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Catania, F.

Publications and source records attributed to Catania, F..

4 recordsLinked to original sources

Fifty generations of amitosis: tracing asymmetric allele segregation in polyploid cells with single-cell DNA sequencing

Amitosis is a widespread form of unbalanced nuclear division whose biomedical and evolutionary significance remain unclear. Traditionally, insights into the genetics of amitosis are acquired by assessing the rate of phenotypic assortment. The phenotypic diversification of heterozygous clones during successive cell divisions reveals the random segregation of alleles to daughter nuclei. Though powerful, this experimental approach relies on the availability of phenotypic markers. Here, we present an approach that overcomes the requirement for phenotypic assortment. Leveraging Paramecium tetraurelia, a unicellular eukaryote with nuclear dimorphism and a highly polyploid somatic nucleus, we use single-cell whole-genome sequencing to track the assortment of developmentally acquired somatic DNA variants. Accounting for genome representation biases, we measure the effect of amitosis on allele segregation across the first [~]50 amitotic divisions post self-fertilization and compare our empirical findings with theoretical predictions estimated via mathematical modeling. In line with our simulations, we show that amitosis in P. tetraurelia produces measurable but modest levels of somatic assortment. In forgoing the requirement for phenotypic assortment and employing developmental, environmentally induced somatic variation as molecular markers, our work provides a new powerful approach to investigate the consequences of amitosis in polyploid cells.

genomics↗

Prolonged exposure to constant environmental conditions prompts nonrandom genetic variation

Long-term environmental exposure under selection-free conditions has no consequences for fitness under the neo-Darwinian paradigm but it may provoke adaptive developmental buffering if environmental pressures foster directional organismal changes. To test this hypothesis, we revisited a Mutation Accumulation (MA) experiment where isogenic lines of the ciliate Paramecium were propagated for >40 sexual cycles ([~]4 years) in a nearly selection-free and nutrient-rich environment. We find that these MA lines somatic genome is enriched with intervening segments of DNA (IESs), which are normally eliminated during germline-soma differentiation. Across independent replicate MA lines, an excess of these somatic IESs fall into a class of epigenetically controlled sequences, map to the same genomic locations, and preferentially disrupt loci that regulate nutrient metabolism. Although further work is needed to assess the phenotypic consequences of somatic IESs, these findings support a model where environmentally induced developmental variants may restore an adaptive fit between phenotype and environment. In this model, positive selection is surprisingly dispensable for adaptation.

evolutionary biology↗

Sex enhances survival in Paramecium

The pervasiveness of sex despite its well-known costs is a long-standing puzzle in evolutionary biology. Current explanations for the success of sex in nature largely rely on the adaptive significance of the new or rare genotypes that sex may generate. Less explored is the possibility that sex-underlying molecular mechanisms can enhance fitness and convey benefits to the individuals that bear the immediate costs of sex. Here we show that self-fertilization can increase stress resistance in the ciliate Paramecium tetraurelia. This advantage is independent of new genetic variation, coupled with a reduced nutritional input, and offers fresh insights into the mechanistic origin of sex. In addition to providing evidence that the molecular underpinnings of sexual reproduction and the stress response are linked in P. tetraurelia, these findings supply an explanation for the persistence of self-fertilization in this ciliate.

evolutionary biology↗

Enhanced plasticity of programmed DNA elimination boosts adaptive potential in suboptimal environments

The impact of ecological changes on the development of new somatic genomes has thus far been neglected. This oversight yields an incomplete understanding of the mechanisms that underlie environmental adaptation and can be tackled leveraging the biological properties of ciliates. When Paramecium reproduces sexually, its polyploid somatic genome regenerates from the germline genome via a developmental process, Programmed DNA elimination (PDE), that involves the removal of thousands of ORF-interrupting germline sequences. Here, we demonstrate that exposure to sub-optimal temperatures impacts PDE efficiency, prompting the emergence of hundreds of alternative DNA splicing variants that dually embody cryptic (germline) variation and de novo induced (somatic) mutations. In contrast to trivial biological errors, many of these alternative DNA isoforms display a patterned genomic topography, are epigenetically controlled, inherited trans-somatically, and under purifying selection. Developmental thermoplasticity in Paramecium is a likely source of evolutionary innovation.

evolutionary biology↗