RESUMEN
Antagonistic relationships such as host-virus interactions potentially lead to rapid evolution and specificity in interactions. The Orsay virus is so far the only horizontal virus naturally infecting the nematode C. elegans. In contrast, several related RNA viruses infect its congener C. briggsae, including Santeuil (SANTV) and Le Blanc (LEBV) viruses. Here we focus on the host's intraspecific variation in sensitivity to these two intestinal viruses. Many temperate-origin C. briggsae strains, including JU1264 and JU1498, are sensitive to both, while many tropical strains, such as AF16, are resistant to both. Interestingly, some C. briggsae strains exhibit a specific resistance, such as the HK104 strain, specifically resistant to LEBV. The viral sensitivity pattern matches the strains' geographic and genomic relationships. The heavily infected strains mount a seemingly normal small RNA response that is insufficient to suppress viral infection, while the resistant strains show no small RNA response, suggesting an early block in viral entry or replication. We use a genetic approach from the host side to map genomic regions participating in viral resistance polymorphisms. Using Advanced Intercrossed Recombinant Inbred Lines (RILs) between virus-resistant AF16 and SANTV-sensitive HK104, we detect Quantitative Trait Loci (QTLs) on chromosomes IV and III. Building RILs between virus-sensitive JU1498 and LEBV-resistant HK104 followed by bulk segregant analysis, we identify a chromosome II QTL. In both cases, further introgressions of the regions confirmed the QTLs. This diversity provides an avenue for studying virus entry, replication, and exit mechanisms, as well as host-virus specificity and the host response to a specific virus infection.
Asunto(s)
Caenorhabditis , Animales , Caenorhabditis/genética , Caenorhabditis/virología , Virus ARN/genética , Especificidad del Huésped , Infecciones por Virus ARN/virologíaRESUMEN
Although evolution is driven by changes in how regulatory pathways control development, we know little about the molecular details underlying these transitions. The TRA-2 domain that mediates contact with TRA-1 is conserved in Caenorhabditis. By comparing the interaction of these proteins in two species, we identified a striking change in how sexual development is controlled. Identical mutations in this domain promote oogenesis in Caenorhabditis elegans but promote spermatogenesis in Caenorhabditis briggsae. Furthermore, the effects of these mutations involve the male-promoting gene fem-3 in C. elegans but are independent of fem-3 in C. briggsae. Finally, reciprocal mutations in these genes show that C. briggsae TRA-2 binds TRA-1 to prevent expression of spermatogenesis regulators. By contrast, in C. elegans TRA-1 sequesters TRA-2 in the germ line, allowing FEM-3 to initiate spermatogenesis. Thus, we propose that the flow of information within the sex determination pathway has switched directions during evolution. This result has important implications for how evolutionary change can occur.
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Proteínas de Caenorhabditis elegans , Caenorhabditis elegans , Procesos de Determinación del Sexo , Espermatogénesis , Animales , Proteínas de Caenorhabditis elegans/genética , Proteínas de Caenorhabditis elegans/metabolismo , Caenorhabditis elegans/genética , Masculino , Espermatogénesis/genética , Femenino , Caenorhabditis/genética , Evolución Biológica , Proteínas de Unión al ARN/genética , Proteínas de Unión al ARN/metabolismo , Mutación , Oogénesis/genética , Evolución Molecular , Autofecundación , Proteínas de Unión al ADN , Factores de TranscripciónRESUMEN
Gene duplication is an important substrate for the evolution of new gene functions, but the impacts of gene duplicates on their own activities and on the developmental networks in which they act are poorly understood. Here, we use a natural experiment of lin-12/Notch gene duplication within the nematode genus Caenorhabditis, combined with characterization of loss- and gain-of-function mutations, to uncover functional distinctions between the duplicate genes in 1 species (Caenorhabditis briggsae) and their single-copy ortholog in Caenorhabditis elegans. First, using improved genomic sequence and gene model characterization, we confirm that the C. briggsae genome includes 2 complete lin-12 genes, whereas most other genes encoding proteins that participate in the LIN-12 signaling pathway retain a one-to-one orthology with C. elegans. We use CRISPR-mediated genome editing to introduce alleles predicted to cause gain-of-function (gf) or loss-of-function (lf) into each C. briggsae gene and find that the gf mutations uncover functional distinctions not apparent from the lf alleles. Specifically, Cbr-lin-12.1(gf), but not Cbr-lin-12.2(gf), causes developmental defects similar to those observed in Cel-lin-12(gf). In contrast to Cel-lin-12(gf), however, the Cbr-lin-12.1(gf) alleles do not cause dominant phenotypes as compared to the wild type, and the mutant phenotype is observed only when 2 gf alleles are present. Our results demonstrate that gene duplicates can exhibit differential capacities to compensate for each other and to interfere with normal development, and uncover coincident gene duplication and evolution of developmental sensitivity to LIN-12/Notch activity.
