread and it is usually considered to result from sexually antagonistic selection; however differential expression can also be caused by asymmetrical sequence degeneration in non-recombining sex chromosomes, which has been very little studied. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal to investigate the extent to which differential gene expression is associated with sequence degeneration because: 1) separate haploid cultures of opposite mating types help identify differential expression, 2) its mating-type chromosomes display multiple evolutionary strata reflecting successive events of gene linkage to the mating-type loci, and 3) antagonistic selection is unlikely between isogamous haploid mating types. We therefore tested the hypothesis that differential gene expression between mating types resulted from sequence degeneration. We found that genes showing differential expression between haploid mating types were enriched only on the oldest evolutionary strata of the mating-type chromosomes and were associated with multiple signatures of sequence degeneration. We found that differential expression between mating types was associated with elevated differences between alleles in non-synonymous substitution rates, indels and premature stop codons, transposable element insertions, and altered intron and GC content. Our findings strongly suggest that degenerative mutations are important in the evolution of differential expression in non-recombining regions. Our results are relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions of recombination suppression, showing that differential expression should not be taken as necessarily arising from antagonistic selection.\n\nAuthor SummaryDifferences between males and females, from morphology to behavior and physiology, are considered to largely reflect differential expression of genes that maximize fitness benefits relative to costs that are specific to one sex. However, there is an unexplored alternative to such sexually antagonistic selection to explain differential expression. Reproductive compatibility is often determined by genes located in large non-recombining chromosomal regions, where degenerative mutations are expected to accumulate and may separately affect the expression of alternate alleles of genes. We tested the role of genetic degeneration in determining differential expression between the isogamous haploid mating types of the anther-smut fungus, Microbotryum lychnidis-dioicae, where sexually antagonistic selection is not a confounding factor. We show that differentially expressed genes are highly enriched in the non-recombining mating-type chromosomes, and that they are associated with various forms of degenerative mutations, some of which indicate that the less expressed allele suffers greater mutational effects. Our finding of the role for degenerative mutations in the evolution of differential expression is relevant for a broad range of organisms where reproductive compatibility or sex is determined by genes in regions of suppressed recombination, and shows that differential expression should not be taken as necessarily arising from antagonistic selection.

evolutionary biology↗