Biology subjects

Dumas, Z.

Publications and source records attributed to Dumas, Z..

16 recordsLinked to original sources

bioRxiv2025

Hybridogenesis as an intermediate step between sexual reproduction and parthenogenesis

Many organisms reproduce through non-canonical modes such as parthenogenesis or hybridogenesis (clonal transmission of one parents chromosomes), but whether these arise abruptly or stepwise from each other remains unclear. We address this in the stick-insect genus Bacillus, which harbors several hybrid lineages with diverse reproductive modes. From haplotype-resolved phylogenies of >500 wild-caught individuals, we infer a single, recent ([~]8,000 years) origin of all hybrids. The ancestral hybrid reproduced via hybridogenesis, which subsequently diversified into parthenogenesis and, twice independently, into triploid lineages. Laboratory crosses recapitulate this trajectory, where each step facilitated the next. These findings reveal how a single genomic perturbation can act as a catalyst for evolutionary innovation, turning the loss of sex into a driver of diversification rather than a dead end.

evolutionary biology↗

bioRxiv2025

Dosage compensation and meiotic sex chromosome inactivation are maintained in the absence of selection

Dosage compensation and meiotic sex chromosome inactivation (MSCI) are key mechanisms regulating gene expression from the X chromosome in male-heterogametic species. While the convergent evolution of these mechanisms is well-documented, their evolutionary fate under relaxed selection remains poorly understood. Here, we test whether dosage compensation and MSCI persist following three independent transitions to parthenogenesis in stick insects, where selection on male phenotypes is relaxed. Using rare males occasionally produced by parthenogenetic females, chromosome-level genome assemblies, RNA-seq from multiple tissues, and immunocytochemistry, we find that dosage compensation is fully conserved across all nine studied somatic tissues. This is even the case in the oldest, approximately 1.5 million years old all-female lineage, and for tissue-specific genes for which dosage variation is not expected to be very deleterious. Meiotic X inactivation in the germline is also conserved. Surprisingly however, expression data and cytological markers indicate that MSCI signatures are even stronger in parthenogenetic males, a pattern likely driven by prolonged autosomal transcription during meiosis. These results indicate that X-targeting dosage compensation and MSCI are highly stable over evolutionary time and may be maintained in all-female lineages by a combination of evolutionary constraint, pleiotropy, or very weak selection, whereas autosomal expression during meiosis shifts rapidly under relaxed selection. Significance StatementSex chromosomes are regulated by specialized mechanisms that balance gene expression between males and females in somatic tissues (dosage compensation) and silence the X chromosome during male meiosis (meiotic sex chromosome inactivation, MSCI). These processes are thought to decay when they become redundant, yet suitable systems to test this prediction are scarce. We studied rare males from parthenogenetic stick insect lineages that have been evolving without sex for up to 1.5 million years. Surprisingly, both dosage compensation and MSCI remain fully functional, despite relaxed selection. Instead, we find altered autosomal expression during meiosis. Our results reveal that sex chromosome regulation is evolutionarily stable and constrained, persisting even after the loss of its purpose.

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↗

bioRxiv2024

Recent neo-X and Y sex chromosomes in an ant cricket

In eukaryotes with separate sexes, sex determination often involves heteromorphic sex chromosomes which have diverged as a consequence of recombination suppression. In species with very old heteromorphic sex chromosomes, mechanisms such as dosage compensation and meiotic sex chromosome inactivation adjust for the fact that sex chromosomes occur as a single copy in the heterogametic sex. However, how such mechanisms evolve remains largely unknown because species with young sex chromosomes characterised by recent recombination suppression remain understudied. We discovered such young neo-sex chromosomes in the ant cricket Myrmecophilus myrmecophilus, which displays a neo-XY system. We generated a chromosomal-level assembly of the female genome and compared it to male genomic data and identified four evolutionary strata on the X, with varying degrees of Y chromosome degeneration. Phylogenetic studies and genomic comparisons with closely related species revealed two cases of taxonomic synonymies and that the Myrmecophilus neo-sex chromosomes likely evolved approximately 7 million years ago from an X-autosome fusion. The X strata subsequently emerged as a consequence of two localised events of recombination suppression. Ant crickets thus represent a promising new model for studying the early stages of sex chromosome degeneration and the establishment of processes such as dosage compensation or meiotic sex chromosome inactivation.