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Proteínas de Caenorhabditis elegans , Evolución Molecular , Duplicación de Gen , Receptores Notch , Animales , Proteínas de Caenorhabditis elegans/genética , Proteínas de Caenorhabditis elegans/metabolismo , Receptores Notch/genética , Receptores Notch/metabolismo , Caenorhabditis elegans/genética , Caenorhabditis/genética , Transducción de Señal/genéticaRESUMEN
Body size is a fundamental trait that drives multiple evolutionary and ecological patterns. Caenorhabditis inopinata is a fig-associated nematode that is exceptionally large relative to other members of the genus, including Caenorhabditis elegans. We previously showed that C. inopinata is large primarily due to postembryonic cell size expansion that occurs during the larval-to-adult transition. Here, we describe gene expression patterns in C. elegans and C. inopinata throughout this developmental period to understand the transcriptional basis of body size change. We performed RNA-seq in both species across the L3, L4, and adult stages. Most genes are differentially expressed across all developmental stages, consistent with C. inopinata's divergent ecology and morphology. We also used a model comparison approach to identify orthologues with divergent dynamics across this developmental period between the 2 species. This included genes connected to neurons, behavior, stress response, developmental timing, and small RNA/chromatin regulation. Multiple hypodermal collagens were also observed to harbor divergent developmental dynamics across this period, and genes important for molting and body morphology were also detected. Genes associated with transforming growth factor ß signaling revealed idiosyncratic and unexpected transcriptional patterns given their role in body size regulation in C. elegans. This widespread transcriptional divergence between these species is unexpected and maybe a signature of the ecological and morphological divergence of C. inopinata. Alternatively, transcriptional turnover may be the rule in the Caenorhabditis genus, indicative of widespread developmental system drift among species. This work lays the foundation for future functional genetic studies interrogating the bases of body size evolution in this group.
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Tamaño Corporal , Regulación del Desarrollo de la Expresión Génica , Animales , Tamaño Corporal/genética , Caenorhabditis elegans/genética , Caenorhabditis elegans/crecimiento & desarrollo , Evolución Biológica , Caenorhabditis/genética , Perfilación de la Expresión Génica , Transcriptoma , Evolución Molecular , Factor de Crecimiento Transformador beta/metabolismo , Factor de Crecimiento Transformador beta/genéticaRESUMEN
Transposable elements are DNA sequences capable of moving within genomes and significantly influence genomic evolution. The nematode Caenorhabditis inopinata exhibits a much higher transposable element copy number than its sister species, Caenorhabditis elegans. In this study, we identified a novel autonomous transposable element belonging to the hAT superfamily from a spontaneous transposable element-insertion mutant in C. inopinata and named this transposon Ci-hAT1. Further bioinformatic analyses uncovered 3 additional autonomous hAT elements-Ci-hAT2, Ci-hAT3, and Ci-hAT4-along with over 1,000 copies of 2 nonautonomous miniature inverted-repeat transposable elements, mCi-hAT1 and mCi-hAT4, likely derived from Ci-hAT1 and Ci-hAT4 through internal deletion. We tracked at least 3 sequential transpositions of Ci-hAT1 over several years. However, the transposition rates of the other 3 autonomous hAT elements were lower, suggesting varying activity levels. Notably, the distribution patterns of the 2 miniature inverted-repeat transposable element families differed significantly: mCi-hAT1 was primarily located in the chromosome arms, a pattern observed in the transposable elements of other Caenorhabditis species, whereas mCi-hAT4 was more evenly distributed across chromosomes. Additionally, interspecific transcriptome analysis indicated that C. inopinata genes with upstream or intronic these miniature inverted-repeat transposable element insertions tend to be more highly expressed than their orthologous genes in C. elegans. These findings highlight the significant role of de-silenced transposable elements in driving the evolution of genomes and transcriptomes, leading to species-specific genetic diversity.
