Genome Size Changes by Duplication, Divergence, and Insertion in Caenorhabditis Worms

Genome size has been measurable since the 1940s but we still do not understand genome size variation. Caenorhabditis nematodes show strong conservation of chromosome number but vary in genome size between closely related species. Androdioecy, where populations are composed of males and self-fertile hermaphrodites, evolved from outcrossing, female-male dioecy, three times in this group. In Caenorhabditis, androdioecious genomes are 10–30% smaller than dioecious species, but in the nematode Pristionchus, androdioecy evolved six times and does not correlate with genome size. Previous hypotheses include genome size evolution through: 1) Deletions and “genome shrinkage” in androdioecious species; 2) Transposable element (TE) expansion and DNA loss through large deletions (the “accordion model”); and 3) Differing TE dynamics in androdioecious and dioecious species. We analyzed nematode genomes and found no evidence for these hypotheses. Instead, nematode genome sizes had strong phylogenetic inertia with increases in a few dioecious species, contradicting the “genome shrinkage” hypothesis. TEs did not explain genome size variation with the exception of the DNA transposon Mutator which was twice as abundant in dioecious genomes. Across short and long evolutionary distances Caenorhabditis genomes evolved through small structural mutations including gene-associated duplications and insertions. Seventy-one protein families had significant, parallel decreases across androdioecious Caenorhabditis including genes involved in the sensory system, regulatory proteins and membrane-associated immune responses. Our results suggest that within a dynamic landscape of frequent small rearrangements in Caenorhabditis, reproductive mode mediates genome evolution by altering the precise fates of individual genes, proteins, and the phenotypes they underlie.