Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing

Cutter, Asher D.; Wasmuth, James D.; Washington, Nicole

doi:10.1534/genetics.107.085787

Cited by 87 publications

(144 citation statements)

References 97 publications

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“…Instead, we see very little evidence for genetic variation or population structure on a worldwide scale (Barriere and Felix 2005;Haber et al 2005;Cutter 2006;Rockman and Kruglyak 2009). This observation provides support for the view that most extant C. elegans populations may have diverged from one another relatively recently (Phillips 2006;Cutter et al 2008).…”

Section: Discussion Evolutionary Implicationsmentioning

confidence: 49%

Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans

Denver¹,

Howe²,

Wilhelm³

et al. 2010

Genome Res.

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Deleterious mutation poses a serious threat to human health and the persistence of small populations. Although adaptive recovery from deleterious mutation has been well-characterized in prokaryotes, the evolutionary mechanisms by which multicellular eukaryotes recover from deleterious mutation remain unknown. We applied high-throughput DNA sequencing to characterize genomic divergence patterns associated with the adaptive recovery from deleterious mutation using a Caenorhabditis elegans recovery-line system. The C. elegans recovery lines were initiated from a low-fitness mutationaccumulation (MA) line progenitor and allowed to independently evolve in large populations (N ; 1000) for 60 generations. All lines rapidly regained levels of fitness similar to the wild-type (N2) MA line progenitor. Although there was a near-zero probability of a single mutation fixing due to genetic drift during the recovery experiment, we observed 28 fixed mutations. Cross-generational analysis showed that all mutations went from undetectable population-level frequencies to a fixed state in 10-20 generations. Many recovery-line mutations fixed at identical timepoints, suggesting that the mutations, if not beneficial, hitchhiked to fixation during selective sweep events observed in the recovery lines. No MA line mutation reversions were detected. Parallel mutation fixation was observed for two sites in two independent recovery lines. Analysis using a C. elegans interactome map revealed many predicted interactions between genes with recovery linespecific mutations and genes with previously accumulated MA line mutations. Our study suggests that recovery-line mutations identified in both coding and noncoding genomic regions might have beneficial effects associated with compensatory epistatic interactions.[Supplemental material is available online at http://www.genome.org. The sequence data from this study have been submitted to the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/Traces/sra/sra.cgi) under accession no. SRA023539.]The accumulation of deleterious mutations under conditions of relaxed selection threatens the persistence of organisms evolving in small populations (Lynch et al. 1993;Lande 1994) and is especially relevant to small captive populations of endangered species living in benign environments (Lande 1995). The recovery from deleterious mutations also serves as an analog to adaptation to a novel environment in which previously favored alleles are now detrimental. The evolutionary mechanisms by which organisms suffering from deleterious mutation are able to recover fitness have been well-studied in bacteriophage and bacterial laboratory evolution settings that showed rapid fitness recovery and a high incidence of parallel beneficial mutation fixation in independent experimental lineages (Reynolds 2000;Maisnier-Patin et al. 2002;. For example, DNA sequencing analysis of bacteriophage FX174 lines that had recovered from previously accumulated deleterious mutations revealed that ;30% of the beneficial mutations respo...

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Section: Discussion Evolutionary Implicationsmentioning

confidence: 49%

Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans

Denver¹,

Howe²,

Wilhelm³

et al. 2010

Genome Res.

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“…Recent dissection of the partially redundant Holiday junction resolvases in C. elegans (Saito et al 2013;O'Neil et al 2013;Agostinho et al 2013) leads us to the hypothesis that slx-1, which is disproportionately responsible for noncrossover gene conversion in chromosome centers (Saito et al 2013), may be more prone to BGC than the other resolvases. BGC is expected to have very weak effects on equilibrium GC content in selfing organisms (Marais et al 2004), due to the scarcity of heterozygotes, but it could persist in C. elegans from evolution in its outcrossing ancestor (Cutter et al 2008).…”

