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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.


Comparison of intergenic spaces between autosomes and X chromosomes.(a) Kernel smoothed distribution of intergenic spaces across the entire genome for C. elegans, C. briggsae and C. remanei. (b) Intergenic spaces differ between autosomes and the X chromosome in C. briggsae (Kruskal-Wallis χ2 = 556.09, df = 1, p < 2x10−16), C. elegans (Kruskal-Wallis χ2 = 476.32, df = 1, p < 2x10−16) and C. remanei (Kruskal-Wallis χ2 = 76.76, df = 1, p < 2x10−16). The boxplot indicates the bottom and top quartiles (black lines), middle quartiles (blue boxes), and median value (central notch) with outliers are shown as black dots. Intergenic spaces differ significantly between species on autosomes (Kruskal-Wallis χ2 = 328.4957; df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 2x10−16, C. remanei:C. briggsaep < 0.039; C. briggsae:C. elegansp < 2x10−16) and the X chromosome (Kruskal-Wallis χ2 = 112.52, df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 1.6x10−7, C. remanei:C. briggsaep < 2x10−16; C. briggsae:C. elegansp < 0.0005).
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pgen.1005323.g003: Comparison of intergenic spaces between autosomes and X chromosomes.(a) Kernel smoothed distribution of intergenic spaces across the entire genome for C. elegans, C. briggsae and C. remanei. (b) Intergenic spaces differ between autosomes and the X chromosome in C. briggsae (Kruskal-Wallis χ2 = 556.09, df = 1, p < 2x10−16), C. elegans (Kruskal-Wallis χ2 = 476.32, df = 1, p < 2x10−16) and C. remanei (Kruskal-Wallis χ2 = 76.76, df = 1, p < 2x10−16). The boxplot indicates the bottom and top quartiles (black lines), middle quartiles (blue boxes), and median value (central notch) with outliers are shown as black dots. Intergenic spaces differ significantly between species on autosomes (Kruskal-Wallis χ2 = 328.4957; df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 2x10−16, C. remanei:C. briggsaep < 0.039; C. briggsae:C. elegansp < 2x10−16) and the X chromosome (Kruskal-Wallis χ2 = 112.52, df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 1.6x10−7, C. remanei:C. briggsaep < 2x10−16; C. briggsae:C. elegansp < 0.0005).

Mentions: Intergenic distances vary widely within Caenorhabditis genomes, with some genes located in co-transcribed operons that are separated by a few nucleotides and other genes separated by many kilobases of sequence. Autosomal intergenic spacing for C. remanei exceeded that of both C. briggsae and C. elegans, despite these being lower bound values for C. remanei because of the potential for unincluded, unassembled regions probably underestimate C. remanei intergenic distances (Fig 3; Table 2). Across the entire genome (including scaffolds not included in linkage groups) the total intergenic content of C. remanei was 0.79Mb larger than that of C. briggsae and 10.73Mb larger than that of C. elegans.


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)

Comparison of intergenic spaces between autosomes and X chromosomes.(a) Kernel smoothed distribution of intergenic spaces across the entire genome for C. elegans, C. briggsae and C. remanei. (b) Intergenic spaces differ between autosomes and the X chromosome in C. briggsae (Kruskal-Wallis χ2 = 556.09, df = 1, p < 2x10−16), C. elegans (Kruskal-Wallis χ2 = 476.32, df = 1, p < 2x10−16) and C. remanei (Kruskal-Wallis χ2 = 76.76, df = 1, p < 2x10−16). The boxplot indicates the bottom and top quartiles (black lines), middle quartiles (blue boxes), and median value (central notch) with outliers are shown as black dots. Intergenic spaces differ significantly between species on autosomes (Kruskal-Wallis χ2 = 328.4957; df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 2x10−16, C. remanei:C. briggsaep < 0.039; C. briggsae:C. elegansp < 2x10−16) and the X chromosome (Kruskal-Wallis χ2 = 112.52, df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 1.6x10−7, C. remanei:C. briggsaep < 2x10−16; C. briggsae:C. elegansp < 0.0005).
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pgen.1005323.g003: Comparison of intergenic spaces between autosomes and X chromosomes.(a) Kernel smoothed distribution of intergenic spaces across the entire genome for C. elegans, C. briggsae and C. remanei. (b) Intergenic spaces differ between autosomes and the X chromosome in C. briggsae (Kruskal-Wallis χ2 = 556.09, df = 1, p < 2x10−16), C. elegans (Kruskal-Wallis χ2 = 476.32, df = 1, p < 2x10−16) and C. remanei (Kruskal-Wallis χ2 = 76.76, df = 1, p < 2x10−16). The boxplot indicates the bottom and top quartiles (black lines), middle quartiles (blue boxes), and median value (central notch) with outliers are shown as black dots. Intergenic spaces differ significantly between species on autosomes (Kruskal-Wallis χ2 = 328.4957; df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 2x10−16, C. remanei:C. briggsaep < 0.039; C. briggsae:C. elegansp < 2x10−16) and the X chromosome (Kruskal-Wallis χ2 = 112.52, df = 2, p < 2x10−16; Bonferroni-adjusted Pairwise Wilcoxon Rank Sum C. remanei:C. elegansp < 1.6x10−7, C. remanei:C. briggsaep < 2x10−16; C. briggsae:C. elegansp < 0.0005).
Mentions: Intergenic distances vary widely within Caenorhabditis genomes, with some genes located in co-transcribed operons that are separated by a few nucleotides and other genes separated by many kilobases of sequence. Autosomal intergenic spacing for C. remanei exceeded that of both C. briggsae and C. elegans, despite these being lower bound values for C. remanei because of the potential for unincluded, unassembled regions probably underestimate C. remanei intergenic distances (Fig 3; Table 2). Across the entire genome (including scaffolds not included in linkage groups) the total intergenic content of C. remanei was 0.79Mb larger than that of C. briggsae and 10.73Mb larger than that of C. elegans.

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.