Biology subjects

Toubiana, W.

Publications and source records attributed to Toubiana, W..

11 recordsLinked to original sources

bioRxiv2026

Drivers of tandem repeats variation within and between stick insect genomes

Tandemly repeated sequences are noncoding, highly variable, yet integral components of eukaryotic genomes. Empirical research has so far largely focused on a few well-characterized, functional tandem repeats (TRs) or documented the broad diversity and rapid evolution of these repeats without explicitly testing the forces driving their evolution. By characterizing TR abundance and TR sequence composition within and between chromosomes and species in the stick insect genus Timema, we uncover that TR loads are enriched in genomic regions of high recombination but tend to be reduced in species with higher effective population sizes. These results suggest that there is a mutational effect of recombination that generates increased TR loads and that the bulk of TRs experience weak selection, leading to their rapid turnover over short evolutionary timescales. Finally, comparisons of centromere and non-centromere TRs reveal that the rapid divergence of centromeres is best explained by the combination of the fast-evolving nature of TRs per se and centromere-specific evolutionary forces. Overall, this study provides the first in-depth investigation of genome-wide TR evolution, while integrating the effects of recombination, genetic drift, and centromeric position along the genome.

evolutionary biology↗

bioRxiv2024

Dynamics of recombination, X inactivation and centromere proteins during stick insect spermatogenesis

In eukaryotes, the cellular processes contributing to gamete formation form the building blocks of genetic inheritance across generations. While traditionally viewed as conserved across model organisms, emerging studies reveal significant variation in meiotic and post-meiotic processes. Extending our knowledge to non-model organisms is therefore critical to improve our understanding of the evolutionary origin and significance of modifications associated with gamete formation. We describe the cytological patterns underlying chromosome segregation, recombination, and meiotic sex chromosome inactivation during male meiosis in the stick insect group Timema. Our results provide a detailed description of centromere protein loading dynamics during spermatogenesis, and further reveal that 1) recombination initiates before synapsis (unlike Drosophila meiosis), and 2) that the X remains actively silenced despite two waves of transcriptional activation in autosomes during spermatogenesis. Together, our observations help understand the evolutionary significance of key cellular events related to spermatogenesis and shed light on the diversity of their associated molecular processes among species, including Timema stick insects.

cell biology↗

bioRxiv2024

Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development

Differentiated sex chromosomes are frequently associated with major transcriptional changes: the evolution of dosage compensation (DC) to equalize gene expression between the sexes and the establishment of meiotic sex chromosome inactivation (MSCI). Our study investigates the mechanisms and developmental dynamics of dosage compensation and meiotic sex chromosome inactivation in the stick insect species T. poppense. Stick insects are characterized by XX/XO sex determination and an X chromosome which likely evolved prior to the diversification of insects over 450 Mya. We generated a chromosome-level genome assembly and analyzed gene expression from various tissues (brain, gut, antennae, leg, and reproductive tract) across developmental stages in both sexes. Our results show that complete dosage compensation is maintained in male somatic tissues throughout development, mediated by upregulation of the single X chromosome. Contrarily, in male reproductive tissues, dosage compensation is present only in the early nymphal stages. As males reach the 4th nymphal stage and adulthood, X-linked gene expression diminishes, coinciding with the onset of MSCI. This reduction is associated with histone modifications indicative of transcriptional silencing, aligning with meiotic progression. These findings reveal the dynamic regulation of X-linked gene expression in T. poppense, and suggest that reduced X-expression in insect testes is generally driven by MSCI rather than an absence of dosage compensation mechanisms. Our work provides critical insights into sex chromosome evolution and the complex interplay of dosage compensation and MSCI across tissues and developmental stages.

evolutionary biology↗

bioRxiv2024

Functional monocentricity with holocentric characteristics andchromosome-specific centromeres in a stick insect

Centromeres are specialized genomic regions that are critical for chromosome segregation in eukaryotes. However, how the diversity of centromeres evolved, ranging from localized centromeres in monocentric species to complex chromosome-wide distributed centromere regions in holocentric species, remains elusive. Our cellular and genomic analyses in Timema stick insects reveal that within cell variation of the major centromere protein CenH3 recapitulates the variation typically observed across species. While CenH3-containing nucleosomes are distributed in a monocentric fashion on autosomes and bind tandem repeat sequences specific to individual or small groups of chromosomes, they exhibit a holocentric-like distribution on the sex chromosome and bind to more complex intergenic regions. Despite this contrasting distribution, all chromosomes, including the sex chromosome, attach to spindle microtubules at a single location, marking the first instance of a functionally monocentric species with holocentric-like attributes. Together, our findings highlight the potential for gradual transitions towards holocentricity or CenH3-independent centromere determination, and help to understand the rapid centromere sequence divergence between species.

