Biology subjects

Fracassetti, M.

Publications and source records attributed to Fracassetti, M..

7 recordsLinked to original sources

bioRxiv2026

Evolutionary consequences of repeated loss of distyly in Linum

The breakdown of distyly, a polymorphism that promotes disassortative pollination between two floral morphs, is often assumed to increase self-fertilization, reducing the efficacy of selection and challenging long-term species persistence. We tested whether repeated losses of distyly Linum were associated with genomic signatures of selfing by 1) testing for relaxed selective pressure in homostylous relative to distylous lineages, and 2) by characterising population genomic patterns of the homostylous Linum leonii in comparison to its distylous close relative Linum perenne. We generated whole-genome sequences and target-capture data from sixteen Linum species, and additionally built a high-quality genome assembly and acquired population-level whole-genome sequencing data for L. leonii (n=20). We reconstructed plastome phylogenies, estimated selective pressure for chloroplast and nuclear genes, inferred ancestral floral morph states, and tested for signatures of selfing in homostylous lineages. Compared to theoretical expectations, results were mixed, with partial identification of relaxed selective pressure in homostyles. Population genomic analyses of L. leonii revealed a moderate selfing rate of 0.32, suggesting that loss of distyly was associated with mixed mating rather than selfing, contrary to previous results on loss of distyly. Reduced nucleotide diversity and evidence for relaxed selection efficacy in L. leonii were instead consistent with a historical bottleneck. In Linum, the genomic consequences are more heterogeneous than generally assumed, and likely depend on species-specific evo-demographic history. This study highlights the complex evolutionary dynamics associated with the breakdown of distyly and emphasizes the need for comparative population genomic studies to clarify how such transitions shape evolutionary processes. Significance statementPlant mating system variation is central to evolution as it shapes genetic diversity, adaptability and fitness. Loss of distyly, an iconic example of a complex mating system favouring cross-pollination, can drive shifts from outcrossing to selfing, with potentially severe evolutionary consequences for the long-term persistence of the species in which it occurs. Using high-quality genome assembly and omic data for multiple Linum species, we tested for relaxed selective pressure in homostylous compared to distylous lineages, and tested for a population genomic signature of selfing in homostylous Linum leonii compared to the closely related distylous Linum perenne. Contrary to theoretical expectations, evidence for relaxation of selection was mixed in Linum homostyles and L. leonii did not exhibit a genomic signature of selfing. Our study reveals multiple evolutionary pathways following the loss of distyly, and highlights how mating system transitions, together with complex demographic processes, shape plant genetic diversity and evolution.

evolutionary biology↗

bioRxiv2025

Genomic studies in Linum shed light on the evolution of the distyly supergene and the molecular basis of convergent floral evolution

O_LIDistyly, an example of convergent evolution, is governed by a supergene called the S- locus. Recent studies highlight similar genetic architectures of independently evolved S-loci, but whether similar regulatory pathways underlie convergent evolution of distyly remains unclear. C_LIO_LIWe examined the evolution of supergenes and mechanisms underlying distyly in Linum species that diverged [~]33 Mya. Using haplotype-resolved genomes and population genomics, we identified and characterized the S-loci of Linum perenne (distylous) and Linum grandiflorum (style length dimorphic), and compared them to that of Linum tenue (distylous). We then tested for a conserved hormonal mechanism regulating style length polymorphism in Linum. C_LIO_LIHemizygosity in short-styled individuals is a shared feature of the Linum S-locus supergene, though its size, gene content, repeat elements, and extent of recombination suppression vary greatly among species. Two distyly candidate genes, TSS1 (style length) and WDR-44 (anther height/pollen self-incompatibility) are conserved at the C_LIO_LIS-locus. Consistent with a brassinosteroid-dependent role of TSS1, epibrassinolide treatment revealed a conserved, morph-specific effect on style length. C_LIO_LIS-locus genetic architecture, key S-locus genes and mechanisms regulating style length remain conserved >30 Mya in Linum. In combination with findings from other systems, our results suggest that the brassinosteroid pathway frequently contributes to style length polymorphism. C_LI

evolutionary biology↗

bioRxiv2023

Genomic analyses elucidate the causes and consequences of breakdown of distyly in Linum trigynum

