Zoé Dumas

University of Lausanne

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Co-Authors

Tanja Schwander

University of Lausanne

Jens Bast

University of Cologne

Darren J. Parker

University of Lausanne

Marc Robinson‐Rechavi

University of Lausanne

Dominique Colinet

Université Côte d'Azur

Elzemiek Geuverink

University of Groningen

Camille Meslin

Institut d'écologie et des sciences de l'environnement de Paris

Emmanuelle Jacquin‐Joly

Institut d'écologie et des sciences de l'environnement de Paris

Rosanna Salvia

University of Basilicata

Stéphanie Robin

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Cooperative Institutions

University of Lausanne

Centre National de la Recherche Scientifique

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

University of Göttingen

SIB Swiss Institute of Bioinformatics

Institut de Recherche pour le Développement

University of Münster

Université de Rennes

ETH Zurich

Institut National de la Recherche Agronomique

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Cost of cooperation rules selection for cheats in bacterial metapopulations

Journal of Evolutionary Biology (2011)

Zoé Dumas Rolf Kümmerli

Abstract Bacteria secrete a large variety of beneficial metabolites into the environment, which can be shared as public goods among producing bacteria, but also be exploited by nonproducing cheats. Here, we focus on cooperative production of iron‐chelating molecules (siderophores) in the bacterium Pseudomonas aeruginosa to study how relevant ecological factors influence selection for cheating. We designed patch‐structured metapopulations that allowed us introducing among‐patch ecological variation. We found that cheating readily evolved in uniform iron‐limited environments. This finding is explained by severe iron limitation demanding high siderophore‐production efforts, which results in high metabolic costs accruing to cooperators, and thereby facilitates the spread of cheats. In contrast, we observed a significant reduction or even negation of selection for cheating in metapopulations where we introduced patches with increased iron availability and/or opportunities to recycle siderophores. These findings are compatible with the view that cheats are less likely to invade in environments that allow bacteria to reduce siderophore‐production efforts, as this lowers the overall metabolic costs accruing to cooperators. Because we increased iron availability and siderophore recycling opportunities moderately, and only in some patches, our findings demonstrate that already‐small local variations in ecological conditions as occurring in nature can significantly affect selection for public‐goods secretion in microbes. In addition, we found that most (84.6%) of the evolved cheats were partially deficient for siderophore production and not loss‐of‐function mutants. Genetic considerations indicate that mutations leading to partial deficiency occur more frequent than mutations leading to loss of function, but also suggest that partially deficient mutants might often be the more competitive cheats.

Metapopulation

10.1111/j.1420-9101.2011.02437.x

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Citations (84)

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

Heredity (2022)

Jelisaveta Djordjevic Zoé Dumas Marc Robinson‐Rechavi Tanja Schwander Darren J. Parker

Sexually 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.

Sexual dimorphism

Dosage compensation

Developmental Biology

Melanogaster

Sexual Differentiation

10.1038/s41437-022-00536-y

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Citations (31)

Consequences of Asexuality in Natural Populations: Insights from Stick Insects

Molecular Biology and Evolution (2018)

Jens Bast Darren J. Parker Zoé Dumas Kirsten Jalvingh Patrick Tran Van

Recombination is a fundamental process with significant impacts on genome evolution. Predicted consequences of the loss of recombination include a reduced effectiveness of selection, changes in the amount of neutral polymorphisms segregating in populations, and an arrest of GC-biased gene conversion. Although these consequences are empirically well documented for nonrecombining genome portions, it remains largely unknown if they extend to the whole genome scale in asexual organisms. We identify the consequences of asexuality using de novo transcriptomes of five independently derived, obligately asexual lineages of stick insects, and their sexual sister-species. We find strong evidence for higher rates of deleterious mutation accumulation, lower levels of segregating polymorphisms and arrested GC-biased gene conversion in asexuals as compared with sexuals. Taken together, our study conclusively shows that predicted consequences of genome evolution under asexuality can indeed be found in natural populations.

