Biology subjects

Charlesworth, D.

Publications and source records attributed to Charlesworth, D..

16 recordsLinked to original sources

bioRxiv2025

A trade-off mechanism underpins the evolution of a young two-gene sex-determining system in plants

Sexual systems in animals and plants are remarkably diverse, with dioecy having evolved independently in numerous lineages. In plants, dioecy often evolved more recently than in the best-studied animal systems, making plants especially important for understanding how separate sexes evolved independently from functionally hermaphrodite ancestors. Despite long-standing theories of developmental trade-offs in sex allocation, the underlying genetic mechanisms remain elusive. Here, we show that the XY sex determination system in the dioecious plant species Eurycorymbus cavaleriei in Sapindaceae involves two Y-linked mutations that act jointly within the developmental male-female trade-off: YUN{Delta}, a truncated allele that lowers the dosage of the D-class MADS-box gene YUN, and SUNMAO, a novel sRNA locus that silences the X-linked SUN allele. In females, SUN stabilizes the HD-ZIP transcription factor KUN, which is a known sex determinant in another dioecious plant, thereby promoting femaleness by increasing YUN expression; loss of SUN expression, together with the effect of YUN{Delta}, shifts development toward males. Two interlocking regulatory loops in this "SKY" module (SUN-KUN-YUN) fine-tunes YUN dosage. This dioecious system in E. cavaleriei likely evolved by sequential mutations in genes acting in the predicted male-female trade-off system, with their close linkage reflecting a translocation, and later recombination-suppressing inversions.

plant 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↗

bioRxiv2025

Evidence for evolution of a new sex chromosome within the Marchantiales haploid plant lineage

Sex chromosomes have evolved independently in numerous lineages across the tree of life, in both diploid-dominant species, including many animals and plants, and the less studied haploid-dominant plants and algae. Strict genetic sex determination ensures that individuals reproduce by outcrossing. However, species with separate sexes (termed dioecy in diploid plants, and dioicy in haploid plants) may sometimes evolve different sex systems, and become monoicous, with the ability to self-fertilize. Here, we study dioicy-monoicy transitions in the ancient liverwort haploid plant lineage, using three telomere-to-telomere gapless chromosome-scale reference genome assemblies from the Ricciaceae group of Marchantiales. Ancestral liverworts are believed to have been dioicous, with U and V chromosomes (chromosome 9) determining femaleness and maleness, respectively. We confirm the finding that monoicy in Ricciocarpos natans evolved from a dioicous ancestor, and most ancestrally U chromosomal genes have been retained on autosomes in this species. We also describe evidence suggesting the possible re-evolution of dioicy in the genus Riccia, with probable de novo establishment of a sex chromosome from an autosome (chromosome 5), and further translocations of genes from the new sex chromosome to autosomes. Our results also indicated that m-chromosomes are consistent genomic features, and may have evolved independently from sex chromosomes in Ricciocarpos and Riccia lineages.

evolutionary biology↗

bioRxiv2024

Evolution and functioning of an X-A balance sex determination system in hops

Chromosomal sex determining systems with male heterogamety include actively male-determining-Y and X-A balance systems, both of which are found in animals and plants. The sex-determining genes have been identified in several active-Y plant systems, but the evolution and functioning of X-A balance systems remains mysterious. To study this, we sequenced and compared the genomes of two hop species. The evolution of the hop X-A balance system involved an ancient recombination suppression event across a large X chromosome region shared by both species. In one species, an autosome fused to this ancestral sex chromosome, and recombination was subsequently suppressed again. The two evolutionary strata created in this neo-X have degenerated to different degrees, and evolved correspondingly different dosage compensation levels that correlate with histone modification patterns. Finally, we identified an X-specific ETR1-like ethylene receptor in the ancestral X region. Its dosage may affect sex determination, as part of the counting mechanism of this X-A balance system. One sentence summaryBased on whole genome sequences of the cultivated hop, Humulus lupulus, and its wild relative H. japonicus, we describe the evolution of sex chromosomal regions, three of which that evolved region-specific dosage compensation, and identify a candidate gene involved in their X-A balance sex determining system.

