A Novel Sperm-Delivered Toxin Causes Late-Stage Embryo Lethality and Transmission Ratio Distortion in C. elegans

Abstract

A sperm-delivered toxin and an embryo-expressed antidote form a co-adapted gene complex in C. elegans that promotes its own transmission to the detriment of organisms carrying it.

A New Player in the Spermiogenesis Pathway of Caenorhabditis elegans

“…It appears at approximately the same time that the FB-MOs begin to form and initially colocalizes with PEEL-1::GFP, an FB-MO label (Seidel et al 2011). Further, early SPE-47::mCherry localization was disrupted in a mutant with no FBs (spe-6 KO; Varkey et al 1993) but was normal in a mutant with no MOs (spe-39 KO; Zhu and L'Hernault 2003), suggesting that SPE-47 associates specifically with the FB.…”

“…Instead, the observed pattern of fluorescence bears striking resemblance to that of the FB-MOs during spermatogenesis (Kulkarni et al 2012). We created a double reporter strain, combining SPE-47::mCherry with a PEEL-1::GFP translational reporter that labels the MOs (Seidel et al 2011). Fluorescence from the two reporters overlaps in the early stage of expression, but the two appear separate by the stage at which the primary spermatocytes begin the first meiotic division (Figure 9), which is approximately the same stage at which they bud from the gonad rachis.…”

Sexually Antagonistic Zygotic Drive: A New Form of Genetic Conflict between the Sex Chromosomes

“…In worms (Caenorhabditis elegans), a molecular mechanism leading to zygotic drive was recently discovered. Here a zygotic driver is coded by a pair of tightly linked genes, in which an allele at one gene ( peel-1) produces a toxin, the driver locus, which is packaged in the sperm and transmitted to the zygote, whereas an allele at another gene (zeel-1) produces an antidote (the protective allele, which is expressed very early in development) that rescues only those embryos that inherit zeel-1 (and usually also the tightly linked driver, peel-1) (Seidel et al 2011). Zygotic drive on the autosomes is expected to be difficult to evolve-and therefore to be relatively rare in genomes-because it requires an improbable phenotype (i.e., a functionally coupled driver gene product and a responder gene sequence or product) and genotype (i.e., very close linkage between the loci coding for the driver and responder).…”

Reproductive isolation in the Elegans-Group of Caenorhabditis

“…As gastrulation is the earliest arrest stage observed in ElegansGroup hybrids, dysgenic interactions in these embryos likely involve at least one zygotically expressed gene. However, in this context it should be noted that in C. elegans, the paternally delivered PEEL-1 protein causes lethality well after the completion of gastrulation [60]. Embryonic elongation occurs during the later half of embryogenesis.…”

“…ElegansGroup hybrids that arrest at the onset of elongation likely have defects in epidermal development and those that arrest at the two-fold stage likely have defects in the development or function of the body wall musculature. PEEL-1-induced lethality in C. elegans intraspecific hybrids occurs at the two-fold stage and results from defects in muscular and epidermal tissues [60].…”