Ubiquitous Selfish Toxin-Antidote Elements in Caenorhabditis Species

Ben-David, Eyal; Pliota, Pinelopi; Widen, Sonya A.; Koreshova, Alevtina; Lemus-Vergara, Tzitziki; Verpukhovskiy, Philipp; Mandali, Sridhar; Braendle, Christian; Burga, Alejandro; Kruglyak, Leonid

doi:10.1016/j.cub.2020.12.013

Cited by 31 publications

(80 citation statements)

References 59 publications

(83 reference statements)

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“…These haplotypes are hypothesized to be remnants of genetic diversity present in the outcrossing ancestor that has been maintained by long-term balancing selection since the evolution of selfing ( Thompson et al 2015 ; Lee et al 2021 ). Similar hyper-divergent regions have been reported in both C. briggsae ( Lee et al 2021 ) and C. tropicalis another related selfing Caenorhabditis species ( Ben-David et al 2021 ; Noble et al 2021 ). To quantify the genome-wide divergence between the three sequenced C. briggsae strains, we aligned the AF16 and VX34 reference genomes to QX1410, calculated alignment identity, and called variants (SNVs and indels).…”

Section: Resultssupporting

confidence: 80%

Chromosome-Level Reference Genomes for Two Strains of Caenorhabditis briggsae: An Improved Platform for Comparative Genomics

Stevens

Moya

Tanny

et al. 2022

Genome Biology and Evolution

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The publication of the Caenorhabditis briggsae reference genome in 2003 enabled the first comparative genomics studies between C. elegans and C. briggsae, shedding light on the evolution of genome content and structure in the Caenorhabditis genus. However, despite being widely used, the currently available C. briggsae reference genome is substantially less complete and structurally accurate than the C. elegans reference genome. Here, we used high-coverage Oxford Nanopore long-read and chromosome conformation capture data to generate chromosome-level reference genomes for two C. briggsae strains: QX1410, a new reference strain closely related to the laboratory AF16 strain, and VX34, a highly divergent strain isolated in China. We also sequenced 99 recombinant inbred lines (RILs) generated from reciprocal crosses between QX1410 and VX34 to create a recombination map and identify chromosomal domains. Additionally, we used both short- and long-read RNA sequencing (RNA-seq) data to generate high-quality gene annotations. By comparing these new reference genomes to the current reference, we reveal that hyper-divergent haplotypes cover large portions of the C. briggsae genome, similar to recent reports in C. elegans and C. tropicalis. We also show that the genomes of selfing Caenorhabditis species have undergone more rearrangement than their outcrossing relatives, which has biased previous estimates of rearrangement rate in Caenorhabditis. These new genomes provide a substantially improved platform for comparative genomics in Caenorhabditis and narrow the gap between the quality of genomic resources available for C. elegans and C. briggsae.

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Section: Resultssupporting

confidence: 80%

Chromosome-Level Reference Genomes for Two Strains of Caenorhabditis briggsae: An Improved Platform for Comparative Genomics

Stevens

Moya

Tanny

et al. 2022

Genome Biology and Evolution

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“…In short, when a genetic element drives, what prevents it from reaching fixation and becoming undetectable due to the lack of polymorphism? Maternal-effect post-segregational killers have been detected in ants [ 8 ], beetles [ 32 ], nematodes [ 33 ] and many bacteria, including endosymbionts [ 6 , 9 ]. In such systems, a maternally expressed toxin linked to a zygotically expressed antidote causes the death of progeny that did not inherit the element [ 9 , 34 ].…”

Section: Discussionmentioning

confidence: 99%

Unbalanced selection: the challenge of maintaining a social polymorphism when a supergene is selfish

