Mapping of multiple complementary sex determination loci in a parasitoid wasp

Abstract

Sex determination has evolved in a variety of ways and can depend on environmental and genetic signals. A widespread form of genetic sex determination is haplodiploidy, where unfertilized, haploid eggs develop into males and fertilized diploid eggs into females. One of the molecular mechanisms underlying haplodiploidy in Hymenoptera, a 5 large insect order comprising ants, bees and wasps, is known as complementary sex determination (CSD). In species with CSD, heterozygosity at one or several loci induces female development. Here, we identify the genomic regions putatively underlying multi-locus CSD in the parasitoid wasp Lysiphlebus fabarum using restriction-site associated DNA sequencing. By analysing segregation patterns at polymorphic sites 10 among 331 diploid males and females, we identify four CSD candidate regions, all on different chromosomes. None of the candidate regions feature evidence for homology with the csd gene from the honeybee, the only species in which CSD has been characterized, suggesting that CSD in L. fabarum is regulated via a novel molecular mechanism. Moreover, no homology is shared between the candidate loci, in contrast to 15 the idea that multi-locus CSD should emerge from duplications of an ancestral single-locus system. Taken together, our results suggest that the molecular mechanisms underlying CSD in Hymenoptera are not conserved between species, raising the question as to whether CSD may have evolved multiple times independently in the group. Author summary 20The genetic or environmental signals that govern whether an organism develops into a male or female differ across species, and understanding their evolution is a key aspect of biology. 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. Our results suggest a different molecular mechanism underlying CSD in the wasp and that multiple CSD 30 regions do not necessarily arise from duplications as generally thought.65 75 CSD regions, all on different chromosomes and of which three are close to putative centromeric regions. These loci feature no homology to each other or the known CSD locus in the honeybee, suggesting that the molecular mechanism underlying April 26, 2019 2/21 90 Such vestigial (haploid) male production is fairly common in asexuals [14,15]. Since our approach relies on the comparison of heterozygosity between diploid males and females, haploid males are not informative. Because haploid and diploid males are phenotypically identical in L. fabarum, we used 899 high confidence SNPs with a minimum s...

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

“…In contrast, there is no evidence of duplication in sex determination genes in L. fabarum. This supports the idea that complementary sex determination (CSD) in sexually reproducing L. fabarum populations is based on up-stream cues that differ from those known in other CSD species [101], whereas the CSD locus known from other hymenopterans is a paralog of transformer [102]. In addition to the core sex determination genes, we identified homologs of several genes related to sex determination ( Supplementary Table 18).…”

Conservation insights from wild bee genetic studies: Geographic differences, susceptibility to inbreeding, and signs of local adaptation

“…It is possible that in bees, multiple mechanisms of sex determination have evolved. In hymenopterans, three mechanisms are known, the single‐locus CSD in honey bees Apis mellifera (Hasselmann et al, 2008), multi‐locus CSD in the parasitoid wasp Lysiphlebus fabarum (Matthey‐Doret et al, 2019), and parental genome imprinting in the jewel wasp Nasonia vitripennis (Zou et al, 2020). An alternative mechanism to single‐locus CSD may explain why diploid males are at lower levels than expected in some inbred wild bee populations (Boff et al, 2014).…”

Absence of complementary sex determination in twoLeptopilinaspecies (Figitidae, Hymenoptera) and a reconsideration of its incompatibility with endosymbiont‐induced thelytoky

“…For the honeybee ( Apis mellifera ) an sl‐CSD locus has been identified (Beye et al ., 2003) and this csd gene is a duplication (paralog) of feminizer, the A. mellifera ortholog of transformer ( tra ) (Hasselmann et al ., 2008). No ml‐CSD loci have been characterized (but see Matthey‐Doret et al ., 2019 for an attempt).…”