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Caenorhabditis , Elementos Transponibles de ADN , Animales , Elementos Transponibles de ADN/genética , Caenorhabditis/genética , Genoma de los Helmintos , Evolución Molecular , Regulación de la Expresión Génica , Caenorhabditis elegans/genéticaRESUMEN
Genomic imprinting-the non-equivalence of maternal and paternal genomes-is a critical process that has evolved independently in many plant and mammalian species1,2. According to kinship theory, imprinting is the inevitable consequence of conflictive selective forces acting on differentially expressed parental alleles3,4. Yet, how these epigenetic differences evolve in the first place is poorly understood3,5,6. Here we report the identification and molecular dissection of a parent-of-origin effect on gene expression that might help to clarify this fundamental question. Toxin-antidote elements (TAs) are selfish elements that spread in populations by poisoning non-carrier individuals7-9. In reciprocal crosses between two Caenorhabditis tropicalis wild isolates, we found that the slow-1/grow-1 TA is specifically inactive when paternally inherited. This parent-of-origin effect stems from transcriptional repression of the slow-1 toxin by the PIWI-interacting RNA (piRNA) host defence pathway. The repression requires PIWI Argonaute and SET-32 histone methyltransferase activities and is transgenerationally inherited via small RNAs. Remarkably, when slow-1/grow-1 is maternally inherited, slow-1 repression is halted by a translation-independent role of its maternal mRNA. That is, slow-1 transcripts loaded into eggs-but not SLOW-1 protein-are necessary and sufficient to counteract piRNA-mediated repression. Our findings show that parent-of-origin effects can evolve by co-option of the piRNA pathway and hinder the spread of selfish genes that require sex for their propagation.
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Caenorhabditis , Impresión Genómica , ARN de Interacción con Piwi , Secuencias Repetitivas de Ácidos Nucleicos , Animales , Femenino , Masculino , Alelos , Proteínas Argonautas/genética , Proteínas Argonautas/metabolismo , Caenorhabditis/genética , Caenorhabditis/metabolismo , Cruzamientos Genéticos , Padre , Genoma/genética , Impresión Genómica/genética , Organismos Hermafroditas/genética , Histona Metiltransferasas/genética , Histona Metiltransferasas/metabolismo , Madres , Oocitos/metabolismo , ARN de Interacción con Piwi/genética , Biosíntesis de Proteínas , Secuencias Repetitivas de Ácidos Nucleicos/genética , ARN Mensajero/genética , Toxinas Biológicas/genética , Transcripción GenéticaRESUMEN
The evolution of reproductive mode is expected to have profound impacts on the genetic composition of populations. At the same time, ecological interactions can generate close associations among species, which can in turn generate a high degree of overlap in their spatial distributions. Caenorhabditis elegans is a hermaphroditic nematode that has enabled extensive advances in developmental genetics. Caenorhabditis inopinata, the sister species of C. elegans, is a gonochoristic nematode that thrives in figs and obligately disperses on fig wasps. Here, we describe patterns of genomic diversity in C. inopinata. We performed RAD-seq on individual worms isolated from the field across three Okinawan island populations. C. inopinata is about five times more diverse than C. elegans. Additionally, C. inopinata harbors greater differences in diversity among functional genomic regions (such as between genic and intergenic sequences) than C. elegans. Conversely, C. elegans harbors greater differences in diversity between high-recombining chromosome arms and low-recombining chromosome centers than C. inopinata. FST is low among island population pairs, and clear population structure could not be easily detected among islands, suggesting frequent migration of wasps between islands. These patterns of population differentiation appear comparable with those previously reported in its fig wasp vector. These results confirm many theoretical population genetic predictions regarding the evolution of reproductive mode and suggest C. inopinata population dynamics may be driven by wasp dispersal. This work sets the stage for future evolutionary genomic studies aimed at understanding the evolution of sex as well as the evolution of ecological interactions.
