{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T12:31:57Z","timestamp":1791289917031,"version":"4.3.0"},"reference-count":52,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2020,10,28]],"date-time":"2020-10-28T00:00:00Z","timestamp":1603843200000},"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":["1541959"],"award-info":[{"award-number":["1541959"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,2,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The phallic glans of the American alligator (Alligator mississippiensis) is the distal termination of the semen-conducting sulcus spermaticus and during copulation has the closest, most intimate mechanical interactions with the female urodeum, the middle cloacal chamber that contains the opening to the vaginal passages and oviducts. However, the details of this interface leading to insemination and gamete uptake are unclear. Here, we: (1) histologically characterize the underlying tissue types and morphologically quantify the shape changes associated with glans inflation into the copulatory conformation, (2) digitally reconstruct from MRI the 3D shape of functional tissue compartments, and (3) diffusible iodine-based contrast-enhanced computed tomography image the copulatory fit between male phallus and female cloaca. We discuss these results in relation to tissue type material properties, the transfer on intromittent forces, establishing potential copulatory lock, inflated glans volume scaling with body mass\/length, the mechanics of semen targeting and insemination, and potential female cryptic choice impacting multiple clutch paternity. In part, this study further clarifies the phallic morphological variation observed among crocodylians and begins to investigate the role(s) these divergent male forms play during copulation interacting with female cloacal forms to increase reproductive success.<\/jats:p>","DOI":"10.1093\/biolre\/ioaa197","type":"journal-article","created":{"date-parts":[[2020,10,28]],"date-time":"2020-10-28T13:10:59Z","timestamp":1603890659000},"page":"374-386","source":"Crossref","is-referenced-by-count":7,"title":["Glans inflation morphology and female cloaca copulatory interactions of the male American alligator phallus\u2020"],"prefix":"10.1093","volume":"104","author":[{"given":"Brandon C","family":"Moore","sequence":"first","affiliation":[{"name":"College of Veterinary Medicine, Department of Biomedical Science, University of Missouri, Columbia, MO, USA"},{"name":"Biology Department, Sewanee: The University of the South, Sewanee, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia L R","family":"Brennan","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Mount Holyoke College, South Hadley, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachel","family":"Francis","sequence":"additional","affiliation":[{"name":"Biology Department, Sewanee: The University of the South, Sewanee, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samuel","family":"Penland","sequence":"additional","affiliation":[{"name":"Biology Department, Sewanee: The University of the South, Sewanee, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kelsie","family":"Shiavone","sequence":"additional","affiliation":[{"name":"Biology Department, Sewanee: The University of the South, Sewanee, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn","family":"Wayne","sequence":"additional","affiliation":[{"name":"Biology Department, Sewanee: The University of the South, Sewanee, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allan R","family":"Woodward","sequence":"additional","affiliation":[{"name":"Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Gainesville, FL, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark D","family":"Does","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dong Kyu","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diane A","family":"Kelly","sequence":"additional","affiliation":[{"name":"Department of Psychological and Brain Sciences, University of Massachusetts, Amherst MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,10,28]]},"reference":[{"key":"2021103112031460500_ref1","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1093\/icb\/icw102","article-title":"Developmental and evolutionary origins of the Amniote phallus","volume":"56","author":"Gredler","year":"2016","journal-title":"Integr Comp Biol"},{"key":"2021103112031460500_ref2","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.tree.2003.11.012","article-title":"Sexual selection and genital evolution","volume":"19","author":"Hosken","year":"2004","journal-title":"Trends Ecol Evol"},{"key":"2021103112031460500_ref3","doi-asserted-by":"crossref","DOI":"10.4159\/harvard.9780674330702","volume-title":"Sexual Selection and Animal Genitalia","author":"Eberhard","year":"1985"},{"key":"2021103112031460500_ref4","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1016\/j.juro.2007.01.011","article-title":"Male genital morphology and function: An evolutionary perspective","volume":"177","author":"Simmons","year":"2007","journal-title":"J Urol"},{"key":"2021103112031460500_ref5","doi-asserted-by":"crossref","first-page":"a017749","DOI":"10.1101\/cshperspect.a017749","article-title":"Mechanisms and evidence of genital coevolution: The roles of natural selection, mate choice, and sexual conflict","volume":"7","author":"Brennan","year":"2015","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"2021103112031460500_ref6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/aen.12053","article-title":"Sexual selection and genital evolution","volume":"53","author":"Simmons","year":"2014","journal-title":"Austral Entomol"},{"key":"2021103112031460500_ref7","doi-asserted-by":"crossref","DOI":"10.1093\/icb\/icw018","article-title":"Studying genital coevolution to understand Intromittent organ morphology","author":"Brennan","year":"2016","journal-title":"Integr Comp Biol"},{"key":"2021103112031460500_ref8","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/bs.asb.2020.01.001","article-title":"Copulatory behavior and its relationship to