Revisiting the hymenopteran diploid male vortex: A review of avoidance mechanisms and incidence

All hymenopterans (bees, ants, wasps, and sawflies) have haplodiploid sex determination. Generally, this involves haploid males developing from unfertilized eggs and diploid females developing from fertilized eggs, but diploid male production (DMP) frequently occurs. Some species have complementary sex determination (CSD), in which heterozygotes of a csd locus or loci are diploid females, hemizygotes are haploid males, and homozygotes are typically sterile diploid males. These diploid males underlie the diploid male vortex (DMV), the phenomenon of inbreeding reducing csd allelic diversity and causing increasingly higher production of sterile diploid males until the population dies out. The DMV has been cited as an extinction risk for many species across the order and a danger to both human-controlled and natural hymenopteran populations important in biological control, pollination, and endangered species conservation. However, it has been unclear how frequently it occurs. We review the known mechanisms for DMV avoidance. Many of these mechanisms are linked to lifestyle, and so we structure our investigation around eusocial lifestyle and non-eusocial (solitary or gregarious) species. We also review documented DMV incidence to make an inference about its prevalence. There are many means to avoid inbreeding or diploid male production, including eusocial-exclusive polygyny, polyandry, and diploid queen execution. For both eusocial and non-eusocial species these include biological mechanisms such as multi-locus CSD or non-CSD sex determination, diploid male inviability or brood removal, partial diploid male fecundity, and mating avoidance of kin or diploid males; or population genetic mechanisms such as gene flow and dispersal, balancing selection of csd alleles (with some being more prominent in eusocial vs. non-eusocial species). Documented cases of DMV are uncommon, and incidence is often tied to exacerbatory conditions such as habitat fragmentation and host declines. With this review we suggest that due to numerous avoidance mechanisms, DMV risk may not be as high as previously believed, and requires specific circumstances. In doing so we aim to better inform hymenopteran breeding and conservation efforts.