{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T05:07:21Z","timestamp":1789016841392,"version":"build-2803163510"},"reference-count":43,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T00:00:00Z","timestamp":1788825600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004901","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de Minas Gerais","doi-asserted-by":"publisher","award":["APQ-00325-22"],"award-info":[{"award-number":["APQ-00325-22"]}],"id":[{"id":"10.13039\/501100004901","id-type":"DOI","asserted-by":"publisher"}]},{"award":["APQ-00325-22"],"award-info":[{"award-number":["APQ-00325-22"]}],"id":[{"id":"https:\/\/ror.org\/00nc55f03","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["404696\/2021-0"],"award-info":[{"award-number":["404696\/2021-0"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["307847\/2021-7"],"award-info":[{"award-number":["307847\/2021-7"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["304957\/2024-0"],"award-info":[{"award-number":["304957\/2024-0"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"award":["404696\/2021-0"],"award-info":[{"award-number":["404696\/2021-0"]}],"id":[{"id":"https:\/\/ror.org\/03swz6y49","id-type":"ROR","asserted-by":"publisher"}]},{"award":["307847\/2021-7"],"award-info":[{"award-number":["307847\/2021-7"]}],"id":[{"id":"https:\/\/ror.org\/03swz6y49","id-type":"ROR","asserted-by":"publisher"}]},{"award":["304957\/2024-0"],"award-info":[{"award-number":["304957\/2024-0"]}],"id":[{"id":"https:\/\/ror.org\/03swz6y49","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior-Brasil","doi-asserted-by":"crossref","award":["001"],"award-info":[{"award-number":["001"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"crossref"}]},{"award":["001"],"award-info":[{"award-number":["001"]}],"id":[{"id":"https:\/\/ror.org\/00x0ma614","id-type":"ROR","asserted-by":"publisher"}]},{"name":"PRPPG\/UNIFAL-MG","award":["23087.015081\/2026-82"],"award-info":[{"award-number":["23087.015081\/2026-82"]}]},{"name":"FINEP-Financiadora de Estudos e Projetos"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Post-embryonic gonad development determines when insects acquire reproductive competence, yet this process remains poorly characterized in Bruchinae seed beetles. Here, we examined ovarian and testicular development in the capital-breeding bean weevil Zabrotes subfasciatus, from larval stages to four-day-old adults, using stereomicroscopy, light microscopy, and scanning electron microscopy. Female gonads were already recognizable in larvae as ovaries composed of three ovarioles, each dominated by a proliferative germarial region and posterior duct-like domains. During pharate-pupal and pupal development, these structures remained largely previtellogenic but showed ductal integration associated with future calyx formation. The most extensive ovarian reorganization occurred in pharate adults, when terminal filaments, individualized oocytes, follicular cells, trophic cords, and the germarium\u2013vitellarium transition became evident; acidophilic inclusions consistent with early yolk deposition further indicate that vitellogenesis begins before emergence. Male gonads also differentiated early, with larval testes containing germ stem cells, spermatogonia, spermatocytes, spermatids, cyst cells, and the internal portion of the efferent ducts. From the pharate-pupal stage onward, spermiogenesis intensified, and four-day-old adults displayed a fully organized reproductive tract. Together, these findings show that gonad development begins during larval life but attains functional organization mainly during late metamorphosis, supporting rapid reproductive readiness in this capital-breeding pest.<\/jats:p>","DOI":"10.3390\/insects17090938","type":"journal-article","created":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T09:02:24Z","timestamp":1788858144000},"page":"938","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Post-Embryonic Gonad Development in the Capital-Breeding Seed Beetle Zabrotes subfasciatus (Bruchinae): A Morphological View"],"prefix":"10.3390","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7185-6477","authenticated-orcid":false,"given":"Juliana Ramos","family":"Martins","sequence":"first","affiliation":[{"name":"Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade Federal de Alfenas (UNIFAL-MG), Alfenas CEP 