TY - JOUR AB - Since the commercialization of brine shrimp (genus Artemia) in the 1950s, this lineage, and in particular the model species Artemia franciscana, has been the subject of extensive research. However, our understanding of the genetic mechanisms underlying various aspects of their reproductive biology, including sex determination, is still lacking. This is partly due to the scarcity of genomic resources for Artemia species and crustaceans in general. Here, we present a chromosome-level genome assembly of A. franciscana (Kellogg 1906), from the Great Salt Lake, United States. The genome is 1 GB, and the majority of the genome (81%) is scaffolded into 21 linkage groups using a previously published high-density linkage map. We performed coverage and FST analyses using male and female genomic and transcriptomic reads to quantify the extent of differentiation between the Z and W chromosomes. Additionally, we quantified the expression levels in male and female heads and gonads and found further evidence for dosage compensation in this species. AU - Bett, Vincent K AU - Macon, Ariana AU - Vicoso, Beatriz AU - Elkrewi, Marwan N ID - 15009 IS - 1 JF - Genome Biology and Evolution TI - Chromosome-level assembly of Artemia franciscana sheds light on sex chromosome differentiation VL - 16 ER - TY - DATA AB - Since the commercialization of brine shrimp (genus Artemia) in the 1950s, this lineage, and in particular the model species Artemia franciscana, has been the subject of extensive research. However, our understanding of the genetic mechanisms underlying various aspects of their reproductive biology, including sex determination, are still lacking. This is partly due to the scarcity of genomic resources for Artemia species and crustaceans in general. Here, we present a chromosome-level genome assembly of Artemia franciscana (Kellogg 1906), from the Great Salt Lake, USA. The genome is 1GB, and the majority of the genome (81%) is scaffolded into 21 linkage groups using a previously published high-density linkage map. We performed coverage and FST analyses using male and female genomic and transcriptomic reads to quantify the extent of differentiation between the Z and W chromosomes. Additionally, we quantified the expression levels in male and female heads and gonads and found further evidence for dosage compensation in this species. AU - Elkrewi, Marwan N ID - 14705 KW - sex chromosome evolution KW - genome assembly KW - dosage compensation TI - Data from "Chromosome-level assembly of Artemia franciscana sheds light on sex-chromosome differentiation" ER - TY - JOUR AB - Understanding population divergence that eventually leads to speciation is essential for evolutionary biology. High species diversity in the sea was regarded as a paradox when strict allopatry was considered necessary for most speciation events because geographical barriers seemed largely absent in the sea, and many marine species have high dispersal capacities. Combining genome-wide data with demographic modelling to infer the demographic history of divergence has introduced new ways to address this classical issue. These models assume an ancestral population that splits into two subpopulations diverging according to different scenarios that allow tests for periods of gene flow. Models can also test for heterogeneities in population sizes and migration rates along the genome to account, respectively, for background selection and selection against introgressed ancestry. To investigate how barriers to gene flow arise in the sea, we compiled studies modelling the demographic history of divergence in marine organisms and extracted preferred demographic scenarios together with estimates of demographic parameters. These studies show that geographical barriers to gene flow do exist in the sea but that divergence can also occur without strict isolation. Heterogeneity of gene flow was detected in most population pairs suggesting the predominance of semipermeable barriers during divergence. We found a weak positive relationship between the fraction of the genome experiencing reduced gene flow and levels of genome-wide differentiation. Furthermore, we found that the upper bound of the ‘grey zone of speciation’ for our dataset extended beyond that found before, implying that gene flow between diverging taxa is possible at higher levels of divergence than previously thought. Finally, we list recommendations for further strengthening the use of demographic modelling in speciation research. These include a more balanced representation of taxa, more consistent and comprehensive modelling, clear reporting of results and simulation studies to rule out nonbiological explanations for general results. AU - De Jode, Aurélien AU - Le Moan, Alan AU - Johannesson, Kerstin AU - Faria, Rui AU - Stankowski, Sean AU - Westram, Anja M AU - Butlin, Roger K. AU - Rafajlović, Marina AU - Fraisse, Christelle ID - 11479 IS - 2 JF - Evolutionary Applications TI - Ten years of demographic modelling of divergence and speciation in the sea VL - 16 ER - TY - JOUR AB - Experimental evolution studies are powerful approaches to examine the evolutionary history of lab populations. Such studies have shed light on how selection changes phenotypes and genotypes. Most of these studies have not examined the time course of adaptation under sexual selection manipulation, by resequencing the populations’ genomes at multiple time points. Here, we analyze allele frequency trajectories in Drosophila pseudoobscura where we altered their sexual selection regime for 200 generations and sequenced pooled populations at 5 time points. The intensity of sexual selection was either relaxed in monogamous populations (M) or elevated in polyandrous lines (E). We present a comprehensive study of how selection alters population genetics parameters at the chromosome and gene level. We investigate differences in the effective population size—Ne—between the treatments, and perform a genome-wide scan to identify signatures of selection from the time-series data. We found genomic signatures of adaptation to both regimes in D. pseudoobscura. There are more significant variants in E lines as expected from stronger sexual selection. However, we found that the response on the X chromosome was substantial in both treatments, more pronounced in E and restricted to the more recently sex-linked chromosome arm XR in M. In the first generations of experimental evolution, we estimate Ne to be lower on the X in E lines, which might indicate a swift adaptive response at the onset of selection. Additionally, the third chromosome was affected by elevated polyandry whereby its distal end harbors a region showing a strong signal of adaptive evolution especially in E lines. AU - De Castro Barbosa Rodrigues Barata, Carolina AU - Snook, Rhonda R. AU - Ritchie, Michael G. AU - Kosiol, Carolin ID - 13260 IS - 7 JF - Genome biology and evolution TI - Selection on the fly: Short-term adaptation to an altered sexual selection regime in Drosophila pseudoobscura VL - 15 ER - TY - JOUR AB - Differentiated X chromosomes are expected to have higher rates of adaptive divergence than autosomes, if new beneficial mutations are recessive (the “faster-X effect”), largely because these mutations are immediately exposed to selection in males. The evolution of X chromosomes after they stop recombining in males, but before they become hemizygous, has not been well explored theoretically. We use the diffusion approximation to infer substitution rates of beneficial and deleterious mutations under such a scenario. Our results show that selection is less efficient on diploid X loci than on autosomal and hemizygous X loci under a wide range of parameters. This “slower-X” effect is stronger for genes affecting primarily (or only) male fitness, and for sexually antagonistic genes. These unusual dynamics suggest that some of the peculiar features of X chromosomes, such as the differential accumulation of genes with sex-specific functions, may start arising earlier than previously appreciated. AU - Mrnjavac, Andrea AU - Khudiakova, Kseniia AU - Barton, Nicholas H AU - Vicoso, Beatriz ID - 12521 IS - 1 JF - Evolution Letters KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 2056-3744 TI - Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution VL - 7 ER - TY - JOUR AB - Sex