Biology subjects

Robinson-Rechavi, M.

Publications and source records attributed to Robinson-Rechavi, M..

10 recordsLinked to original sources

bioRxiv2018

Genomic signatures accompanying the dietary shift to phytophagy in polyphagous beetles

BackgroundThe diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. Indeed the largest beetle suborder, Polyphaga, mostly includes plant-eaters among its ~315,000 species. In particular, plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing.\n\nResultsTo address this, we explored the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representing the two most species-rich beetle suborders. We contrasted the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We found gene repertoire evolution to be more dynamic, with significantly more adaptive lineage-specific expansions, in the more speciose Polyphaga. Testing the specific hypothesis of adaptation to plant-feeding, we identified families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There was especially strong support for the selection hypothesis on large gene families for glutathione S-transferase and carboxylesterase detoxification enzymes.\n\nConclusionsOur explicit modeling of the evolution of gene repertoires across 18 species identifies adaptive lineage-specific gene family expansions that accompany the dietary shift towards plants in beetles. These genomic signatures support the popular hypothesis of a key role for interactions with plant chemical defenses, and for plant-feeding in general, in driving beetle diversification.

evolutionary biology↗

bioRxiv2018

Genes involved in the convergent evolution of asexuality in stick insects

Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. While the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In particular, it is completely unknown whether the repeated evolution of asexual phenotypes involves similar molecular changes, as previous studies have focused on changes occurring in single lineages. Here we investigate the extent of convergent gene expression changes across five independent transitions to asexuality in stick insects. We compared gene expression of asexual females to females of close sexual relatives in whole-bodies, reproductive tracts, and legs. We identified a striking amount of convergent gene expression change (up to 8% of genes), greatly exceeding that expected by chance. Convergent changes were also tissue-specific, and most likely driven by selection for functional changes. Genes showing convergent changes in the reproductive tract were associated with meiotic spindle formation and centrosome organization. These genes are particularly interesting as they can influence the production of unreduced eggs, a key barrier to asexual reproduction. Changes in legs and whole-bodies were likely involved in female sexual trait decay, with enrichment in terms such as sperm-storage and pigmentation. By identifying changes occurring across multiple independent transitions to asexuality, our results provide a rare insight into the molecular basis of asexual phenotypes and suggest that the evolutionary path to asexuality is highly constrained, requiring repeated changes to the same key genes.

evolutionary biology↗

bioRxiv2018

Cross-species functional modules link proteostasis to human normal aging

The evolutionarily conserved nature of the few well-known anti-aging interventions that affect lifespan, such as caloric restriction, suggests that aging-related research in model organisms is directly relevant to human aging. Since human lifespan is a complex trait, a systems-level approach will contribute to a more comprehensive understanding of the underlying aging landscape. Here, we integrate evolutionary and functional information of normal aging across human and model organisms at three levels: gene-level, process-level, and network-level. We identify evolutionarily conserved modules of normal aging across diverse taxa, and importantly, we show that proteostasis involvement is conserved in healthy aging. Additionally, we find that mechanisms related to protein quality control network are enriched in 22 age-related genome-wide association studies (GWAS) and are associated to caloric restriction. These results demonstrate that a systems-level approach, combined with evolutionary conservation, allows the detection of candidate aging genes and pathways relevant to human normal aging.\n\nHighlightsO_LINormal aging is evolutionarily conserved at the module level.\nC_LIO_LICore pathways in healthy aging are related to mechanisms of protein quality network\nC_LIO_LIThe evolutionarily conserved pathways of healthy aging react to caloric restriction.\nC_LIO_LIOur integrative approach identifies evolutionarily conserved functional modules and showed enrichment in several age-related GWAS studies.\nC_LI

systems biology↗

bioRxiv2017

Modeling codon rate variation improves protein positive selection inference and detects nucleotide selection

There are numerous sources of variation in the rate of synonymous substitutions inside genes, such as direct selection on the nucleotide sequence, or mutation rate variation. Yet scans for positive selection rely on codon models which incorporate an assumption of effectively neutral synonymous substitution rate, constant between sites of each gene. Here we perform a large-scale comparison of approaches which incorporate codon substitution rate variation and propose our own simple yet effective modification of existing models. We find strong effects of substitution rate variation on positive selection inference. More than 70% of the genes detected by the classical branch-site model are presumably false positives caused by the incorrect assumption of uniform synonymous substitution rate. We propose a new model which is strongly favored by the data while remaining computationally tractable. With the new model we can capture signatures of nucleotide level selection acting on translation initiation and on splicing sites within the coding region. Finally, we show that rate variation is highest in the highly recombining regions, and we propose that recombination and mutation rate variation, such as high CpG mutation rate, are the two main sources of nucleotide rate variation. While we detect fewer genes under positive selection in Drosophila than without rate variation, the genes which we detect contain a stronger signal of adaptation of dynein, which could be associated with Wolbachia infection. We provide software to perform positive selection analysis using the new model.