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Caenorhabditis , Ficus , Animales , Caenorhabditis elegans/genética , Ficus/genética , Caenorhabditis/genética , Genética de Población , GenómicaRESUMEN
Male/hermaphrodite species have arisen multiple times from a male/female ancestral state in nematodes, providing a model to study behavioral adaptations to different reproductive strategies. Here, we examined the mating behaviors of male/female (gonochoristic) Caenorhabditis species in comparison with male/hermaphrodite (androdiecious) close relatives. We find that females from two species in the Elegans group chemotax to volatile odor from males, but hermaphrodites do not. Females, but not hermaphrodites, also display known mating-receptive behaviors such as sedation when male reproductive structures contact the vulva. Focusing on the male/female species C. nigoni, we show that female chemotaxis to males is limited to adult females approaching adult or near-adult males and relies upon the AWA neuron-specific transcription factor ODR-7, as does male chemotaxis to female odor as previously shown in C. elegans. However, female receptivity during mating contact is odr-7 independent. All C. nigoni female behaviors are suppressed by mating and all are absent in young hermaphrodites from the sister species C. briggsae. However, latent receptivity during mating contact can be uncovered in mutant or aged C. briggsae hermaphrodites that lack self-sperm. These results reveal two mechanistically distinct components of the shift from female to hermaphrodite behavior: the loss of female-specific odr-7-dependent chemotaxis and a sperm-dependent state of reduced receptivity to mating contact. Hermaphrodites from a second androdioecious species, C. tropicalis, recover all female behaviors upon aging, including chemotaxis to males. Regaining mating receptivity after sperm depletion could maximize hermaphrodite fitness across their lifespan.
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Caenorhabditis elegans , Caenorhabditis , Animales , Femenino , Masculino , Semen , Reproducción , EspermatozoidesRESUMEN
Glycoproteins result from post-translational modification of proteins by glycans attached to certain side chains, with possible heterogeneity due to different structures being possible at the same glycosylation site.In contrast to the mammalian systems, analysis of invertebrate glycans presents a challenge in analysis as there exist unfamiliar epitopes and a high degree of structural and isomeric variation between different species-Caenorhabditis elegans is no exception. Simple screening using lectins and antibodies can yield hints regarding which glycan epitopes are present in wild-type and mutant strains, but detailed analysis is necessary for determining more exact glycomic information. Here, our analytical approach is to analyze N- and O-glycans involving "off-line" RP-HPLC MALDI-TOF MS/MS. Enrichment and labeling steps facilitate the analysis of single structures and provide isomeric separation. Thereby, the "simple" worm expresses over 200 N-glycan structures varying depending on culture conditions or the genetic background.