chromosomes have evolved independently multiple times, but why some are conserved for more than 100 million years whereas others turnover rapidly remains an open question. Here, we examine the homology of sex chromosomes across nine orders of insects, plus the outgroup springtails. We find that the X chromosome is likely homologous across insects and springtails; the only exception is in the Lepidoptera, which has lost the X and now has a ZZ/ZW sex-chromosome system. These results suggest the ancestral insect X chromosome has persisted for more than 450 million years—the oldest known sex chromosome to date. Further, we propose that the shrinking of gene content the dipteran X chromosome has allowed for a burst of sex-chromosome turnover that is absent from other speciose insect orders. AU - Toups, Melissa A AU - Vicoso, Beatriz ID - 14604 IS - 11 JF - Evolution TI - The X chromosome of insects likely predates the origin of class Insecta VL - 77 ER - TY - GEN AB - Sex chromosomes have evolved independently multiple times, but why some are conserved for more than 100 million years whereas others turnover rapidly remains an open question. Here, we examine the homology of sex chromosomes across nine orders of insects, plus the outgroup springtails. We find that the X chromosome is likely homologous across insects and springtails; the only exception is in the Lepidoptera, which has lost the X and now has a ZZ/ZW sex chromosome system. These results suggest the ancestral insect X chromosome has persisted for more than 450 million years – the oldest known sex chromosome to date. Further, we propose that the shrinking of gene content of the Dipteran X chromosome has allowed for a burst of sex-chromosome turnover that is absent from other speciose insect orders. AU - Toups, Melissa A AU - Vicoso, Beatriz ID - 14616 TI - The X chromosome of insects likely predates the origin of Class Insecta ER - TY - GEN AB - Sex chromosomes have evolved independently multiple times, but why some are conserved for more than 100 million years whereas others turnover rapidly remains an open question. Here, we examine the homology of sex chromosomes across nine orders of insects, plus the outgroup springtails. We find that the X chromosome is likely homologous across insects and springtails; the only exception is in the Lepidoptera, which has lost the X and now has a ZZ/ZW sex chromosome system. These results suggest the ancestral insect X chromosome has persisted for more than 450 million years – the oldest known sex chromosome to date. Further, we propose that the shrinking of gene content of the Dipteran X chromosome has allowed for a burst of sex-chromosome turnover that is absent from other speciose insect orders. AU - Toups, Melissa A AU - Vicoso, Beatriz ID - 14617 TI - The X chromosome of insects likely predates the origin of Class Insecta ER - TY - THES AB - Females and males across species are subject to divergent selective pressures arising from di↵erent reproductive interests and ecological niches. This often translates into a intricate array of sex-specific natural and sexual selection on traits that have a shared genetic basis between both sexes, causing a genetic sexual conflict. The resolution of this conflict mostly relies on the evolution of sex-specific expression of the shared genes, leading to phenotypic sexual dimorphism. Such sex-specific gene expression is thought to evolve via modifications of the genetic networks ultimately linked to sex-determining transcription factors. Although much empirical and theoretical evidence supports this standard picture of the molecular basis of sexual conflict resolution, there still are a few open questions regarding the complex array of selective forces driving phenotypic di↵erentiation between the sexes, as well as the molecular mechanisms underlying sexspecific adaptation. I address some of these open questions in my PhD thesis. First, how do patterns of phenotypic sexual dimorphism vary within populations, as a response to the temporal and spatial changes in sex-specific selective forces? To tackle this question, I analyze the patterns of sex-specific phenotypic variation along three life stages and across populations spanning the whole geographical range of Rumex hastatulus, a wind-pollinated angiosperm, in the first Chapter of the thesis. Second, how do gene expression patterns lead to phenotypic dimorphism, and what are the molecular mechanisms underlying the observed transcriptomic variation? I address this question by examining the sex- and tissue-specific expression variation in newly-generated datasets of sex-specific expression in heads and gonads of Drosophila melanogaster. I additionally used two complementary approaches for the study of the genetic basis of sex di↵erences in gene expression in the second and third Chapters of the thesis. Third, how does intersex correlation, thought to be one of the main aspects constraining the ability for the two sexes to decouple, interact with the evolution of sexual dimorphism? I develop models of sex-specific stabilizing selection, mutation and drift to formalize common intuition regarding the patterns of covariation between intersex correlation and sexual dimorphism in the fourth Chapter of the thesis. Alltogether, the work described in this PhD thesis provides useful insights into the links between genetic, transcriptomic and phenotypic layers of sex-specific variation, and contributes to our general understanding of the dynamics of sexual dimorphism evolution. AU - Puixeu Sala, Gemma ID - 14058 SN - 2663-337X TI - The molecular basis of sexual dimorphism: Experimental and theoretical characterization of phenotypic, transcriptomic and genetic patterns of sex-specific adaptation ER - TY - JOUR AB - The regulatory architecture of gene expression is known to differ substantially between sexes in Drosophila, but most studies performed so far used whole-body data and only single crosses, which may have limited their scope to detect patterns that are robust across tissues and biological replicates. Here, we use allele-specific gene expression of parental and reciprocal hybrid crosses between 6 Drosophila melanogaster inbred lines to quantify cis- and trans-regulatory variation in heads and gonads of both sexes separately across 3 replicate crosses. Our results suggest that female and male heads, as well as ovaries, have a similar regulatory architecture. On the other hand, testes display more and substantially different cis-regulatory effects, suggesting that sex differences in the regulatory architecture that have been previously observed may largely derive from testis-specific effects. We also examine the difference in cis-regulatory variation of genes across different levels of sex bias in gonads and heads. Consistent with the idea that intersex correlations constrain expression and can lead to sexual antagonism, we find more cis variation in unbiased and moderately biased genes in heads. In ovaries, reduced cis variation is observed for male-biased genes, suggesting that cis variants acting on these genes in males do not lead to changes in ovary expression. Finally, we examine the dominance patterns of gene expression and find that sex- and tissue-specific patterns of inheritance as well as trans-regulatory variation are highly variable across biological crosses, although these were performed in highly controlled experimental conditions. This highlights the importance of using various genetic backgrounds to infer generalizable patterns. AU - Puixeu Sala, Gemma AU - Macon, Ariana AU - Vicoso, Beatriz ID - 14077 IS - 8 JF - G3: Genes, Genomes, Genetics KW - Genetics (clinical) KW - Genetics KW - Molecular Biology SN - 2160-1836 TI - Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster VL - 13 ER - TY - DATA AB - Datasets of the publication "Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster". AU - Puixeu Sala, Gemma ID - 12933 TI - Data from: Sex-specific estimation of cis and trans regulation of gene expression in heads and gonads of Drosophila melanogaster ER - TY - JOUR AB - Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life. AU - Lucek, Kay AU - Giménez, Mabel D. AU - Joron, Mathieu AU - Rafajlović, Marina AU - Searle, Jeremy B. AU - Walden, Nora AU - Westram, Anja M AU - Faria, Rui ID - 14742 IS - 11 JF - Cold Spring Harbor