Asexuality

Gene conversion

Gene pool

Genetic Fitness

Mutation Accumulation

Lineage (genetic)

10.1093/molbev/msy058

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Citations (72)

Convergent consequences of parthenogenesis on stick insect genomes

Science Advances (2022)

Kamil S. Jaroň Darren J. Parker Yoann Anselmetti Patrick Tran Van Jens Bast

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 reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references and 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, suggesting that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Parthenogenetic species did not show increased transposable element (TE) accumulation, likely because there is little TE activity in the genus. By using replicated sexual-parthenogenetic comparisons, our study reveals how the absence of sex affects genome evolution in natural populations, providing empirical support for the negative consequences of parthenogenesis as predicted by theory.

Parthenogenesis

Sexual reproduction

Asexual reproduction

10.1126/sciadv.abg3842

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Citations (35)

X chromosomes show relaxed selection and complete somatic dosage compensation acrossTimemastick insect species

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Darren J. Parker Kamil S. Jaroň Zoé Dumas Marc Robinson‐Rechavi Tanja Schwander

Abstract 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.

Dosage compensation

Epistasis

Skewed X-inactivation

10.1101/2021.11.28.470265

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Citations (2)

Sex-biased gene expression is repeatedly masculinized in asexual females

Nature Communications (2019)

Darren J. Parker Jens Bast Kirsten Jalvingh Zoé Dumas Marc Robinson‐Rechavi

Abstract Males and females feature strikingly different phenotypes, despite sharing most of their genome. A 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. Here 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 in 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.

Obligate

Asexual reproduction

10.1038/s41467-019-12659-8

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Citations (30)

Additional file 9 of Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

Figshare (2020)

Alice B. Dennis Gabriel Ballesteros Stéphanie Robin Lukas Schrader Jens Bast

Additional file 9. Venom gene annotations. Annotation details of venom genes in L. fabarum and A. ervi.

10.6084/m9.figshare.12398870

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Ever-Young Sex Chromosomes in European Tree Frogs

PLoS Biology (2011)

Matthias Stöck Agnès Horn Christine Grossen Dorothea Lindtke Roberto Sermier

Non-recombining sex chromosomes are expected to undergo evolutionary decay, ending up genetically degenerated, as has happened in birds and mammals. Why are then sex chromosomes so often homomorphic in cold-blooded vertebrates? One possible explanation is a high rate of turnover events, replacing master sex-determining genes by new ones on other chromosomes. An alternative is that X-Y similarity is maintained by occasional recombination events, occurring in sex-reversed XY females. Based on mitochondrial and nuclear gene sequences, we estimated the divergence times between European tree frogs (Hyla arborea, H. intermedia, and H. molleri) to the upper Miocene, about 5.4–7.1 million years ago. Sibship analyses of microsatellite polymorphisms revealed that all three species have the same pair of sex chromosomes, with complete absence of X-Y recombination in males. Despite this, sequences of sex-linked loci show no divergence between the X and Y chromosomes. In the phylogeny, the X and Y alleles cluster according to species, not in groups of gametologs. We conclude that sex-chromosome homomorphy in these tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination. Seemingly young sex chromosomes may thus carry old-established sex-determining genes, a result at odds with the view that sex chromosomes necessarily decay until they are replaced. This raises intriguing perspectives regarding the evolutionary dynamics of sexually antagonistic genes and the mechanisms that control X-Y recombination.

Pseudoautosomal region

10.1371/journal.pbio.1001062

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Citations (187)

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

bioRxiv (Cold Spring Harbor Laboratory) (2024)

William Toubiana Zoé Dumas Patrick Tran Van Darren J. Parker Vincent Mérel

ABSTRACT 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.

10.1101/2024.06.30.601385

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Citations (1)

Data from: Cost of cooperation rules selection for cheats in bacterial metapopulations

Zoé Dumas Rolf Kuemmerli

Metapopulation

10.5061/dryad.2f4g2h90

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Citations (0)