Section: Discussionmentioning

confidence: 99%

Crossover Heterogeneity in the Absence of Hotspots inCaenorhabditis elegans

Kaur

Rockman

2014

Genetics

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Crossovers play mechanical roles in meiotic chromosome segregation, generate genetic diversity by producing new allelic combinations, and facilitate evolution by decoupling linked alleles. In almost every species studied to date, crossover distributions are dramatically nonuniform, differing among sexes and across genomes, with spatial variation in crossover rates on scales from whole chromosomes to subkilobase hotspots. To understand the regulatory forces dictating these heterogeneous distributions a crucial first step is the fine-scale characterization of crossover distributions. Here we define the wild-type distribution of crossovers along a region of the C. elegans chromosome II at unprecedented resolution, using recombinant chromosomes of 243 hermaphrodites and 226 males. We find that well-characterized large-scale domains, with little fine-scale rate heterogeneity, dominate this region's crossover landscape. Using the Gini coefficient as a summary statistic, we find that this region of the C. elegans genome has the least heterogeneous fine-scale crossover distribution yet observed among model organisms, and we show by simulation that the data are incompatible with a mammalian-type hotspot-rich landscape. The large-scale structural domains-the low-recombination center and the high-recombination arm-have a discrete boundary that we localize to a small region. This boundary coincides with the armcenter boundary defined both by nuclear-envelope attachment of DNA in somatic cells and GC content, consistent with proposals that these features of chromosome organization may be mechanical causes and evolutionary consequences of crossover recombination. MEIOTIC recombination creates novel combinations of parental alleles and is a powerful force shaping the genetic variation observed within a population. The frequency of recombination has a profound impact on the efficacy of natural selection in both purging deleterious mutations and in the formation of beneficial allelic combinations (Hill and Robertson 1966;Cutter and Payseur 2013). However, the intensity of recombination in different parts of a genome is rarely constant. Heterogeneity in the meiotic recombination rate has been observed across chromosome lengths and at finer scales of a few kilobase in diverse organisms.In Caenorhabditis elegans, meiotic recombination rates show a striking and reproducible chromosome-wide pattern of variation. Genetic maps of the five autosomes and X chromosome show that each has a low-recombination central domain flanked by high-recombination arm domains (Barnes et al. 1995;Rockman and Kruglyak 2009). This domain structure has dramatic effects on genetic variation and evolution (Cutter and Payseur 2003;Rockman et al. 2010;Andersen et al. 2012), but the underlying causes generating this pattern are not completely understood.The domain structure relates to unusual characteristics of the C. elegans chromosomes. The chromosomes lack localized centromeres and exhibit holocentric segregation during mitosis, with kinetochore pro...

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“…It also seems unlikely that a property such as sustained, high levels of transcript synthesis would underlie inclusion in operons, because both oogenesis in hermaphrodites (and females) and spermatogenesis in males require this characteristic. Although C. elegans males are currently rare in nature (Barrière and Felix 2007), a relatively recent origin of hermaphroditism (Cutter et al 2008) means that spermatogenesis gene expression in males is most relevant to their exclusion from operons over the course of evolution.…”

Section: Discussionmentioning

confidence: 99%

Germline Expression Influences Operon Organization in theCaenorhabditis elegansGenome

Reinke

Cutter

2009

Genetics

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Operons are found across multiple kingdoms and phyla, from prokaryotes to chordates. In the nematode Caenorhabditis elegans, the genome contains .1000 operons that compose $15% of the protein-coding genes. However, determination of the force(s) promoting the origin and maintenance of operons in C. elegans has proved elusive. Compared to bacterial operons, genes within a C. elegans operon often show poor coexpression and only sometimes encode proteins with related functions. Using analysis of microarray and large-scale in situ hybridization data, we demonstrate that almost all operon-encoded genes are expressed in germline tissue. However, genes expressed during spermatogenesis are excluded from operons. Operons group together along chromosomes in local clusters that also contain monocistronic germline-expressed genes. Additionally, germline expression of genes in operons is largely independent of the molecular function of the encoded proteins. These analyses demonstrate that mechanisms governing germline gene expression influence operon origination and/or maintenance. Thus, gene expression in a specific tissue can have profound effects on the evolution of genome organization.

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Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing

Cited by 87 publications

References 97 publications

Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans

Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans

Crossover Heterogeneity in the Absence of Hotspots inCaenorhabditis elegans

Germline Expression Influences Operon Organization in theCaenorhabditis elegansGenome

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