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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.


Comparative analysis of protein diversity.(a) The 30 most significantly enriched protein domains (p < 0.001) in the C. remanei genome (as compared to the C. elegans genome), and the corresponding interproscan annotations across Caenorhabditis and P. pacificus. The value shown is scaled relative to the top protein domain identified in each species. The species are plotted in phylogenetic order and protein kinase domains, F-box domains, GPCRs, domain of unknown function 38, and protein of unknown function DUF3557 are found in low numbers outside the Elegans group. (b) The relative representation of each 7TM GPCR family across Caenorhabditis and P. pacificus. The species are plotted in phylogenetic order and each value is scaled relative to the top 7TM GPCR family identified in each species.
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pgen.1005323.g005: Comparative analysis of protein diversity.(a) The 30 most significantly enriched protein domains (p < 0.001) in the C. remanei genome (as compared to the C. elegans genome), and the corresponding interproscan annotations across Caenorhabditis and P. pacificus. The value shown is scaled relative to the top protein domain identified in each species. The species are plotted in phylogenetic order and protein kinase domains, F-box domains, GPCRs, domain of unknown function 38, and protein of unknown function DUF3557 are found in low numbers outside the Elegans group. (b) The relative representation of each 7TM GPCR family across Caenorhabditis and P. pacificus. The species are plotted in phylogenetic order and each value is scaled relative to the top 7TM GPCR family identified in each species.

Mentions: Caenorhabditis genomes have large numbers of nematode-specific and species-specific proteins [46], and high divergence makes it difficult to conclusively identify individual genes that are present in outcrossing Caenorhabditis but lost in the selfers. To accommodate this, we characterized functional divergence between self-fertile and outcrossing Caenorhabditis by analyzing putative protein domains in the genomes of Caenorhabditis and the distantly related P. pacificus (Fig 5). We found no functional groups that were significantly enriched in the outcrossing Caenorhabditis relative to the selfing Caenorhabditis. There are numerous species-specific differences, however. For example, we identified between 191 and 1,721 proteins with F-box domains (IPR001810) in C. briggsae, C. sinica, C. remanei, C. tropicalis, C. brenneri and C. elegans, 5–18 times as many as identified in C. japonica, C. angaria and P. pacificus.


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)

Comparative analysis of protein diversity.(a) The 30 most significantly enriched protein domains (p < 0.001) in the C. remanei genome (as compared to the C. elegans genome), and the corresponding interproscan annotations across Caenorhabditis and P. pacificus. The value shown is scaled relative to the top protein domain identified in each species. The species are plotted in phylogenetic order and protein kinase domains, F-box domains, GPCRs, domain of unknown function 38, and protein of unknown function DUF3557 are found in low numbers outside the Elegans group. (b) The relative representation of each 7TM GPCR family across Caenorhabditis and P. pacificus. The species are plotted in phylogenetic order and each value is scaled relative to the top 7TM GPCR family identified in each species.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482642&req=5

pgen.1005323.g005: Comparative analysis of protein diversity.(a) The 30 most significantly enriched protein domains (p < 0.001) in the C. remanei genome (as compared to the C. elegans genome), and the corresponding interproscan annotations across Caenorhabditis and P. pacificus. The value shown is scaled relative to the top protein domain identified in each species. The species are plotted in phylogenetic order and protein kinase domains, F-box domains, GPCRs, domain of unknown function 38, and protein of unknown function DUF3557 are found in low numbers outside the Elegans group. (b) The relative representation of each 7TM GPCR family across Caenorhabditis and P. pacificus. The species are plotted in phylogenetic order and each value is scaled relative to the top 7TM GPCR family identified in each species.
Mentions: Caenorhabditis genomes have large numbers of nematode-specific and species-specific proteins [46], and high divergence makes it difficult to conclusively identify individual genes that are present in outcrossing Caenorhabditis but lost in the selfers. To accommodate this, we characterized functional divergence between self-fertile and outcrossing Caenorhabditis by analyzing putative protein domains in the genomes of Caenorhabditis and the distantly related P. pacificus (Fig 5). We found no functional groups that were significantly enriched in the outcrossing Caenorhabditis relative to the selfing Caenorhabditis. There are numerous species-specific differences, however. For example, we identified between 191 and 1,721 proteins with F-box domains (IPR001810) in C. briggsae, C. sinica, C. remanei, C. tropicalis, C. brenneri and C. elegans, 5–18 times as many as identified in C. japonica, C. angaria and P. pacificus.

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.