Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression

Abstract Background Transposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content varies widely across eukaryotes and the dynamics of TE activity and TE silencing across evolutionary time is poorly understood. Results Here, we used experimentally evolved populations of C. elegans to study the dynamics of TE expression over 409 generations. The experimental populations were evolved at population sizes of 1, 10 and 100 individuals to manipulate the efficiency of natural selection versus genetic drift. We demonstrate increased TE expression relative to the ancestral population, with the largest increases occurring in the smallest populations. We show that the transcriptional activation of TEs within active regions of the genome is associated with failure of piRNA-mediated silencing, whilst desilenced TEs in repressed chromatin domains retain small RNAs. Additionally, we find that the sequence context of the surrounding region influences the propensity of TEs to lose silencing through failure of small RNA-mediated silencing. Conclusions Our results show that natural selection in C. elegans is responsible for maintaining low levels of TE expression, and provide new insights into the epigenomic features responsible.

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Long-term experimental evolution reveals purifying selection on piRNA-mediated control of transposable element expression

10.1101/666693 ◽

2019 ◽

Cited By ~ 1

Author(s):

Ulfar Bergthorsson ◽

Caroline J. Sheeba ◽

Anke Konrad ◽

Tony Belicard ◽

Toni Beltran ◽

...

Keyword(s):

Natural Selection ◽

Transcriptional Activation ◽

Small Rnas ◽

Active Regions ◽

Purifying Selection ◽

Ancestral Population ◽

Sequence Context ◽

C Elegans ◽

Population Sizes

AbstractTransposable elements (TEs) are an almost universal constituent of eukaryotic genomes. In animals, Piwi-interacting small RNAs (piRNAs) and repressive chromatin often play crucial roles in preventing TE transcription and thus restricting TE activity. Nevertheless, TE content varies widely across eukaryotes and the dynamics of TE activity and TE silencing across evolutionary time is poorly understood. Here we used experimentally evolved populations of C. elegans to study the dynamics of TE expression over 400 generations. The experimental populations were evolved at three different population sizes to manipulate the efficiency of natural selection versus genetic drift. We demonstrate increased TE expression relative to the ancestral population, with the largest increases occurring in the smallest populations. We show that the transcriptional activation of TEs within active regions of the genome is associated with failure of piRNA-mediated silencing, whilst desilenced TEs in repressed chromatin domains retain small RNAs. Additionally, we find that the sequence context of the surrounding region influences the propensity of TEs to lose silencing through failure of small RNA-mediated silencing. Together, our results show that natural selection in C. elegans is responsible for maintaining low levels of TE expression, and provide new insights into the epigenomic features responsible.

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Gene-level quantitative trait mapping in an expandedC. elegansmultiparent experimental evolution panel

10.1101/589432 ◽

2019 ◽

Cited By ~ 6

Author(s):

Luke M. Noble ◽

Matthew V. Rockman ◽

Henrique Teotónio

Keyword(s):

Experimental Evolution ◽

Recombinant Inbred Lines ◽

Single Gene ◽

Ancestral Population ◽

C Elegans ◽

Quantitative Trait Mapping ◽

Trait Variance ◽

Gene Level ◽

Evolution Experiment

ABSTRACTTheCaenorhabditis elegansmultiparental experimental evolution (CeMEE) panel is a collection of genome-sequenced, cryopreserved recombinant inbred lines useful for mapping the genetic basis and evolution of quantitative traits. We have expanded the resource with new lines and new populations, and here report updated additive and epistatic mapping simulations and the genetic and haplotypic composition of CeMEE version 2. Additive QTL explaining 3% of trait variance are detected with >80% power, and the median detection interval is around the length of a single gene on the highly recombinant chromosome arms. Although CeMEE populations are derived from a long-term evolution experiment, genetic structure is dominated by variation present in the ancestral population and is not obviously associated with phenotypic differentiation.C. elegansprovides exceptional experimental advantages for the study of phenotypic evolution.

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Genome evolution in bacteria isolated from million-year-old subseafloor sediments

10.1101/2020.12.19.423498 ◽

2020 ◽

Author(s):

William D Orsi ◽

Tobias Magritsch ◽

Sergio Vargas ◽

Omer K Coskun ◽

Aurele Vuillemin ◽

...

