Biology subjects

Barrett, S. C. H.

Publications and source records attributed to Barrett, S. C. H..

14 recordsLinked to original sources

bioRxiv2025

Rapid evolution of synteny associated with multiple origins of dioecy and XY sex determination

Chromosomal rearrangements are a major driver of evolutionary innovation, shaping processes including local adaptation, speciation, and sex chromosome evolution. Multispecies synteny datasets are rich in information on the drivers of genomic rearrangement, but statistical approaches that enable insights to be obtained from this information are still in their infancy. Here, we present a novel framework for the application of phylogenetic comparative methods to multispecies synteny datasets. We apply this approach to Rumex, a clade of flowering plants that exhibits rapid karyotypic evolution, including multiple origins of XY sex determination from hermaphroditic ancestors. Leveraging new genome assemblies, we find evidence for accelerated syntenic evolution associated with evolutionary transitions to dioecy, highlighting how explicit phylogenetic hypothesis testing can generate new insights into adaptive hypotheses for rearrangements.

evolutionary biology↗

bioRxiv2025

Widespread loss of Y expression in the absence of transcriptional dosage compensation in Rumex hastatulus

There is growing interest in the potential role of gene regulatory evolution in the expansion and degeneration of Y chromosomes. Evolutionarily young sex chromosomes, such as those found in the flowering plant Rumex hastatulus, can provide insights into the early stages of this process. Using a new high-quality genome assembly with a well-assembled Y chromosome and a highly replicated transcriptome dataset, we found widespread underexpression of Y genes compared to their homologous counterparts on the X chromosome. We also found evidence for increased expression differences for more distantly diverged gametologs, suggestive of progressive loss of expression of Y linked genes over time. Genes with greater expression loss on the Y chromosome also showed elevated rates of protein evolution, as expected if silencing alleles mask the effects of deleterious mutations on the Y and/or if selective interference drives early degeneration in regulatory sequences. However, in contrast with the predictions of recent models of sex chromosome expansion and degeneration by regulatory evolution, there was no evidence of early dosage compensation. Overall, we conclude that in Rumex Hill-Robertson interference alone may be the main driver of Y chromosome degeneration, although further understanding of the temporal order of regulatory changes could help further untangle cause and effect.

genomics↗

bioRxiv2025

Selective contexts favouring asymmetry: a theoretical and empirical study of pollen transfer in mirror-image flowers

Reciprocal herkogamy has evolved multiple times in flowering plants and is thought to enhance cross-pollination and reduce reproductive interference. Mirror-image flowers represent a form of reciprocal herkogamy in which plants have either right-or left-deflected styles (dimorphic enantiostyly) or produce both stylar orientations (monomorphic enantiostyly). The ecological conditions under which these two forms of enantiostyly originate and persist remain poorly understood. Here, we investigate how floral asymmetry affects pollen transfer dynamics and mating outcomes, and under which conditions enantiostyly provides a fitness advantage over straight-styled floral morphologies. We integrate field observations of dimorphic enantiostylous Wachendorfia paniculata with a mathematical model simulating pollen transfer in plants with straight-styled, monomorphic, and dimorphic enantiostylous flowers. The model incorporates pollinator pathways, pollen carryover, and floral display size, and was parameterized using our ecological data. Enantiostylous flowers received more outcrossed pollen than straight-styled flowers, with dimorphism outperforming monomorphism. However, enantiostyly increased stochasticity in pollen transfer due to variation in pollinator pathways. Intrafloral self-pollination was extremely low in enantiostylous flowers and did not differ between monomorphic and dimorphic forms. Dimorphic enantiostylous plants exhibited longer pollen carryover curves and exported more pollen to more mates potentially increasing siring success and mate diversity. Enantiostyly, particularly in dimorphic systems, can provide a selective advantage by improving pollen receipt and export components of fitness through enhanced outcrossing. This mating advantage may be reduced under conditions of pollen limitation or when autogamy in straight-styled flowers is low. Our findings clarify the functional significance of enantiostyly and offer a framework for understanding the evolution of floral asymmetry in angiosperms.

