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Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes.

Fierst JL, Willis JH, Thomas CG, Wang W, Reynolds RM, Ahearne TE, Cutter AD, Phillips PC - PLoS Genet. (2015)

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, United States of America.

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.

No MeSH data available.


Whole chromosome comparisons among C. elegans, C. briggsae, and C. remanei.The C. remanei The linkage map was sufficient to assemble and order 98.93% of the scaffolds with orthologous genes aligning to C. elegans chromosome X, 78.38% of the scaffolds with orthologous genes aligning to C. elegans chromosome II and 81.40% of the scaffolds with orthologous genes aligning to C. elegans chromosome IV. (a) C. remanei linkage groups were assigned to chromosomes based on gene orthology to C. elegans chromosomes. Reproductive incompatibility between the C. remanei strains used to construct the linkage map resulted in over-dispersion of the linkage map and 13 linkage groups instead of the 6 chromosomes expected (both C. elegans and C. briggsae have 6 chromosomes, respectively). (b) The cumulative size and orthologous gene alignments for scaffolds that were not assigned to linkage groups. c-e) Orthologous gene alignments indicated blocks of syntenic DNA between C. elegans, C. briggsae, and C. remanei. The panels c-e show orthologous genes on chromosomes X, II, and IV, with chromosome size scaled to linkage group size in C. remanei (X 18.5Mb, II 12.5Mb, IV 14.5 Mb). Orthologous genes were connected between species pairs, and grouped together if the genes were within 50,000 nucleotides of each other. Single gene translocations were excluded for clarity. Green indicates orthologs identified between C. elegans and C. remanei, blue indicates orthologs identified between C. remanei and C. briggsae, and grey indicates orthologs identified between C. briggsae and C. elegans. The outer rings are chromosomes X, II, and IV in each species. Each gray line is an orthologous gene located on the same chromosome in the other species and each black line is an orthologous gene that is located on a different chromosome in one of the other species. There are few blocks of interchromosomal translocation, and few black lines. White indicates regions of the chromosome where there were no orthologous genes identified between the species. (c) There was a large region of divergence (roughly 3.6Mb) on the C. remanei X; (d) Chromosome II is not completely assembled in C. remanei, and there were several regions of C. elegans and C. briggsae chromosome II that were not represented in C. remanei; (e) Chromosome IV.
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pgen.1005323.g002: Whole chromosome comparisons among C. elegans, C. briggsae, and C. remanei.The C. remanei The linkage map was sufficient to assemble and order 98.93% of the scaffolds with orthologous genes aligning to C. elegans chromosome X, 78.38% of the scaffolds with orthologous genes aligning to C. elegans chromosome II and 81.40% of the scaffolds with orthologous genes aligning to C. elegans chromosome IV. (a) C. remanei linkage groups were assigned to chromosomes based on gene orthology to C. elegans chromosomes. Reproductive incompatibility between the C. remanei strains used to construct the linkage map resulted in over-dispersion of the linkage map and 13 linkage groups instead of the 6 chromosomes expected (both C. elegans and C. briggsae have 6 chromosomes, respectively). (b) The cumulative size and orthologous gene alignments for scaffolds that were not assigned to linkage groups. c-e) Orthologous gene alignments indicated blocks of syntenic DNA between C. elegans, C. briggsae, and C. remanei. The panels c-e show orthologous genes on chromosomes X, II, and IV, with chromosome size scaled to linkage group size in C. remanei (X 18.5Mb, II 12.5Mb, IV 14.5 Mb). Orthologous genes were connected between species pairs, and grouped together if the genes were within 50,000 nucleotides of each other. Single gene translocations were excluded for clarity. Green indicates orthologs identified between C. elegans and C. remanei, blue indicates orthologs identified between C. remanei and C. briggsae, and grey indicates orthologs identified between C. briggsae and C. elegans. The outer rings are chromosomes X, II, and IV in each species. Each gray line is an orthologous gene located on the same chromosome in the other species and each black line is an orthologous gene that is located on a different chromosome in one of the other species. There are few blocks of interchromosomal translocation, and few black lines. White indicates regions of the chromosome where there were no orthologous genes identified between the species. (c) There was a large region of divergence (roughly 3.6Mb) on the C. remanei X; (d) Chromosome II is not completely assembled in C. remanei, and there were several regions of C. elegans and C. briggsae chromosome II that were not represented in C. remanei; (e) Chromosome IV.

Mentions: We estimated residual polymorphism in our inbred PX356 strain to occur at just ~0.01% of sites in well-assembled genic regions. In comparison, analyses of the previously assembled draft C. remanei genome [19] found allelic dimorphism for 4.7% of defined C. elegans orthologous genes and a sizable portion of DNA aligning to the C. elegans Chromosome IV (~10% of the total genome). Unfortunately, cryptic reproductive incompatibilities between PX356 and PX439 led to significant segregation distortion for several linkage groups in our genetic map. Overall, our assembly appears to provide good coverage for linkage groups orthologous to C. elegans Chromosomes II, IV, and X, with more fragmented coverage of Chromosomes I, III, and V (Fig 2). Nevertheless, gene assemblies within these large fragments are excellent. This therefore represents the first well-assembled genome from a highly polymorphic outcrossing species from this group. When looking at the evolution of genome structure we concentrate on the subset of well-assembled chromosomes, while when looking at the evolution of gene structure, we include the entire genome assembly.


Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes.

