Interpreting Morphological Adaptations Associated with Viviparity in the Tsetse Fly Glossina morsitans (Westwood) by Three-Dimensional Analysis

Abstract

Tsetse flies (genus Glossina), the sole vectors of African trypanosomiasis, are distinct from most other insects, due to dramatic morphological and physiological adaptations required to support their unique biology. These adaptations are driven by demands associated with obligate hematophagy and viviparous reproduction. Obligate viviparity entails intrauterine larval development and the provision of maternal nutrients for the developing larvae. The reduced reproductive capacity/rate associated with this biology results in increased inter- and intra-sexual competition. Here, we use phase contrast microcomputed tomography (pcMicroCT) to analyze morphological adaptations associated with viviparous biology. These include (1) modifications facilitating abdominal distention required during blood feeding and pregnancy, (2) abdominal and uterine musculature adaptations for gestation and parturition of developed larvae, (3) reduced ovarian structure and capacity, (4) structural features of the male-derived spermatophore optimizing semen/sperm delivery and inhibition of insemination by competing males and (5) structural features of the milk gland facilitating nutrient incorporation and transfer into the uterus. Three-dimensional analysis of these features provides unprecedented opportunities for examination and discovery of internal morphological features not possible with traditional microscopy techniques and provides new opportunities for comparative morphological analyses over time and between species.

Incorporating effects of age on energy dynamics predicts nonlinear maternal allocation patterns in iteroparous animals

“…Tsetse are relatively long-lived flies, surviving up to three months in the wild [36][37][38], with the potential for allocation trade-offs between each birth similar to long-lived vertebrates [10,15,16]. Reproduction is highly costly for tsetse as mothers can give birth to offspring as large as themselves [36,39]. Maternal allocation is key for offspring survival [40,41], as there is no self-feeding after birth: larvae pupate, relying on maternal reserves until emerging as an adult 20-30 days later [38,42].…”

Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis

“…During the mating process, 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 – 6 ]. Because tsetse’s viviparous reproductive strategy results in the production of relatively few offspring, targeting reproduction can be a most effective approach to reduce tsetse populations.…”

Infection with endosymbiotic Spiroplasma disrupts tsetse (Glossina fuscipes fuscipes) metabolic and reproductive homeostasis

“…Despite the longer larval development period we observed for progeny of Spi + compared to Spimoms, the weight of pupal offspring deposited was similar between the two groups. Because female tsetse produce unusually few offspring (6)(7)(8) over the course of their lifespan (compared to other insects), an increase in GC length would likely result in a significant reduction in population size over time. In fact, infection with a trypanosome strain that induces a metabolically costly immune response also lengthens tsetse's GC by a duration similar to that (approximately 2 days) induced by infection with Spiroplasma [43].…”

“…83 Once in the female's uterus, this mixture forms into a proteinaceous spermatophore that 84 facilitates successful transfer of sperm into the spermathecae for long-term storage [2][3][4][5][6].…”