Tafreshi

Otto

Chapuisat

2022

Phil. Trans. R. Soc. B

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Supergenes often have multiple phenotypic effects, including unexpected detrimental ones, because recombination suppression maintains associations among co-adapted alleles but also allows the accumulation of recessive deleterious mutations and selfish genetic elements. Yet, supergenes often persist over long evolutionary periods. How are such polymorphisms maintained in the face of selection, drive and drift? We present a population genetic model that investigates the conditions necessary for a stable polymorphic equilibrium when one of the supergene haplotypes is a selfish genetic element. The model fits the characteristics of the Alpine silver ant, Formica selysi , in which a large supergene underlies colony social organization, and one haplotype distorts Mendelian transmission by killing progeny that did not inherit it. The model shows that such maternal-effect killing strongly limits the maintenance of social polymorphism. Under random mating, transmission ratio distortion prevents rare single-queen colonies from invading populations of multiple-queen colonies, regardless of the fitness of each genotype. A stable polymorphic equilibrium can, however, be reached when high rates of assortative mating are combined with large fitness differences among supergene genotypes. The model reveals that the persistence of the social polymorphism is non-trivial and expected to occur only under restrictive conditions that deserve further empirical investigation. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

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“…These haplotypes are hypothesized to be remnants of genetic diversity present in the outcrossing ancestor that have been maintained by long-term balancing selection since the evolution of selfing (Thompson et al 2015;Lee et al 2021). Similar hyper-divergent regions have been reported in both C. briggsae (Lee et al 2021) and in the related selfing species, C. tropicalis (Noble et al 2021;Ben-David et al 2021). To quantify the genome-wide divergence between the three sequenced C. briggsae strains, we aligned the AF16 and VX34 reference genomes to QX1410, calculated alignment identity, and called variants (SNVs and indels).…”

Section: High Divergence Among the C Briggsae Reference Genomesmentioning

confidence: 54%

Chromosome-level reference genomes for two strains of Caenorhabditis briggsae: an improved platform for comparative genomics

Stevens¹,

Moya

Tanny

et al. 2021

Preprint

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The publication of the Caenorhabditis briggsae reference genome in 2003 enabled the first comparative genomics studies between C. elegans and C. briggsae, shedding light on the evolution of genome content and structure in the Caenorhabditis genus. However, despite being widely used, the currently available C. briggsae reference genome is substantially less complete and structurally accurate than the C. elegans reference genome. Here, we used high-coverage Oxford Nanopore long-read and chromosome conformation capture data to generate chromosomally resolved reference genomes for two C. briggsae strains: QX1410, a new reference strain closely related to the laboratory AF16 strain, and VX34, a highly divergent strain isolated in China. We also sequenced 99 recombinant inbred lines (RILs) generated from reciprocal crosses between QX1410 and VX34 to create a recombination map and identify chromosomal domains. Additionally, we used both short- and long-read RNA sequencing (RNA-seq) data to generate high-quality gene annotations. By comparing these new reference genomes to the current reference, we reveal that hyper-divergent haplotypes cover large portions of the C. briggsae genome, similar to recent reports in C. elegans and C. tropicalis. We also show that the genomes of selfing Caenorhabditis species have undergone more rearrangement than their outcrossing relatives, which has biased previous estimates of rearrangement rate in Caenorhabditis. These new genomes provide a substantially improved platform for comparative genomics in Caenorhabditis and narrow the gap between the quality of genomic resources available for C. elegans and C. briggsae.

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Ubiquitous Selfish Toxin-Antidote Elements in Caenorhabditis Species

Abstract: Highlights d Toxin-antidote elements (TAs) are present in all known Caenorhabditis selfing species d slow-1/grow-1 is a novel TA that causes developmental delay in C. tropicalis d TAs can antagonize each other, leading to more stable genetic incompatibilities

Cited by 31 publications

References 59 publications

Chromosome-Level Reference Genomes for Two Strains of Caenorhabditis briggsae: An Improved Platform for Comparative Genomics

Chromosome-Level Reference Genomes for Two Strains of Caenorhabditis briggsae: An Improved Platform for Comparative Genomics

Unbalanced selection: the challenge of maintaining a social polymorphism when a supergene is selfish

Chromosome-level reference genomes for two strains of Caenorhabditis briggsae: an improved platform for comparative genomics

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