{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,4,9]],"date-time":"2025-04-09T04:03:35Z","timestamp":1744171415100,"version":"3.40.3"},"reference-count":31,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2024,4,8]],"date-time":"2024-04-08T00:00:00Z","timestamp":1712534400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["G20130315164474"],"award-info":[{"award-number":["G20130315164474"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007231","name":"Cornell University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007231","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,12,20]]},"abstract":"<jats:title>Synopsis<\/jats:title>\n               <jats:p>The \u201cadaptive sterilization hypothesis\u201d argues that the tendency of sexually transmitted infections (STIs) to cause infertility likely reflects an evolutionary adaptation of these pathogens. For example, some STIs can lead to bilateral occlusions of the oviducts and sterile matings. Cycling females that do not spend time gestating and lactating are ready to mate sooner than fertile females, and therefore, likely to mate more frequently and possibly more promiscuously. These sexual activities are associated with enhanced transmissibility of STIs, and tubal occlusion is a proximate mechanism by which STIs can increase fitness. Our principal objectives were to determine whether female mice inoculated with Chlamydia muridarum mate more frequently than mice inoculated with sterile saline and to test the hypothesis that tubal occlusion following C. muridarum infection modulates mating behavior in a manner that might increase transmissibility of Chlamydia. Similar to C. trachomatis infections in human females, C. muridarum can ascend the reproductive tract of mice, damage and occlude the oviducts, and cause infertility. However, ovarian function and mating activity are maintained following tubal occlusion. A total of 20 C57Bl\/6 mice with regular estrous cycles were given intravaginal inocula of C. muridarum and 32 days later paired with a male for 90 days. A total of nine saline-treated females served as controls. A total of three Chlamydia-inoculated females were rendered infertile due to bilateral oviductal damage and mated eight (\u00b10.0) times. Control females mated on average 4.6 (\u00b10.3) times, and 17 Chlamydia-inoculated fertile females, including six females with only a single oviduct occluded, mated on average 4.7 (\u00b10.2) times. Chlamydia-inoculated fertile females with unilateral oviductal damage had significantly smaller average litter sizes as compared to females inoculated with saline. Females with unilateral tubal occlusion also tended to wean fewer pups than saline controls over the course of 90 days. Female mice with Chlamydia-induced tubal infertility mated more frequently (approximately every 11 d) than did fertile females (approximately every 20 days), which is consistent with the adaptive sterilization hypothesis. To determine whether Chlamydia-induced sterilization is truly adaptive, future studies will need to demonstrate increased sexual transmissibility, and possibly increased promiscuity, within populations of freely breeding mice.<\/jats:p>","DOI":"10.1093\/icb\/icae010","type":"journal-article","created":{"date-parts":[[2024,4,8]],"date-time":"2024-04-08T17:22:00Z","timestamp":1712596920000},"page":"1661-1666","source":"Crossref","is-referenced-by-count":1,"title":["Testing the Adaptive Sterilization Hypothesis in Mice Inoculated with <i>Chlamydia muridarum<\/i>"],"prefix":"10.1093","volume":"64","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8341-7527","authenticated-orcid":false,"given":"Ned J","family":"Place","sequence":"first","affiliation":[{"name":"Departments of Population Medicine and Diagnostic Sciences , 240 Farrier Rd, Schurman Hall S1-088, Ithaca, NY, 14853 ,","place":["USA"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David T","family":"Peck","sequence":"additional","affiliation":[{"name":"Neurobiology and Behavior, Cornell University , 215 Tower Road, Ithaca, NY 14853 ,","place":["USA"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2024,4,8]]},"reference":[{"key":"2025040800022165000_bib1","doi-asserted-by":"crossref","first-page":"e1005229","DOI":"10.1371\/journal.ppat.1005229","article-title":"Beyond mortality: sterility as a neglected component of parasite virulence","volume":"11","author":"Abbate","year":"2015","journal-title":"PLoS Pathog"},{"key":"2025040800022165000_bib2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1242\/jeb.082511","article-title":"Neural parasitology: how parasites manipulate host