Selfing is the safest sex for Caenorhabditis tropicalis

Abstract

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.

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

“…Consistent with recent findings in C. elegans and C. tropicalis (Lee et al 2021;Noble et al 2021), we find that hyper-divergent haplotypes are widespread across the genomes of all three C. briggsae strains (Fig. 3).…”

“…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).…”

“…In selfing Caenorhabditis species, evidence suggests that selective pressure to maintain linkage between coadapted alleles might lead to incompatibilities between interbreeding populations (Seidel et al 2008;Rockman and Kruglyak 2009;Ross et al 2011;Noble et al 2021). A strong departure from the neutral expectation in allele frequencies was observed in chromosomes I, II, and IV (Figure 2B).…”

“…Similarly, it is now possible to generate long-read RNA sequencing data to assemble full-length transcripts and substantially improve the quality of automated gene annotations. Substantially improved reference genomes generated using these technologies have recently been published for several nematode species, including for Caenorhabditis tropicalis and Caenorhabditis remanei (Noble et al 2021;Teterina et al 2020), Oscheius tipulae (Gonzalez de la Rosa et al 2021), and the ruminant parasite Haemonchus contortus (Doyle et al 2020). These technologies have even been used to identify and extend multiple repetitive regions that are collapsed in the C. elegans N2 reference genome (Tyson et al 2018;Yoshimura et al 2019), widely regarded as one of the highest quality eukaryotic reference genomes available.…”

Transcriptomic profiling of sex-specific olfactory neurons reveals subset-specific receptor expression inCaenorhabditis elegans

“…C. tropicalis, like C. elegans and C. briggsae, is a hermaphroditic Caenorhabditis species for which male mating is optional (NOBLE et al 2021). C. tropicalis encodes a reduced number of ascr#8 receptor gene paralogs, with no Cel-dmsr-12 paralogs, and only one Cel-srw-97 paralog (Figure 6).…”