Distyly is an iconic floral polymorphism governed by a supergene, which promotes efficient pollen transfer and outcrossing through reciprocal differences in the position of sexual organs in flowers, often coupled with heteromorphic self-incompatibility (SI). Distyly has evolved convergently in multiple flowering plant lineages, but has also broken down repeatedly, often resulting in homostylous, self-compatible populations with elevated rates of self-fertilization. Here, we aimed to study the genetic causes and genomic consequences of the shift to homostyly in Linum trigynum, which is closely related to distylous Linum tenue. Building on a high-quality genome assembly, we show that L. trigynum harbors a genomic region homologous to the dominant haplotype of the distyly supergene conferring long stamens and short styles in L. tenue, suggesting that loss of distyly first occurred in a short-styled individual. In contrast to homostylous Primula and Fagopyrum, L. trigynum harbors no fixed loss-of-function mutations in coding sequences of S-linked distyly candidate genes. Instead, floral gene expression analyses and controlled crosses suggest that mutations downregulating the S-linked LtWDR-44 candidate gene for male SI and/or anther height could underlie homostyly and self-compatibility (SC) in L. trigynum. Population genomic analyses of 224 whole-genome sequences further demonstrate that L. trigynum is highly self-fertilizing, exhibits significantly lower genetic diversity genome-wide, and is experiencing relaxed purifying selection and less frequent positive selection on nonsynonymous mutations relative to L. tenue. Our analyses shed light on the loss of distyly in L. trigynum, and advance our understanding of a common evolutionary transition in flowering plants.

evolutionary biology↗

bioRxiv2022

Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level

Supergenes govern balanced polymorphisms in a wide range of systems. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown if hemizygosity is pervasive among distyly S-loci. Here we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes. The chromosome-level genome assembly and detailed characterization of the distyly S-locus in L. tenue will facilitate elucidation of molecular mechanisms underlying the different forms of flowers described by Darwin.

evolutionary biology↗

bioRxiv2021

Genomic signatures of sexual selection on pollen-expressed genes in Arabis alpina

Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.

evolutionary biology↗

bioRxiv2020

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ~ 0.02 to 18 million years of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection of the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution. Significance statementRepeated evolution tends to be more predictable. The impressive spectrum of recent reports on genomic parallelism, however, revealed that the fraction of the genome that evolves in parallel largely varies, possibly reflecting different evolutionary scales investigated. Here, we demonstrate divergence-dependent parallelism using a comprehensive genome-wide dataset comprising 12 cases of parallel alpine adaptation and identify decreasing probability of adaptive re-use of genetic variation as the major underlying cause. This finding empirically demonstrates that evolutionary predictability is scale dependent and suggests that availability of pre-existing variation drives parallelism within and among populations and species. Altogether, our results inform the ongoing discussion about the (un)predictability of evolution, relevant for applications in pest control, nature conservation, or the evolution of pathogen resistance.

evolutionary biology↗

bioRxiv2018

Genetic basis and timing of a major mating system shift in Capsella

Shifts from outcrossing to self-fertilisation have occurred repeatedly in many different lineages of flowering plants, and often involve the breakdown of genetic outcrossing mechanisms. In the Brassicaceae, self-incompatibility (SI) allows plants to ensure outcrossing by recognition and rejection of self-pollen on the stigma. This occurs through the interaction of female and male specificity components, consisting of a pistil based receptor and a pollen-coat protein, both of which are encoded by tightly linked genes at the S-locus. When benefits of selfing are higher than costs of inbreeding, theory predicts that loss-of-function mutations in the male (pollen) SI component should be favoured, especially if they are dominant. However, it remains unclear whether mutations in the male component of SI are predominantly responsible for shifts to self-compatibility, and testing this prediction has been difficult due to the challenges of sequencing the highly polymorphic and repetitive ~100 kbp S-locus. The crucifer genus Capsella offers an excellent opportunity to study multiple transitions from outcrossing to self-fertilization, but so far, little is known about the genetic basis and timing of loss of SI in the self-fertilizing diploid Capsella orientalis. Here, we show that loss of SI in C. orientalis occurred within the past 2.6 Mya and maps as a dominant trait to the S-locus. Using targeted long-read sequencing of multiple complete S-haplotypes, we identify a frameshift deletion in the male specificity gene SCR that is fixed in C. orientalis, and we confirm loss of male SI specificity. We further analyze RNA sequencing data to identify a conserved, S-linked small RNA (sRNA) that is predicted to cause dominance of self-compatibility. Our results suggest that degeneration of pollen SI specificity in dominant S-alleles is important for shifts to self-fertilization in the Brassicaceae.\n\nAuthor SummaryAlready Darwin was fascinated by the widely varying modes of plant reproduction. The shift from outcrossing to self-fertilization is considered one of the most frequent evolutionary transitions in flowering plants, yet we still know little about the genetic basis of these shifts. In the Brassicaceae, outcrossing is enforced by a self-incompatibility (SI) system that enables the recognition and rejection of self pollen. This occurs through the action of two tightly linked genes at the S-locus, that encode a receptor protein located on the stigma (female component) and a pollen ligand protein (male component), respectively. Nevertheless, SI has frequently been lost, and theory predicts that mutations in the male component should have an advantage during the loss of SI, especially if they are dominant. To test this hypothesis, we mapped the loss of SI in a selfing species from the genus Capsella, a model system for evolutionary genomics. We found that loss of SI mapped to the S-locus, which harbored a dominant loss-of-function mutation in the male SI protein, and as expected, we found that male specificity was indeed lost in C. orientalis. Our results suggest that transitions to selfing often involve parallel genetic changes.

evolutionary biology↗