behaviour","volume":"216","author":"Adamo","year":"2013","journal-title":"J Exp Biol"},{"key":"2025040800022165000_bib3","doi-asserted-by":"crossref","first-page":"e1004111","DOI":"10.1371\/journal.ppat.1004111","article-title":"Why sexually transmitted infections tend to cause infertility: an evolutionary hypothesis","volume":"10","author":"Apari","year":"2014","journal-title":"PLoS Pathog"},{"key":"2025040800022165000_bib4","doi-asserted-by":"crossref","first-page":"pdb.prot092387","DOI":"10.1101\/pdb.prot092387","article-title":"Selecting female mice in estrus and checking plugs","volume":"2016","author":"Behringer","year":"2016","journal-title":"Cold Spring Harb Protoc"},{"key":"2025040800022165000_bib5","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1086\/203798","article-title":"Cause of conjugal dissolution: a cross-cultural study","volume":"30","author":"Betzig","year":"1989","journal-title":"Curr Anthropol"},{"key":"2025040800022165000_bib6","doi-asserted-by":"crossref","first-page":"45","DOI":"10.4103\/0974-1208.112381","article-title":"Ovulation and rate of implantation following unilateral ovariectomy in mice","volume":"6","author":"Bhattacharya","year":"2013","journal-title":"J Hum Reprod Sci"},{"article-title":"Chlamydia\u2014CDC Detailed Fact Sheet. Sexually Transmitted Disease Surveillance, 2021","year":"2023","author":"Center for Disease Control and Prevention","key":"2025040800022165000_bib7"},{"key":"2025040800022165000_bib8","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1111\/1365-2435.13766","article-title":"Horizontal transmission of a murine retrovirus is driven by males within semi-natural enclosures","volume":"35","author":"Cornwall","year":"2021","journal-title":"Funct Ecol"},{"key":"2025040800022165000_bib9","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1086\/283319","article-title":"The cost of mating","volume":"112","author":"Daly","year":"1978","journal-title":"Am Nat"},{"key":"2025040800022165000_bib10","doi-asserted-by":"crossref","first-page":"4141","DOI":"10.1111\/j.1365-294X.2006.03068.x","article-title":"The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus)","volume":"15","author":"Dean","year":"2006","journal-title":"Mol Ecol"},{"key":"2025040800022165000_bib11","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.1111\/j.1420-9101.2008.01612.x","article-title":"The frequency of multiple paternity predicts variation in testes size among island populations of house mice","volume":"21","author":"Firman","year":"2008","journal-title":"J Evol Biol"},{"key":"2025040800022165000_bib12","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1093\/beheco\/arm158","article-title":"Polyandry, sperm competition, and reproductive success in mice","volume":"19","author":"Firman","year":"2008","journal-title":"Behav Ecol"},{"key":"2025040800022165000_bib13","doi-asserted-by":"crossref","first-page":"939944","DOI":"10.3389\/fcimb.2022.939944","article-title":"The hormonal environment and estrogen receptor signaling alters Chlamydia muridarum infection in vivo","volume":"12","author":"Gravitte","year":"2022","journal-title":"Front Cell Infect Microbiol"},{"key":"2025040800022165000_bib14","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1111\/j.1469-185X.1996.tb01281.x","article-title":"Sexually transmitted diseases in animals: ecological and evolutionary implications","volume":"71","author":"Lockhart","year":"1996","journal-title":"Biol Rev"},{"key":"2025040800022165000_bib15","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1111\/2049-632X.12032","article-title":"OT-1 mice display minimal upper genital tract pathology following primary intravaginal Chlamydia muridarum infection","volume":"67","author":"Manam","year":"2013","journal-title":"Pathog Dis"},{"key":"2025040800022165000_bib16","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1111\/evo.13718","article-title":"Why is sterility virulence most common in sexually transmitted infections? Examining the role of epidemiology","volume":"73","author":"Mcleod","year":"2019","journal-title":"Evolution"},{"key":"2025040800022165000_bib17","first-page":"195","article-title":"Central circadian control of female reproductive function","volume":"4","author":"Miller","year":"2013","journal-title":"Front Endocrinol"},{"key":"2025040800022165000_bib18","doi-asserted-by":"crossref","first-page":"S96","DOI":"10.1086\/652393","article-title":"Duration of untreated chlamydial genital infection and factors associated with clearance: review of animal studies","volume":"201 Suppl 2","author":"Miyairi","year":"2010","journal-title":"J Infect