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↗

bioRxiv2023

Evidence for cryptic gene flow in parthenogenetic stick insects of the genus Timema

Obligately parthenogenetic species are expected to be short lived since the lack of sex and recombination should translate into a slower adaptation rate and increased accumulation of deleterious alleles. Some, however, are thought to have been reproducing without males for millions of years. It is not clear how these old parthenogens can escape the predicted long-term costs of parthenogenesis, but an obvious explanation is cryptic sex. In this study we screen for signatures of cryptic sex in eight populations of four parthenogenetic species of Timema stick insects, some estimated to be older than 1M yrs. Low genotype diversity, homozygosity of individuals and high linkage disequilibrium (LD) unaffected by marker distances support exclusively parthenogenetic reproduction in six populations. However, in two populations (namely, of the species Timema douglasi and T. monikensis) we find strong evidence for cryptic sex, most likely mediated by rare males. These populations had comparatively high genotype diversities, lower LD, and a clear LD decay with genetic distance. Rare sex in species that are otherwise largely parthenogenetic could help explain the unusual success of parthenogenesis in the Timema genus and raises the question whether episodes of rare sex are in fact the simplest explanation for the persistence of many old parthenogens in nature.

evolutionary biology↗

bioRxiv2021

X chromosomes show a faster evolutionary rate and complete somatic dosage compensation across Timema stick insect species

Sex chromosomes have evolved repeatedly across the tree of life. As they are present in different copy numbers in males and females, they are expected to experience different selection pressures than the autosomes, with consequences including a faster rate of evolution, increased accumulation of sexually antagonistic alleles, and the evolution of dosage compensation. Whether these consequences are general or linked to idiosyncrasies of specific taxa is not clear as relatively few taxa have been studied thus far. Here we use wholegenome sequencing to identify and characterize the evolution of the X chromosome in five species of Timema stick insects with XX:X0 sex determination. The X chromosome had a similar size (approximately 11% of the genome) and gene content across all five species, suggesting that the X chromosome originated prior to the diversification of the genus. Genes on the X showed evidence of relaxed selection (elevated dN/dS) and a slower evolutionary rate (dN + dS) than genes on the autosomes, likely due to sex-biased mutation rates. Genes on the X also showed almost complete dosage compensation in somatic tissues (heads and legs), but dosage compensation was absent in the reproductive tracts. Contrary to prediction, sex-biased genes showed little enrichment on the X, suggesting that the advantage X-linkage provides to the accumulation of sexually antagonistic alleles is weak. Overall, we found the consequences of X-linkage on gene sequences and expression to be similar across Timema species, showing the characteristics of the X chromosome are surprisingly consistent over 30 million years of evolution.

evolutionary biology↗

bioRxiv2021

Dynamics of sex-biased gene expression over development in the stick insect Timema californicum

AO_SCPLOWBSTRACTC_SCPLOWSexually dimorphic phenotypes are thought to arise primarily from sex-biased gene expression during development. Major changes in developmental strategies, such as the shift from hemimetabolous to holometabolous development, are therefore expected to have profound consequences for the dynamics of sex-biased gene expression. However, no studies have previously examined sex-biased gene expression during development in hemimetabolous insects, precluding comparisons between developmental strategies. Here we characterized sex-biased gene expression at three developmental stages in a hemimetabolous stick insect (Timema californicum): hatchlings, juveniles, and adults. As expected, the proportion of sex-biased genes gradually increased during development, mirroring the gradual increase of phenotypic sexual dimorphism. Sex-biased genes identified at early developmental stages were generally consistently male- or female-biased at later stages, suggesting their importance in sexual differentiation. Additionally, we compared the dynamics of sex-biased gene expression during development in T. californicum to those of the holometabolous fly Drosophila melanogaster by reanalyzing publicly available RNA-seq data from third instar larval, pupal and adult stages. In D. melanogaster, 84% of genes were sex-biased at the adult stage (compared to only 20% in T. californicum), and sex-biased gene expression increased abruptly at the adult stage when morphological sexual dimorphism is manifested. Our findings are consistent with the prediction that the dynamics of sex-biased gene expression during development differ extensively between holometabolous and hemimetabolous insect species.

evolutionary biology↗

bioRxiv2020

Haplotype divergence supports ancient asexuality in the oribatid mite Oppiella nova

Sex strongly impacts genome evolution via recombination and segregation. In the absence of these processes, haplotypes within lineages of diploid organisms are predicted to accumulate mutations independently of each other and diverge over time. This so-called Meselson effect is regarded as a strong indicator of the long-term evolution under obligate asexuality. Here, we present genomic and transcriptomic data of three populations of the asexual oribatid mite species Oppiella nova and its sexual relative Oppiella subpectinata. We document strikingly different patterns of haplotype divergence between the two species, strongly supporting Meselson effect like evolution and ancient asexuality in O. nova: (I) Variation within individuals exceeds variation between populations in O. nova but vice versa in O. subpectinata. (II) Two O. nova sub-lineages feature a high proportion of heterozygous genotypes and lineage-specific haplotypes, indicating that haplotypes diverged independently within the two lineages after their split. (III) The deepest split in gene trees generally separates haplotypes in O. nova, but populations in O. subpectinata. (IV) Tree topologies of the two haplotypes match each other. Our findings provide positive evidence for the absence of sex over evolutionary time in O. nova and suggest that asexual oribatid mites can escape the dead-end fate usually associated with asexual lineages.

