Within-population genome size variation is mediated by multiple genomic elements that segregate independently during meiosis

Abstract

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 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 beyond a minimum diploid genome size. 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 minimum 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 behaviour), can effectively address most scenarios of short-term evolutionary change of genome size in a population.

Genome structure ofBrachionus asplanchnoidis, a Eukaryote with intrapopulation variation in genome size

“…The smallest observed genome size in B. asplanchnoidis was 404Mb (2C, nuclear DNA content). Individuals at or close to this basal genome size are completely lacking independently segregating elements, while in larger individuals, genome size scales with the amount of independently segregating elements [7].…”

“…The genomes of Eukaryotic organisms display remarkable diversity in size, overall spanning approximately five orders of magnitude [1]. In addition, genome size may vary substantially among closely related species [2,3], within a species [e.g., 4,5,6], and sometimes even within a population [7]. Most of the variation in genome size stems from differences in the proportion of various kinds of non-coding DNA and/or transposable elements, which can reach excessive levels in species with giant genomes [8,9].…”

“…Intraspecific genome size variation (IGV) has been described in several species of Eukaryotes [some examples are summarized in 7,14]. IGV may be associated with variation in the number of chromosomes [e.g., B-chromosomes 14], but there are also examples where IGV is not reflected in the karyotype [2,6].…”

“…IGV may be associated with variation in the number of chromosomes [e.g., B-chromosomes 14], but there are also examples where IGV is not reflected in the karyotype [2,6]. One of the most recent additions to IGV model organisms was the monogonont rotifer B. asplanchnoidis, which displays a nearly 2-fold variation in genome size even among individuals within a geographic population [7]. Monogonont rotifers are short-lived (1-2 weeks), small aquatic metazoans, only a few hundred micrometers in size, common in fresh and brackish water habitats throughout the world.…”

“…In the present study, we focus on a population of B. asplanchnoidis from Obere Halbjochlacke (OHJ), a shallow alkaline lake in Eastern Austria [7,17]. Individuals of this population can be crossed with each other -even if they substantially differ in genome size -and they will produce offspring with intermediate genome sizes close to the parental mean.…”