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Caenorhabditis , Espectrometría de Masas en Tándem , Animales , Glicosilación , Glicoproteínas/química , Caenorhabditis elegans/genética , Polisacáridos/química , Epítopos , Espectrometría de Masa por Láser de Matriz Asistida de Ionización Desorción , MamíferosRESUMEN
The Caenorhabditis Intervention Testing Program (CITP) is an NIH-funded research consortium of investigators who conduct analyses at three independent sites to identify chemical interventions that reproducibly promote health and lifespan in a robust manner. The founding principle of the CITP is that compounds with positive effects across a genetically diverse panel of Caenorhabditis species and strains are likely engaging conserved biochemical pathways to exert their effects. As such, interventions that are broadly efficacious might be considered prominent compounds for translation for pre-clinical research and human clinical applications. Here, we report results generated using a recently streamlined pipeline approach for the evaluation of the effects of chemical compounds on lifespan and health. We studied five compounds previously shown to extend C. elegans lifespan or thought to promote mammalian health: 17α-estradiol, acarbose, green tea extract, nordihydroguaiaretic acid, and rapamycin. We found that green tea extract and nordihydroguaiaretic acid extend Caenorhabditis lifespan in a species-specific manner. Additionally, these two antioxidants conferred assay-specific effects in some studies-for example, decreasing survival for certain genetic backgrounds in manual survival assays in contrast with extended lifespan as assayed using automated C. elegans Lifespan Machines. We also observed that GTE and NDGA impact on older adult mobility capacity is dependent on genetic background, and that GTE reduces oxidative stress resistance in some Caenorhabditis strains. Overall, our analysis of the five compounds supports the general idea that genetic background and assay type can influence lifespan and health effects of compounds, and underscores that lifespan and health can be uncoupled by chemical interventions.
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Antioxidantes , Caenorhabditis , Animales , Humanos , Anciano , Antioxidantes/farmacología , Masoprocol/farmacología , Masoprocol/metabolismo , Caenorhabditis elegans/genética , Longevidad , Promoción de la Salud , Extractos Vegetales/farmacología , Té/metabolismo , MamíferosRESUMEN
Studies of model organisms have provided important insights into how natural genetic differences shape trait variation. These discoveries are driven by the growing availability of genomes and the expansive experimental toolkits afforded to researchers using these species. For example, Caenorhabditis elegans is increasingly being used to identify and measure the effects of natural genetic variants on traits using quantitative genetics. Since 2016, the C. elegans Natural Diversity Resource (CeNDR) has facilitated many of these studies by providing an archive of wild strains, genome-wide sequence and variant data for each strain, and a genome-wide association (GWA) mapping portal for the C. elegans community. Here, we present an updated platform, the Caenorhabditis Natural Diversity Resource (CaeNDR), that enables quantitative genetics and genomics studies across the three Caenorhabditis species: C. elegans, C. briggsae and C. tropicalis. The CaeNDR platform hosts several databases that are continually updated by the addition of new strains, whole-genome sequence data and annotated variants. Additionally, CaeNDR provides new interactive tools to explore natural variation and enable GWA mappings. All CaeNDR data and tools are accessible through a freely available web portal located at caendr.org.
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Caenorhabditis , Bases de Datos Genéticas , Animales , Caenorhabditis/clasificación , Caenorhabditis/genética , Caenorhabditis elegans/genética , Genoma , Estudio de Asociación del Genoma Completo , GenómicaRESUMEN
The heterochronic genes of Caenorhabditis elegans comprise the best-studied pathway controlling the timing of tissue and organ formation in an animal. To begin to understand the evolution of this pathway and the significance of the relationships among its components, we characterized 11 Caenorhabditis briggsae orthologs of C. elegans heterochronic genes. Using CRISPR/Cas9, we made a variety of alleles and found that several mutant phenotypes differ in significant ways from those of C. elegans. Although most mutant orthologs displayed defects in developmental timing, their phenotypes could differ in which stages were affected, the penetrance and expressivity of the phenotypes, or by having additional pleiotropies that were not obviously connected to developmental timing. However, when examining pairwise epistasis and synergistic relationships, we found those paralleled the known relationships between their C. elegans orthologs, suggesting that the arrangements of these genes in functional modules are conserved, but the modules' relationships to each other and/or to their targets has drifted since the time of the species' last common ancestor. Furthermore, our investigation has revealed a relationship between this pathway to other aspects of the animal's growth and development, including gonad development, which is relevant to both species.
