Abstract
The self-fertile nematode worms Caenorhabditis elegans, C. briggsae, and C. tropicalis evolved independently from outcrossing male-female ancestors and have genomes 20-40% smaller than closely related outcrossing relatives. This pattern of smaller genomes for selfing species and larger genomes for closely related outcrossing species is also seen in plants. We use comparative genomics, including the first high quality genome assembly for an outcrossing member of the genus (C. remanei) to test several hypotheses for the evolution of genome reduction under a change in mating system. Unlike plants, it does not appear that reductions in the number of repetitive elements, such as transposable elements, are an important contributor to the change in genome size. Instead, all functional genomic categories are lost in approximately equal proportions. Theory predicts that self-fertilization should equalize the effective population size, as well as the resulting effects of genetic drift, between the X chromosome and autosomes. Contrary to this, we find that the self-fertile C. briggsae and C. elegans have larger intergenic spaces and larger protein-coding genes on the X chromosome when compared to autosomes, while C. remanei actually has smaller introns on the X chromosome than either self-reproducing species. Rather than being driven by mutational biases and/or genetic drift caused by a reduction in effective population size under self reproduction, changes in genome size in this group of nematodes appear to be caused by genome-wide patterns of gene loss, most likely generated by genomic adaptation to self reproduction per se.
Highlights
Self reproduction increases the probability of homozygosity at single loci, reducing the effective size of the population by a factor of two [1,2,3]
What should be the genomic consequences of a transition in mating system from outcrossing to selfing? The reduction in population size means that genetic drift should become more prominent, allowing for the accumulation of slightly deleterious features, such as repetitive elements, which should lead to an increase in genome size [6]
The combination of general comparisons across the phylogeny with specific comparisons between C. elegans, C. briggsae, and C. remanei shows that, while these nematodes share the general pattern of genome size reduction with plants, they appear to achieve it in different ways and that the particulars of the changes likely result from an interaction between genomic architecture and changes in population size and the frequency of interactions between the sexes
Summary
Related species can vary widely in genome size, yet the genetic and evolutionary forces responsible for these differences are poorly understood. Constructing a high quality de novo genome assembly in C. remanei, we find that this outcrossing species has many more protein coding genes than the self-fertilizing Caenorhabditis. Intergenic spaces are larger on the X chromosome and smaller on autosomes for both selfing and outcrossing Caenorhabditis, but protein-coding genes are larger on the X chromosome in the self-fertile C. briggsae and C. elegans and larger on autosomes in the outcrossing C. remanei. This contrasting pattern of contracting genomes and expanding genes is likely mediated by changes in the balance between genetic drift and natural selection accompanying the transition to self-fertilization
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