Perspectives in Biology KW - General Biochemistry KW - Genetics and Molecular Biology SN - 1943-0264 TI - The impact of chromosomal rearrangements in speciation: From micro- to macroevolution VL - 15 ER - TY - JOUR AB - Many insects carry an ancient X chromosome - the Drosophila Muller element F - that likely predates their origin. Interestingly, the X has undergone turnover in multiple fly species (Diptera) after being conserved for more than 450 MY. The long evolutionary distance between Diptera and other sequenced insect clades makes it difficult to infer what could have contributed to this sudden increase in rate of turnover. Here, we produce the first genome and transcriptome of a long overlooked sister-order to Diptera: Mecoptera. We compare the scorpionfly Panorpa cognata X-chromosome gene content, expression, and structure, to that of several dipteran species as well as more distantly-related insect orders (Orthoptera and Blattodea). We find high conservation of gene content between the mecopteran X and the dipteran Muller F element, as well as several shared biological features, such as the presence of dosage compensation and a low amount of genetic diversity, consistent with a low recombination rate. However, the two homologous X chromosomes differ strikingly in their size and number of genes they carry. Our results therefore support a common ancestry of the mecopteran and ancestral dipteran X chromosomes, and suggest that Muller element F shrank in size and gene content after the split of Diptera and Mecoptera, which may have contributed to its turnover in dipteran insects. AU - Lasne, Clementine AU - Elkrewi, Marwan N AU - Toups, Melissa A AU - Layana Franco, Lorena Alexandra AU - Macon, Ariana AU - Vicoso, Beatriz ID - 14613 IS - 12 JF - Molecular Biology and Evolution KW - Genetics KW - Molecular Biology KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0737-4038 TI - The scorpionfly (Panorpa cognata) genome highlights conserved and derived features of the peculiar dipteran X chromosome VL - 40 ER - TY - DATA AB - Many insects carry an ancient X chromosome—the Drosophila Muller element F—that likely predates their origin. Interestingly, the X has undergone turnover in multiple fly species (Diptera) after being conserved for more than 450 My. The long evolutionary distance between Diptera and other sequenced insect clades makes it difficult to infer what could have contributed to this sudden increase in rate of turnover. Here, we produce the first genome and transcriptome of scorpionflies (genus Panorpa), an insect belonging to a long overlooked sister-order to Diptera: Mecoptera. Combining our genome assembly with genomic short-read data, we obtain genome coverage and identify X-linked super-scaffolds. We further perform a gene homology analysis between the Panorpa X and a closely related Diptera species, and we assess the conservation of the Panorpa X-linked gene content with that of more distantly related insect species. We explored the structure of the Panorpa X by determining its repeat content, GC content, and nucleotide diversity. Finally, we used RNAseq data to detect the presence of dosage compensation in somatic tissues, as well as to explore gene expression tissue-specificity, and sex-bias in gene expression. We find high conservation of gene content between the mecopteran X and the dipteran Muller F element, as well as several shared biological features, such as the presence of dosage compensation and a low amount of genetic diversity, consistent with a low recombination rate. However, the 2 homologous X chromosomes differ strikingly in their size and number of genes they carry. Our results therefore support a common ancestry of the mecopteran and ancestral dipteran X chromosomes, and suggest that Muller element F shrank in size and gene content after the split of Diptera and Mecoptera, which may have contributed to its turnover in dipteran insects. AU - Lasne, Clementine AU - Elkrewi, Marwan N ID - 14614 KW - Panorpa KW - scorpionfly KW - genome KW - transcriptome TI - The scorpionfly (Panorpa cognata) genome highlights conserved and derived features of the peculiar dipteran X chromosome ER - TY - JOUR AB - The t-haplotype of mice is a classical model for autosomal transmission distortion. A largely non-recombining variant of the proximal region of chromosome 17, it is transmitted to more than 90% of the progeny of heterozygous males through the disabling of sperm carrying a standard chromosome. While extensive genetic and functional work has shed light on individual genes involved in drive, much less is known about the evolution and function of the rest of its hundreds of genes. Here, we characterize the sequence and expression of dozens of t-specific transcripts and of their chromosome 17 homologues. Many genes showed reduced expression of the t-allele, but an equal number of genes showed increased expression of their t-copy, consistent with increased activity or a newly evolved function. Genes on the t-haplotype had a significantly higher non-synonymous substitution rate than their homologues on the standard chromosome, with several genes harbouring dN/dS ratios above 1. Finally, the t-haplotype has acquired at least two genes from other chromosomes, which show high and tissue-specific expression. These results provide a first overview of the gene content of this selfish element, and support a more dynamic evolutionary scenario than expected of a large genomic region with almost no recombination. AU - Kelemen, Réka K AU - Elkrewi, Marwan N AU - Lindholm, Anna K. AU - Vicoso, Beatriz ID - 10767 IS - 1968 JF - Proceedings of the Royal Society B: Biological Sciences TI - Novel patterns of expression and recruitment of new genes on the t-haplotype, a mouse selfish chromosome VL - 289 ER - TY - JOUR AB - Conflict over reproduction between females and males exists because of anisogamy and promiscuity. Together they generate differences in fitness optima between the sexes and result in antagonistic coevolution of female and male reproductive traits. Mounting duration is likely to be a compromise between male and female interests whose outcome depends on the intensity of sexual selection. The timing of sperm transfer during mounting is critical. For example, mountings may be interrupted before sperm is transferred as a consequence of female or male choice, or they may be prolonged to function as mate guarding. In the highly promiscuous intertidal snail Littorina saxatilis, mountings vary substantially in duration, from less than a minute to more than an hour, and it has been assumed that mountings of a few minutes do not result in any sperm being transferred. Here, we examined the timing of sperm transfer, a reproductive trait that is likely affected by sexual conflict. We performed time-controlled mounting trials using L. saxatilis males and virgin females, aiming to examine indirectly when the transfer of sperm starts. We observed the relationship between mounting duration and the proportion of developing embryos out of all eggs and embryos in the brood pouch. Developing embryos were observed in similar proportions in all treatments (i.e. 1, 5 and 10 or more minutes at which mountings were artificially interrupted), suggesting that sperm transfer begins rapidly (within 1 min) in L. saxatilis and very short matings do not result in sperm shortage in the females. We discuss how the observed pattern can be influenced by predation risk, population density, and female status and receptivity. AU - Perini, Samuel AU - Butlin, Rogerk AU - Westram, Anja M AU - Johannesson, Kerstin ID - 10926 IS - 1 JF - Journal of Molluscan Studies SN - 0260-1230 TI - Very short mountings are enough for sperm transfer in Littorina saxatilis VL - 88 ER - TY - JOUR AB - Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction. AU - Freitas, Susana AU - Westram, Anja M AU - Schwander, Tanja AU - Arakelyan, Marine AU - Ilgaz, Çetin AU - Kumlutas, Yusuf AU - Harris, David James AU - Carretero, Miguel A. AU - Butlin, Roger K. ID - 11334 IS - 5 JF - Evolution SN - 0014-3820 TI - Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization VL - 76 ER - TY - JOUR AB - Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions. AU - Westram, Anja M AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger AU - Barton, Nicholas H ID - 