Opposing Forces of A/T-Biased Mutations and G/C-Biased Gene Conversions Shape the Genome of the Nematode <i>Pristionchus pacificus</i>

Weller, Andreas M.; Rödelsperger, Christian; Eberhardt, Gabi; Molnar, Ruxandra I.; Sommer, Ralf J.

doi:10.1534/genetics.113.159863

Cited by 47 publications

(39 citation statements)

References 39 publications

(59 reference statements)

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“…The accumulation of divergence between P. pacificus and its sister species P. exspectatus is homogenous across the genome. The latter observation is consistent with results of the accompanying article in this issue (Weller et al 2014), which presents a mutation accumulation experiment that shows that the P. pacificus genome does not exhibit strong mutation rate variation on large physical scales and that synonymous and nonsynonymous mutations occur at their expected frequency. By analyzing the ratio of synonymous and nonsynonymous differences between strains at various distances and mutations at different frequencies, we characterized the strength of purifying selection on coding regions.…”

Section: Discussionsupporting

confidence: 88%

Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

et al. 2014

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The hermaphroditic nematode Pristionchus pacificus is an established model system for comparative studies with Caenorhabditis elegans in developmental biology, ecology, and population genetics. In this study, we present whole-genome sequencing data of 104 P. pacificus strains and the draft assembly of the obligate outcrossing sister species P. exspectatus. We characterize genetic diversity within P. pacificus and investigate the population genetic processes shaping this diversity. P. pacificus is 10 times more diverse than C. elegans and exhibits substantial population structure that allows us to probe its evolution on multiple timescales. Consistent with reduced effective recombination in this self-fertilizing species, we find haplotype blocks that span several megabases. Using the P. exspectatus genome as an outgroup, we polarized variation in P. pacificus and found a site frequency spectrum (SFS) that decays more rapidly than expected in neutral models. The SFS at putatively neutral sites is U shaped, which is a characteristic feature of pervasive linked selection. Based on the additional findings (i) that the majority of nonsynonymous variation is eliminated over timescales on the order of the separation between clades, (ii) that diversity is reduced in gene-rich regions, and (iii) that highly differentiated clades show very similar patterns of diversity, we conclude that purifying selection on many mutations with weak effects is a major force shaping genetic diversity in P. pacificus.

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Section: Discussionsupporting

confidence: 88%

Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

et al. 2014

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“…The compositional genome heterogeneity among vertebrates cannot be attributed merely to the transition from anamniotes to amniotes as generally accepted before this study. The genomic DNA base architecture in vertebrates appears to rather result from a interplay of multiple opposing forces, for example, AT‐biased mutations and GC‐biased gene conversions (e.g., Weller et al., ), genome and chromosome sizes (e.g., Romiguier et al., ), selection for GC and drift, and by diverse cellular, metabolic (Chaurasia et al., ) and environmental (e.g., Uliano et al., ; Chaurasia et al., ) factors influenced by physical and chemical properties of AT/GC and their role in the regulation of gene expression (Vinogradov, ). In gars, such interplay should be explored with regard to their metabolic adaptations (sensu Uliano et al., ; Chaurasia et al., , ).…”

Section: Discussionmentioning

confidence: 99%

Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray‐Finned Fish

et al. 2016

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Genomic GC content can vary locally, and GC-rich regions are usually associated with increased DNA thermostability in thermophilic prokaryotes and warm-blooded eukaryotes. Among vertebrates, fish and amphibians appeared to possess a distinctly less heterogeneous AT/GC organization in their genomes, whereas cytogenetically detectable GC heterogeneity has so far only been documented in mammals and birds. The subject of our study is the gar, an ancient "living fossil" of a basal ray-finned fish lineage, known from the Cretaceous period. We carried out cytogenomic analysis in two gar genera (Atractosteus and Lepisosteus) uncovering a GC chromosomal pattern uncharacteristic for fish. Bioinformatic analysis of the spotted gar (Lepisosteus oculatus) confirmed a GC compartmentalization on GC profiles of linkage groups. This indicates a rather mammalian mode of compositional organization on gar chromosomes. Gars are thus the only analyzed extant ray-finned fishes with a GC compartmentalized genome. Since gars are cold-blooded anamniotes, our results contradict the generally accepted hypothesis that the phylogenomic onset of GC compartmentalization occurred near the origin of amniotes. Ecophysiological findings of other authors indicate a metabolic similarity of gars with mammals. We hypothesize that gars might have undergone convergent evolution with the tetrapod lineages leading to mammals on both metabolic and genomic levels. Their metabolic adaptations might have left footprints in their compositional genome evolution, as proposed by the metabolic rate hypothesis. The genome organization described here in gars sheds new light on the compositional genome evolution in vertebrates generally and contributes to better understanding of the complexities of the mechanisms involved in this process.

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“…30ºC. Because we have estimates of the number of generations it took to generate the 325" diversity of each of the major clades [37,38], we can estimate the amount of time it 326" took for this adaptation to occur. For instance, in clade C, within 5.6×10 5 generations, 327" a low temperature tolerant strain had adapted by 2ºC to a high temperature tolerant 328" strain.…”

Section: "mentioning

confidence: 99%

“…However, two previous results suggest that this scenario would occur 335" only rarely. First, analysis of mutation accumulation lines indicates that different 336" clades are separated by millions of generations and it seems unlikely that 337" polymorphisms would be maintained for such long periods [38]. In accordance with 338" this, comparison of nucleotide diversity between clades shows very little (<7%) 339" shared variation [20].…”

Section: "mentioning

confidence: 99%

Parallel adaptation to higher temperatures in divergent clades of the nematodePristionchus pacificus

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Kayhan

McGaughran

et al. 2016

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Studying the effect of temperature on fertility is particularly important in the light of ongoing climate change. We need to know if organisms can adapt to higher temperatures and, if so, what are the evolutionary mechanisms behind such adaptation. Such studies have been hampered by the lack different populations of sufficient sizes with which to relate the phenotype of temperature tolerance to the underlying genotypes. Here, we examined temperature adaptation in populations of the nematodePristionchus pacificus, in which individual strains are able to successfully reproduce at 30°C. Analysis of the frequency of heat tolerant strains in different temperature zones on La Réunion supports that this trait is subject to natural selection. Reconstruction of ancestral states along the phylogeny of highly differentiatedP. pacificusclades suggests that heat tolerance evolved multiple times independently. This is further supported by genome wide association studies showing that heat tolerance is a polygenic trait and that different loci are used by individualP. pacificusclades to develop heat tolerance. More precisely, analysis of allele frequencies indicated that most genetic markers that are associated with heat tolerance are only polymorphic in individual clades. While in someP. pacificusclades, parallel evolution of heat tolerance can be explained by ancestral polymorphism or by gene flow across clades, we observe at least one clearly distinct and independent scenario where heat tolerance emerged byde novomutation. Thus, temperature tolerance evolved at least two times independently in the evolutionary history of this species. Our data suggest that studies of wild populations ofP. pacificuswill reveal distinct cellular mechanisms driving temperature adaptation.

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Opposing Forces of A/T-Biased Mutations and G/C-Biased Gene Conversions Shape the Genome of the Nematode Pristionchus pacificus

Cited by 47 publications

References 39 publications

Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray‐Finned Fish

Parallel adaptation to higher temperatures in divergent clades of the nematodePristionchus pacificus

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