QTL Mapping of Sex Determination Loci Supports an Ancient Pathway in Ants and Honey Bees

Abstract

Sex determination mechanisms play a central role in life-history characteristics, affecting mating systems, sex ratios, inbreeding tolerance, etc. Downstream components of sex determination pathways are highly conserved, but upstream components evolve rapidly. Evolutionary dynamics of sex determination remain poorly understood, particularly because mechanisms appear so diverse. Here we investigate the origins and evolution of complementary sex determination (CSD) in ants and bees. The honey bee has a well-characterized CSD locus, containing tandemly arranged homologs of the transformer gene [complementary sex determiner (csd) and feminizer (fem)]. Such tandem paralogs appear frequently in aculeate hymenopteran genomes. However, only comparative genomic, but not functional, data support a broader role for csd/fem in sex determination, and whether species other than the honey bee use this pathway remains controversial. Here we used a backcross to test whether csd/fem acts as a CSD locus in an ant (Vollenhovia emeryi). After sequencing and assembling the genome, we computed a linkage map, and conducted a quantitative trait locus (QTL) analysis of diploid male production using 68 diploid males and 171 workers. We found two QTLs on separate linkage groups (CsdQTL1 and CsdQTL2) that jointly explained 98.0% of the phenotypic variance. CsdQTL1 included two tandem transformer homologs. These data support the prediction that the same CSD mechanism has indeed been conserved for over 100 million years. CsdQTL2 had no similarity to CsdQTL1 and included a 236-kb region with no obvious CSD gene candidates, making it impossible to conclusively characterize it using our data. The sequence of this locus was conserved in at least one other ant genome that diverged >75 million years ago. By applying QTL analysis to ants for the first time, we support the hypothesis that elements of hymenopteran CSD are ancient, but also show that more remains to be learned about the diversity of CSD mechanisms.

Balancing selection maintains sex determining alleles in multiple‐locus complementary sex determination

“…Though the idea that species may have more than one CSD locus was first proposed over 80 years ago (Snell ; Crozier ), the identification of species with ml ‐CSD has only occurred recently (de Boer et al. ; ; Miyakawa and Mikheyev ; Paladino et al. ).…”

“…Though the idea that species may have more than one CSD locus was first proposed over 80 years ago (Snell 1935;Crozier 1971), the identification of species with ml-CSD has only occurred recently Miyakawa and Mikheyev 2015;Paladino et al 2015). It seems reasonable to expect ml-CSD will be identified in many other hymenopteran species as molecular and statistical techniques improve.…”

“…; ; Paladino et al. ; Miyakawa and Mikheyev ). Populations with ml‐ CSD may have substantially lower rates of diploid male production than comparable sl ‐CSD populations (Crozier ; de Boer et al.…”

“…The population genetics of CSD and the associated consequences for population growth are best understood in species with a single CSD locus (sl-CSD) (Yokoyama and Nei 1979;Stouthamer et al 1992;Zayed and Packer 2005;Hasselmann et al 2008); a group that includes the well-studied honey bee (Apis mellifera). However, an increasing number of hymenopteran species are now thought to have multiple-locus CSD (ml-CSD) where female development requires heterozygosity at just one of two or more independently functioning CSD loci Paladino et al 2015;Miyakawa and Mikheyev 2015). Populations with ml-CSD may have substantially lower rates of diploid male production than comparable sl-CSD populations (Crozier 1971;de Boer et al 2008) and may be less vulnerable to extinctions and more likely to establish from small populations.…”

Mapping of multiple complementary sex determination loci in a parasitoid wasp

“…In this paper, we focus on complementary sex determination (CSD), a genetic sex determination system found in many species of bees, ants and wasps where heterozygosity at one or multiple genetic regions determines the sex of the individual. 25 We identify multiple genetic regions in the parasitoid wasp species Lysiphlebus fabarum that are likely underlying CSD. We show that these candidate CSD regions share no similarity with each other and that they differ from the CSD region known in the honey April 26, 2019 1/21 bee, the only species with a well-characterized CSD system.…”