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

Attardo, Geoffrey M.; Tam, Nicole; Parkinson, Dula; Mack, Lindsey K.; Zahnle, Xavier J.; Arguellez, Joceline; Takáč, Peter; Malacrida, Anna R.

doi:10.3390/insects11100651

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

Journal Article · Wed Sep 23 00:00:00 EDT 2020 · Insects

DOI:https://doi.org/10.3390/insects11100651· OSTI ID:2386995

; Tam, Nicole; ; ; ; Arguellez, Joceline; Takáč, Peter; Malacrida, Anna R.

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 Journal Article

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); Slovak Research and Development Agency; USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2386995

Alternate ID(s):: OSTI ID: 1765570

Journal Information:: Insects, Journal Name: Insects Journal Issue: 10 Vol. 11; ISSN INSEHI; ISSN 2075-4450

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Switzerland

Language:: English

References (40)

MicroCT for molecular imaging: Quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs Metscher, Brian D.; Müller, Gerd B. Developmental Dynamics, Vol. 240, Issue 10 https://doi.org/10.1002/dvdy.22733	journal	September 2011
The regulation of ovulation in the tsetse-fly,Glossina pallidipes Austen Odhiambo, Thomas R. Journal of Experimental Zoology, Vol. 177, Issue 4 https://doi.org/10.1002/jez.1401770406	journal	August 1971
Some effects of mating in female tsetse,Glossina austeni newst Ejezie, G. C.; Davey, K. G. Journal of Experimental Zoology, Vol. 200, Issue 2 https://doi.org/10.1002/jez.1402000211	journal	May 1977
Virtual memory palaces: immersion aids recall Krokos, Eric; Plaisant, Catherine; Varshney, Amitabh Virtual Reality, Vol. 23, Issue 1 https://doi.org/10.1007/s10055-018-0346-3	journal	May 2018
Composition of the gut contents of third-instar tsetse larvae (Glossina morsitans westwood) Cmelik, S. H. W.; Bursell, E.; Slack, Ella Comparative Biochemistry and Physiology, Vol. 29, Issue 1 https://doi.org/10.1016/0010-406X(69)91764-2	journal	April 1969
Lipid content and composition of the tse-tse fly, Glossina morsitans Westwood Cmelik, S. H. W.; Hurrell, D. P.; Lunat, M. Comparative Biochemistry and Physiology, Vol. 31, Issue 1 https://doi.org/10.1016/0010-406X(69)92169-0	journal	October 1969
Mating, insemination, and ovulation in the tsetse fly, Glossina morsitans Saunders, D. S.; Dodd, C. W. H. Journal of Insect Physiology, Vol. 18, Issue 2 https://doi.org/10.1016/0022-1910(72)90119-9	journal	February 1972
Dynamics of the pregnancy cycle in the tsetse Glossina morsitans Denlinger, David L.; Ma, Wei-Chun Journal of Insect Physiology, Vol. 20, Issue 6 https://doi.org/10.1016/0022-1910(74)90143-7	journal	June 1974
Mating, ovulation and oöcyte development in Glossina morsitans Saunders, D. S. Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 64, Issue 1 https://doi.org/10.1016/0035-9203(70)90241-5	journal	January 1970
Spermatophores in tsetse flies Pollock, J. N. Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 66, Issue 2 https://doi.org/10.1016/0035-9203(72)90182-4	journal	January 1972
Structural modulations in the tsetse fly milk gland during a pregnancy cycle Ma, Wei-Chun; Denlinger, David L.; Järlfors, Ulla Tissue and Cell, Vol. 7, Issue 2 https://doi.org/10.1016/0040-8166(75)90008-7	journal	January 1975
Nutrient transfer during the reproductive cycle in Glossina austeni newst.: Histology and histochemistry of the milk gland, fat body, and oenocytes Tobe, S. S.; Davey, K. G.; Huebner, E. Tissue and Cell, Vol. 5, Issue 4 https://doi.org/10.1016/S0040-8166(73)80050-3	journal	January 1973
