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

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.

Within-Population Genome Size Variation is Mediated by Multiple Genomic Elements That Segregate Independently during Meiosis.

Within-species variation in genome size has been documented in many animals and plants. Despite its importance for understanding eukaryotic genome diversity, there is only sparse knowledge about how individual-level processes mediate genome size variation in populations. Here, we study a natural population of the rotifer Brachionus asplanchnoidis whose members differ up to 1.9-fold in diploid genome size, but were still able to interbreed and produce viable offspring. We show that genome size is highly heritable and can be artificially selected up or down, but not below a certain basal diploid genome size for this species. Analyses of segregation patterns in haploid males reveal that large genomic elements (several megabases in size) provide the substrate of genome size variation. These elements, and their segregation patterns, explain the generation of new genome size variants, the short-term evolutionary potential of genome size change in populations, and some seemingly paradoxical patterns, like an increase in genome size variation among highly inbred lines. Our study suggests that a conceptual model involving only two variables, 1) a basal genome size of the population, and 2) a vector containing information on additional elements that may increase genome size in this population (size, number, and meiotic segregation behavior), can effectively address most scenarios of short-term evolutionary change of genome size in a population.