evolutionary biology↗

bioRxiv2023

Evolution of alternative reproductive systems in Bacillus stick insects

Reproduction is a key feature of all organisms, yet the way in which it is achieved varies greatly across the tree of life. One striking example of this variation is the stick insect genus Bacillus, in which five different reproductive modes have been described: sex, facultative and obligate parthenogenesis, and two highly unusual reproductive modes: hybridogenesis and androgenesis. Under hybridogenesis, the entire genome from the paternal species is eliminated, and replaced each generation by mating with the corresponding species. Under androgenesis, an egg is fertilized but the developing diploid offspring bear two paternal genomes, and no maternal genome, as a consequence of unknown mechanisms. Here, we re-evaluate previous descriptions of Bacillus lineages and the proposed F1 hybrid ancestries of the hybridogenetic and obligately parthenogenetic lineages (based on allozymes and karyotypes) from Sicily, where all these reproductive modes are found. We generate a chromosome-level genome assembly for a facultative parthenogenetic species (B. rossius) and combine extensive field sampling with RADseq and mtDNA data. We identify and genetically corroborate all previously described species and confirm the ancestry of hybrid lineages. All hybrid lineages have fully retained their F1 hybrid constitution throughout the genome, indicating that the elimination of the paternal genome in hybridogens is always complete and that obligate parthenogenesis in Bacillus hybrid species is not associated with an erosion of heterozygosity as known in other hybrid asexuals. Our results provide a stepping stone towards understanding the transitions between reproductive modes and the proximate mechanisms of genome elimination.

evolutionary biology↗

bioRxiv2022

Transcriptome-based phylogeny of the semi-aquatic bugs (Hemiptera: Heteroptera: Gerromorpha) reveals patterns of lineage expansion in a series of new adaptive zones

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, they have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. The monophyletic group of water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a group of insects that transited to live on the water-air interface and diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones, representing distinct niches of water surfaces, and further diversification of the group. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

evolutionary biology↗

bioRxiv2020

Pleiotropy promotes male exaggerated weapon and its associated fighting behaviour in a water strider

Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body 1-3. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented 4,5. Here we show that the hyperallometric legs in the males of the water strider Microvelia longipes are associated with a specific signature of gene expression during development. Using RNAi knockdown, we demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric coefficient and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope in females. Furthermore, our data show that a tissue specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Overall, we demonstrate a genetic correlation between male body size, the exaggerated weapon, and the intense fighting behaviour associated with it in M. longipes. Our results provide evidence for a role of pleiotropy in the evolution of allometric slope.

evolutionary biology↗

bioRxiv2020

Impact of trait exaggeration on sex-biased gene expression and genome architecture in a water strider

Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of sex-specific phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the lack of a representative genome and transcriptomes to study the development of secondary sexual traits. Here we present the genome and developmental transcriptomes, focused on the legs of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs used as weapons. The quality of the genome assembly is such that over 90% of the sequence is captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in sex-biased genes, indicating a specific signature of gene expression in association with sex-specific trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. Interestingly, we found that female-biased genes that are expressed in the third legs only, but not male-biased genes, were over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed that they can arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Our findings shed light on how directional sexual selection drives sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

genomics↗

bioRxiv2018

Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon

Sexually selected traits can reach high degrees of expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait expression is poorly understood. The water strider Microvelia longipes displays a striking case of exaggeration and phenotypic variation where males display extreme differences in the size of their rear legs. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioral and morphometric experiments in a sample of Microvelia species. We uncovered differences both in the mating behavior and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behavior where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

evolutionary biology↗

bioRxiv2018

millepattes micropeptides are an ancient developmental switch required for embryonic patterning

Small open reading frames (smORFs) that code for \"micropeptides\" (10-100 amino acids) exhibit remarkable evolutionary complexity. Conserved micropeptides encoded by the millepattes (mlpt) gene are essential in Tribolium for embryogenesis but in Drosophila, function only in leg and cuticle differentiation. We find that a module identified in Drosophila trichome patterning, comprising Mlpt, UBR3, and Shaven-baby (Svb), coordinates early embryo patterning in several insect orders. Intriguingly, Mlpt segmentation function can be re-awakened in the Drosophila blastoderm, demonstrating the potency of an ancestral developmental switch retained despite evolving embryonic patterning modes. smORFs like millepattes thus illustrate plasticity of micropeptide functions despite constraints of essential genetic networks.\n\nOne sentence summaryA module comprising the small ORFs mlpt/pri/tal, the transcription factor Svb, and the ubiquitin ligase UBR3, possesses an ancestral function in insect embryo patterning which is lost in flies but reactivated when Svb expression is restored.

developmental biology↗

bioRxiv2017

Fitness effects of cis-regulatory variants in the Saccharomyces cerevisiae TDH3 promoter

Variation in gene expression is widespread within and between species, but fitness consequences of this variation are generally unknown. Here we use mutations in the Saccharomyces cerevisiae TDH3 promoter to assess how changes in TDH3 expression affect cell growth. From these data, we predict the fitness consequences of de novo mutations and natural polymorphisms in the TDH3 promoter. Nearly all mutations and polymorphisms in the TDH3 promoter were found to have no significant effect on fitness in the environment assayed, suggesting that the wild type allele of this promoter is robust to the effects of most new cis-regulatory mutations.

genetics↗