evolutionary biology↗

bioRxiv2023

Insights into spinach domestication from genomes sequences of two wild spinach progenitors, Spinacia turkestanica and S. tetrandra

Cultivated spinach (Spinacia oleracea) is a dioecious species (with male and female flowers on separate individuals). We report high-quality genome assemblies for its two closest wild relatives, S. turkestanica and S. tetrandra, which are also dioecious, to study the genetics of spinach domestication. Using a combination of genomic approaches, we assembled genome sequences of both these species, and analysed them in comparison to the previously assembled S. oleracea genome. These species diverged approximately 6.3 million years ago (Mya), while cultivated spinach split from S. turkestanica (its probable direct progenitor) 0.8 Mya. A common feature of all three species is that all six chromosomes include very large gene-poor, repeat-rich regions. In S. oleracea, these correspond with pericentromeric regions with very low recombination rates in both male and female genetic maps, and we infer that the similar pericentromeric regions in the wild species also recombine rarely. Although these regions include a low proportion of Spinacia genes, many genes are nevertheless within them, and they must be considered when analyzing selection during domestication. As a first approach to the difficult question of detecting genes involved in spinach domestication, we characterized 282 structural variants (SVs) whose frequencies are higher in a set of spinach accessions than in the wild species, suggesting that they mark genome regions that have been selected during domestication. These regions include genes associated with leaf margin type and flowering time. We also describe evidence that the downy mildew resistance loci of cultivated spinach are derived from introgression from both wild spinach species.

genomics↗

bioRxiv2023

Two wild Spinacia species, S. turkestanica and S. tetrandra, genomes reveal a sex chromosome turnover in the genus

Spinach (Spinacia oleracea) is a dioecious species (with male and female flowers on separate individuals). Spinach and its closest wild relative, S. turkestanica, has homomorphic sex chromosomes, but the more distant relative S. tetrandra has heteromorphic sex chromosomes. We report high-quality genome assemblies for S. turkestanica and S. tetrandra. These diverged approximately 6.3 million years ago (Mya), while S. turkestanica split from S. oleracea much more recently, around 0.8 Mya, supporting previous suggestions that S. turkestanica is the direct progenitor of cultivated spinach. Using a combination of genomic approaches, we identified a sex-linked region (SLR) of [~]133 Mb in S. tetrandra. In all three species, the SLRs are within a large pericentromeric region of chromosome 4. We describe evidence that, in S. tetrandra, this region has completely stopped recombining in male meiosis, creating a large Y-linked region (YLR) that has partially degenerated; loss of recombination appears to have evolved in two events that created two "evolutionary strata", one of which and is highly rearranged, relative to the X. The SLRs of S. turkestanica and S. oleracea are much smaller: both include only a 10 Mb Y-specific region which is not detected in S. tetrandra. This was duplicated into a 14 Mb inverted region, and is termed the Y-duplicated region, or "YDR". These findings suggest that a turnover event created the YDR before these species diverged, replacing an extensive ancestral Y-linked region like the S. tetrandra YLR.

genomics↗

bioRxiv2023

Gap-free X and Y chromosomes of Salix arbutifolia reveal an evolutionary change from male to female heterogamety in willows, without a change in the sex-determining region