11546 IS - 1856 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - Inversions and parallel evolution VL - 377 ER - TY - JOUR AB - Polyploidization may precipitate dramatic changes to the genome, including chromosome rearrangements, gene loss, and changes in gene expression. In dioecious plants, the sex-determining mechanism may also be disrupted by polyploidization, with the potential evolution of hermaphroditism. However, while dioecy appears to have persisted through a ploidy transition in some species, it is unknown whether the newly formed polyploid maintained its sex-determining system uninterrupted, or whether dioecy re-evolved after a period of hermaphroditism. Here, we develop a bioinformatic pipeline using RNA-sequencing data from natural populations to demonstrate that the allopolyploid plant Mercurialis canariensis directly inherited its sex-determining region from one of its diploid progenitor species, M. annua, and likely remained dioecious through the transition. The sex-determining region of M. canariensis is smaller than that of its diploid progenitor, suggesting that the non-recombining region of M. annua expanded subsequent to the polyploid origin of M. canariensis. Homeologous pairs show partial sexual subfunctionalization. We discuss the possibility that gene duplicates created by polyploidization might contribute to resolving sexual antagonism. AU - Toups, Melissa A AU - Vicoso, Beatriz AU - Pannell, John R. ID - 11703 IS - 7 JF - PLoS Genetics TI - Dioecy and chromosomal sex determination are maintained through allopolyploid speciation in the plant genus Mercurialis VL - 18 ER - TY - JOUR AB - Eurasian brine shrimp (genus Artemia) have closely related sexual and asexual lineages of parthenogenetic females, which produce rare males at low frequencies. Although they are known to have ZW chromosomes, these are not well characterized, and it is unclear whether they are shared across the clade. Furthermore, the underlying genetic architecture of the transmission of asexuality, which can occur when rare males mate with closely related sexual females, is not well understood. We produced a chromosome-level assembly for the sexual Eurasian species Artemia sinica and characterized in detail the pair of sex chromosomes of this species. We combined this new assembly with short-read genomic data for the sexual species Artemia sp. Kazakhstan and several asexual lineages of Artemia parthenogenetica, allowing us to perform an in-depth characterization of sex-chromosome evolution across the genus. We identified a small differentiated region of the ZW pair that is shared by all sexual and asexual lineages, supporting the shared ancestry of the sex chromosomes. We also inferred that recombination suppression has spread to larger sections of the chromosome independently in the American and Eurasian lineages. Finally, we took advantage of a rare male, which we backcrossed to sexual females, to explore the genetic basis of asexuality. Our results suggest that parthenogenesis is likely partly controlled by a locus on the Z chromosome, highlighting the interplay between sex determination and asexuality. AU - Elkrewi, Marwan N AU - Khauratovich, Uladzislava AU - Toups, Melissa A AU - Bett, Vincent K AU - Mrnjavac, Andrea AU - Macon, Ariana AU - Fraisse, Christelle AU - Sax, Luca AU - Huylmans, Ann K AU - Hontoria, Francisco AU - Vicoso, Beatriz ID - 12248 IS - 2 JF - Genetics KW - Genetics SN - 1943-2631 TI - ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp VL - 222 ER - TY - DATA AB - Eurasian brine shrimp (genus Artemia) have closely related sexual and asexual lineages of parthenogenetic females, which produce rare males at low frequencies. Although they are known to have ZW chromosomes, these are not well characterized, and it is unclear whether they are shared across the clade. Furthermore, the underlying genetic architecture of the transmission of asexuality, which can occur when rare males mate with closely related sexual females, is not well understood. We produced a chromosome-level assembly for the sexual Eurasian species A. sinica and characterized in detail the pair of sex chromosomes of this species. We combined this new assembly with short-read genomic data for the sexual species A. sp. Kazakhstan and several asexual lineages of A. parthenogenetica, allowing us to perform an in-depth characterization of sex-chromosome evolution across the genus. We identified a small differentiated region of the ZW pair that is shared by all sexual and asexual lineages, supporting the shared ancestry of the sex chromosomes. We also inferred that recombination suppression has spread to larger sections of the chromosome independently in the American and Eurasian lineages. Finally, we took advantage of a rare male, which we backcrossed to sexual females, to explore the genetic basis of asexuality. Our results suggest that parthenogenesis is likely partly controlled by a locus on the Z chromosome, highlighting the interplay between sex determination and asexuality. AU - Elkrewi, Marwan N ID - 11653 TI - Data from Elkrewi, Khauratovich, Toups et al. 2022, "ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp" ER - TY - JOUR AB - The Mytilus complex of marine mussel species forms a mosaic of hybrid zones, found across temperate regions of the globe. This allows us to study ‘replicated’ instances of secondary contact between closely related species. Previous work on this complex has shown that local introgression is both widespread and highly heterogeneous, and has identified SNPs that are outliers of differentiation between lineages. Here, we developed an ancestry‐informative panel of such SNPs. We then compared their frequencies in newly sampled populations, including samples from within the hybrid zones, and parental populations at different distances from the contact. Results show that close to the hybrid zones, some outlier loci are near to fixation for the heterospecific allele, suggesting enhanced local introgression, or the local sweep of a shared ancestral allele. Conversely, genomic cline analyses, treating local parental populations as the reference, reveal a globally high concordance among loci, albeit with a few signals of asymmetric introgression. Enhanced local introgression at specific loci is consistent with the early transfer of adaptive variants after contact, possibly including asymmetric bi‐stable variants (Dobzhansky‐Muller incompatibilities), or haplotypes loaded with fewer deleterious mutations. Having escaped one barrier, however, these variants can be trapped or delayed at the next barrier, confining the introgression locally. These results shed light on the decay of species barriers during phases of contact. AU - Simon, Alexis AU - Fraisse, Christelle AU - El Ayari, Tahani AU - Liautard‐Haag, Cathy AU - Strelkov, Petr AU - Welch, John J AU - Bierne, Nicolas ID - 8708 IS - 1 JF - Journal of Evolutionary Biology SN - 1010061X TI - How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels VL - 34 ER - TY - JOUR AB - About eight million animal species are estimated to live on Earth, and all except those belonging to one subphylum are invertebrates. Invertebrates are incredibly diverse in their morphologies, life histories, and in the range of the ecological niches that they occupy. A great variety of modes of reproduction and sex determination systems is also observed among them, and their mosaic-distribution across the phylogeny shows that transitions between them occur frequently and rapidly. Genetic conflict in its various forms is a long-standing theory to explain what drives those evolutionary transitions. Here, we review (1) the different modes of reproduction among invertebrate species, highlighting sexual reproduction as the probable ancestral state; (2) the paradoxical diversity of sex determination systems; (3) the different types of genetic conflicts that could drive the evolution of such different systems. AU - Picard, Marion A L AU - Vicoso, Beatriz AU - Bertrand, Stéphanie AU - Escriva, Hector ID - 9908 IS - 8 JF - Genes TI - Diversity of modes of reproduction and sex determination systems in invertebrates, and the putative contribution of genetic conflict VL - 12 ER - TY - JOUR AB - Schistosomes, the human parasites responsible for snail fever, are female-heterogametic. Different parts of