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Proteínas de Caenorhabditis elegans , Caenorhabditis , Animales , Caenorhabditis elegans/genética , Caenorhabditis/genética , Proteínas de Caenorhabditis elegans/genéticaRESUMEN
Behavioral plasticity helps humans and animals to achieve their goals by adapting their behaviors to different environments.1,2 Although behavioral plasticity is ubiquitous, many innate species-specific behaviors, such as mating, are often assumed to be stereotyped and unaffected by plasticity or learning, especially in invertebrates. Here, we describe a novel case of behavioral plasticity in the nematode C. elegans. Under standard lab conditions (agar plates with bacterial food), the male performs parallel mating,3,4,5 a largely two-dimensional behavioral strategy where his body and tail remain flat on the surface and slide alongside the partner's body from initial contact to copulation. But when placed in liquid media, the male performs spiral mating, a distinctly three-dimensional behavioral strategy where he winds around the partner's body in a helical embrace. The performance of spiral mating does not require a long-term change in growing conditions, but it does improve with experience. This experience-dependent improvement appears to involve a critical period-a time window around the L4 larval stage to the early adult stage-which coincides with the development of most male-specific neurons. We tested several wild isolates of C. elegans and other Caenorhabditis species and found that most were capable of parallel mating on surfaces and spiral mating in liquids. We suggest that two- and three-dimensional mating strategies in Caenorhabditis are plastic, conditionally expressed phenotypes conserved across the genus, which can be genetically "fixed" in some species.
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Proteínas de Caenorhabditis elegans , Caenorhabditis , Animales , Humanos , Masculino , Caenorhabditis elegans/genética , Proteínas de Caenorhabditis elegans/genética , Reproducción , Caenorhabditis/genética , NeuronasRESUMEN
BACKGROUND: Homology-based recombination (HR) is the cornerstone of genetic mapping. However, a lack of sufficient sequence homology or the presence of a genomic rearrangement prevents HR through crossing, which inhibits genetic mapping in relevant genomic regions. This is particularly true in species hybrids whose genomic sequences are highly divergent along with various genome arrangements, making the mapping of genetic loci, such as hybrid incompatibility (HI) loci, through crossing impractical. We previously mapped tens of HI loci between two nematodes, Caenorhabditis briggsae and C. nigoni, through the repeated backcrossing of GFP-linked C. briggsae fragments into C. nigoni. However, the median introgression size was over 7 Mb, indicating apparent HR suppression and preventing the subsequent cloning of the causative gene underlying a given HI phenotype. Therefore, a robust method that permits recombination independent of sequence homology is desperately desired. RESULTS: Here, we report a method of highly efficient targeted recombination (TR) induced by CRISPR/Cas9 with dual guide RNAs (gRNAs), which circumvents the HR suppression in hybrids between the two species. We demonstrated that a single gRNA was able to induce efficient TR between highly homologous sequences only in the F1 hybrids but not in the hybrids that carry a GFP-linked C. briggsae fragment in an otherwise C. nigoni background. We achieved highly efficient TR, regardless of sequence homology or genetic background, when dual gRNAs were used that each specifically targeted one parental chromosome. We further showed that dual gRNAs were able to induce efficient TR within genomic regions that had undergone inversion, in which HR-based recombination was expected to be suppressed, supporting the idea that dual-gRNA-induced TR can be achieved through nonhomology-based end joining between two parental chromosomes. CONCLUSIONS: Recombination suppression can be circumvented through CRISPR/Cas9 with dual gRNAs, regardless of sequence homology or the genetic background of the species hybrid. This method is expected to be applicable to other situations in which recombination is suppressed in interspecies or intrapopulation hybrids.
