A toxin-antidote selfish element increases fitness of its host

Elife. 2023 Oct 24:12:e81640. doi: 10.7554/eLife.81640.

Abstract

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 Caenorhabditis elegans called zeel-1;peel-1. Two major haplotypes of this locus, with and without the selfish element, segregate in C. elegans. We evaluate the fitness consequences of the zeel-1;peel-1 element outside of its role in gene drive in non-outcrossing animals and demonstrate that loss of the toxin peel-1 decreased fitness of hermaphrodites and resulted in reductions in fecundity and body size. These findings suggest a biological role for peel-1 beyond toxin lethality. 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.

Keywords: C. elegans; evolutionary biology; fitness; genomic conflict; selfish genetic elements; toxin-antidote elements.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antidotes
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans Proteins* / genetics
  • Fertility
  • Gene Frequency
  • Repetitive Sequences, Nucleic Acid
  • Toxins, Biological*

Substances

  • Antidotes
  • peel-1 protein, C elegans
  • Toxins, Biological
  • Caenorhabditis elegans Proteins