Sex Change by Gene Conversion in a <i>Caenorhabditis elegans fog-2</i> Mutant

Katju, Vaishali; LaBeau, Elisa M.; Lipinski, Kendra J.; Bergthorsson, Ulfar

doi:10.1534/genetics.108.090035

Cited by 34 publications

(67 citation statements)

References 29 publications

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“…Furthermore, a positive correlation between gene conversion and decelerated evolution (Supplemental Fig. S4) likely suggests a role of gene conversion in maintaining the functional integrity of redundant genes (Katju et al 2008;Marais et al 2010;Fawcett and Innan 2011). Although gene conversion often affects essential, highly constrained genes, we did not detect any significant difference in the levels of sequence conservation (represented by the sequence identity level between nonhybrid orthologs in T. asahii and T. faecale) between genes affected by gene conversion and those that were unaffected.…”

Section: Discussionmentioning

confidence: 70%

Global deceleration of gene evolution following recent genome hybridizations in fungi

Sriswasdi

Takashima

Manabe³

et al. 2016

Genome Res.

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Polyploidization events such as whole-genome duplication and inter-species hybridization are major evolutionary forces that shape genomes. Although long-term effects of polyploidization have been well-characterized, early molecular evolutionary consequences of polyploidization remain largely unexplored. Here, we report the discovery of two recent and independent genome hybridizations within a single clade of a fungal genus, Trichosporon. Comparative genomic analyses revealed that redundant genes are experiencing decelerations, not accelerations, of evolutionary rates. We identified a relationship between gene conversion and decelerated evolution suggesting that gene conversion may improve the genome stability of young hybrids by restricting gene functional divergences. Furthermore, we detected large-scale gene losses from transcriptional and translational machineries that indicate a global compensatory mechanism against increased gene dosages. Overall, our findings illustrate counteracting mechanisms during an early phase of post-genome hybridization and fill a critical gap in existing theories on genome evolution. [Supplemental material is available for this article.]Polyploidization events such as whole-genome duplication (WGD) and inter-species hybridization are major evolutionary forces that shape eukaryotic genomes (Dehal and Boore 2005;Scannell et al. 2007;Sémon and Wolfe 2007;Jaillon et al. 2009; Van de Peer et al. 2009). Ohno (1970 proposed an important theory that explains the enhanced evolutionary capability of polyploid genomes, stating that the emergence of functionally redundant genes would relax their evolutionary constraints and accelerate divergent evolution of their functions. This theory has been confirmed in a wide range of eukaryotes from ancient Vertebrata (Brunet et al. 2006), Saccharomycetaceae fungi (Kellis et al. 2004;Byrne and Wolfe 2007), Paramecia (McGrath et al. 2014), and Brassicaceae plants (Arabidopsis Genome Initiative 2000;Vision et al. 2000). Nonetheless, although these studies established long-term benefits of polyploidization, early consequences and mechanisms of polyploidization remain largely unexplored.Genome hybridization, in contrast to WGD, which is a rare event, is estimated to occur in >25% of plant and 10% of animal species (Mallet 2005) and generally involves younger species. In fungi, a multitude of hybrids have given rise to species that are instrumental in industrial fermentation and critical plant and animal pathogens. Furthermore, in addition to the issue of globally increased gene dosage that is common between WGD and genome hybridization, a hybrid species has to resolve the issue of incompatible genes and proteins encoded by its two parental genomes. Recent analyses of several fungal hybrids have revealed mechanisms such as extensive loss of heterozygosity Louis et al. 2012;Stukenbrock et al. 2012) and gene expression reprogramming (Tirosh et al. 2009) that may help hybrid genomes stabilize. Gene conversion, which is capable of homogenizing redundant paralogs...

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Section: Discussionmentioning

confidence: 70%

Global deceleration of gene evolution following recent genome hybridizations in fungi

Sriswasdi

Takashima

Manabe³

et al. 2016

Genome Res.