their ZW sex chromosomes have stopped recombining in distinct lineages, creating “evolutionary strata” of various ages. Although the Z-chromosome is well characterized at the genomic and molecular level, the W-chromosome has remained largely unstudied from an evolutionary perspective, as only a few W-linked genes have been detected outside of the model species Schistosoma mansoni. Here, we characterize the gene content and evolution of the W-chromosomes of S. mansoni and of the divergent species S. japonicum. We use a combined RNA/DNA k-mer based pipeline to assemble around 100 candidate W-specific transcripts in each of the species. About half of them map to known protein coding genes, the majority homologous to S. mansoni Z-linked genes. We perform an extended analysis of the evolutionary strata present in the two species (including characterizing a previously undetected young stratum in S. japonicum) to infer patterns of sequence and expression evolution of W-linked genes at different time points after recombination was lost. W-linked genes show evidence of degeneration, including high rates of protein evolution and reduced expression. Most are found in young lineage-specific strata, with only a few high expression ancestral W-genes remaining, consistent with the progressive erosion of nonrecombining regions. Among these, the splicing factor u2af2 stands out as a promising candidate for primary sex determination, opening new avenues for understanding the molecular basis of the reproductive biology of this group. AU - Elkrewi, Marwan N AU - Moldovan, Mikhail A. AU - Picard, Marion A L AU - Vicoso, Beatriz ID - 10167 JF - Molecular Biology and Evolution KW - sex chromosomes KW - evolutionary strata KW - W-linked gene KW - sex determining gene KW - schistosome parasites SN - 0737-4038 TI - Schistosome W-Linked genes inform temporal dynamics of sex chromosome evolution and suggest candidate for sex determination ER - TY - JOUR AB - Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence. It allows for the identification of genomic regions underlying barriers to gene flow. It also provides insights into spatial patterns of allele frequency change, informing about the interplay between environmental factors, dispersal and selection. However, when only a single hybrid zone is analysed, it is difficult to separate patterns generated by selection from those resulting from chance. Therefore, it is beneficial to look for repeatable patterns across replicate hybrid zones in the same system. We applied this approach to the marine snail Littorina saxatilis, which contains two ecotypes, adapted to wave-exposed rocks vs. high-predation boulder fields. The existence of numerous hybrid zones between ecotypes offered the opportunity to test for the repeatability of genomic architectures and spatial patterns of divergence. We sampled and phenotyped snails from seven replicate hybrid zones on the Swedish west coast and genotyped them for thousands of single nucleotide polymorphisms. Shell shape and size showed parallel clines across all zones. Many genomic regions showing steep clines and/or high differentiation were shared among hybrid zones, consistent with a common evolutionary history and extensive gene flow between zones, and supporting the importance of these regions for divergence. In particular, we found that several large putative inversions contribute to divergence in all locations. Additionally, we found evidence for consistent displacement of clines from the boulder–rock transition. Our results demonstrate patterns of spatial variation that would not be accessible without continuous spatial sampling, a large genomic data set and replicate hybrid zones. AU - Westram, Anja M AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger ID - 10838 IS - 15 JF - Molecular Ecology KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0962-1083 TI - Using replicate hybrid zones to understand the genomic basis of adaptive divergence VL - 30 ER - TY - JOUR AB - While sexual reproduction is widespread among many taxa, asexual lineages have repeatedly evolved from sexual ancestors. Despite extensive research on the evolution of sex, it is still unclear whether this switch represents a major transition requiring major molecular reorganization, and how convergent the changes involved are. In this study, we investigated the phylogenetic relationship and patterns of gene expression of sexual and asexual lineages of Eurasian Artemia brine shrimp, to assess how gene expression patterns are affected by the transition to asexuality. We find only a few genes that are consistently associated with the evolution of asexuality, suggesting that this shift may not require an extensive overhauling of the meiotic machinery. While genes with sex-biased expression have high rates of expression divergence within Eurasian Artemia, neither female- nor male-biased genes appear to show unusual evolutionary patterns after sexuality is lost, contrary to theoretical expectations. AU - Huylmans, Ann K AU - Macon, Ariana AU - Hontoria, Francisco AU - Vicoso, Beatriz ID - 10166 IS - 1959 JF - Proceedings of the Royal Society B: Biological Sciences KW - asexual reproduction KW - parthenogenesis KW - sex-biased genes KW - sexual conflict KW - automixis KW - crustaceans SN - 0962-8452 TI - Transitions to asexuality and evolution of gene expression in Artemia brine shrimp VL - 288 ER - TY - DATA AU - Vicoso, Beatriz ID - 9949 TI - Data from Hyulmans et al 2021, "Transitions to asexuality and evolution of gene expression in Artemia brine shrimp" ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9799 TI - Simulation code for Fig S1 from the distribution of epistasis on simple fitness landscapes ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9798 TI - Simulation code for Fig S2 from the distribution of epistasis on simple fitness landscapes ER - TY - JOUR AB - Sewall Wright developed FST for describing population differentiation and it has since been extended to many novel applications, including the detection of homomorphic sex chromosomes. However, there has been confusion regarding the expected estimate of FST for a fixed difference between the X‐ and Y‐chromosome when comparing males and females. Here, we attempt to resolve this confusion by contrasting two common FST estimators and explain why they yield different estimates when applied to the case of sex chromosomes. We show that this difference is true for many allele frequencies, but the situation characterized by fixed differences between the X‐ and Y‐chromosome is among the most extreme. To avoid additional confusion, we recommend that all authors using FST clearly state which estimator of FST their work uses. AU - Gammerdinger, William J AU - Toups, Melissa A AU - Vicoso, Beatriz ID - 8099 IS - 6 JF - Molecular Ecology Resources SN - 1755-098X TI - Disagreement in FST estimators: A case study from sex chromosomes VL - 20 ER - TY - JOUR AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA (small nucleolar RNA). Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 6467 IS - 4 JF - Biology Letters SN - 17449561 TI - The distribution of epistasis on simple fitness landscapes VL - 15 ER - TY - JOUR AB - New genes are a major source of novelties, and a disproportionate amount of them are known to show testis expression in later phases of male gametogenesis in different groups such as mammals and plants. Here, we propose that this enhanced expression is a consequence of haploid selection during the latter stages of male gametogenesis. Because emerging adaptive mutations will be fixed faster if their phenotypes are expressed by haploid rather than diploid genotypes, new genes with advantageous functions arising during this unique stage of development have a better chance to become fixed. To test this hypothesis, expression levels of genes of differing evolutionary age were examined at various stages of Drosophila spermatogenesis. We found, consistent with a model based on haploid selection, that new Drosophila genes are both expressed in later haploid phases of spermatogenesis and harbor a significant enrichment of adaptive mutations. Additionally, the observed overexpression of new genes in the latter phases of spermatogenesis was limited to the autosomes. Because all male cells exhibit hemizygous expression for X-linked