{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T00:59:36Z","timestamp":1789174776677,"version":"build-2803163510"},"reference-count":47,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2020,9,23]],"date-time":"2020-09-23T00:00:00Z","timestamp":1600819200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100006492","name":"Division of Intramural Research, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["1R21AI128523-01A1"],"award-info":[{"award-number":["1R21AI128523-01A1"]}],"id":[{"id":"10.13039\/100006492","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000015","name":"U.S. Department of Energy","doi-asserted-by":"publisher","award":["ALS-11046"],"award-info":[{"award-number":["ALS-11046"]}],"id":[{"id":"10.13039\/100000015","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005357","name":"Agent\u00fara na Podporu V\u00fdskumu a V\u00fdvoja","doi-asserted-by":"publisher","award":["APVV-15-0604"],"award-info":[{"award-number":["APVV-15-0604"]}],"id":[{"id":"10.13039\/501100005357","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004493","name":"International Atomic Energy Agency","doi-asserted-by":"publisher","award":["D42015"],"award-info":[{"award-number":["D42015"]}],"id":[{"id":"10.13039\/501100004493","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>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.<\/jats:p>","DOI":"10.3390\/insects11100651","type":"journal-article","created":{"date-parts":[[2020,9,23]],"date-time":"2020-09-23T09:28:08Z","timestamp":1600853288000},"page":"651","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Interpreting Morphological Adaptations Associated with Viviparity in the Tsetse Fly Glossina morsitans (Westwood) by Three-Dimensional Analysis"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6265-2969","authenticated-orcid":false,"given":"Geoffrey M","family":"Attardo","sequence":"first","affiliation":[{"name":"Department of Entomology and Nematology, University of California, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicole","family":"Tam","sequence":"additional","affiliation":[{"name":"Department of Entomology and Nematology, University of California, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1817-0716","authenticated-orcid":false,"given":"Dula","family":"Parkinson","sequence":"additional","affiliation":[{"name":"Lawrence Berkeley National Lab., Berkeley, CA 94720, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6659-779X","authenticated-orcid":false,"given":"Lindsey K","family":"Mack","sequence":"additional","affiliation":[{"name":"Department of Entomology and Nematology, University of California, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5454-8165","authenticated-orcid":false,"given":"Xavier J","family":"Zahnle","sequence":"additional","affiliation":[{"name":"Department of Entomology and Nematology, University of California, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joceline","family":"Arguellez","sequence":"additional","affiliation":[{"name":"Department of Entomology and Nematology, University of California, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Tak\u00e1\u010d","sequence":"additional","affiliation":[{"name":"Department of Animal Systematics, Institute of Zoology, Slovak Academy of Sciences, 84506 Bratislava, Slovakia"},{"name":"Scientica, Ltd., 831 06 Bratislava, Slovakia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna R","family":"Malacrida","sequence":"additional","affiliation":[{"name":"Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,9,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Aksoy, S., Buscher, P., Lehane, M., Solano, P., and Van Den Abbeele, J. (2017). Human African trypanosomiasis control: Achievements and challenges. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005454"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Tirados, I., Esterhuizen, J., Kovacic, V., Mangwiro, T.N., Vale, G.A., Hastings, I., Solano, P., Lehane, M.J., and Torr, S.J. (2015). Tsetse Control and Gambian Sleeping Sickness; Implications for Control Strategy. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0003822"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1146\/annurev-ento-010814-020834","article-title":"Adenotrophic viviparity in tsetse flies: Potential for population control and as an insect model for lactation","volume":"60","author":"Benoit","year":"2015","journal-title":"Annu. Rev. Entomol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1017\/S0007485300006933","article-title":"Physiology of tsetse flies (Glossina spp.) (Diptera: Glossinidae): A review","volume":"67","author":"Langley","year":"1977","journal-title":"Bull. Entomol. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1016\/0022-1910(74)90143-7","article-title":"Dynamics of the pregnancy cycle in the tsetse Glossina morsitans","volume":"20","author":"Denlinger","year":"1974","journal-title":"J. Insect Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1603\/0022-0493-93.1.123","article-title":"Glossina austeni (Diptera: Glossinidae) eradicated on the island of Unguja, Zanzibar, using the sterile insect technique","volume":"93","author":"Vreysen","year":"2000","journal-title":"J. Econ. Entomol."