37133-840, MG, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5619-6378","authenticated-orcid":false,"given":"M\u00e1rcia Maria Gentile","family":"Bitondi","sequence":"additional","affiliation":[{"name":"Departamento de Biologia, Faculdade de Filosofia, Ci\u00eancias e Letras de Ribeir\u00e3o Preto, Universidade de S\u00e3o Paulo (USP), Ribeir\u00e3o Preto CEP 14049-900, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0251-9167","authenticated-orcid":false,"given":"S\u00edlvia de Oliveira","family":"Miranda","sequence":"additional","affiliation":[{"name":"Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade Federal de Alfenas (UNIFAL-MG), Alfenas CEP 37133-840, MG, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Talita Sarah","family":"Mazzoni","sequence":"additional","affiliation":[{"name":"Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade Federal de Alfenas (UNIFAL-MG), Alfenas CEP 37133-840, MG, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8417-2763","authenticated-orcid":false,"given":"Angel Roberto","family":"Barchuk","sequence":"additional","affiliation":[{"name":"Departamento de Biologia Celular e do Desenvolvimento, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade Federal de Alfenas (UNIFAL-MG), Alfenas CEP 37133-840, MG, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1146\/annurev.en.24.010179.002313","article-title":"Biology of the Bruchidae","volume":"24","author":"Southgate","year":"1979","journal-title":"Annu. Rev. Entomol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/phen.70011","article-title":"Early Adaptation to an Unusual Host in the Bean Weevil Zabrotes subfasciatus Is Associated with Changes in Body Size and Reproductive Physiology","volume":"51","author":"Benedito","year":"2026","journal-title":"Physiol. Entomol."},{"key":"ref_3","unstructured":"Kingsolver, J.M. (2004). Handbook of the Bruchidae of the United States and Canada (Insecta, Coleoptera). Volume 2. Illustrations, Agricultural Research Service."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Kutcherov, D. (2020). Stagewise Resolution of Temperature-Dependent Embryonic and Postembryonic Development in the Cowpea Seed Beetle Callosobruchus maculatus (F.). BMC Ecol., 20.","DOI":"10.1186\/s12898-020-00318-2"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1603\/AN11129","article-title":"Description and Differentiation of the Four Larval Instars of Acanthoscelides macrophthalmus (Coleoptera: Chrysomelidae: Bruchinae)","volume":"105","author":"Wu","year":"2012","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.4039\/Ent991298-12","article-title":"A possible mechanism for the regulation of the female reproductive cycle in Tenebrio molitor (COLEOPTERA: TENEBRIONIDAE)","volume":"99","author":"Gerber","year":"1967","journal-title":"Can. Entomol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1093\/aesa\/77.2.165","article-title":"Food Discrimination and Ovarian Development in Burying Beetles (Coleoptera: Silphidae: Nicrophorus)","volume":"77","author":"Wilson","year":"1984","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"57","DOI":"10.2307\/3545800","article-title":"Capital and Income Breeding as Alternative Tactics of Resource Use in Reproduction","volume":"78","year":"1997","journal-title":"Oikos"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Miranda, S.d.O., Cruz, B.d.O., Martins, J.R., Mazzoni, T.S., Miranda, W.d.O., Moda, L.M.R., Caixeta, E.S., Teixeira, I.R.D.V., and Barchuk, A.R. (2025). Ovary Activation Dynamics in the Bean Weevil Zabrotes subfasciatus (Bruchinae): The Essential Roles of Seeds and Males. Insects, 16.","DOI":"10.20944\/preprints202507.1843.v1"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Schoenherr, C.J. (1833). Genera et species Curculionidum, cum synonymia hujus familiae. Synonymia Insectorum, Oder: Versuch Einer Synonymie Aller Bisher Bekannten Insecten; Nach Fabricii Systema Eleutheratorum & c. Geordnet, Roret.","DOI":"10.5962\/bhl.title.8952"},{"key":"ref_11","first-page":"245","article-title":"Spermophagus\u00a0semifasicatus","volume":"6","author":"Lucas","year":"1858","journal-title":"Ann. Soci\u00e9t\u00e9 Entomol. Fr."},{"key":"ref_12","unstructured":"Valencia G., C.A., Cardona Mej\u00eda, C., and Schoonhoven, A.v. (2026, January 15). Main Insect Pests of Stored Beans and Their Control [Tutorial Unit]. Available online: https:\/\/hdl.handle.net\/10568\/54486."