genes (and therefore effectively haploid), there is no expectation that selection acting on late spermatogenesis will have a different effect on X-linked genes in comparison to initial diploid phases. Together, our proposed hypothesis and the analyzed data suggest that natural selection in haploid cells elucidates several aspects of the origin of new genes by explaining the general prevalence of their testis expression, and a parsimonious solution for new alleles to avoid being lost by genetic drift or pseudogenization. AU - Raices, Julia AU - Otto, Paulo AU - Vibranovski, Maria ID - 6658 IS - 7 JF - Genome Research TI - Haploid selection drives new gene male germline expression VL - 29 ER - TY - JOUR AB - Sexual dimorphism in morphology, physiology or life history traits is common in dioecious plants at reproductive maturity, but it is typically inconspicuous or absent in juveniles. Although plants of different sexes probably begin to diverge in gene expression both before their reproduction commences and before dimorphism becomes readily apparent, to our knowledge transcriptome-wide differential gene expression has yet to be demonstrated for any angiosperm species. AU - Cossard, Guillaume AU - Toups, Melissa A AU - Pannell, John ID - 6710 IS - 7 JF - Annals of botany SN - 0305-7364 TI - Sexual dimorphism and rapid turnover in gene expression in pre-reproductive seedlings of a dioecious herb VL - 123 ER - TY - JOUR AB - Differentiated sex chromosomes are accompanied by a difference in gene dose between X/Z-specific and autosomal genes. At the transcriptomic level, these sex-linked genes can lead to expression imbalance, or gene dosage can be compensated by epigenetic mechanisms and results into expression level equalization. Schistosoma mansoni has been previously described as a ZW species (i.e., female heterogamety, in opposition to XY male heterogametic species) with a partial dosage compensation, but underlying mechanisms are still unexplored. Here, we combine transcriptomic (RNA-Seq) and epigenetic data (ChIP-Seq against H3K4me3, H3K27me3,andH4K20me1histonemarks) in free larval cercariae and intravertebrate parasitic stages. For the first time, we describe differences in dosage compensation status in ZW females, depending on the parasitic status: free cercariae display global dosage compensation, whereas intravertebrate stages show a partial dosage compensation. We also highlight regional differences of gene expression along the Z chromosome in cercariae, but not in the intravertebrate stages. Finally, we feature a consistent permissive chromatin landscape of the Z chromosome in both sexes and stages. We argue that dosage compensation in schistosomes is characterized by chromatin remodeling mechanisms in the Z-specific region. AU - Picard, Marion A L AU - Vicoso, Beatriz AU - Roquis, David AU - Bulla, Ingo AU - Augusto, Ronaldo C. AU - Arancibia, Nathalie AU - Grunau, Christoph AU - Boissier, Jérôme AU - Cosseau, Céline ID - 6755 IS - 7 JF - Genome biology and evolution TI - Dosage compensation throughout the Schistosoma mansoni lifecycle: Specific chromatin landscape of the Z chromosome VL - 11 ER - TY - JOUR AB - To determine the visual sensitivities of an organism of interest, quantitative reverse transcription–polymerase chain reaction (qRT–PCR) is often used to quantify expression of the light‐sensitive opsins in the retina. While qRT–PCR is an affordable, high‐throughput method for measuring expression, it comes with inherent normalization issues that affect the interpretation of results, especially as opsin expression can vary greatly based on developmental stage, light environment or diurnal cycles. We tested for diurnal cycles of opsin expression over a period of 24 hr at 1‐hr increments and examined how normalization affects a data set with fluctuating expression levels using qRT–PCR and transcriptome data from the retinae of the cichlid Pelmatolapia mariae. We compared five methods of normalizing opsin expression relative to (a) the average of three stably expressed housekeeping genes (Ube2z, EF1‐α and β‐actin), (b) total RNA concentration, (c) GNAT2, (the cone‐specific subunit of transducin), (d) total opsin expression and (e) only opsins expressed in the same cone type. Normalizing by proportion of cone type produced the least variation and would be best for removing time‐of‐day variation. In contrast, normalizing by housekeeping genes produced the highest daily variation in expression and demonstrated that the peak of cone opsin expression was in the late afternoon. A weighted correlation network analysis showed that the expression of different cone opsins follows a very similar daily cycle. With the knowledge of how these normalization methods affect opsin expression data, we make recommendations for designing sampling approaches and quantification methods based upon the scientific question being examined. AU - Yourick, Miranda R. AU - Sandkam, Benjamin A. AU - Gammerdinger, William J AU - Escobar-Camacho, Daniel AU - Nandamuri, Sri Pratima AU - Clark, Frances E. AU - Joyce, Brendan AU - Conte, Matthew A. AU - Kocher, Thomas D. AU - Carleton, Karen L. ID - 6821 IS - 6 JF - Molecular Ecology Resources TI - Diurnal variation in opsin expression and common housekeeping genes necessitates comprehensive normalization methods for quantitative real-time PCR analyses VL - 19 ER - TY - JOUR AB - * Understanding the mechanisms causing phenotypic differences between females and males has long fascinated evolutionary biologists. An extensive literature exists on animal sexual dimorphism but less information is known about sex differences in plants, particularly the extent of geographical variation in sexual dimorphism and its life‐cycle dynamics. * Here, we investigated patterns of genetically based sexual dimorphism in vegetative and reproductive traits of a wind‐pollinated dioecious plant, Rumex hastatulus, across three life‐cycle stages using open‐pollinated families from 30 populations spanning the geographic range and chromosomal variation (XY and XY1Y2) of the species. * The direction and degree of sexual dimorphism was highly variable among populations and life‐cycle stages. Sex‐specific differences in reproductive function explained a significant amount of temporal change in sexual dimorphism. For several traits, geographical variation in sexual dimorphism was associated with bioclimatic parameters, likely due to the differential responses of the sexes to climate. We found no systematic differences in sexual dimorphism between chromosome races. * Sex‐specific trait differences in dioecious plants largely result from a balance between sexual and natural selection on resource allocation. Our results indicate that abiotic factors associated with geographical context also play a role in modifying sexual dimorphism during the plant life‐cycle. AU - Puixeu Sala, Gemma AU - Pickup, Melinda AU - Field, David AU - Barrett, Spencer C.H. ID - 6831 IS - 3 JF - New Phytologist TI - Variation in sexual dimorphism in a wind-pollinated plant: The influence of geographical context and life-cycle dynamics VL - 224 ER - TY - GEN AB - Understanding the mechanisms causing phenotypic differences between females and males has long fascinated evolutionary biologists. An extensive literature exists on animal sexual dimorphism but less is known about sex differences in plants, particularly the extent of geographical variation in sexual dimorphism and its life-cycle dynamics. Here, we investigate patterns of genetically-based sexual dimorphism in vegetative and reproductive traits of a wind-pollinated dioecious plant, Rumex hastatulus, across three life-cycle stages using open-pollinated families from 30 populations spanning the geographic range and chromosomal variation (XY and XY1Y2) of the species. The direction and degree of sexual dimorphism was highly variable among populations and life-cycle stages. Sex-specific differences in reproductive function explained a significant amount of temporal change in sexual dimorphism. For several traits, geographical variation in sexual dimorphism was associated with bioclimatic parameters, likely due to the differential responses of the sexes to climate. We found no systematic differences in sexual dimorphism between chromosome races. Sex-specific trait differences in dioecious plants largely