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

1
Department of Entomology and Nematology, University of California, Davis, CA 95616, USA
2
Lawrence Berkeley National Lab., Berkeley, CA 94720, USA
3
Department of Animal Systematics, Institute of Zoology, Slovak Academy of Sciences, 84506 Bratislava, Slovakia
4
Scientica, Ltd., 831 06 Bratislava, Slovakia
5
Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, Italy
*
Author to whom correspondence should be addressed.
Insects 2020, 11(10), 651; https://doi.org/10.3390/insects11100651
Received: 4 September 2020 / Revised: 17 September 2020 / Accepted: 19 September 2020 / Published: 23 September 2020
(This article belongs to the Special Issue Advances in Diptera Biology)
Tsetse flies, the sole transmitters of African Sleeping Sickness parasites, have a unique reproductive biology. They only develop one offspring at a time, they carry that offspring in their uterus for its entire immature development and provide nourishment for that offspring via milk-like secretions. This specialized reproductive biology has required dramatic modifications to the morphology of the reproductive organs in these and related flies. Here, we use phase contrast micro-Computed Tomography (Micro-CT) to visualize these adaptations in three dimensions for the first time. These adaptations include cuticular modifications allowing increased abdominal volume, expanded abdominal and uterine musculature, reduced egg development capacity, structural features of the male seminal secretions and detailed visualization of the gland responsible for synthesis and secretion of “milk” to feed intrauterine larvae. The ability to examine these tissues within the context of the rest of the organ systems in the fly provides new functional insights into how these changes have facilitated the evolution of the mating and reproductive biology of these flies.
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. View Full-Text
Keywords: MicroCT; Glossina; tsetse; reproduction; morphology; computed tomography; viviparity; trypanosomiasis MicroCT; Glossina; tsetse; reproduction; morphology; computed tomography; viviparity; trypanosomiasis
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Attardo, G.M.; Tam, N.; Parkinson, D.; Mack, L.K.; Zahnle, X.J.; Arguellez, J.; Takáč, P.; Malacrida, A.R. Interpreting Morphological Adaptations Associated with Viviparity in the Tsetse Fly Glossina morsitans (Westwood) by Three-Dimensional Analysis. Insects 2020, 11, 651.

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