Dis"},{"key":"2025040800022165000_bib19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1749-6632.2011.06078.x","article-title":"Evolutionary approaches to sexually transmitted infections","volume":"1230","author":"Nesse","year":"2011","journal-title":"Ann NY Acad Sci"},{"key":"2025040800022165000_bib20","doi-asserted-by":"crossref","first-page":"4027","DOI":"10.4049\/jimmunol.179.6.4027","article-title":"Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease","volume":"179","author":"O'connell","year":"2007","journal-title":"J Immunol"},{"key":"2025040800022165000_bib21","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/B978-0-12-394445-0.00001-1","article-title":"The cycling and pregnant mouse: gross anatomy","volume-title":"The Guide to Investigation of Mouse Pregnancy","author":"Pang","year":"2014"},{"key":"2025040800022165000_bib22","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/S0169-5347(98)01473-6","article-title":"Chemical signals and parasite-mediated sexual selection","volume":"13","author":"Penn","year":"1998","journal-title":"Trends Ecol Evol"},{"key":"2025040800022165000_bib23","doi-asserted-by":"crossref","first-page":"e00143","DOI":"10.1128\/IAI.00143-18","article-title":"T cell-independent gamma interferon and B cells cooperate to prevent mortality associated with disseminated Chlamydia muridarum genital tract infection","volume":"86","author":"Poston","year":"2018","journal-title":"Infect Immun"},{"key":"2025040800022165000_bib24","doi-asserted-by":"crossref","first-page":"6148","DOI":"10.1128\/IAI.71.11.6148-6154.2003","article-title":"Characterization of chlamydial genital infection resulting from sexual transmission from male to female guinea pigs and determination of infectious dose","volume":"71","author":"Rank","year":"2003","journal-title":"Infect Immun"},{"key":"2025040800022165000_bib25","first-page":"927","article-title":"Pathogenesis of endometritis and salpingitis in a guinea pig model of chlamydial genital infection","volume":"140","author":"Rank","year":"1992","journal-title":"Am J Pathol"},{"key":"2025040800022165000_bib26","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1097\/00007435-199501000-00008","article-title":"Increased incidence of oviduct pathology in the guinea pig after repeat vaginal inoculation with the chlamydial agent of guinea pig inclusion conjunctivitis","volume":"22","author":"Rank","year":"1995","journal-title":"Sex Transm Dis"},{"key":"2025040800022165000_bib27","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1163\/156853903771980639","article-title":"Free female choice in house mice: leaving best for last","volume":"140","author":"Rolland","year":"2003","journal-title":"Behaviour"},{"volume-title":"Mating and Pregnancy. Mouse Genetics, Concepts and Applications","year":"1995","author":"Silver","key":"2025040800022165000_bib28"},{"key":"2025040800022165000_bib29","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1002\/ece3.920","article-title":"Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass","volume":"4","author":"Thonhauser","year":"2014","journal-title":"Ecology and Evolution"},{"key":"2025040800022165000_bib30","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.1210\/endo-95-5-1486","article-title":"Serum progesterone levels in the pregnant and postpartum laboratory mouse","volume":"95","author":"Virgo","year":"1974","journal-title":"Endocrinology"},{"key":"2025040800022165000_bib31","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1002\/evan.21776","article-title":"Male-mediated prenatal loss: functions and mechanisms","volume":"28","author":"Zipple","year":"2019","journal-title":"Evol Anthropol"}],"container-title":["Integrative And Comparative Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/icb\/advance-article-pdf\/doi\/10.1093\/icb\/icae010\/57306326\/icae010.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/icb\/article-pdf\/64\/6\/1661\/57306326\/icae010.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/icb\/article-pdf\/64\/6\/1661\/57306326\/icae010.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,8]],"date-time":"2025-04-08T03:10:40Z","timestamp":1744081840000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/icb\/article\/64\/6\/1661\/7642245"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,8]]},"references-count":31,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,4,8]]},"published-print":{"date-parts":[[2024,12,20]]}},"URL":"https:\/\/doi.org\/10.1093\/icb\/icae010","relation":{},"ISSN":["1540-7063","1557-7023"],"issn-type":[{"type":"print","value":"1540-7063"},{"type":"electronic","value":"1557-7023"}],"subject":[],"published-other":{"date-parts":[[2024,12]]},"published":{"date-parts":[[2024,4,8]]}}}