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Cordaux, R.

Publications and source records attributed to Cordaux, R..

10 recordsLinked to original sources

Identification of a sex-determining locus potentially involved in a conflict over sex-ratio

Sex-determining genes remain largely uncharacterized outside classical models in vertebrates and insects, leaving a gap in our understanding of their evolutionary emergence and sex chromosome formation. Terrestrial isopods, particularly the common pill bug Armadillidium vulgare, provide an excellent model for investigating these processes due to the rapid turnover in sex-determination mechanisms they undergo. In A. vulgare, multiple genetic determinants coexist. Notably, a feminizing factor is transmitted at a rate exceeding Mendelian expectations, resulting in female-biased populations. Some lineages possess a masculinizing allele at a locus referred to as the "M gene", which is functionally analogous to an XY system. Its masculinizing dominant allele is hypothesized to have been selected due to the deficit of males caused by the feminizing factor. The existence of the M gene was inferred from crosses carried out in the 1990s, but its molecular nature remains unresolved. Here, we conducted a genome-wide SNP analysis combining pooled sequencing of male and female progenies with sequencing of individual parents across two families. Bayesian estimation of haplotype frequencies in progenies enabled us to delimit a candidate genomic region of approximately two megabases containing 34 annotated genes. Most notably, one of these genes encodes the androgenic gland hormone, a protein involved in male sexual differentiation. Our findings lay the groundwork for detailed genetic and functional investigations of the M gene, offering novel insights into the dynamics of sex determination in terrestrial isopods and into the turnover of sex chromosomes in response to sex-ratio distortion.

genomics↗

Within-host environmental heterogeneity is associated with phenotypic but not genomic diversity in Wolbachia endosymbionts

The mechanisms underlying within-host diversification in parasite populations are poorly understood. Yet, phenotypic and genotypic variation in parasites can shape their evolutionary trajectories and have important epidemiological consequences. Our aim was to determine whether the constraints associated with infecting different host tissues lead to the emergence and coexistence of multiple parasite sub-populations with distinct phenotypes. We tested this hypothesis using the most widespread bacterial endosymbiont, Wolbachia. We injected Wolbachia bacteria isolated from three tissues of the common pill-bug (Armadillidium vulgare) into uninfected individuals and monitored the growth rate and virulence of each bacterial sub-population in the new hosts. Our results highlight that within-host tissue heterogeneity leads to diverse Wolbachia phenotypes. High-depth genome re-resequencing of Wolbachia sub-populations revealed that this polymorphism was not due to genomic variation but was more likely a result of phenotypic plasticity. Indeed, we found no recurrent tissue-specific genomic variation among infected individuals. Our single nucleotide polymorphism (SNP) filtration pipeline, developed to ensure SNP validity, detected only one substitution. This Wolbachia variant, observed in one female, was present in all three bacterial sub-populations, with frequencies ranging from 24% to 58% depending on the tissue. Overall, our results support the stability of the Wolbachia genome with respect to the rarity of point mutations, in agreement with reports from other symbiotic systems. From a methodological perspective, our study highlights the need for considerable caution when detecting variants in endosymbiont populations, as our conservative approach led us to exclude more than 99.5% of the initially called variants.

evolutionary biology↗

Temporal stability of sex ratio distorter prevalence in natural populations of the isopod Armadillidium vulgare

AbstractIn the terrestrial isopod Armadillidium vulgare, many females produce progenies with female-biased sex ratios due to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and a nuclear non-mendelian locus called the f element. To investigate the potential impact of these SRD on the evolution of host sex determination, we analyzed their temporal distribution in six A. vulgare populations sampled up to six times over 12 years, for a total of 29 time points. SRD distribution was heterogeneous among populations despite their close geographic locations, so that when one SRD was frequent in a population, the other SRD was rare. In contrast with spatial heterogeneity, our results overall did not reveal substantial temporal variability in SRD prevalence within populations, suggesting equilibria in SRD evolutionary dynamics may have been reached or nearly so. Temporal stability was also generally reflected in mitochondrial and nuclear variation. Nevertheless, in a population, a Wolbachia strain replacement coincided with changes in mitochondrial composition but no change in nuclear composition, thus constituting a typical example of mitochondrial sweep caused by endosymbiont rise in frequency. Rare incongruence between Wolbachia strains and mitochondrial haplotypes suggested the occurrence of intraspecific horizontal transmission, making it a biologically relevant parameter for Wolbachia evolutionary dynamics in A. vulgare. Overall, our results provide an empirical basis for future studies on SRD evolutionary dynamics in the context of multiple sex determination factors co-existing within a single species, to ultimately evaluate the impact of SRD on the evolution of host sex determination mechanisms and sex chromosomes.