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“…Barring mutation in sex determination [29,55,88,89], maintenance of androdioecy in C. elegans depends on the male reproductive success relative to the hermaphrodite reproductive success (α), on the embryo to maturity survivorship difference between hermaphrodites and males (σ), on the proportion of non-cross-fertilised oocytes that are self-fertilised (β) and on inbreeding depression for fitness components (δ). C. elegans hermaphrodites are protandrous in that they first produce sperm and then irreversibly switch to oogenesis upon reproductive maturation [78].…”

Section: Modelling the Evolution Of The Fitness Components Of Outcrosmentioning

confidence: 99%

Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans

et al. 2014

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Background: Evolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems. The hypothesis of 'reproductive assurance' suggests that transitions to selfing occur because selfers that are able to reproduce on their own ensure the persistence of populations in environments where mates or pollination agents are unavailable. Here we test this hypothesis by performing experimental evolution in Caenorhabditis elegans. Results: We show that self-compatible hermaphrodites provide reproductive assurance to a male-female population facing a novel environment where outcrossing is limiting. Invasions of hermaphrodites in male-female populations, and subsequent experimental evolution in the novel environment, led to successful transitions to selfing and adaptation. Adaptation was not due to the loss of males during transitions, as shown by evolution experiments in exclusively hermaphroditic populations and in male-hermaphrodite populations. Instead, adaptation was due to the displacement of females by hermaphrodites. Genotyping of single-nucleotide polymorphisms further indicated that the observed evolution of selfing rates was not due to selection of standing genetic diversity. Finally, numerical modelling and evolution experiments in male-female populations demonstrate that the improvement of male fitness components may diminish the opportunity for reproductive assurance. Conclusions: Our findings support the hypothesis that reproductive assurance can drive the transition from outcrossing to selfing, and further suggest that the success of transitions to selfing hinges on adaptation of obligate outcrossing populations to the environment where outcrossing was once a limiting factor.

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“…In experimental populations of C. elegans , a gene conversion event led to the repair of a loss-of-function mutation with an extreme phenotypic consequence of sex reversion [39]. C. elegans is one of two species in its genus exhibiting an androdioecious mode of reproduction with populations composed largely of self-fertile hermaphrodites and males in low-frequency [57].…”

Section: Population-genetic and Phenotypic Effects Of Interlocus Gmentioning

confidence: 99%

Genomic and Population-Level Effects of Gene Conversion in Caenorhabditis Paralogs

Katju¹,

Bergthorsson²

2010

Genes

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Interlocus gene conversion, the nonreciprocal exchange of genetic material between genes, is facilitated by high levels of sequence identity between DNA sequences and has the dual effect of homogenizing intergenic sequences while increasing intragenic variation. Gene conversion can have important consequences for the evolution of paralogs subsequent to gene duplication, as well as result in misinterpretations regarding their evolution. We review the current state of research on gene conversion in paralogs within Caenorhabditis elegans and its congeneric species, including the relative rates of gene conversion, the range of observable conversion tracts, the genomic variables that strongly influence the frequency of gene conversion and its contribution to concerted evolution of multigene families. Additionally, we discuss recent studies that examine the phenotypic and population-genetic effects of interlocus gene conversion between the sex-determination locus fog-2 and its paralog ftr-1 in natural and experimental populations of C. elegans. In light of the limitations of gene conversion detection methods that rely solely on the statistical distribution of identical nucleotides between paralogs, we suggest that analyses of gene conversion in C. elegans take advantage of mutation accumulation experiments and sequencing projects of related Caenorhabditis species.

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Sex Change by Gene Conversion in a Caenorhabditis elegans fog-2 Mutant

Cited by 34 publications

References 29 publications

Global deceleration of gene evolution following recent genome hybridizations in fungi

Global deceleration of gene evolution following recent genome hybridizations in fungi

Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans

Genomic and Population-Level Effects of Gene Conversion in Caenorhabditis Paralogs

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