evolutionary biology↗

bioRxiv2020

First annotated draft genomes of non-marine ostracods (Ostracoda, Crustacea) with different reproductive modes

ABSTRACTSOstracods are one of the oldest crustacean groups with an excellent fossil record and high importance for phylogenetic analyses but genome resources for this class are still lacking. We have successfully assembled and annotated the first reference genomes for three species of non-marine ostracods; two with obligate sexual reproduction (Cyprideis torosa and Notodromas monacha) and the putative ancient asexual Darwinula stevensoni. This kind of genomic research has so far been impeded by the small size of most ostracods and the absence of genetic resources such as linkage maps or BAC libraries that were available for other crustaceans. For genome assembly, we used an Illumina-based sequencing technology, resulting in assemblies of similar sizes for the three species (335-382Mb) and with scaffold numbers and their N50 (19-56 kb) in the same orders of magnitude. Gene annotations were guided by transcriptome data from each species. The three assemblies are relatively complete with BUSCO scores of 92-96%, and thus exceed the quality of several other published crustacean genomes obtained with similar techniques. The number of predicted genes (13,771-17,776) is in the same range as Branchiopoda genomes but lower than in most malacostracan genomes. These three reference genomes from non-marine ostracods provide the urgently needed basis to further develop ostracods as models for evolutionary and ecological research.

evolutionary biology↗

bioRxiv2020

Convergent consequences of parthenogenesis on stick insect genomes

The shift from sexual reproduction to parthenogenesis has occurred repeatedly in animals, but how the loss of sex affects genome evolution remains poorly understood. We generated de novo reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references in combination with population genomic data, we show that parthenogenesis results in an extreme reduction of heterozygosity, and often leads to genetically uniform populations. We also find evidence for less effective positive selection in parthenogenetic species, supporting the view that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Contrary to studies of non-recombining genome portions in sexual species, genomes of parthenogenetic species do not accumulate transposable elements (TEs), likely because successful parthenogens derive from sexual ancestors with inactive TEs. Because we are able to conduct replicated comparisons across five species pairs, our study reveals, for the first time, how animal genomes evolve in the absence of sex in natural populations, providing empirical support for the negative consequences of parthenogenetic reproduction as predicted by theory.

evolutionary biology↗

bioRxiv2019

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts. ResultsWe present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids. ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.

genomics↗

bioRxiv2019

Sex-biased gene expression is masculinized in asexual females

Males and females feature strikingly different phenotypes, despite sharing most of their genome. The resolution of this apparent paradox is through differential gene expression, whereby genes are expressed at different levels in each sex. This resolution, however, is likely to be incomplete, leading to conflict between males and females over the optimal expression of genes. We test the hypothesis that gene expression in females is constrained from evolving to its optimum level due to sexually antagonistic selection on males, by examining changes sex-biased gene expression in five obligate asexual species of stick insect, which do not produce males. We predicted that the transcriptome of asexual females would be feminized as asexual females do not experience any sexual conflict. Contrary to our prediction we find that asexual females feature masculinized gene expression, and hypothesise that this is due to shifts in female optimal gene expression levels following the suppression of sex.

evolutionary biology↗

bioRxiv2018

Genes involved in the convergent evolution of asexuality in stick insects

Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. While the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In particular, it is completely unknown whether the repeated evolution of asexual phenotypes involves similar molecular changes, as previous studies have focused on changes occurring in single lineages. Here we investigate the extent of convergent gene expression changes across five independent transitions to asexuality in stick insects. We compared gene expression of asexual females to females of close sexual relatives in whole-bodies, reproductive tracts, and legs. We identified a striking amount of convergent gene expression change (up to 8% of genes), greatly exceeding that expected by chance. Convergent changes were also tissue-specific, and most likely driven by selection for functional changes. Genes showing convergent changes in the reproductive tract were associated with meiotic spindle formation and centrosome organization. These genes are particularly interesting as they can influence the production of unreduced eggs, a key barrier to asexual reproduction. Changes in legs and whole-bodies were likely involved in female sexual trait decay, with enrichment in terms such as sperm-storage and pigmentation. By identifying changes occurring across multiple independent transitions to asexuality, our results provide a rare insight into the molecular basis of asexual phenotypes and suggest that the evolutionary path to asexuality is highly constrained, requiring repeated changes to the same key genes.

evolutionary biology↗