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"baaa062","DOI":"10.1093\/database\/baaa062","article-title":"NCBI Taxonomy: A Comprehensive Update on Curation, Resources and Tools","volume":"2020","author":"Schoch","year":"2020","journal-title":"Database"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/phen.12358","article-title":"Life History Trait Response to Ambient Temperature and Food Availability Variations in the Bean Weevil Zabrotes subfasciatus","volume":"46","author":"Parreiras","year":"2021","journal-title":"Physiol. Entomol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1017\/S0007485300049580","article-title":"Some Laboratory Observations on the Rates of Development, Mortality and Oviposition of Several Species of Bruchidae Breeding in Stored Pulses","volume":"55","author":"Howe","year":"1964","journal-title":"Bull. Entomol. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1111\/phen.12329","article-title":"Adult Feeding and Host Type Modulate the Life History Traits of the Capital Breeder Zabrotes subfasciatus","volume":"45","author":"Capizzani","year":"2020","journal-title":"Physiol. Entomol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1017\/S0007485310000660","article-title":"Evolutionary Diversification of Bruchine Beetles: Climate-Dependent Traits and Development Associated with Pest Status","volume":"101","author":"Tuda","year":"2011","journal-title":"Bull. Entomol. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"843","DOI":"10.1590\/S0100-204X2008000700008","article-title":"Diversidade gen\u00e9tica estimada com marcadores ISSR em popula\u00e7\u00f5es brasileiras de Zabrotes subfasciatus","volume":"43","author":"Carvalho","year":"2008","journal-title":"Pesq. Agropec. Bras."},{"key":"ref_19","unstructured":"Bondar, G.G. (1937). Notas Biologicas Sobre Bruchideros Observados no Brasil, Tip. do Jornal do Commercio."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"246","DOI":"10.1111\/j.1365-3032.2009.00682.x","article-title":"Females of the Weevil Zabrotes subfasciatus Manipulate the Size and Number of Eggs According to the Host Seed Availability","volume":"34","author":"Teixeira","year":"2009","journal-title":"Physiol. Entomol."},{"key":"ref_21","unstructured":"Teixeira, I., and Gris, C. (2011). Genetic Diversity of Grains, Storage Pests and Their Effects on the Worldwide Bean Supply. Beans: Nutrition, Consumption and Health, Nova Science Publishers."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1111\/j.1744-7917.2011.01425.x","article-title":"Intraspecific Competition in Zabrotes subfasciatus: Physiological and Behavioral Adaptations to Different Amounts of Host","volume":"19","author":"Teixeira","year":"2012","journal-title":"Insect Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1177\/10406387231160767","article-title":"Histology of the Whole Body of Honey Bees: Tissue Fixation and Processing","volume":"35","author":"Lussier","year":"2023","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_24","unstructured":"Kiernan, J. (2015). Histological and Histochemical Methods, Scion Publishing Ltd.. [5th ed.]."},{"key":"ref_25","first-page":"137A","article-title":"A Formaldehyde-Glutaraldehyde Fixative of High Osmolality for Use in Electron Microscopy","volume":"27","author":"Karnovsky","year":"1964","journal-title":"J. Cell Biol."},{"key":"ref_26","first-page":"777","article-title":"On the Rapid Conversion of Haematoxylin into Haematein in Staining Reactions","volume":"3","author":"Harris","year":"1900","journal-title":"J. Appl. Microsc. Lab. Methods"},{"key":"ref_27","first-page":"23","article-title":"Morfolog\u00eda Del Aparato Reproductor En Odontotaenius Striatopunctatus (Percheron, 1835) (Coleoptera: Passalidae)","volume":"24","author":"Cruz","year":"2008","journal-title":"ACTA Zool. Mex."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1007\/s00435-016-0321-z","article-title":"Morpho-Anatomy of the Male Reproductive Tract and Spermatogenesis of the South American Spasalus Silvarum Kuwert (Coleoptera: Passalidae)","volume":"135","author":"Salazar","year":"2016","journal-title":"Zoomorphology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1258","DOI":"10.1093\/micmic\/ozad024","article-title":"Anatomical and Histological Structures of Male Reproductive System in Long-Horned Beetle Isotomus Speciosus (Schneider, 1787) (Coleoptera: Cerambycidae): Light and Scanning Electron Microscopic Study","volume":"29","author":"Candan","year":"2023","journal-title":"Microsc. Microanal."