},{"key":"ref_7","first-page":"397","article-title":"Principles of area-wide integrated tsetse fly control using the sterile insect technique","volume":"61","author":"Vreysen","year":"2001","journal-title":"Med. Trop."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1038\/185121b0","article-title":"Ovaries of Glossina morsitans","volume":"185","author":"Saunders","year":"1960","journal-title":"Nature"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1017\/S0031182000044619","article-title":"The role of the choriothete in tsetse flies","volume":"64","author":"Roberts","year":"1972","journal-title":"Parasitology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1016\/S0040-8166(73)80050-3","article-title":"Nutrient transfer during the reproductive cycle in Glossina austeni Newst.: Histology and histochemistry of the milk gland, fat body, and oenocytes","volume":"5","author":"Tobe","year":"1973","journal-title":"Tissue Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1038\/247301a0","article-title":"Secretory discharge and microflora of milk gland in tsetse flies","volume":"247","author":"Ma","year":"1974","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/0040-8166(75)90008-7","article-title":"Structural modulations in the tsetse fly milk gland during a pregnancy cycle","volume":"7","author":"Ma","year":"1975","journal-title":"Tissue Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"8475","DOI":"10.1073\/pnas.1505797112","article-title":"Integrated 3D view of postmating responses by the Drosophila melanogaster female reproductive tract, obtained by micro-computed tomography scanning","volume":"112","author":"Mattei","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"13912","DOI":"10.1073\/pnas.0710997105","article-title":"Mating induces an immune response and developmental switch in the Drosophila oviduct","volume":"105","author":"Kapelnikov","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","unstructured":"Maramorosch, K., and Mahmood, F. (1999). Establishment and Maintenance of Small Scale Tsetse Colonies. Maintenance of Human, Animal and Plant Pathogen Vectors, Science Publishers, Inc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/0022-1910(72)90119-9","article-title":"Mating, Insemination, and Ovulation in Tsetse Fly, Glossina morsitans","volume":"18","author":"Saunders","year":"1972","journal-title":"J. Insect Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1107\/S1600577518005787","article-title":"Xi-cam: A versatile interface for data visualization and analysis","volume":"25","author":"Pandolfi","year":"2018","journal-title":"J. Synchrotron Radiat."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1188","DOI":"10.1107\/S1600577514013939","article-title":"TomoPy: A framework for the analysis of synchrotron tomographic data","volume":"21","author":"Xiao","year":"2014","journal-title":"J. Synchrotron Radiat."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1139\/z72-133","article-title":"Volume Relationships During Pregnancy Cycle of Tsetse Fly Glossina austeni","volume":"50","author":"Tobe","year":"1972","journal-title":"Can. J. Zool."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1038\/nature11135","article-title":"Discovery of a sensory organ that coordinates lunge feeding in rorqual whales","volume":"485","author":"Pyenson","year":"2012","journal-title":"Nature"},{"key":"ref_21","first-page":"197","article-title":"Diptera\u2014ovary structure and oogenesis in midges and flies","volume":"36","author":"Kubrakiewicz","year":"1998","journal-title":"Folia Histochem. Cytobiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/0035-9203(70)90241-5","article-title":"Mating, ovulation and oocyte development in Glossina morsitans","volume":"64","author":"Saunders","year":"1970","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1017\/S0031182000026263","article-title":"Experimental work on reproduction in the tsetse fly, Glossina palpalis","volume":"1","author":"Mellanby","year":"1937","journal-title":"Parasitology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1111\/j.1365-3032.1981.tb00271.x","article-title":"The control of receptivity and ovulation in the tsetse fly, Glossina morsitans","volume":"6","author":"Gillott","year":"1981","journal-title":"Physiol. Entomol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1002\/jez.1402000211","article-title":"Some effects of mating in female tsetse, Glossina austeni Newst","volume":"200","author":"Ejezie","year":"1977","journal-title":"J. Exp. Zool."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1002\/jez.1401770406","article-title":"Regulation of Ovulation in Tsetse-Fly, Glossina pallidipes Austen","volume":"177","author":"Odhiambo","year":"1971","journal-title":"J. Exp. Zool."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/j.1365-3032.1993.tb00470.x","article-title":"The Mating-Behavior of Tsetse-Flies (Glossina)\u2014A Review","volume":"18","author":"Wall","year":"1993","journal-title":"Physiol. Entomol."},{"key":"ref_28","first-page":"161","article-title":"Evidence of Neuroendocrine Relationships Between Mating and Ovulation in the Tsetse-Fly, Glossina morsitans morsitans","volume":"1","author":"Chaudhury","year":"1981","journal-title":"Insect Sci. Appl."