evolutionary biology↗

bioRxiv2025

Cis-regulation of gene expression between sexes and life stages in Rumex hastatulus

The potential for conflict between sexes and life stages while sharing predominantly the same genome has important evolutionary consequences. In dioecious angiosperms, genes beneficial for the haploid pollen stage may reduce the fitness of diploid offspring of both males and females. However, we still lack an understanding of the extent of shared genetic architecture for gene expression between the sexes or life stages in plants, a key component for predicting the potential for conflict. We performed expression quantitative trait loci (eQTL) mapping to test if standing variation affects sexes and life stages differently using a population sample of the dioecious outcrossing plant Rumex hastatulus. We compared effect sizes and allele frequencies of cis-eQTLs in male and female leaf tissues and pollen and tested for genotype-by-sex interactions for gene expression. We found stronger shared genetic architecture between sexes than between life stages, suggesting greater potential for ongoing sexual conflict in leaves, which have been shown to be sexually dimorphic in earlier studies. In contrast, conflict over optimal gene expression between pollen and leaves may be easily resolved due to their distinct genetic architectures. Additionally, our burden of rare allele test suggested a signature of stabilizing selection against extreme gene expression in leaves. Our study highlights the use of eQTLs to investigate selection on gene expression and the evolution of conflict between sexes and life stages in dioecious species.

evolutionary biology↗

bioRxiv2025

Genetic architecture of the S-locus supergene revealed in a tetraploid distylous species

SummaryO_LIHeterostyly is a polymorphic floral adaptation controlled by supergenes and maintained in populations by disassortative mating. The molecular basis of distyly has been investigated in several unrelated families. Previous studies have been limited to diploid species and have not included Rubiaceae, which has the highest number of heterostylous species. C_LIO_LIHere, we investigate the genetic architecture of tetraploid Schizomussaenda henryi (Rubiaceae) to identify candidate style-length genes, evidence for hemizygosity and the potential role of gene duplication in the evolution of the S-locus. Chromosome-level genome assemblies and transcriptomic approaches identified the S-locus region comprised of four hemizygous genes. C_LIO_LIThe candidate gene SchzAUX22 may regulate style length and filament growth by acting in the auxin signaling pathway. Comparative studies of the two sub-genomes of S. henryi indicated strong similarities and no significant sub-genome dominance, as expected from autotetraploidy. Evidence from haplotype-resolved assemblies of a short-styled plant indicated that it possessed the ssSS genotype, consistent with autotetraploidy, which was estimated to have originated [~]3.6 Mya. Analysis of Ks values between S-locus genes and their paralogs indicated that the S-locus likely originated through stepwise duplication. C_LIO_LIOur study provides comprehensive genomic analysis of distyly in a polyploid and demonstrates that despite whole genome doubling the S-locus supergene remains intact and functional as an outbreeding mechanism. Our results contrast with many other heterostylous lineages where polyploidy is associated with breakdown of the polymorphism and transitions to self-fertilization. C_LI

plant biology↗

bioRxiv2024

Style deflection is determined by the handedness of phyllotaxis and differential cell elongation in a species with mirror-image flowers

Many animals and plants show left-right (LR) asymmetry. In some animal systems, handedness has a simple genetic basis, which has allowed identifying how handedness is determined at the molecular level, even if its functional relevance often remains unclear. Mirror-image flowers represent an example of LR asymmetry of clear functional significance, with the reciprocal placement of male and female organs in left- versus right-handed flowers promoting cross-pollination. Here, we use the South African geophyte Cyanella alba to study how handedness of its mirror-image flowers is determined and elaborated during development. Inflorescences of C. alba produce flowers with a largely consistent handedness. However, we find that this handedness has no simple genetic basis, and individual plants can switch their predominant handedness between years. Rather, it is the direction of the phyllotactic spiral that determines floral handedness. Cellular analysis combined with biophysical modelling demonstrates that style deflection is driven by increased cell expansion in the adaxial carpel facing the next oldest flower compared to the other adaxial carpel. The more expanding carpel shows transcriptional signatures of increased auxin signaling compared to the less expanding one, and auxin application to the latter can reverse the orientation of style deflection. We propose that a recently described inherent LR auxin asymmetry in the initiating organs of spiral phyllotaxis determines handedness in C. alba, representing a conserved non-genetic mechanism for creating a stable floral polymorphism. This mechanism links chirality across different levels of plant development and exploits a developmental constraint in a core patterning process to produce morphological variation of ecological relevance.