Modulation of cortical activity in 2D versus 3D virtual reality environments: An EEG study Slobounov, Semyon M.; Ray, William; Johnson, Brian International Journal of Psychophysiology, Vol. 95, Issue 3 https://doi.org/10.1016/j.ijpsycho.2014.11.003	journal	March 2015
Analysis of milk gland structure and function in Glossina morsitans: Milk protein production, symbiont populations and fecundity Attardo, Geoffrey M.; Lohs, Claudia; Heddi, Abdelaziz Journal of Insect Physiology, Vol. 54, Issue 8 https://doi.org/10.1016/j.jinsphys.2008.06.008	journal	August 2008
Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia Briceño, R. D.; Eberhard, W. G. Journal of Insect Physiology, Vol. 55, Issue 11 https://doi.org/10.1016/j.jinsphys.2009.07.001	journal	November 2009
Physiology of tsetse flies ( Glossina spp.) (Diptera: Glossinidae): a review Langley, P. A. Bulletin of Entomological Research, Vol. 67, Issue 4 https://doi.org/10.1017/S0007485300006933	journal	December 1977
Experimental work on reproduction in the tsetse fly, Glossina palpalis Mellanby, Helen Parasitology, Vol. 29, Issue 1 https://doi.org/10.1017/S0031182000026263	journal	January 1937
The role of the choriothete in tsetse flies Roberts, Michael J. Parasitology, Vol. 64, Issue 1 https://doi.org/10.1017/S0031182000044619	journal	February 1972
Spermatophore of the tsetse, Glossina morsitans morsitans Westwood: an ultrastructural study Kokwaro, Elizabeth D.; Odhiambo, Thomas R. International Journal of Tropical Insect Science, Vol. 1, Issue 02 https://doi.org/10.1017/S1742758400000370	journal	June 1981
Ovaries of Glossina morsitans Saunders, D. S. Nature, Vol. 185, Issue 4706 https://doi.org/10.1038/185121b0	journal	January 1960
Sperm Transfer by Spermatophores in Glossina austeni Newstead Pollock, J. N. Nature, Vol. 225, Issue 5237 https://doi.org/10.1038/2251063b0	journal	March 1970
Secretory discharge and microflora of milk gland in tsetse flies Ma, Wei-Chun; Denlinger, David L. Nature, Vol. 247, Issue 5439 https://doi.org/10.1038/247301a0	journal	February 1974
Discovery of a sensory organ that coordinates lunge feeding in rorqual whales Pyenson, Nicholas D.; Goldbogen, Jeremy A.; Vogl, A. Wayne Nature, Vol. 485, Issue 7399 https://doi.org/10.1038/nature11135	journal	May 2012
The Spermatophore in Glossina morsitans morsitans: Insights into Male Contributions to Reproduction Scolari, Francesca; Benoit, Joshua B.; Michalkova, Veronika Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep20334	journal	February 2016
Mating induces an immune response and developmental switch in the Drosophila oviduct Kapelnikov, A.; Zelinger, E.; Gottlieb, Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 37 https://doi.org/10.1073/pnas.0710997105	journal	August 2008
Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning Mattei, Alexandra L.; Riccio, Mark L.; Avila, Frank W. Proceedings of the National Academy of Sciences, Vol. 112, Issue 27 https://doi.org/10.1073/pnas.1505797112	journal	June 2015
Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants Fredericksen, Maridel A.; Zhang, Yizhe; Hazen, Missy L. Proceedings of the National Academy of Sciences, Vol. 114, Issue 47 https://doi.org/10.1073/pnas.1711673114	journal	November 2017
TomoPy: a framework for the analysis of synchrotron tomographic data Gürsoy, Dogˇa; De Carlo, Francesco; Xiao, Xianghui Journal of Synchrotron Radiation, Vol. 21, Issue 5 https://doi.org/10.1107/S1600577514013939	journal	August 2014