result from a balance between sexual and natural selection on resource allocation. Our results indicate that abiotic factors associated with geographical context also play a role in modifying sexual dimorphism during the plant life cycle. AU - Puixeu Sala, Gemma AU - Pickup, Melinda AU - Field, David AU - Barrett, Spencer C.H. ID - 9803 TI - Data from: Variation in sexual dimorphism in a wind-pollinated plant: the influence of geographical context and life-cycle dynamics ER - TY - JOUR AB - Malaria, a disease caused by parasites of the Plasmodium genus, begins when Plasmodium-infected mosquitoes inject malaria sporozoites while searching for blood. Sporozoites migrate from the skin via blood to the liver, infect hepatocytes, and form liver stages which in mice 48 h later escape into blood and cause clinical malaria. Vaccine-induced activated or memory CD8 T cells are capable of locating and eliminating all liver stages in 48 h, thus preventing the blood-stage disease. However, the rules of how CD8 T cells are able to locate all liver stages within a relatively short time period remains poorly understood. We recently reported formation of clusters consisting of variable numbers of activated CD8 T cells around Plasmodium yoelii (Py)-infected hepatocytes. Using a combination of experimental data and mathematical models we now provide additional insights into mechanisms of formation of these clusters. First, we show that a model in which cluster formation is driven exclusively by T-cell-extrinsic factors, such as variability in “attractiveness” of different liver stages, cannot explain distribution of cluster sizes in different experimental conditions. In contrast, the model in which cluster formation is driven by the positive feedback loop (i.e., larger clusters attract more CD8 T cells) can accurately explain the available data. Second, while both Py-specific CD8 T cells and T cells of irrelevant specificity (non-specific CD8 T cells) are attracted to the clusters, we found no evidence that non-specific CD8 T cells play a role in cluster formation. Third and finally, mathematical modeling suggested that formation of clusters occurs rapidly, within few hours after adoptive transfer of CD8 T cells, thus illustrating high efficiency of CD8 T cells in locating their targets in complex peripheral organs, such as the liver. Taken together, our analysis provides novel insights into and attempts to discriminate between alternative mechanisms driving the formation of clusters of antigen-specific CD8 T cells in the liver. AU - Kelemen, Réka K AU - Rajakaruna, H AU - Cockburn, IA AU - Ganusov, VV ID - 6983 JF - Frontiers in Immunology SN - 1664-3224 TI - Clustering of activated CD8 T cells around Malaria-infected hepatocytes is rapid and is driven by antigen-specific cells VL - 10 ER - TY - JOUR AB - Prevailing models of sex-chromosome evolution were largely inspired by the stable and highly differentiated XY pairs of model organisms, such as those of mammals and flies. Recent work has uncovered an incredible diversity of sex-determining systems, bringing some of the assumptions of these traditional models into question. One particular question that has arisen is what drives some sex chromosomes to be maintained over millions of years and differentiate fully, while others are replaced by new sex-determining chromosomes before differentiation has occurred. Here, I review recent data on the variability of sex-determining genes and sex chromosomes in different non-model vertebrates and invertebrates, and discuss some theoretical models that have been put forward to account for this diversity. AU - Vicoso, Beatriz ID - 7146 IS - 12 JF - Nature Ecology & Evolution SN - 2397-334X TI - Molecular and evolutionary dynamics of animal sex-chromosome turnover VL - 3 ER - TY - JOUR AB - X and Y chromosomes can diverge when rearrangements block recombination between them. Here we present the first genomic view of a reciprocal translocation that causes two physically unconnected pairs of chromosomes to be coinherited as sex chromosomes. In a population of the common frog (Rana temporaria), both pairs of X and Y chromosomes show extensive sequence differentiation, but not degeneration of the Y chromosomes. A new method based on gene trees shows both chromosomes are sex‐linked. Furthermore, the gene trees from the two Y chromosomes have identical topologies, showing they have been coinherited since the reciprocal translocation occurred. Reciprocal translocations can thus reshape sex linkage on a much greater scale compared with inversions, the type of rearrangement that is much better known in sex chromosome evolution, and they can greatly amplify the power of sexually antagonistic selection to drive genomic rearrangement. Two more populations show evidence of other rearrangements, suggesting that this species has unprecedented structural polymorphism in its sex chromosomes. AU - Toups, Melissa A AU - Rodrigues, Nicolas AU - Perrin, Nicolas AU - Kirkpatrick, Mark ID - 7421 IS - 8 JF - Molecular Ecology SN - 0962-1083 TI - A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog VL - 28 ER - TY - JOUR AB - Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination. AU - Veltsos, Paris AU - Ridout, Kate E. AU - Toups, Melissa A AU - González-Martínez, Santiago C. AU - Muyle, Aline AU - Emery, Olivier AU - Rastas, Pasi AU - Hudzieczek, Vojtech AU - Hobza, Roman AU - Vyskot, Boris AU - Marais, Gabriel A. B. AU - Filatov, Dmitry A. AU - Pannell, John R. ID - 7400 IS - 3 JF - Genetics SN - 0016-6731 TI - Early sex-chromosome evolution in the diploid dioecious plant Mercurialis annua VL - 212 ER - TY - JOUR AB - We read with great interest the recent work in PNAS by Bergero et al. (1) describing differences in male and female recombination patterns on the guppy (Poecilia reticulata) sex chromosome. We fully agree that recombination in males is largely confined to the ends of the sex chromosome. Bergero et al. interpret these results to suggest that our previous findings of population-level variation in the degree of sex chromosome differentiation in this species (2) are incorrect. However, we suggest that their results are entirely consistent with our previous report, and that their interpretation presents a false controversy. AU - Wright, Alison E. AU - Darolti, Iulia AU - Bloch, Natasha I. AU - Oostra, Vicencio AU - Sandkam, Benjamin A. AU - Buechel, Séverine D. AU - Kolm, Niclas AU - Breden, Felix AU - Vicoso, Beatriz AU - Mank, Judith E. ID - 6621 IS - 26 JF - Proceedings of the National Academy of Sciences of the United States of America TI - On the power to detect rare recombination events VL - 116 ER - TY - JOUR AB - Males and females of Artemia franciscana, a crustacean commonly used in the aquarium trade, are highly dimorphic. Sex is determined by a pair of ZW chromosomes, but the nature and extent of differentiation of these chromosomes is unknown. Here, we characterize the Z chromosome by detecting genomic regions that show lower genomic coverage in female than in male samples, and regions that harbor an excess of female-specific SNPs. We detect many Z-specific genes, which no longer have homologs on the W, but also Z-linked genes that appear to have diverged very recently from their existing W-linked homolog. We assess patterns of male and female expression in two tissues with extensive morphological dimorphism, gonads, and heads. In agreement with their morphology, sex-biased expression is common in both tissues. Interestingly, the Z chromosome is not enriched for sex-biased genes, and seems to in fact have a mechanism of dosage compensation that leads to equal expression in males and in females. Both of these patterns are contrary to most ZW systems studied so far, making A. franciscana an excellent model for investigating the interplay between the evolution of sexual dimorphism and dosage compensation, as well as Z chromosome evolution in general. AU - Huylmans, Ann K AU - Toups, Melissa A AU - Macon, Ariana AU - Gammerdinger, William J AU - Vicoso, Beatriz ID - 6418 IS - 4 JF - Genome biology and evolution TI - Sex-biased gene expression and dosage compensation on the Artemia franciscana Z-chromosome VL - 11 ER - TY - DATA AU - Vicoso, Beatriz ID - 6060 TI - Supplementary data for "Sex-biased gene expression and dosage compensation on the Artemia