Abstract
Honey bee (Apis mellifera) queens have a remarkable organ, the spermatheca, which successfully stores sperm for years after a virgin queen mates. This study uniquely characterized and quantified the transcriptomes of the spermathecae from mated and virgin honey bee queens via RNA sequencing to identify differences in mRNA levels based on a queen’s mating status. The transcriptome of drone semen was analyzed for comparison. Samples from three individual bees were independently analyzed for mated queen spermathecae and virgin queen spermathecae, and three pools of semen from ten drones each were collected from three separate colonies. In total, the expression of 11,233 genes was identified in mated queen spermathecae, 10,521 in virgin queen spermathecae, and 10,407 in drone semen. Using a cutoff log2 fold-change value of 2.0, we identified 212 differentially expressed genes between mated and virgin spermathecal queen tissues: 129 (1.4% of total) were up-regulated and 83 (0.9% of total) were down-regulated in mated queen spermathecae. Three genes in mated queen spermathecae, three genes in virgin queen spermathecae and four genes in drone semen that were more highly expressed in those tissues from the RNA sequencing data were further validated by real time quantitative PCR. Among others, expression of Kielin/chordin-like and Trehalase mRNAs was highest in the spermathecae of mated queens compared to virgin queen spermathecae and drone semen. Expression of the mRNA encoding Alpha glucosidase 2 was higher in the spermathecae of virgin queens. Finally, expression of Facilitated trehalose transporter 1 mRNA was greatest in drone semen. This is the first characterization of gene expression in the spermathecae of honey bee queens revealing the alterations in mRNA levels within them after mating. Future studies will extend to other reproductive tissues with the purpose of relating levels of specific mRNAs to the functional competence of honey bee queens and the colonies they head.
Highlights
Success during sexual reproduction is achieved by the implementation of speciesand sex-specific strategies that involve direct contact between the male’s sperm and seminal fluid and the female’s eggs and the epithelial cells along the female’s reproductive tract
The purpose was to start to address the molecular mechanism through which honey bee queens store viable sperm for several years after mating
This is the first report of the complete transcriptome of the spermathecae of mated and virgin honey bee queens, in which over 10,000 genes were identified
Summary
Success during sexual reproduction is achieved by the implementation of speciesand sex-specific strategies that involve direct contact between the male’s sperm and seminal fluid and the female’s eggs and the epithelial cells along the female’s reproductive tract. The myriad of sperm storage organs that have evolved in fruit fly species in the genus Drosophila [5] have been optimized such that one male’s seminal fluid and accessory gland proteins increase the survival of all other males’ ejaculates collected by a female during mating [6,7]. In another dipteran species, the mosquito Aedes aegypti, females mate with only one male but store their mate’s sperm for a long period of time [8,9]. A recent RNA sequencing study of the spermatheca of virgin and mated A. aegypti females found eight spermatheca-specific transcripts that are responsible for the nourishment, maintenance and protection of male sperm [4]
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