Uncovered: A new mode of reproduction that produces chimeric males in yellow crazy ants

Male yellow crazy ants (Anoplolepis gracilipes) are chimeras of two separate genetic lineages, researchers report in a study that reveals a unique mode of reproduction in this species – one previously unknown to science. While most multicellular organisms develop from a single-cell zygote into a collection of genetically identical cells – a hallmark of biological inheritance – the new findings show that yellow crazy ants deviate from this expectation. According to the study, all male yellow crazy ants are instead composed of haploid cells with two district genetic compositions. “Although chimeras have been described before in a number of species, including marmosets and humans, the regular production of chimeras from single fertilization events has not previously been reported,” writes Daniel Kronauer in a related Perspective. The yellow crazy ant is one of the plant’s most problematic invasive species. Previous genetic studies of this species have revealed unresolved discrepancies between queen, male, and worker genotypes. To better understand these observations, Hugo Darras and colleagues used population genetic and phylogeographic approaches on ants sampled from across southeast Asia and found that two interdependent genetic lineages (R and W) coexist within crazy yellow ant populations. Queens always have R/R genotypes and eggs fertilized by W sperm develop into female R/W workers. However, according to the findings, eggs fertilized by W sperm can also develop into males, but unlike in female-destined eggs, there is no fusion between the maternal and parental nuclei. Instead, the parental nuclei divide independently within the same egg, producing chimeric males with bodies composed of both haploid R and W cells. While chimerism has been observed in a wide range of species, it usually stems from rare developmental accidents or the fusion of separate individuals later in development. The new findings demonstrate an obligate form of chimerism that occurs at the onset of development to produce the male of the A. gracilipes species. Darras et al. suggest that this unusual mode of reproduction may be associated with a genetic conflict between two co-occurring genetic lineages over representation in the germ line. In the Perspective, Kronauer briefly addresses why such a complicated reproductive system could contribute to the success of these ants as invasive species—including that it may prevent inbreeding depression and ensure that W genomes remain in circulation.

A related podcast will be available at https://www.science.org/podcasts on Thursday, April 6.