evolutionary biology↗

The Silene latifolia genome and its giant Y chromosome

In some species, the Y is a tiny chromosome but the dioecious plant Silene latifolia has a giant [~]550 Mb Y chromosome, which has remained unsequenced so far. Here we used a hybrid approach to obtain a high-quality male S. latifolia genome. Using mutants for sexual phenotype, we identified candidate sex-determining genes on the Y. Comparative analysis of the sex chromosomes with outgroups showed the Y is surprisingly rearranged and degenerated for a [~]11 MY-old system. Recombination suppression between X and Y extended in a stepwise process, and triggered a massive accumulation of repeats on the Y, as well as in the non-recombining pericentromeric region of the X, leading to giant sex chromosomes. One-Sentence SummaryThis work uncovers the structure, function, and evolution of one of the largest giant Y chromosomes, that of the model plant Silene latifolia, which is almost 10 times larger than the human Y, despite similar genome sizes.

genomics↗

Distribution of sex ratio distorters in natural populations of the isopod Armadillidium vulgare

In the isopod Armadillidium vulgare, many females produce progenies with female-biased sex ratios, due to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and the f element. We investigated the distribution and population dynamics of these SRD and mitochondrial DNA variation in 16 populations from Europe and Japan. Confirming and extending results from the 1990s, we found that the SRD are present at variable frequencies in populations, and that the f element is overall more frequent than Wolbachia. The two SRD never co-occur at high frequency in any population, suggesting an apparent mutual exclusion. We also detected Wolbachia or the f element in some males, which likely reflects insufficient titer to induce feminization or presence of masculinizing alleles. Our results are consistent with a single integration event of a Wolbachia genome in the A. vulgare genome at the origin of the f element, which contradicts an earlier hypothesis of frequent losses and gains. We identified strong linkage between Wolbachia strains and mitochondrial haplotypes, but no association between the f element and mitochondrial background. Our results open new perspectives on SRD evolutionary dynamics in A. vulgare, the evolution of genetic conflicts and their impact on the variability of sex determination systems.

evolutionary biology↗

Characterization of a sex-determining region and its genomic context via statistical estimates of haplotype frequencies in daughters and sons sequenced in pools

Sex chromosomes are generally derived from a pair of autosomes that have acquired a locus controlling sex. Sex chromosomes usually evolve reduced recombination around this locus and undergo a long process of molecular divergence. Although sex chromosomes have been intensively studied in several model taxa, the actual loci controlling sex are difficult to identify in highly diverged sex chromosomes, hence they are known in relatively few species. Taxa with evolutionarily young sex chromosomes can help fill this gap in knowledge. Here we aimed at pinpointing the sex-determining region (SDR) of Armadillidium vulgare, a terrestrial isopod with female heterogamety (ZW females and ZZ males) and which presumably presents evolutionarily young sex chromosomes. To locate the SDR, we assessed SNP allele frequencies in F1 daughters and sons sequenced in pools (pool-seq) in several families. We developed a Bayesian method that uses the SNP genotypes of individually sequenced parents and poolseq data from F1 siblings to estimate the genetic distance between a given genomic region (contig) and the SDR. This allowed us to assign more than 43 Megabases of contigs to sex chromosomes. By taking advantage of the several F1 families, we delineated a very short genomic region (~65 kilobases) that did not show evidence for recombination with the SDR. In this region, the comparison of sequencing depths between sexes outlined female-specific genes that may be involved in sex determination. Overall, our results provide strong evidence for an extremely low divergence of sex chromosomes in A. vulgare.

evolutionary biology↗

Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod

Sex chromosomes are highly variable in some taxonomic groups, but the evolutionary mechanisms underlying this diversity are not well understood. In terrestrial isopod crustaceans, evolutionary turnovers in sex chromosomes are frequent, possibly caused by Wolbachia, a vertically-transmitted endosymbiont causing male-to-female sex reversal. Here, we use surgical manipulations and genetic crosses, plus genome sequencing, to examine sex chromosomes in the terrestrial isopod Trachelipus rathkei. Although an earlier cytogenetics study suggested a ZZ/ZW sex chromosome system in this species, we surprisingly find multiple lines of evidence that in our study population, sex is determined by an XX/XY system. Consistent with a recent evolutionary origin for this XX/XY system, the putative male-specific region of the genome is small. The genome shows evidence of Y-linked duplications of the gene encoding the androgenic gland hormone, a major component of male sexual differentiation in isopods. Our analyses also uncover sequences horizontally acquired from past Wolbachia infections, consistent with the hypothesis that Wolbachia may have interfered with the evolution of sex determination in T. rathkei. Overall, these results provide evidence for the co-occurrence of multiple sex chromosome systems within T. rathkei, further highlighting the relevance of terrestrial isopods as models for the study of sex chromosome evolution.

