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Linking genome size variation to population phenotypic variation within the rotifer, Brachionus asplanchnoidis.

ABSTRACT: Eukaryotic organisms usually contain much more genomic DNA than expected from their biological complexity. In explaining this pattern, selection-based hypotheses suggest that genome size evolves through selection acting on correlated life history traits, implicitly assuming the existence of phenotypic effects of (extra) genomic DNA that are independent of its information content. Here, we present conclusive evidence of such phenotypic effects within a well-mixed natural population that shows heritable variation in genome size. We found that genome size is positively correlated with body size, egg size, and embryonic development time in a population of the monogonont rotifer Brachionus asplanchnoidis. The effect on embryonic development time was mediated partly by an indirect effect (via egg size), and a direct effect, the latter indicating an increased replication cost of the larger amounts of DNA during mitosis. Our results suggest that selection-based change of genome size can operate in this population, provided it is strong enough to overcome drift or mutational change of genome size.

SUBMITTER: Stelzer CP

PROVIDER: S-EPMC8134563 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundEukaryotic genomes are known to display an enormous variation in size, but the evolutionary causes of this phenomenon are still poorly understood. To obtain mechanistic insights into such variation, previous studies have often employed comparative genomics approaches involving closely related species or geographically isolated populations within a species. Genome comparisons among individuals of the same population remained so far understudied-despite their great potential in providing a microevolutionary perspective to genome size evolution. The rotifer Brachionus asplanchnoidis represents one of the most extreme cases of within-population genome size variation among eukaryotes, displaying almost twofold variation within a geographic population.ResultsHere, we used a whole-genome sequencing approach to identify the underlying DNA sequence differences by assembling a high-quality reference genome draft for one individual of the population and aligning short reads of 15 individuals from the same geographic population including the reference individual. We identified several large, contiguous copy number variable regions (CNVs), up to megabases in size, which exhibited striking coverage differences among individuals, and whose coverage overall scaled with genome size. CNVs were of remarkably low complexity, being mainly composed of tandemly repeated satellite DNA with only a few interspersed genes or other sequences, and were characterized by a significantly elevated GC-content. CNV patterns in offspring of two parents with divergent genome size and CNV patterns in several individuals from an inbred line differing in genome size demonstrated inheritance and accumulation of CNVs across generations.ConclusionsBy identifying the exact genomic elements that cause within-population genome size variation, our study paves the way for studying genome size evolution in contemporary populations rather than inferring patterns and processes a posteriori from species comparisons.

Project description:BackgroundUnderstanding gene expression changes over lifespan in diverse animal species will lead to insights to conserved processes in the biology of aging and allow development of interventions to improve health. Rotifers are small aquatic invertebrates that have been used in aging studies for nearly 100 years and are now re-emerging as a modern model system. To provide a baseline to evaluate genetic responses to interventions that change health throughout lifespan and a framework for new hypotheses about the molecular genetic mechanisms of aging, we examined the transcriptome of an asexual female lineage of the rotifer Brachionus manjavacas at five life stages: eggs, neonates, and early-, late-, and post-reproductive adults.ResultsThere are widespread shifts in gene expression over the lifespan of B. manjavacas; the largest change occurs between neonates and early reproductive adults and is characterized by down-regulation of developmental genes and up-regulation of genes involved in reproduction. The expression profile of post-reproductive adults was distinct from that of other life stages. While few genes were significantly differentially expressed in the late- to post-reproductive transition, gene set enrichment analysis revealed multiple down-regulated pathways in metabolism, maintenance and repair, and proteostasis, united by genes involved in mitochondrial function and oxidative phosphorylation.ConclusionsThis study provides the first examination of changes in gene expression over lifespan in rotifers. We detected differential expression of many genes with human orthologs that are absent in Drosophila and C. elegans, highlighting the potential of the rotifer model in aging studies. Our findings suggest that small but coordinated changes in expression of many genes in pathways that integrate diverse functions drive the aging process. The observation of simultaneous declines in expression of genes in multiple pathways may have consequences for health and longevity not detected by single- or multi-gene knockdown in otherwise healthy animals. Investigation of subtle but genome-wide change in these pathways during aging is an important area for future study.

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Linking genome size variation to population phenotypic variation within the rotifer, Brachionus asplanchnoidis.

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