In the Vetrix clade of Salix, a genus of woody flowering plants, sex determination involves chromosome 15, but an XY system has changed to a ZW system. We used genome sequencing (with chromosome conformation capture (Hi-C) and PacBio HiFi high-fidelity reads) to study the evolutionary history of the sex-linked regions before and after the transition. We assembled chromosome level gap-free X and Y chromosomes of Salix arbutifolia, and distinguished the haplotypes in the 15X- and 15Y-linked regions. This revealed "micro-heteromorphism" differentiating the haplotypes of the Y- and X-linked regions, including insertions, deletions and duplications. Unusually, the X-linked region is considerably larger than the corresponding Y region, and we show that this primarily reflects extensive accumulation of repetitive sequences and gene duplications. The phylogenies of single-copy orthogroups within the sex-linked regions of S. arbutifolia (X and Y) and S. purpurea (Z and W) indicate that they possess a common ancestral sex-linked region that is physically small and located in a repeat-rich region near the chromosome 15 centromere. During the change in heterogamety, the W-linked region was derived from the X-linked one and the Z from the Y. The W may subsequently have evolved a region in which recombination became suppressed. We also detected accumulation of genes with opposite sex-biases in the sex-linked regions.

plant biology↗

bioRxiv2023

Rapid and dynamic evolution of a giant Y chromosome in Silene latifolia

To test hypotheses about the evolution of massive sex-linked regions in plants, we sequenced the genome of Silene latifolia, whose giant heteromorphic sex chromosomes were first discovered in 1923. It has long been known that the Y consists mainly of a male-specific region which does not recombine with the X in male meiosis, and that this region carries the primary sex-determining genes, and other genes contributing to male functioning. However, only with a whole Y chromosome assembly can the candidates be validated experimentally, as we describe. Our new results also illuminate the genomic changes as the ancestral chromosome evolved into the current XY pair, testing ideas about why large regions of sex-linkage evolve, and the mechanisms creating the present recombination pattern. One sentence summaryBased on the whole genome sequences of Silene latifolia, a model species for plant sex chromosome evolution, we describe discovery of genes underlying male-female flower differences, and relate the results to ideas about the evolution of the vast non-recombining regions of the Y chromosome.

genetics↗

bioRxiv2023

Has recombination changed during the recent evolution of the guppy Y chromosome?

Genome sequencing and genetic mapping of molecular markers has demonstrated Y-linkage across most of the guppy (Poecilia reticulata) XY chromosome pair. However, they also revealed exchanges with the X, consistent with classical genetic observations of occasional exchanges of factors controlling visible male-specific phenotypic traits. It remains unclear whether this fish species has an extensive sex-determining region without crossing over (whose suppressed recombination could have evolved under selection created by sexually antagonistic effects of male coloration factors), or whether the fully Y-linked region is very small, perhaps within a single gene. Population genomic data support cytogenetic results indicating that it is within the terminal 5 Mb of the 26.5 Mb chromosome 12, just proximal to a highly recombining pseudo-autosomal region, PAR1. Using molecular markers, we studied recombination, focusing on this region of the XY pair. Despite assembly errors in the small terminal PAR1, our mapping identifies very similar genetic PAR boundaries in sires from four populations, suggesting that their crossover patterns have not changed. Our results also confirmed occasional crossovers proximal to the male-determining region, defining a second pseudo-autosomal region, PAR2, recombining much more rarely than PAR1. The crossover positions suggest that the male-determining factor is within a repetitive region near 21 Mb in the female assembly. A sex-reversed XX male had few crossovers in PAR2, suggesting that this regions low crossover rate depends on the phenotypic, not the genetic, sex. Thus rare sex changes, and/or occasional crossovers in males can explain the failure to detect fully Y-linked variants.

genetics↗

bioRxiv2022

Partial sex linkage and linkage disequilibrium on the guppy sex chromosome

The guppy Y chromosome has been considered a model system for the evolution of suppressed recombination between sex chromosomes, and it has been proposed that complete sex-linkage has evolved across about 3 Mb surrounding this fishs sex-determining locus, followed by recombination suppression across a further 7 Mb of the 23 Mb XY pair, forming younger "evolutionary strata". Sequences of the guppy genome show that Y is very similar to the X chromosome, making it important to understand which parts of the Y are completely non-recombining, and whether there is indeed a large completely non-recombining region. Here, we describe new evidence that supports a different interpretation of the data that suggested the presence of such a region. We analysed PoolSeq data in samples from multiple natural populations from Trinidad. This yields evidence for linkage disequilibrium (LD) between sequence variants and the sex-determining locus. Downstream populations have higher diversity than upstream ones (which display the expected signs of bottlenecks). The associations we observe conform to predictions for a genome region with infrequent recombination that carries one or more sexually antagonistic polymorphisms. They also suggest the region in which the sex-determining locus must be located. However, no consistently male-specific variants were found, supporting the suggestion that any completely sex-linked region may be very small.