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1038\/2251063b0","article-title":"Sperm transfer by spermatophores in Glossina austeni newstead","volume":"225","author":"Pollock","year":"1970","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/0035-9203(72)90182-4","article-title":"Spermatophores in tsetse flies","volume":"66","author":"Pollock","year":"1972","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"20334","DOI":"10.1038\/srep20334","article-title":"The Spermatophore in Glossina morsitans morsitans: Insights into Male Contributions to Reproduction","volume":"6","author":"Scolari","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_32","first-page":"227","article-title":"Histochemical and Ultrastructural Studies of the Male Accessory Reproductive Glands and Spermatophore of the Tsetse, Glossina morsitans morsitans Westwood","volume":"4","author":"Odhiambo","year":"1983","journal-title":"Insect Sci. Appl."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1017\/S1742758400000370","article-title":"Spermatophore of the tsetse, Glossina morsitans morsitans Westwood: An ultrastructural study","volume":"1","author":"Kokwaro","year":"1981","journal-title":"Int. J. Trop. Insect Sci."},{"key":"ref_34","unstructured":"Mann, T. (1984). Spermatophores: Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa, Springer."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1016\/j.jinsphys.2009.07.001","article-title":"Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia","volume":"55","author":"Eberhard","year":"2009","journal-title":"J. Insect Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1186\/s13059-019-1768-2","article-title":"Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes","volume":"20","author":"Attardo","year":"2019","journal-title":"Genome Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/0010-406X(69)92169-0","article-title":"Lipid content and composition of the tse-tse fly, Glossina morsitans Westwood","volume":"31","author":"Cmelik","year":"1969","journal-title":"Comp. Biochem. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/0010-406X(69)91764-2","article-title":"Composition of Gut Contents of Third-Instar Tsetse Larvae (Glossina morsitans Westwood)","volume":"29","author":"Cmelik","year":"1969","journal-title":"Comp. Biochem. Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1016\/j.jinsphys.2008.06.008","article-title":"Analysis of milk gland structure and function in Glossina morsitans: Milk protein production, symbiont populations and fecundity","volume":"54","author":"Attardo","year":"2008","journal-title":"J. Insect Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5965","DOI":"10.1128\/AEM.00741-08","article-title":"The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly","volume":"74","author":"Pais","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/j.ijpsycho.2014.11.003","article-title":"Modulation of cortical activity in 2D versus 3D virtual reality environments: An EEG study","volume":"95","author":"Slobounov","year":"2015","journal-title":"Int. J. Psychophysiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1109\/TVCG.2012.42","article-title":"Effects of immersion on visual analysis of volume data","volume":"18","author":"Laha","year":"2012","journal-title":"IEEE Trans. Vis. Comput. Graph."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10055-018-0346-3","article-title":"Virtual memory palaces: Immersion aids recall","volume":"23","author":"Krokos","year":"2019","journal-title":"Virtual Real."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2301","DOI":"10.1002\/dvdy.22733","article-title":"MicroCT for molecular imaging: Quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs","volume":"240","author":"Metscher","year":"2011","journal-title":"Dev. Dyn."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Mart\u00edn-Vega, D., Clark, B., Ferrer, L.M., L\u00f3pez-Tamayo, S., Panadero, R., Cepeda-Palacios, R., Colwell, D.D., and Hall, M.J.R. (2020). Major differences in the larval anatomy of the digestive and excretory systems of three Oestridae species revealed by micro-CT. Med. Vet. Entomol.","DOI":"10.1111\/mve.12476"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Tiulpin, A., Finnil\u00e4, M., Lehenkari, P., Nieminen, H.J., and Saarakkala, S. (2020). Deep-Learning for Tidemark Segmentation in Human Osteochondral Tissues Imaged with Micro-computed Tomography. Lecture Notes in Computer Science, Proceedings of the Advanced Concepts for Intelligent Vision Systems, Auckland, New Zealand, 10\u201314 February 2020, Springer International Publishing.","DOI":"10.1007\/978-3-030-40605-9_12"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"12590","DOI":"10.1073\/pnas.1711673114","article-title":"Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants","volume":"114","author":"Fredericksen","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/11\/10\/651\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:12:40Z","timestamp":1760177560000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/11\/10\/651"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,23]]},"references-count":47,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2020,10]]}},"alternative-id":["insects11100651"],"URL":"https:\/\/doi.org\/10.3390\/insects11100651","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.06.12.147587","asserted-by":"object"}]},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,23]]}}}