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Caenorhabditis , Animales , Caenorhabditis/genética , Sistemas CRISPR-Cas , Mapeo Cromosómico , Genoma , Recombinación GenéticaRESUMEN
BACKGROUND: The nematode Caenorhabditis briggsae has been used as a model in comparative genomics studies with Caenorhabditis elegans because of their striking morphological and behavioral similarities. However, the potential of C. briggsae for comparative studies is limited by the quality of its genome resources. The genome resources for the C. briggsae laboratory strain AF16 have not been developed to the same extent as C. elegans. The recent publication of a new chromosome-level reference genome for QX1410, a C. briggsae wild strain closely related to AF16, has provided the first step to bridge the gap between C. elegans and C. briggsae genome resources. Currently, the QX1410 gene models consist of software-derived gene predictions that contain numerous errors in their structure and coding sequences. In this study, a team of researchers manually inspected over 21,000 gene models and underlying transcriptomic data to repair software-derived errors. RESULTS: We designed a detailed workflow to train a team of nine students to manually curate gene models using RNA read alignments. We manually inspected the gene models, proposed corrections to the coding sequences of over 8,000 genes, and modeled thousands of putative isoforms and untranslated regions. We exploited the conservation of protein sequence length between C. briggsae and C. elegans to quantify the improvement in protein-coding gene model quality and showed that manual curation led to substantial improvements in the protein sequence length accuracy of QX1410 genes. Additionally, collinear alignment analysis between the QX1410 and AF16 genomes revealed over 1,800 genes affected by spurious duplications and inversions in the AF16 genome that are now resolved in the QX1410 genome. CONCLUSIONS: Community-based, manual curation using transcriptome data is an effective approach to improve the quality of software-derived protein-coding genes. The detailed protocols provided in this work can be useful for future large-scale manual curation projects in other species. Our manual curation efforts have brought the QX1410 gene models to a comparable level of quality as the extensively curated AF16 gene models. The improved genome resources for C. briggsae provide reliable tools for the study of Caenorhabditis biology and other related nematodes.
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Caenorhabditis , Humanos , Animales , Caenorhabditis/genética , Caenorhabditis elegans/genética , Exones , Secuencia de Aminoácidos , Perfilación de la Expresión GénicaRESUMEN
In social groups, infection risk is not distributed evenly across individuals. Individual behaviour is a key source of variation in infection risk, yet its effects are difficult to separate from other factors (e.g., age). Here, we combine epidemiological experiments with chemical, transcriptomic, and automated behavioural analyses in clonal ant colonies, where behavioural individuality emerges among identical workers. We find that: (1) Caenorhabditis-related nematodes parasitise ant heads and affect their survival and physiology, (2) differences in infection emerge from behavioural variation alone, and reflect spatially-organised division of labour, (3) infections affect colony social organisation by causing infected workers to stay in the nest. By disproportionately infecting some workers and shifting their spatial distribution, infections reduce division of labour and increase spatial overlap between hosts, which should facilitate parasite transmission. Thus, division of labour, a defining feature of societies, not only shapes infection risk and distribution but is also modulated by parasites.
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Hormigas , Caenorhabditis , Trabajo de Parto , Humanos , Animales , Embarazo , Femenino , Perfilación de la Expresión Génica , Grupo SocialRESUMEN
Caenorhabditis nematodes form an excellent model for studying how the mode of reproduction affects genetic diversity, as some species reproduce via outcrossing whereas others can self-fertilize. Currently, chromosome-level patterns of diversity and recombination are only available for self-reproducing Caenorhabditis, making the generality of genomic patterns across the genus unclear given the profound potential influence of reproductive mode. Here we present a whole-genome diversity landscape, coupled with a new genetic map, for the outcrossing nematode C. remanei. We demonstrate that the genomic distribution of recombination in C. remanei, like the model nematode C. elegans, shows high recombination rates on chromosome arms and low rates toward the central regions. Patterns of genetic variation across the genome are also similar between these species, but differ dramatically in scale, being tenfold greater for C. remanei. Historical reconstructions of variation in effective population size over the past million generations echo this difference in polymorphism. Evolutionary simulations demonstrate how selection, recombination, mutation, and selfing shape variation along the genome, and that multiple drivers can produce patterns similar to those observed in natural populations. The results illustrate how genome organization and selection play a crucial role in shaping the genomic pattern of diversity whereas demographic processes scale the level of diversity across the genome as a whole.
