A Toxin-Antidote Selfish Element Increases Fitness of its Host

Selfish genetic elements can promote their transmission at the expense of individual survival, creating conflict between the element and the rest of the genome. Recently, a large number of toxin-antidote (TA) post-segregation distorters have been identified in non-obligate outcrossing nematodes. Their origin and the evolutionary forces that keep them at intermediate population frequencies are poorly understood. Here, we study a TA element in C. elegans called peel-1/zeel-1. Two major haplotypes of this locus, with and without the selfish element, segregate in C. elegans. Here we study the fitness consequences of the peel-1/zeel-1 element outside of its role in gene drive in non-outcrossing animals. We demonstrate that loss of the toxin peel-1 decreased fitness of hermaphrodites and resulted in reductions in fecundity and body size. This fitness advantage is independent of the antidote zeel-1, suggesting that a distinct peel-1 pathway plays a biological role. This work demonstrates that a TA element can provide a fitness benefit to its hosts, either during their initial evolution or by being co-opted by the animals following their selfish spread. These findings guide our understanding on how TA elements can remain in a population where gene drive is minimized, helping resolve the mystery of prevalent TA elements in selfing animals.