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"112211","DOI":"10.1016\/j.mce.2024.112211","article-title":"Endocrine Factors Modulating Vitellogenesis and Oogenesis in Insects: An Update","volume":"587","author":"Leyria","year":"2024","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"259","DOI":"10.32604\/biocell.2004.28.259","article-title":"Differentiation and Morphogenesis of Triatoma Infestans (Klug 1834) Female Gonads: I-Post Embryonic Development","volume":"28","author":"Bozzini","year":"2004","journal-title":"Biocell"},{"key":"ref_32","first-page":"28","article-title":"Post-Embryonic Development of Ovariole Pedicels in Triatoma Infestans (Klugh 1834). A Morphometrical Approach","volume":"17","author":"Mariano","year":"2008","journal-title":"Acta Microsc."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"114030","DOI":"10.1016\/j.ygcen.2022.114030","article-title":"The Hormonal and Neural Control of Egg Production in the Historically Important Model Insect, Rhodnius prolixus: A Review, with New Insights in This Post-Genomic Era","volume":"321\u2013322","author":"Lange","year":"2022","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1080\/03014223.1981.10427942","article-title":"Reproductive Morphology of the Argentine Stem Weevil, Hyperodes Bonariensis (Coleoptera: Curculionidae)","volume":"8","author":"Goldson","year":"1981","journal-title":"N. Z. J. Zool."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1673\/031.011.17401","article-title":"Metamorphosis and Gonad Maturation in the Horn Fly Haematobia Irritans","volume":"11","author":"Basso","year":"2011","journal-title":"J. Insect Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"53","DOI":"10.2307\/1536580","article-title":"Studies on Insect Spermatogenesis. III. On the Structure of the Nebenkern in the Insect Spermatid and the Origin of Nebenkern Patterns","volume":"42","author":"Bowen","year":"1922","journal-title":"Biol. Bull."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Vedelek, V., Jankovics, F., Z\u00e1dori, J., and Sinka, R. (2024). Mitochondrial Differentiation during Spermatogenesis: Lessons from Drosophila melanogaster. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25073980"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1002\/jmor.1050610110","article-title":"Reproductive System of the Bruchid Beetles Bruchus Quadrimaculatus Fabr., Bruchus (Callosobruchus) Chinensis L., (Bruchidae\u2014Coleoptera)","volume":"61","author":"Mukerji","year":"1937","journal-title":"J. Morphol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1007\/s13592-020-00773-2","article-title":"Testis Development and Spermatogenesis in Drones of the Honey Bee, Apis mellifera L.","volume":"51","author":"Lago","year":"2020","journal-title":"Apidologie"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1111\/j.1744-7917.2008.00218.x","article-title":"Host Preference of the Bean Weevil Zabrotes subfasciatus","volume":"15","author":"Teixeira","year":"2008","journal-title":"Insect Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.jspr.2016.06.003","article-title":"Behavioral and Physiological Responses of the Bean Weevil Zabrotes subfasciatus to Intraspecific Competition","volume":"69","author":"Teixeira","year":"2016","journal-title":"J. Stored Prod. Res."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Sanchez-Cruz, A., Tapia-Maruri, D., and Jim\u00e9nez-P\u00e9rez, A. (2022). Reproductive Apparatus, Gonadic Maturation, and Allometry of Cyclocephala Barrerai Mart\u00ednez (Coleoptera: Melolonthidae: Dynastinae). Insects, 13.","DOI":"10.3390\/insects13070638"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s00441-024-03877-8","article-title":"Anatomical Changes of Tenebrio molitor and Tribolium castaneum during Complete Metamorphosis","volume":"396","author":"Vommaro","year":"2024","journal-title":"Cell Tissue Res."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/938\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T04:16:27Z","timestamp":1789013787000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/17\/9\/938"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,8]]},"references-count":43,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["insects17090938"],"URL":"https:\/\/doi.org\/10.3390\/insects17090938","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,8]]}}}