Keyword(s):

Homologous Recombination ◽

Genome Evolution ◽

Purifying Selection ◽

Small Population ◽

Genomic Evolution ◽

Bacterial Strains ◽

Physical Isolation ◽

Genome Wide ◽

Population Sizes

The nature and extent of genomic evolution in subseafloor microbial populations subsisting for millions of years below the seafloor is unknown. Subseafloor populations have ultra-slow metabolic rates that are hypothesized to restrict reproduction and, consequently, the spread of new traits. Our findings demonstrate that genomes of cultivated bacterial strains from the genus Thalassospira isolated from million-year-old abyssal sediment exhibit greatly reduced levels of homologous recombination, elevated numbers of pseudogenes, and genome-wide evidence of relaxed purifying selection. These substitutions and pseudogenes are fixed into the population, suggesting the genome evolution of these bacteria has been dominated by genetic drift, whereby under long-term physical isolation in small population sizes, and in the absence of homologous recombination, newly acquired mutations accumulate in the genomes of clonal populations over millions of years.

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Genetic purging in captive endangered ungulates with extremely low effective population sizes

Heredity ◽

10.1038/s41437-021-00473-2 ◽

2021 ◽

Author(s):

Eugenio López-Cortegano ◽

Eulalia Moreno ◽

Aurora García-Dorado

Keyword(s):

Natural Selection ◽

Population Size ◽

Inbreeding Depression ◽

Captive Breeding ◽

Random Mating ◽

Management Strategies ◽

Effective Population ◽

Population Sizes ◽

Genetic Purging

AbstractInbreeding threatens the survival of small populations by producing inbreeding depression, but also exposes recessive deleterious effects in homozygosis allowing for genetic purging. Using inbreeding-purging theory, we analyze early survival in four pedigreed captive breeding programs of endangered ungulates where population growth was prioritized so that most adult females were allowed to contribute offspring according to their fitness. We find evidence that purging can substantially reduce inbreeding depression in Gazella cuvieri (with effective population size Ne = 14) and Nanger dama (Ne = 11). No purging is detected in Ammotragus lervia (Ne = 4), in agreement with the notion that drift overcomes purging under fast inbreeding, nor in G. dorcas (Ne = 39) where, due to the larger population size, purging is slower and detection is expected to require more generations. Thus, although smaller populations are always expected to show smaller fitness (as well as less adaptive potential) than larger ones due to higher homozygosis and deleterious fixation, our results show that a substantial fraction of their inbreeding load and inbreeding depression can be purged when breeding contributions are governed by natural selection. Since management strategies intended to maximize the ratio from the effective to the actual population size tend to reduce purging, the search for a compromise between these strategies and purging could be beneficial in the long term. This could be achieved either by allowing some level of random mating and some role of natural selection in determining breeding contributions, or by undertaking reintroductions into the wild at the earliest opportunity.

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Partial selfing eliminates inbreeding depression while maintaining genetic diversity

10.1101/210005 ◽

2017 ◽

Author(s):

Ivo M. Chelo ◽

Bruno Afonso ◽

Sara Carvalho ◽

Ioannis Theologidis ◽

Christine Goy ◽

...

Keyword(s):

