Abstract
Tsetse flies (Glossina spp.) house a population-dependent assortment of microorganisms that can include pathogenic African trypanosomes and maternally transmitted endosymbiotic bacteria, the latter of which mediate numerous aspects of their host's metabolic, reproductive, and immune physiologies. One of these endosymbionts, Spiroplasma, was recently discovered to reside within multiple tissues of field captured and laboratory colonized tsetse flies grouped in the Palpalis subgenera. In various arthropods, Spiroplasma induces reproductive abnormalities and pathogen protective phenotypes. In tsetse, Spiroplasma infections also induce a protective phenotype by enhancing the fly's resistance to infection with trypanosomes. However, the potential impact of Spiroplasma on tsetse's viviparous reproductive physiology remains unknown. Herein we employed high-throughput RNA sequencing and laboratory-based functional assays to better characterize the association between Spiroplasma and the metabolic and reproductive physiologies of G. fuscipes fuscipes (Gff), a prominent vector of human disease. Using field-captured Gff, we discovered that Spiroplasma infection induces changes of sex-biased gene expression in reproductive tissues that may be critical for tsetse's reproductive fitness. Using a Gff lab line composed of individuals heterogeneously infected with Spiroplasma, we observed that the bacterium and tsetse host compete for finite nutrients, which negatively impact female fecundity by increasing the length of intrauterine larval development. Additionally, we found that when males are infected with Spiroplasma, the motility of their sperm is compromised following transfer to the female spermatheca. As such, Spiroplasma infections appear to adversely impact male reproductive fitness by decreasing the competitiveness of their sperm. Finally, we determined that the bacterium is maternally transmitted to intrauterine larva at a high frequency, while paternal transmission was also noted in a small number of matings. Taken together, our findings indicate that Spiroplasma exerts a negative impact on tsetse fecundity, an outcome that could be exploited for reducing tsetse population size and thus disease transmission.
Highlights
Tsetse flies (Glossina spp.), which vector pathogenic African trypanosomes, reproduce via a process called adenotrophic viviparity
To understand the potential effects of Spiroplasma infection on tsetse’s reproductive physiology, we compared the RNA sequencing (RNA-seq) data obtained from the male reproductive organs of Spiroplasma infected (GffSpi+) and uninfected (GffSpi-) individuals obtained from wild populations in Uganda
The variance in PC1 could be explained by differences in sex, with females clustering on the left side along the PC1 axis, and males clustering on the right side along the PC1 axis (Fig 1A)
Summary
Tsetse flies (Glossina spp.), which vector pathogenic African trypanosomes, reproduce via a process called adenotrophic viviparity. Female tsetse ovulate one oocyte per gonotrophic cycle (GC). Following the completion of larvigenesis, the mother gives birth to a fully developed 3rd instar larva that pupates within 30 minutes. This process repeats itself approximately every 10 days [1]. Male tsetse transfer seminal fluid (SF), which contains sperm as well as numerous male accessory gland (MAG) derived proteins, into the reproductive tract of receptive females. Once in the female’s uterus, this mixture forms into a proteinaceous spermatophore that facilitates successful transfer of sperm into the spermathecae for long-term storage [2,3,4,5,6]. The application of sterile male programs has been very successful with tsetse [8] and is currently endorsed to eliminate tsetse populations on the African continent [8,9]
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