franciscana Z-chromosome" (Huylman, Toups et al., 2019). ER - TY - JOUR AB - Pleiotropy is the well-established idea that a single mutation affects multiple phenotypes. If a mutation has opposite effects on fitness when expressed in different contexts, then genetic conflict arises. Pleiotropic conflict is expected to reduce the efficacy of selection by limiting the fixation of beneficial mutations through adaptation, and the removal of deleterious mutations through purifying selection. Although this has been widely discussed, in particular in the context of a putative “gender load,” it has yet to be systematically quantified. In this work, we empirically estimate to which extent different pleiotropic regimes impede the efficacy of selection in Drosophila melanogaster. We use whole-genome polymorphism data from a single African population and divergence data from D. simulans to estimate the fraction of adaptive fixations (α), the rate of adaptation (ωA), and the direction of selection (DoS). After controlling for confounding covariates, we find that the different pleiotropic regimes have a relatively small, but significant, effect on selection efficacy. Specifically, our results suggest that pleiotropic sexual antagonism may restrict the efficacy of selection, but that this conflict can be resolved by limiting the expression of genes to the sex where they are beneficial. Intermediate levels of pleiotropy across tissues and life stages can also lead to maladaptation in D. melanogaster, due to inefficient purifying selection combined with low frequency of mutations that confer a selective advantage. Thus, our study highlights the need to consider the efficacy of selection in the context of antagonistic pleiotropy, and of genetic conflict in general. AU - Fraisse, Christelle AU - Puixeu Sala, Gemma AU - Vicoso, Beatriz ID - 6089 IS - 3 JF - Molecular biology and evolution SN - 0737-4038 TI - Pleiotropy modulates the efficacy of selection in drosophila melanogaster VL - 36 ER - TY - JOUR AB - The German cockroach, Blattella germanica, is a worldwide pest that infests buildings, including homes, restaurants, and hospitals, often living in unsanitary conditions. As a disease vector and producer of allergens, this species has major health and economic impacts on humans. Factors contributing to the success of the German cockroach include its resistance to a broad range of insecticides, immunity to many pathogens, and its ability, as an extreme generalist omnivore, to survive on most food sources. The recently published genome shows that B. germanica has an exceptionally high number of protein coding genes. In this study, we investigate the functions of the 93 significantly expanded gene families with the aim to better understand the success of B. germanica as a major pest despite such inhospitable conditions. We find major expansions in gene families with functions related to the detoxification of insecticides and allelochemicals, defense against pathogens, digestion, sensory perception, and gene regulation. These expansions might have allowed B. germanica to develop multiple resistance mechanisms to insecticides and pathogens, and enabled a broad, flexible diet, thus explaining its success in unsanitary conditions and under recurrent chemical control. The findings and resources presented here provide insights for better understanding molecular mechanisms that will facilitate more effective cockroach control. AU - Harrison, Mark AU - Arning, Nicolas AU - Kremer, Lucas AU - Ylla, Guillem AU - Belles, Xavier AU - Bornberg Bauer, Erich AU - Huylmans, Ann K AU - Jongepier, Evelien AU - Puilachs, Maria AU - Richards, Stephen AU - Schal, Coby ID - 190 JF - Journal of Experimental Zoology Part B: Molecular and Developmental Evolution TI - Expansions of key protein families in the German cockroach highlight the molecular basis of its remarkable success as a global indoor pest VL - 330 ER - TY - JOUR AB - Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity. AU - Harrison, Mark AU - Jongepier, Evelien AU - Robertson, Hugh AU - Arning, Nicolas AU - Bitard Feildel, Tristan AU - Chao, Hsu AU - Childers, Christopher AU - Dinh, Huyen AU - Doddapaneni, Harshavardhan AU - Dugan, Shannon AU - Gowin, Johannes AU - Greiner, Carolin AU - Han, Yi AU - Hu, Haofu AU - Hughes, Daniel AU - Huylmans, Ann K AU - Kemena, Karsten AU - Kremer, Lukas AU - Lee, Sandra AU - López Ezquerra, Alberto AU - Mallet, Ludovic AU - Monroy Kuhn, Jose AU - Moser, Annabell AU - Murali, Shwetha AU - Muzny, Donna AU - Otani, Saria AU - Piulachs, Maria AU - Poelchau, Monica AU - Qu, Jiaxin AU - Schaub, Florentine AU - Wada Katsumata, Ayako AU - Worley, Kim AU - Xie, Qiaolin AU - Ylla, Guillem AU - Poulsen, Michael AU - Gibbs, Richard AU - Schal, Coby AU - Richards, Stephen AU - Belles, Xavier AU - Korb, Judith AU - Bornberg Bauer, Erich ID - 448 IS - 3 JF - Nature Ecology and Evolution TI - Hemimetabolous genomes reveal molecular basis of termite eusociality VL - 2 ER - TY - GEN AB - Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity. AU - Harrison, Mark C. AU - Jongepier, Evelien AU - Robertson, Hugh M. AU - Arning, Nicolas AU - Bitard-Feildel, Tristan AU - Chao, Hsu AU - Childers, Christopher P. AU - Dinh, Huyen AU - Doddapaneni, Harshavardhan AU - Dugan, Shannon AU - Gowin, Johannes AU - Greiner, Carolin AU - Han, Yi AU - Hu, Haofu AU - Hughes, Daniel S. T. AU - Huylmans, Ann K AU - Kemena, Carsten AU - Kremer, Lukas P. M. AU - Lee, Sandra L. AU - Lopez-Ezquerra, Alberto AU - Mallet, Ludovic AU - Monroy-Kuhn, Jose M. AU - Moser, Annabell AU - Murali, Shwetha C. AU - Muzny, Donna M. AU - Otani, Saria AU - Piulachs, Maria-Dolors AU - Poelchau, Monica AU - Qu, Jiaxin AU - Schaub, Florentine AU - Wada-Katsumata, Ayako AU - Worley, Kim C. AU - Xie, Qiaolin AU - Ylla, Guillem AU - Poulsen, Michael AU - Gibbs, Richard A. AU - Schal, Coby AU - Richards, Stephen AU - Belles, Xavier AU - Korb, Judith AU - Bornberg-Bauer, Erich ID - 9841 TI - Data from: Hemimetabolous genomes reveal molecular basis of termite eusociality ER - TY - JOUR AB - Sex-biased genes are central to the study of sexual selection, sexual antagonism, and sex chromosome evolution. We describe a comprehensive de novo assembled transcriptome in the common frog Rana temporaria based on five developmental stages and three adult tissues from both sexes, obtained from a population with karyotypically homomorphic but genetically differentiated sex chromosomes. This allows the study of sex-biased gene expression throughout development, and its effect on the rate of gene evolution while accounting for pleiotropic expression, which is known to negatively correlate with the evolutionary rate. Overall, sex-biased genes had little overlap among developmental stages and adult tissues. Late developmental stages and gonad tissues had the highest numbers of stage-or tissue-specific genes. We find that pleiotropic gene expression is a better predictor than sex bias for the evolutionary rate of genes, though it often interacts with sex bias. Although genetically differentiated, the sex chromosomes were not enriched in sex-biased genes, possibly due to a very recent arrest of XY recombination. These results extend our understanding of the developmental dynamics, tissue specificity, and genomic localization of sex-biased genes. AU - Ma, Wen AU - Veltsos, Paris AU - Toups, Melissa A AU - Rodrigues, Nicolas AU - Sermier, Roberto AU - Jeffries, Daniel AU - Perrin, Nicolas ID - 199 IS - 6 JF - Genes TI - Tissue specificity and dynamics of sex biased gene expression in a common frog population with differentiated, yet homomorphic, sex chromosomes VL - 9 ER - TY - JOUR AB - African cichlids display a remarkable assortment of jaw morphologies, pigmentation patterns, and mating behaviors. In addition to this previously documented diversity, recent studies have documented a rich diversity of sex chromosomes within these fishes. Here we review the known sex-determination network within vertebrates, and the extraordinary number of sex chromosomes systems segregating in African cichlids. We also propose a model for understanding the unusual number of sex chromosome systems within this clade. AU - Gammerdinger, William J AU - Kocher, Thomas ID - 63 IS - 10 JF - Genes TI - Unusual diversity of sex chromosomes in African cichlid fishes VL - 9 ER -