evolutionary biology↗

bioRxiv2020

Improved reference genome uncovers novel sex-linked regions in the guppy (Poecilia reticulata)

Theory predicts that the sexes can achieve greater fitness if loci with sexually antagonistic polymorphisms become linked to the sex determining loci, and this can favour the spread of reduced recombination around sex determining regions. Given that sex-linked regions are frequently repetitive and highly heterozygous, few complete Y chromosome assemblies are available to test these ideas. The guppy system (Poecilia reticulata) has long been invoked as an example of sex chromosome formation resulting from sexual conflict. Early genetics studies revealed that male colour patterning genes are mostly but not entirely Y-linked, and that X-linkage may be most common in low predation populations. More recent population genomic studies of guppies have reached varying conclusions about the size and placement of the Y-linked region. However, this previous work used a reference genome assembled from short-read sequences from a female guppy. Here, we present a new guppy reference genome assembly from a male, using long-read PacBio single-molecule real-time sequencing (SMRT) and chromosome contact information. Our new assembly sequences across repeat- and GC-rich regions and thus closes gaps and corrects mis-assemblies found in the short-read female-derived guppy genome. Using this improved reference genome, we then employed broad population sampling to detect sex differences across the genome. We identified two small regions that showed consistent male-specific signals. Moreover, our results help reconcile the contradictory conclusions put forth by past population genomic studies of the guppy sex chromosome. Our results are consistent with a small Y-specific region and rare recombination in male guppies.

evolutionary biology↗

bioRxiv2020

Using GC content to compare recombination patterns on the sex chromosomes and autosomes of the guppy, Poecilia reticulata, and its close outgroup species

Summary/AbstractGenetic and physical mapping of the guppy (P. reticulata) have shown that recombination patterns differ greatly between males and females. Crossover events occur evenly across the chromosomes in females, but in male meiosis they are restricted to the tip furthest from the centromere of each chromosome, creating very high recombination rates per megabase, similar to the high rates in mammalian sex chromosomes pseudo-autosomal regions (PARs). We here used the intronic GC content to indirectly infer the recombination patterns on guppy chromosomes. This is based on evidence that recombination is associated with GC-biased gene conversion, so that genome regions with high recombination rates should be detectable by high GC content. Using intron sequences, which are likely to be under weak selection, we show that almost all guppy chromosomes, including the sex chromosome (LG12) have very high GC values near their assembly ends, suggesting high recombination rates due to strong crossover localisation in male meiosis. Our test does not suggest that the guppy XY pair has stronger crossover localisation than the autosomes, or than the homologous chromosome in a closely related fish, the platyfish (Xiphophorus maculatus). We therefore conclude that the guppy XY pair has not recently undergone an evolutionary change to a different recombination pattern, or reduced its crossover rate, but that the guppy evolved Y-linkage due to acquiring a male-determining factor that also conferred the male crossover pattern. The results also identify the centromere ends of guppy chromosomes, which were not determined in the guppy genome assembly.

evolutionary biology↗

bioRxiv2020

Locating the sex determining region of linkage group 12 of guppy (Poecilia reticulata)