evolutionary biology↗

Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

Cytosine methylation is an ancient epigenetic modification yet its function and extent within genomes is highly variable across eukaryotes. In mammals, methylation controls transposable elements and regulates the promoters of genes. In insects, DNA methylation is generally restricted to a small subset of transcribed genes, with both intergenic regions and transposable elements (TEs) depleted of methylation. The evolutionary origin and the function of these methylation patterns are poorly understood. Here we characterise the evolution of DNA methylation across the arthropod phylum. While the common ancestor of the arthropods had low levels of TE methylation and did not methylate promoters, both of these functions have evolved independently in centipedes and mealybugs. In contrast, methylation of the exons of a subset of transcribed genes is ancestral and widely conserved across the phylum, but has been lost in specific lineages. Remarkably the same set of genes are likely to be methylated in all species that retained exon-enriched methylation. We show that these genes have characteristic patterns of expression correlating to broad transcription initiation sites and well-positioned nucleosomes, providing new insights into potential mechanisms driving methylation patterns over hundreds of millions of years. Author SummaryAnimals develop from a single cell to form a complex organism with many specialised cells. Almost all of the fantastic variety of cells must have the same sequence of DNA, and yet they have distinct identities that are preserved even when they divide. This remarkable process is achieved by turning different sets of genes on or off in different types of cell using molecular mechanisms known as "epigenetic gene regulation". Surprisingly, though all animals need epigenetic gene regulation, there is a huge diversity in the mechanisms that they use. Characterising and explaining this diversity is crucial in understanding the functions of epigenetic pathways, many of which have key roles in human disease. We studied how one particular type of epigenetic regulation, known as DNA methylation, has evolved within arthropods. Arthropods are an extraordinarily diverse group of animals ranging from horseshoe crabs to fruit flies. We discovered that the levels of DNA methylation and where it is found within the genome changes rapidly throughout arthropod evolution. Nevertheless, there are some features of DNA methylation that seem to be the same across most arthropods-in particular we found that there is a tendency for a similar set of genes to acquire methylation of DNA in most arthropods, and that this is conserved over 350 million years. We discovered that these genes have distinct features that might explain how methylation gets targeted. Our work provides important new insights into the evolution of DNA methylation and gives some new hints to its essential functions.

genetics↗

Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod

Microbial endosymbiosis is widespread in animals, with major ecological and evolutionary implications. Successful symbiosis relies on efficient vertical transmission through host generations. However, when symbionts negatively affect host fitness, hosts are expected to evolve suppression of symbiont effects or transmission. Here we show that sex chromosomes control vertical transmission of feminizing Wolbachia endosymbionts in the isopod Armadillidium nasatum. Theory predicts that the invasion of an XY/XX species by cytoplasmic sex ratio distorters is unlikely because it leads to fixation of the unusual (and often lethal or infertile) YY genotype. We demonstrate that A. nasatum X and Y sex chromosomes are genetically highly similar and YY individuals are viable and fertile, thereby enabling Wolbachia spread in this XY-XX species. Nevertheless, we show that Wolbachia cannot drive fixation of YY individuals because infected YY females do not transmit Wolbachia to their offspring, unlike XX and XY females. The genetic basis fits the model of a Y-linked recessive allele (associated with an X-linked dominant allele), in which the homozygous state suppresses Wolbachia transmission. Moreover, production of all-male progenies by infected YY females restores a balanced sex ratio at the host population level. This suggests that blocking of Wolbachia transmission by YY females may have evolved to suppress feminization, thereby offering a whole new perspective on the evolutionary interplay between microbial symbionts and host sex chromosomes.

evolutionary biology↗

Pan-arthropod analysis reveals somatic piRNAs as an ancestral TE defence

In animals, small RNA molecules termed PIWI-interacting RNAs (piRNAs) silence transposable elements (TEs), protecting the germline from genomic instability and mutation. piRNAs have been detected in the soma in a few animals, but these are believed to be specific adaptations of individual species. Here, we report that somatic piRNAs were likely present in the ancestral arthropod more than 500 million years ago. Analysis of 20 species across the arthropod phylum suggests that somatic piRNAs targeting TEs and mRNAs are common among arthropods. The presence of an RNA-dependent RNA polymerase in chelicerates (horseshoe crabs, spiders, scorpions) suggests that arthropods originally used a plant-like RNA interference mechanism to silence TEs. Our results call into question the view that the ancestral role of the piRNA pathway was to protect the germline and demonstrate that small RNA silencing pathways have been repurposed for both somatic and germline functions throughout arthropod evolution.

evolutionary biology↗