plant biology↗

bioRxiv2024

Genomic evidence for supergene control of Darwin's 'complex marriage arrangement' - the tristylous floral polymorphism

Tristyly is a polymorphism characterized by three flower morphs with reciprocal stigma and anther heights controlled by two epistatically interacting diallelic loci (S and M), hypothesized to be supergenes. Chromosome-level genome assemblies of Eichhornia paniculata identified the S- and M-loci. The S-locus is a supergene consisting of two divergent alleles: The S-allele (2.51Mb) with three S-allele specific genes hemizygous in most S-morph plants and the s-allele (596kb) with five s-allele specific genes. Two of the S-allele specific genes, LAZY1-S and HRGP-S, were specifically expressed in styles and stamens, respectively, making them tristyly candidate genes. The M-locus contained one gene (LAZY1-M), homologous to LAZY1-S, that was present in the M-allele but absent from the m-allele. Estimates of allele ages are consistent with the prediction that the S-locus evolved before the M-locus. Re-use of the same gene family highlights the potential role of gene duplication in the evolution of epistatic multilocus polymorphisms.

evolutionary biology↗

bioRxiv2023

Phylogenomics resolves key relationships in Rumex and uncovers a dynamic history of independently evolving sex chromosomes

Sex chromosomes have evolved independently many times across eukaryotes. Despite a considerable body of literature on the evolution of sex chromosomes, the causes and consequences of variation in the formation, degeneration, and turnover of sex chromosomes remain poorly understood. Comparative approaches in groups with sexual system variation can be valuable for understanding these questions. Plants are well-suited to such comparative studies, with many lineages containing relatively recent origins of dioecy and sex chromosomes as well as hermaphroditic close relatives. Rumex is a diverse genus of flowering plants harboring significant sexual system variation, including hermaphroditic and dioecious clades with XY sex chromosomes. Previous disagreement in the phylogenetic relationships among key species have rendered the history of sex chromosome evolution uncertain. Resolving this history is important to the development of Rumex as a system for the comparative study of sex chromosome evolution. Here, we leverage new transcriptome assemblies from 11 species representing the major clades in the genus, along with a whole-genome assembly generated for a pivotal hermaphroditic species, to further resolve the phylogeny and history of sex chromosome evolution in Rumex. Using phylogenomic approaches, we find evidence for two independent origins of sex chromosomes and introgression from unsampled taxa in the genus. Comparative genomics reveals massive chromosomal rearrangements in a dioecious species, with evidence for a complex origin of the sex chromosomes through multiple chromosomal fusions. However, we see no evidence of elevated rates of fusion on the sex chromosome in comparison with autosomes, providing no support for an adaptive hypothesis for the sex chromosome expansion. Overall, our results highlight the dynamic nature of sex chromosome systems in Rumex and illustrate the utility of the genus as a model for the comparative study of sex chromosome evolution.

evolutionary biology↗

bioRxiv2023

Phased assembly of neo-sex chromosomes reveals extensive Y degeneration and rapid genome evolution in Rumex hastatulus

Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales and evolutionary forces driving degeneration remain unclear. To investigate the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (<10MYA) and neo (<200,000 years) sex chromosomes in the XYY cytotype of the dioecious plant Rumex hastatulus and a hermaphroditic outgroup R. salicifolius. Our assemblies, supported by fluorescence in situ hybridization, confirmed the neo-sex chromosomes were formed by two key events: an X-autosome fusion and a reciprocal translocation between the homologous autosome and the Y chromosome. The enormous sex-linked regions of the X (296 MB) and two Y chromosomes (503 MB) both evolved from large repeat-rich genomic regions with low recombination; however, the complete loss of recombination on the Y still led to over 30% gene loss and major rearrangements. In the older sex-linked region, there has been a significant increase in transposable element abundance, even into and near genes. In the neo sex-linked regions, we observed evidence of extensive rearrangements without gene degeneration and loss. Overall, we inferred significant degeneration during the first 10 million years of Y chromosome evolution but not on very short timescales. Our results indicate that even when sex chromosomes emerge from repetitive regions of already-low recombination, the complete loss of recombination on the Y chromosome still leads to a substantial increase in repetitive element content and gene degeneration.