We describe new genetic mapping results from 6 full-sib families in the guppy (Poecilia reticulata), two of which included recombinants between the X and Y chromosomes. These recombinants confirm that the guppy sex-determining locus is in the region identified by all previous studies, including a recent report suggesting a candidate sex-determining gene in this fish, close to the pseudo-autosomal region (or PAR) at the chromosome terminus. Our results suggest the presence of some errors in the current assembly of the guppy genome. In males, crossing over occurs at a very high rate in the PAR, and our genetic map of the region allows us to correct the marker order. We also identified two unplaced scaffolds carrying genes that map to the PAR. Genetic mapping cannot be used to order markers in the region where crossing over is infrequent. However, our recombinant male is informative about the order, under the reasonable assumption that crossovers are infrequent. Our mapping families and natural population samples also show that the recently proposed candidate for this species sex-determining gene is not completely sex-linked. We detect an association between individuals sex and an SNP in the sex-determining region, but not with a marker 0.9 Mb away from it, suggesting that variants in this region may be in linkage disequilibrium with the actual sex-determining factor, but that the factor itself has not yet been identified. So far, no consistently male-specific variant has been identified in the guppy sex-determining region.

genetics↗

bioRxiv2020

Two antagonistic effect genes mediate separation of sexes in a fully dioecious plant

Plant sex determining systems and sex chromosomes are often evolutionarily young. Here, we present the early stage of sex chromosome in a fully dioecious plant, P. deltoides, by determining separate sequences of the physically small X- and Y-linked regions. Intriguingly, two Y genes are absent from the X counterpart. One gene represses female structures by producing siRNAs that block expression of a gene necessary for development of female structures, via RNA-directed DNA methylation and siRNA-guided mRNA cleavage. The other gene generates long non-coding RNA transcripts that, in males, soak up miRNAs that specifically inhibit androecium development. Transformation experiments in Arabidopsis thaliana show that the two genes affect gynoecium and androecium development independently and antagonistically. Sex determination in the poplar therefore has the properties proposed for the first steps in the evolution of dioecy in flowering plants, with two genes whose joint effects favor close linkage, as is observed in poplar.

plant biology↗

bioRxiv2018

Sexually dimorphic recombination can facilitate the establishment of sexually antagonistic polymorphisms in guppies

Summary/AbstractRecombination suppression between sex chromosomes is often stated to evolve in response to polymorphisms for mutations that affect fitness of males and females in opposite directions (sexually antagonistic, or SA, mutations), but direct empirical support is lacking. The sex chromosomes of the fish Poecilia reticulata (the guppy) carry SA polymorphisms, making them excellent for testing this hypothesis for the evolution of sex linkage. We resequenced genomes of male and female guppies and, unexpectedly, found that variants on the sex chromosome indicate no extensive region with fully sex-linked genotypes, though many variants show strong evidence for partial sex linkage. We present genetic mapping results that help understand the evolution of the guppy sex chromosome pair. We find very different distributions of crossing over in the two sexes, with recombination events in male meiosis detected only at the tips of the chromosomes. The guppy may exemplify a route for sex chromosome evolution in which low recombination in males, likely evolved in a common ancestor, has facilitated the establishment of sexually antagonistic polymorphisms.

evolutionary biology↗

bioRxiv2018

Evolution of sex determination and heterogamety changes in section Otites of the genus Silene

Switches in heterogamety occasionally occur both in animals and plants, although plant sex determination systems are mostly more recently evolved than those of animals, and have had less time for switches to occur. However, our previous research revealed a switch in heterogamety in section Otites of the plant genus Silene.\n\nHere we analyse in detail the evolution of genetic sex determination in section Otites, which is estimated to have evolved about 0.55 MYA. Our study confirms female heterogamety in S. otites and newly reveals female heterogamety in S. borysthenica. Sequence analyses and genetic mapping show that the sex-linked regions of these two species are the same, but the region in S. colpophylla, a close relative with male heterogamety, is different. The sex chromosome pairs of S. colpophylla and S. otites each correspond to an autosome of the other species, and both differ from the XY pair in S. latifolia, in a different section of the genus. Our phylogenetic analysis suggests a possible change from female to male heterogamety within Silene section Otites, making these species suitable for detailed studies of the events involved.

evolutionary biology↗