The Gene csd Is the Primary Signal for Sexual Development in the Honeybee and Encodes an SR-Type Protein

Abstract

Haplodiploid organisms comprise about 20% of animals. Males develop from unfertilized eggs while females are derived from fertilized eggs. The underlying mechanisms of sex determination, however, appear to be diverse and are poorly understood. We have dissected the complementary sex determiner (csd) locus in the honeybee to understand its molecular basis. In this species, csd acts as the primary sex-determining signal with several alleles segregating in populations. Males are hemizygous and females are heterozygous at this locus; nonreproducing diploid males occur when the locus is homozygous. We have characterized csd by positional cloning and repression analysis. csd alleles are highly variable and no transcription differences were found between sexes. These results establish csd as a primary signal that governs sexual development by its allelic composition. Structural similarity of csd with tra genes of Dipteran insects suggests some functional relation of what would otherwise appear to be unrelated sex-determination mechanisms.

The dice of fate: thecsdgene and how its allelic composition regulates sexual development in the honey bee,Apis mellifera

“…1,26) and some available molecular data from other dipteran species, such as Musca domestica and Ceratitis capitata (Fig. 5B shows the C. capitata case), (43)(44)(45) and how this relates to the sex-determining system of the honey bee, (9) which is estimated to have separated from the dipteran insects about 270 million years ago (Fig. 5C).…”

“…(9) The natural occurring trait of female and diploid males in an inbred cross ( Phylogenetic view of sex determination in the insect order Hymenoptera. (23,56) Superfamilies in which species with diploid males have been documented are shown in bold.…”

“…Together with my graduate student Martin Hasselmann, and with collaborators in the US (Robert Page's lab) and Norway (Stig Omholt's lab), we finally succeeded in identifying the gene responsible. (9) In this article, I will review the progress that we have made over recent years in understanding the molecular basis of the complementary initial signal. I will shed some light on the historical aspects of haplodiploid sex determination that spans 150 years of research, (10) from the discovery that unfertilised eggs develop into males (11) to the isolation of the underlying genetic element of complementary sex determination.…”

“…I will shed some light on the historical aspects of haplodiploid sex determination that spans 150 years of research, (10) from the discovery that unfertilised eggs develop into males (11) to the isolation of the underlying genetic element of complementary sex determination. (9) I will discuss the current state of ideas of how the initial signal is implemented in different allelic combinations and of how this may relate to the activation of a downstream pathway. Finally, I will discuss how our findings relate to what is know about the sex-determining cascade of D. melanogaster and the available data from other dipteran insects that should help to elucidate how regulatory hierarchies have evolved over the last 270 million years.…”

The evolution of sex ratios and sex-determining systems

“…Sex determination in honey bees and many other hymenopterans depends on the allelic composition of a single locus, although alternative molecular mechanisms also exist [54,55]. Females typically manipulate the fertilization process, which makes haplodiploidy flexible for sex ratio adaptations under maternal control.…”