Genetic Diversity ◽

Inbreeding Depression ◽

Experimental Evolution ◽

Natural Populations ◽

Ancestral Population ◽

Origin And Evolution ◽

C Elegans ◽

Genome Wide ◽

Adaptive Genetic Diversity

AbstractClassical theory on the origin and evolution of selfing and outcrossing relies on the role of inbreeding depression created by unlinked partially-deleterious recessive alleles to predict that individuals from natural populations predominantly self or outcross. Comparative data indicates, however, that maintenance of partial selfing and outcrossing at intermediate frequencies is common in nature. In part to explain the presence of mixed reproductive modes within populations, several hypotheses regarding the evolution of inbreeding depression have been put forward based on the complex interaction of linkage and identity disequilibrium among fitness loci, together with Hill-Robertson effects. We here ask what is the genetic basis of inbreeding depression so that populations with intermediate selfing rates can eliminate it while maintain potentially adaptive genetic diversity. For this, we use experimental evolution in the nematode C. elegans under partial selfing and compare it to the experimental evolution of populations evolved under exclusive selfing and predominant outcrossing. We find that the ancestral risk of extinction upon enforced inbreeding by selfing is maintained when populations evolve under predominant outcrossing, but reduced when populations evolve under partial or exclusive selfing. Analysis of genome-wide single-nucleotide polymorphism (SNP) during experimental evolution and after enforced inbreeding suggests that, under partial selfing, populations were purged of unlinked deleterious recessive alleles that segregate in the ancestral population, which in turn allowed the expression of unlinked overdominant fitness loci. Taken together, these observations indicate that populations evolving under partial selfing gain the short-term benefits of selfing, in purging deleterious recessive alleles, but also the long-term benefits of outcrossing, in maintaining genetic diversity that may important for future adaptation.

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Evolutionary dynamics of cytoplasmic segregation and fusion: mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

10.1101/034116 ◽

2015 ◽

Author(s):

Arunas L. Radzvilavicius

Keyword(s):

Cell Fusion ◽

Evolutionary Dynamics ◽

Purifying Selection ◽

Theoretical Work ◽

Ancestral Population ◽

Evolution Of Sex ◽

Origin And Evolution ◽

Sexual Cell ◽

The Stability

AbstractSexual reproduction is a trait shared by all complex life, but explaining its origin and evolution remains a major theoretical challenge. Virtually all theoretical work on the evolution of sex has focused on the benefits of reciprocal recombination among nuclear genes, paying little attention to the dynamics of mitochondrial genes. Here I develop a mathematical model to study the evolution of alleles inducing cell fusion in an ancestral population of clonal proto-eukaryotes. Mitochondrial mixing masks the detrimental effects of faulty organelles and drives the evolution of sexual cell fusion despite the declining long-term population fitness. Cell-fusion alleles fix under negative epistatic interactions between mitochondrial mutations and strong purifying selection, low mutation load and weak mitochondrial-nuclear associations. I argue that similar conditions could have been maintained throughout the eukaryogenesis, favoring the evolution of sexual cell fusion and meiotic recombination without compromising the stability of the emerging complex cell.

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Specific features of long-term domestication of australian crayfish Cherax quadricarinatus in conditions of the western part of Russian Federation

Izvestiya TINRO ◽

10.26428/1606-9919-2018-194-188-192 ◽

2018 ◽

Vol 194 ◽

pp. 188-192

Author(s):

D. I. Shokasheva

Keyword(s):

Natural Selection ◽

Russian Federation ◽

Natural Populations ◽

Cherax Quadricarinatus ◽

Local Environments ◽

Local Species ◽

Adaptive Ability

Natural populations of crayfish are in depression in Russia and local species are not cultivated. In this situation, experimental cultivation of allochtonous australian crayfish Cherax quadricarinatus is conducted. This species is distinguished by high reproductive abilities and good consumer properties. It has domesticated in Russia spontaneously and produced 9–10 generations in Astrakhan Region. Certain natural selection in the process of domestication provides adaptive ability of this species to local environments and its capability to reproduce a viable progeny, so there is no doubts in good prospects of its cultivation in industrial conditions.

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The Non-Canonical Aspects of MicroRNAs: Many Roads to Gene Regulation

Cells ◽

10.3390/cells8111465 ◽

2019 ◽

Vol 8 (11) ◽

pp. 1465 ◽

Cited By ~ 30

Author(s):

Christiaan J. Stavast ◽

Stefan J. Erkeland

Keyword(s):