Xi-cam : a versatile interface for data visualization and analysis Pandolfi, Ronald J.; Allan, Daniel B.; Arenholz, Elke Journal of Synchrotron Radiation, Vol. 25, Issue 4 https://doi.org/10.1107/S1600577518005787	journal	May 2018
Effects of Immersion on Visual Analysis of Volume Data Laha, B.; Sensharma, K.; Schiffbauer, J. D. IEEE Transactions on Visualization and Computer Graphics, Vol. 18, Issue 4 https://doi.org/10.1109/TVCG.2012.42	journal	April 2012
The control of receptivity and ovulation in the tsetse fly, Glossina morsitans Gillott, C.; Langley, P. A. Physiological Entomology, Vol. 6, Issue 3 https://doi.org/10.1111/j.1365-3032.1981.tb00271.x	journal	September 1981
The mating behaviour of tsetse flies (Glossina): a review Wall, R.; Langley, P. A. Physiological Entomology, Vol. 18, Issue 2 https://doi.org/10.1111/j.1365-3032.1993.tb00470.x	journal	June 1993
Major differences in the larval anatomy of the digestive and excretory systems of three Oestridae species revealed by micro‐CT Martín‐Vega, D.; Clark, B.; Ferrer, L. M. Medical and Veterinary Entomology, Vol. 35, Issue 1 https://doi.org/10.1111/mve.12476	journal	September 2020
The Obligate Mutualist Wigglesworthia glossinidia Influences Reproduction, Digestion, and Immunity Processes of Its Host, the Tsetse Fly Pais, Roshan; Lohs, Claudia; Wu, Yineng Applied and Environmental Microbiology, Vol. 74, Issue 19 https://doi.org/10.1128/AEM.00741-08	journal	August 2008
Volume relationships during the pregnancy cycle of the tsetse fly Glossina austeni Tobe, S. S.; Davey, K. G. Canadian Journal of Zoology, Vol. 50, Issue 7 https://doi.org/10.1139/z72-133	journal	July 1972
Adenotrophic Viviparity in Tsetse Flies: Potential for Population Control and as an Insect Model for Lactation Benoit, Joshua B.; Attardo, Geoffrey M.; Baumann, Aaron A. Annual Review of Entomology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev-ento-010814-020834	journal	January 2015
Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes Attardo, Geoffrey M.; Abd-Alla, Adly M. M.; Acosta-Serrano, Alvaro Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1768-2	journal	September 2019
Tsetse Control and Gambian Sleeping Sickness; Implications for Control Strategy Tirados, Inaki; Esterhuizen, Johan; Kovacic, Vanja PLOS Neglected Tropical Diseases, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pntd.0003822	journal	August 2015
Human African trypanosomiasis control: Achievements and challenges Aksoy, Serap; Buscher, Phillipe; Lehane, Mike PLOS Neglected Tropical Diseases, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pntd.0005454	journal	April 2017
Glossina austeni (Diptera: Glossinidae) Eradicated on the Island of Unguja, Zanzibar, Using the Sterile Insect Technique Vreysen, Marc J. B.; Saleh, Khalfan M.; Ali, Mashavu Y. Journal of Economic Entomology, Vol. 93, Issue 1 https://doi.org/10.1603/0022-0493-93.1.123	journal	February 2000

Similar Records

Effects of gamma irradiation on the midgut ultrastructure of Glossina palpalis subspecies

Journal Article · Mon May 01 00:00:00 EDT 1989 · Radiat. Res.; (United States) · OSTI ID:5764851

Influence of antibiotics on Glossina morsitans Westwood

Conference · Tue Dec 31 23:00:00 EST 1974 · OSTI ID:4191940

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Glossina
MicroCT
computed tomography
morphology
reproduction
trypanosomiasis
tsetse
viviparity

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

Citation Formats

References (40)

Similar Records

Related Subjects