Fierst JL, Willis JH, Thomas CG, Wang W, Reynolds RM, Ahearne TE, Cutter AD, Phillips PC - PLoS Genet. (2015)

Whole chromosome comparisons among C. elegans, C. briggsae, and C. remanei.The C. remanei The linkage map was sufficient to assemble and order 98.93% of the scaffolds with orthologous genes aligning to C. elegans chromosome X, 78.38% of the scaffolds with orthologous genes aligning to C. elegans chromosome II and 81.40% of the scaffolds with orthologous genes aligning to C. elegans chromosome IV. (a) C. remanei linkage groups were assigned to chromosomes based on gene orthology to C. elegans chromosomes. Reproductive incompatibility between the C. remanei strains used to construct the linkage map resulted in over-dispersion of the linkage map and 13 linkage groups instead of the 6 chromosomes expected (both C. elegans and C. briggsae have 6 chromosomes, respectively). (b) The cumulative size and orthologous gene alignments for scaffolds that were not assigned to linkage groups. c-e) Orthologous gene alignments indicated blocks of syntenic DNA between C. elegans, C. briggsae, and C. remanei. The panels c-e show orthologous genes on chromosomes X, II, and IV, with chromosome size scaled to linkage group size in C. remanei (X 18.5Mb, II 12.5Mb, IV 14.5 Mb). Orthologous genes were connected between species pairs, and grouped together if the genes were within 50,000 nucleotides of each other. Single gene translocations were excluded for clarity. Green indicates orthologs identified between C. elegans and C. remanei, blue indicates orthologs identified between C. remanei and C. briggsae, and grey indicates orthologs identified between C. briggsae and C. elegans. The outer rings are chromosomes X, II, and IV in each species. Each gray line is an orthologous gene located on the same chromosome in the other species and each black line is an orthologous gene that is located on a different chromosome in one of the other species. There are few blocks of interchromosomal translocation, and few black lines. White indicates regions of the chromosome where there were no orthologous genes identified between the species. (c) There was a large region of divergence (roughly 3.6Mb) on the C. remanei X; (d) Chromosome II is not completely assembled in C. remanei, and there were several regions of C. elegans and C. briggsae chromosome II that were not represented in C. remanei; (e) Chromosome IV.
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pgen.1005323.g002: Whole chromosome comparisons among C. elegans, C. briggsae, and C. remanei.The C. remanei The linkage map was sufficient to assemble and order 98.93% of the scaffolds with orthologous genes aligning to C. elegans chromosome X, 78.38% of the scaffolds with orthologous genes aligning to C. elegans chromosome II and 81.40% of the scaffolds with orthologous genes aligning to C. elegans chromosome IV. (a) C. remanei linkage groups were assigned to chromosomes based on gene orthology to C. elegans chromosomes. Reproductive incompatibility between the C. remanei strains used to construct the linkage map resulted in over-dispersion of the linkage map and 13 linkage groups instead of the 6 chromosomes expected (both C. elegans and C. briggsae have 6 chromosomes, respectively). (b) The cumulative size and orthologous gene alignments for scaffolds that were not assigned to linkage groups. c-e) Orthologous gene alignments indicated blocks of syntenic DNA between C. elegans, C. briggsae, and C. remanei. The panels c-e show orthologous genes on chromosomes X, II, and IV, with chromosome size scaled to linkage group size in C. remanei (X 18.5Mb, II 12.5Mb, IV 14.5 Mb). Orthologous genes were connected between species pairs, and grouped together if the genes were within 50,000 nucleotides of each other. Single gene translocations were excluded for clarity. Green indicates orthologs identified between C. elegans and C. remanei, blue indicates orthologs identified between C. remanei and C. briggsae, and grey indicates orthologs identified between C. briggsae and C. elegans. The outer rings are chromosomes X, II, and IV in each species. Each gray line is an orthologous gene located on the same chromosome in the other species and each black line is an orthologous gene that is located on a different chromosome in one of the other species. There are few blocks of interchromosomal translocation, and few black lines. White indicates regions of the chromosome where there were no orthologous genes identified between the species. (c) There was a large region of divergence (roughly 3.6Mb) on the C. remanei X; (d) Chromosome II is not completely assembled in C. remanei, and there were several regions of C. elegans and C. briggsae chromosome II that were not represented in C. remanei; (e) Chromosome IV.
Mentions: We estimated residual polymorphism in our inbred PX356 strain to occur at just ~0.01% of sites in well-assembled genic regions. In comparison, analyses of the previously assembled draft C. remanei genome [19] found allelic dimorphism for 4.7% of defined C. elegans orthologous genes and a sizable portion of DNA aligning to the C. elegans Chromosome IV (~10% of the total genome). Unfortunately, cryptic reproductive incompatibilities between PX356 and PX439 led to significant segregation distortion for several linkage groups in our genetic map. Overall, our assembly appears to provide good coverage for linkage groups orthologous to C. elegans Chromosomes II, IV, and X, with more fragmented coverage of Chromosomes I, III, and V (Fig 2). Nevertheless, gene assemblies within these large fragments are excellent. This therefore represents the first well-assembled genome from a highly polymorphic outcrossing species from this group. When looking at the evolution of genome structure we concentrate on the subset of well-assembled chromosomes, while when looking at the evolution of gene structure, we include the entire genome assembly.

Bottom Line: 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.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.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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon, United States of America.

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.

No MeSH data available.