bioinformatics↗

bioRxiv2017

Developmental constraints on genome evolution in four bilaterian model species

Developmental constraints on genome evolution have been suggested to follow either an early conservation model or an \"hourglass\" model. Both models agree that late development strongly diverges between species, but debate on which developmental period is the most conserved. Here, based on a modified \"Transcriptome Age Index\" approach, i.e. weighting trait measures by expression level, we analyzed the constraints acting on three evolutionary traits of protein coding genes (strength of purifying selection on protein sequences, phyletic age, and duplicability) in four species: nematode worm Caenorhabditis elegans, fly Drosophila melanogaster, zebrafish Danio rerio, and mouse Mus musculus. In general, we found that both models can be supported by different genomic properties. Sequence evolution follows an hourglass model, but the evolution of phyletic age and of duplicability follow an early conservation model. Further analyses indicate that stronger purifying selection on sequences in the middle development are driven by temporal pleiotropy of these genes. In addition, we report evidence that expression in late development is enriched with retrogenes, which usually lack efficient regulatory elements. This implies that expression in late development could facilitate transcription of new genes, and provide opportunities for acquisition of function. Finally, in C. elegans, we suggest that dosage imbalance could be one of the main factors that cause depleted expression of high duplicability genes in early development.

evolutionary biology↗

bioRxiv2017

Adaptive evolution of proteins expressed in late and post-embryonic development in animals

A driving hypothesis of Evo-Devo is that animal morphological diversity is shaped both by adaptation and by developmental constraints. Here we have tested Darwins \"selection opportunity\" hypothesis, according to which high evolutionary divergence in late development is due to strong positive selection. We contrasted it to a \"developmental constraint\" hypothesis, according to which late development is under relaxed negative selection. Indeed, the highest divergence between species, both at the morphological and molecular levels, is observed late in embryogenesis and post-embryonically. To distinguish between adaptation and relaxation hypotheses, we investigated the evidence of positive selection on protein-coding genes in relation to their expression over development, in fly Drosohila melanogaster, zebrafish Danio rerio, and mouse Mus musculus. First, we found that genes specifically expressed in late development have stronger signals of positive selection. Second, over the full transcriptome, genes with evidence for positive selection trend to be expressed in late development. Finally, genes involved in pathways with cumulative evidence of positive selection have higher expression in late development. Overall, there is a consistent signal that positive selection mainly affects genes and pathways expressed in late embryonic development and in adult. Our results imply that the evolution of embryogenesis is mostly conservative, with most adaptive evolution affecting some stages of post-embryonic gene expression, and thus post-embryonic phenotypes. This is consistent with the diversity of environmental challenges to which juveniles and adults are exposed.

evolutionary biology↗

bioRxiv2017

Low Rate of Somatic Mutations in a Long-Lived Oak Tree

Because plants do not possess a proper germline, deleterious somatic mutations can be passed to gametes and a large number of cell divisions separating zygote from gamete formation in long-lived plants may lead to many mutations. We sequenced the genome of two terminal branches of a 234-year-old oak tree and found few fixed somatic single-nucleotide variants (SNVs), whose sequential appearance in the tree could be traced along nested sectors of younger branches. Our data suggest that stem cells of shoot meristems are robustly protected from accumulation of mutations in trees.

plant biology↗

bioRxiv2017

Sex-Specific Changes In Gene Expression And Delayed Sex Differentiation In Response To Estrogen Pollution In Grayling (Salmonidae)