Rna Polymerase Ii ◽

Transcriptional Activation ◽

Small Rnas ◽

Target Genes ◽

Biological Functions ◽

Rnase Iii ◽

Mrna Targets ◽

Argonaute Proteins ◽

Epigenetic Modifiers ◽

Encoding Genes

MicroRNAs (miRNAs) are critical regulators of gene expression. As miRNAs are frequently deregulated in many human diseases, including cancer and immunological disorders, it is important to understand their biological functions. Typically, miRNA-encoding genes are transcribed by RNA Polymerase II and generate primary transcripts that are processed by RNase III-endonucleases DROSHA and DICER into small RNAs of approximately 21 nucleotides. All miRNAs are loaded into Argonaute proteins in the RNA-induced silencing complex (RISC) and act as post-transcriptional regulators by binding to the 3′- untranslated region (UTR) of mRNAs. This seed-dependent miRNA binding inhibits the translation and/or promotes the degradation of mRNA targets. Surprisingly, recent data presents evidence for a target-mediated decay mechanism that controls the level of specific miRNAs. In addition, several non-canonical miRNA-containing genes have been recently described and unexpected functions of miRNAs have been identified. For instance, several miRNAs are located in the nucleus, where they are involved in the transcriptional activation or silencing of target genes. These epigenetic modifiers are recruited by RISC and guided by miRNAs to specific loci in the genome. Here, we will review non-canonical aspects of miRNA biology, including novel regulators of miRNA expression and functions of miRNAs in the nucleus.

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Bayes Estimation of Species Divergence Times and Ancestral Population Sizes Using DNA Sequences From Multiple Loci

Genetics ◽

10.1093/genetics/164.4.1645 ◽

2003 ◽

Vol 164 (4) ◽

pp. 1645-1656 ◽

Cited By ~ 3

Author(s):

Bruce Rannala ◽

Ziheng Yang

Keyword(s):

Dna Sequences ◽

Gene Tree ◽

Species Tree ◽

Bayes Estimation ◽

Ancestral Population ◽

Divergence Times ◽

Gene Trees ◽

Species Divergence ◽

Multiple Loci ◽

Population Sizes

Abstract The effective population sizes of ancestral as well as modern species are important parameters in models of population genetics and human evolution. The commonly used method for estimating ancestral population sizes, based on counting mismatches between the species tree and the inferred gene trees, is highly biased as it ignores uncertainties in gene tree reconstruction. In this article, we develop a Bayes method for simultaneous estimation of the species divergence times and current and ancestral population sizes. The method uses DNA sequence data from multiple loci and extracts information about conflicts among gene tree topologies and coalescent times to estimate ancestral population sizes. The topology of the species tree is assumed known. A Markov chain Monte Carlo algorithm is implemented to integrate over uncertain gene trees and branch lengths (or coalescence times) at each locus as well as species divergence times. The method can handle any species tree and allows different numbers of sequences at different loci. We apply the method to published noncoding DNA sequences from the human and the great apes. There are strong correlations between posterior estimates of speciation times and ancestral population sizes. With the use of an informative prior for the human-chimpanzee divergence date, the population size of the common ancestor of the two species is estimated to be ∼20,000, with a 95% credibility interval (8000, 40,000). Our estimates, however, are affected by model assumptions as well as data quality. We suggest that reliable estimates have yet to await more data and more realistic models.

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The secreted endoribonuclease ENDU-2 from the soma protects germline immortality in C. elegans

Nature Communications ◽

10.1038/s41467-021-21516-6 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Wenjing Qi ◽

Erika D. V. Gromoff ◽

Fan Xu ◽

Qian Zhao ◽

Wei Yang ◽

...

Keyword(s):

Gene Expression ◽

Stem Cell ◽

Small Rnas ◽

C Elegans ◽

Cleavage Activity ◽

Response To Temperature ◽

Multicellular Organisms ◽

Cell Immortality ◽

Mature Mrnas ◽

Endoribonuclease Activity

AbstractMulticellular organisms coordinate tissue specific responses to environmental information via both cell-autonomous and non-autonomous mechanisms. In addition to secreted ligands, recent reports implicated release of small RNAs in regulating gene expression across tissue boundaries. Here, we show that the conserved poly-U specific endoribonuclease ENDU-2 in C. elegans is secreted from the soma and taken-up by the germline to ensure germline immortality at elevated temperature. ENDU-2 binds to mature mRNAs and negatively regulates mRNA abundance both in the soma and the germline. While ENDU-2 promotes RNA decay in the soma directly via its endoribonuclease activity, ENDU-2 prevents misexpression of soma-specific genes in the germline and preserves germline immortality independent of its RNA-cleavage activity. In summary, our results suggest that the secreted RNase ENDU-2 regulates gene expression across tissue boundaries in response to temperature alterations and contributes to maintenance of stem cell immortality, probably via retaining a stem cell specific program of gene expression.

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