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Caenorhabditis , Animales , Caenorhabditis/genética , Caenorhabditis elegans/genética , Polimorfismo Genético , Evolución Biológica , Genómica , Variación GenéticaRESUMEN
Aided by new technologies, the upsurgence of research into mitochondrial genome biology during the past 15 years suggests that we have misunderstood, and perhaps dramatically underestimated, the ongoing biological and evolutionary significance of our long-time symbiotic partner. While we have begun to scratch the surface of several topics, many questions regarding the nature of mutation and selection in the mitochondrial genome, and the nature of its relationship to the nuclear genome, remain unanswered. Although best known for their contributions to studies of developmental and aging biology, Caenorhabditis nematodes are increasingly recognized as excellent model systems to advance understanding in these areas. We review recent discoveries with relevance to mitonuclear coevolution and conflict and offer several fertile areas for future work.
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Caenorhabditis , Animales , Caenorhabditis/genética , Codependencia Psicológica , Evolución Biológica , GenomaRESUMEN
Horizontal gene transfer, the movement of genetic material between species, has been reported across all major eukaryotic lineages. However, the underlying mechanisms of transfer and their impact on genome evolution are still poorly understood. While studying the evolutionary origin of a selfish element in the nematode Caenorhabditis briggsae, we discovered that Mavericks, ancient virus-like transposons related to giant viruses and virophages, are one of the long-sought vectors of horizontal gene transfer. We found that Mavericks gained a novel herpesvirus-like fusogen in nematodes, leading to the widespread exchange of cargo genes between extremely divergent species, bypassing sexual and genetic barriers spanning hundreds of millions of years. Our results show how the union between viruses and transposons causes horizontal gene transfer and ultimately genetic incompatibilities in natural populations.
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Evolución Biológica , Caenorhabditis , Elementos Transponibles de ADN , Transferencia de Gen Horizontal , Virus , Animales , Caenorhabditis/genética , Virus/genética , Vectores GenéticosRESUMEN
The world's astounding biodiversity results from speciation, the process of formation of distinct species. Hybrids between species often have reduced fitness due to negative epistatic interactions between divergent genetic factors, as each lineage accumulated substitutions independently in their evolutionary history. Such negative genetic interactions can manifest as gene misexpression due to divergence in gene regulatory controls from mutations in cis-regulatory elements and trans-acting factors. Gene misexpression due to differences in regulatory controls can ultimately contribute to incompatibility within hybrids through developmental defects such as sterility and inviability. We sought to quantify the contributions of regulatory divergence to postzygotic reproductive isolation using sterile interspecies hybrids of two Caenorhabditis nematodes: Caenorhabditis briggsae and Caenorhabditis nigoni. We analyzed previous transcriptome profiles for two introgression lines with distinct homozygous X-linked fragments from C. briggsae in a C. nigoni genomic background that confers male sterility, owing to defects in spermatogenesis (Li R, et al. 2016. Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-chromosome introgression. Genome Res. 26:1219-1232). Our analysis identified hundreds of genes that show distinct classes of nonadditive expression inheritance and regulatory divergence. We find that these nonoverlapping introgressions affect many of the same genes in the same way and demonstrate that the preponderance of transgressive gene expression is due to regulatory divergence involving compensatory and joint effects of cis- and trans-acting factors. The similar transcriptomic responses to nonoverlapping genetic perturbations of the X-chromosome implicate multiway incompatibilities as an important feature contributing to hybrid male sterility in this system.