The synthetic 17-ethinylestradiol (EE2) is an estrogenic compound of oral contraceptives and therefore a common pollutant that has been suspected to affect the demography of river-dwelling salmonids. We study a population of European grayling (Thymallus thymallus) that suffers from sex ratio distortions. Here we test how ecologically relevant concentrations of EE2 affect sex-specific gene expression around early stages of sex differentiation. We collected gametes from F1s of wild spawners, used them for in vitro fertilizations, and raised the resulting embryos singly under experimentally controlled conditions. Embryos were either exposed to 1ng/L EE2 or sham-exposed. RNA was collected from samples taken 10 days before hatching, at the day of hatching, and towards the end of the yolk-sac stage, to study gene expression and relate it to genetic sex (sdY genotype). We found that EE2 affects gene expression of a very large number of genes especially at the day of hatching. The effects of EE2 on gene expression is strongly sex-specific. At the day of hatching, EE2 affected about twice as many genes in females than in males, and towards the end of the yolk-sac larval stage, EE2 effects were nearly exclusively observed in females. Among the many effects was, for example, a surprising EE2-induced molecular masculinization in the females heads. Histological examination of gonadal development of EE2-treated or sham-exposed juveniles during the first 4.5 months after hatching revealed a delaying effect of EE2 on sex differentiation. Because grayling sex determination goes through an all-male stage (a rare case of undifferentiated gonochorism), the rate of EE2-induced sex reversal could not be unequivocally determined during the observational period. However, two EE2-treated genetic males had ovarian tissues at the end of the study. We conclude that common levels of EE2 pollution affect grayling from very early stages on by interfering with male and female gene expression around the onset of sex differentiation, by delaying sex differentiation, and by feminizing some males.\n\nAuthor contributionMRR and CW initiated the project. OS, DM, LW, LMC, and CW sampled the adult fish, did the experimental in vitro fertilizations, and prepared the embryos for experimental rearing in the laboratory. All further manipulations on the embryos and the larvae were done by OS, DM, LW, and LMC. The RNA-seq data were analyzed by OS, JR, and MRR, the histological analyses were done by DM, supervised by SK, the molecular genetic sexing was performed by OS and DM, and EV supervised the EE2 analytics. OS and CW performed the remaining statistical analyses and wrote the first version of the manuscript that was then critically revised by all other authors.

ecology↗

bioRxiv2017

Sex Differentiation In Grayling (Salmonidae) Goes Through An All-Male Stage And Is Delayed In Genetic Males Who Instead Grow Faster

Fish can be threatened by distorted sex ratios that arise during sex differentiation. It is therefore important to understand sex determination and differentiation, especially in river-dwelling fish that are often exposed to environmental factors that may interfere with sex differentiation. However, sex differentiation is not sufficiently understood in keystone taxa such as the Thymallinae, one of the three salmonid subfamilies. Here we study a wild grayling (Thymallus thymallus) population that suffers from distorted sex ratios. We found sex determination in the wild and in captivity to be genetic and linked to the sdY locus. We therefore studied sex-specific gene expression in embryos and early larvae that were bred and raised under different experimental conditions, and we studied gonadal morphology in five monthly samples taken after hatching. Significant sex-specific changes in gene expression (affecting about 25,000 genes) started around hatching. Gonads were still undifferentiated three weeks after hatching, but about half of the fish showed immature testes around seven weeks after hatching. Over the next few months, this phenotype was mostly replaced by the \"testis-to-ovary\" or \"ovaries\" phenotypes. The gonads of the remaining fish, i.e. approximately half of the fish in each sampling period, remained undifferentiated until six months after fertilization. Genetic sexing of the last two samples revealed that fish with undifferentiated gonads were all males, who, by that time, were on average larger than the genetic females (verified in 8-months old juveniles raised in another experiment). Only 12% of the genetic males showed testicular tissue six months after fertilization. We conclude that sex differentiation starts around hatching, goes through an all-male stage for both sexes (which represents a rare case of \"undifferentiated\" gonochoristic species that usually go through an all-female stage), and is delayed in males who, instead of developing their gonads, grow faster than females during these juvenile stages.\n\nAuthor contributionMRR and CW initiated the project. DM, OS, AU, LMC, LW, and CW sampled the adult fish, did the experimental in vitro fertilizations, and prepared the embryos for experimental rearing in the laboratory. All further manipulations on the embryos and the larvae were done by DM, OS, AU, LMC, and LW. The RNA-seq data were analyzed by OS, JR, and MRR, the histological analyses were done by DM, supervised by SK, and the molecular genetic sexing was performed by DM, OS, AU, and KBM. DM, OS, and CW performed the remaining statistical analyses and wrote the first version of the manuscript that was then critically revised by all other authors.

developmental biology↗

bioRxiv2017

No evidence for the radiation time lag model after whole genome duplications in Teleostei

The short and long term effects of polyploidization on the evolutionary fate of lineages is still unclear despite much interest. First recognized in land plants, it has become clear that polyploidization is widespread in eukaryotes, notably at the origin of vertebrates and teleost fishes. Many hypotheses have been proposed to link the evolutionary success of lineages and whole genome duplications. For instance, the radiation time lag model suggests that paleopolyploidy would favour the apparition of key innovations, although the evolutionary success would not become apparent until a later dispersion event. Some results indicate that this model may be observed during land plant evolution. In this work, we test predictions of the radiation time lag model using both fossil data and molecular phylogenies in ancient and more recent teleost whole genome duplications. We fail to find any evidence of delayed evolutionary success after any of these events and conclude that paleopolyploidization still remains to be unambiguously linked to evolutionary success in fishes.

evolutionary biology↗