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Labedan, M.

Publications and source records attributed to Labedan, M..

7 recordsLinked to original sources

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↗

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↗

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↗

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↗

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↗

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↗

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↗