evolutionary biology↗

bioRxiv2023

Evolution from mixed to fixed handedness in mirror-image flowers: insights from adaptive dynamics

Mirror-image flowers (enantiostyly) involve a form of sexual asymmetry in which a flowers style is deflected either to the left or right side, with a pollinating anther orientated in the opposite direction. This curious floral polymorphism, which was known but not studied by Charles Darwin, occurs in at least 11 unrelated angiosperm families and represents a striking example of adaptive convergence in form and function associated with cross-pollination by insects. In several lineages, dimorphic enantiostyly (one stylar orientation per plant, both forms occurring within populations) has evolved from monomorphic enantiostyly, in which all plants can produce both style orientations. We use a modelling approach to investigate the emergence of dimorphic enantiostyly from monomorphic enantiostyly under gradual evolution. We show using adaptive dynamics that depending on the balance between inbreeding depression following geitonogamy, pollination efficiency and plant density, dimorphism can evolve from an ancestral monomorphic population. In general, the newly emergent dimorphic population is stable against invasion of a monomorphic mutant. However, our model predicts that under certain ecological conditions, e.g., a decline of pollinators, dimorphic enantiostyly may revert to a monomorphic state. We demonstrate using population genetics simulations that the observed evolutionary transitions are possible assuming a plausible genetic architecture.

evolutionary biology↗

bioRxiv2021

Recombination landscape dimorphism contributes to sexchromosome evolution in the dioecious plant Rumexhastatulus

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

genetics↗

bioRxiv2020

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

1Classical models suggest recombination rates on sex chromosomes evolve in a stepwise manner to localize the inheritance of sexually antagonistic variation in the sex where it is beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with pre-existing recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus, a species with a young neo-sex chromosome found in part of its geographical range. We found that the ancestral sex-linked region is located in a large region characterized by low recombination. Furthermore, comparison between the recombination landscape of the neo-sex chromosome and its autosomal homologue indicates that low recombination rates preceded sex linkage. Our findings suggest that ancestrally low rates of recombination have facilitated the formation and evolution of heteromorphic sex chromosomes.

evolutionary biology↗

bioRxiv2019

Ancestral and neo-sex chromosomes contribute to population divergence in a dioecious plant

Empirical evidence from several animal groups suggests that sex chromosomes may disproportionately contribute to reproductive isolation. This occurs particularly when sex chromosomes are associated with turnover of sex determination systems resulting from structural rearrangements to the sex chromosomes. We investigated these predictions in the dioecious plant Rumex hastatulus, which is comprised of populations of two sex chromosome cytotypes. Using population genomic analyses, we investigated the demographic history of R. hastatulus and explored the contributions of ancestral and neo-sex chromosomes to population genetic divergence. Our study revealed that the cytotypes represented genetically divergent populations with evidence for historical but not contemporary gene flow between them. In agreement with classical predictions, we found that the ancestral X chromosome was disproportionately divergent compared with the rest of the genome. Excess differentiation was also observed on the Y chromosome, even when using measures of differentiation that control for differences in effective population size. Our estimates of the timing of the origin of the neo-sex chromosomes in R. hastatulus are coincident with cessation of gene flow, suggesting that the chromosomal fusion event that gave rise to the origin of the XYY cytotype may have also been a key driver of reproductive isolation.

plant biology↗

bioRxiv2018

The effects of haploid selection on Y chromosome evolution in a dioecious plant

The evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male-specific haploid selection might favour the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialise for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y-linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex-specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.

evolutionary biology↗