genital morphology","volume":"52","author":"Brennan","year":"2020","journal-title":"Adv Study Behav"},{"key":"2021103112031460500_ref9","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1093\/icb\/icw058","article-title":"Intromittent organ morphology and biomechanics: Defining the physical challenges of copulation","volume":"56","author":"Kelly","year":"2016","journal-title":"Integr Comp Biol"},{"key":"2021103112031460500_ref10","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1002\/ar.22644","article-title":"Penile anatomy and hypotheses of erectile function in the American alligator (Alligator mississippiensis): Muscular eversion and elastic retraction","volume":"296","author":"Kelly","year":"2013","journal-title":"Anat Rec"},{"key":"2021103112031460500_ref11","doi-asserted-by":"crossref","DOI":"10.1093\/icb\/icw012","article-title":"Morphological characteristics regulating phallic glans engorgement in the American alligator","author":"Moore","year":"2016","journal-title":"Integr Comp Biol"},{"key":"2021103112031460500_ref12","first-page":"16","article-title":"Genital structures and sex identification in crocodiles","volume":"26","author":"Ziegler","year":"2007","journal-title":"Crocodile Spec Gr Newsl"},{"key":"2021103112031460500_ref13","doi-asserted-by":"crossref","DOI":"10.1071\/9781486300679","volume-title":"Biology and Evolution of Crocodylians","author":"Grigg","year":"2015"},{"key":"2021103112031460500_ref14","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.aquaculture.2013.11.002","article-title":"Semen collection and seminal characteristics of the Australian saltwater crocodile (Crocodylus porosus)","volume":"422\u2013423","author":"Johnston","year":"2014","journal-title":"Aquaculture"},{"key":"2021103112031460500_ref15","doi-asserted-by":"publisher","DOI":"10.2994\/sajh-d-18-00083.1","article-title":"Histological investigation of the Nile crocodile (Crocodylus niloticus) phallic glans","author":"Moore","year":"2020","journal-title":"South Am J Herpetol"},{"key":"2021103112031460500_ref16","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1002\/jmor.21126","article-title":"Morphological changes associated with Nile crocodile (Crocodylus niloticus) phallic glans inflation","volume":"281","author":"Moore","year":"2020","journal-title":"J Morphol"},{"key":"2021103112031460500_ref17","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1111\/ahe.12542","article-title":"Crocodylian conservation and evolution insights from an anatomical and histological examination of phalli from male false gharial (Tomistoma schlegelii)","volume":"49","author":"Moore","year":"2020","journal-title":"Anat Histol Embryol"},{"key":"2021103112031460500_ref18","doi-asserted-by":"crossref","DOI":"10.2994\/SAJH-D-14-00037.1","article-title":"Histological investigation of the adult alligator phallic sulcus","volume":"10","author":"Moore","year":"2015","journal-title":"South Am J Herpetol"},{"key":"2021103112031460500_ref19","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1006\/gcen.1996.0005","article-title":"Reduction in penis size and plasma testosterone concentrations in juvenile alligators living in a contaminated environment","volume":"101","author":"Guillette","year":"1996","journal-title":"Gen Comp Endocrinol"},{"key":"2021103112031460500_ref20","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1002\/jez.434","article-title":"Sperm storage in the oviduct of the American alligator","volume":"309","author":"Gist","year":"2008","journal-title":"J Exp Zool Part A Ecol Genet Physiol"},{"key":"2021103112031460500_ref21","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1002\/1097-4687(200008)245:2<168::AID-JMOR7>3.0.CO;2-1","article-title":"Morphology of the cloaca in the estuarine crocodile, Crocodylus porosus, and its plastic response to salinity","volume":"245","author":"Kuchel","year":"2000","journal-title":"J Morphol"},{"key":"2021103112031460500_ref22","doi-asserted-by":"crossref","first-page":"293","DOI":"10.5603\/FM.a2017.0098","article-title":"The morphological characters of the male external genitalia of the European hedgehog (Erinaceus europaeus)","volume":"77","author":"Akbari","year":"2018","journal-title":"Folia Morphol"},{"key":"2021103112031460500_ref23","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.jcz.2015.08.001","article-title":"Penile histomorphology of the neotropical bat Eptesicus furinalis (Chiroptera: Vespertilionidae)","volume":"258","author":"Comelis","year":"2015","journal-title":"Zool Anz"},{"key":"2021103112031460500_ref24","doi-asserted-by":"crossref","first-page":"463","DOI":"10.2108\/zsj.22.463","article-title":"The morphological and histological characters of the male external genitalia of the house musk shrew, Suncus murinus","volume":"22","author":"Kamikawa-Miyado","year":"2005","journal-title":"Zoolog Sci"},{"key":"2021103112031460500_ref25","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1242\/jeb.202.3.253","article-title":"Expansion of the tunica albuginea during penile inflation in the nine-banded armadillo (Dasypus novemcinctus)","volume":"202","author":"Kelly","year":"1999","journal-title":"J Exp Biol"},{"key":"2021103112031460500_ref26","first-page":"261","article-title":"The evolution of genital shape variation in female cetaceans","volume":"72","author":"Orbach","year":"2018","journal-title":"Evolution (N Y)"},{"key":"2021103112031460500_ref27","volume-title":"Experimental Alligator Harvest","author":"Woodward","year":"1992"},{"key":"2021103112031460500_ref28","volume-title":"Bancroft\u2019s Theory and Practice of Histological Techniques","author":"Suvarna","year":"2008","edition":"8th"},{"key":"2021103112031460500_ref29","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1369\/0022155414545787","article-title":"Picrosirius red staining","volume":"62","author":"Lattouf","year":"2014","journal-title":"J Histochem Cytochem"},{"key":"2021103112031460500_ref30","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1369\/0022155417718541","article-title":"Fluorescence of Picrosirius red multiplexed with immunohistochemistry for the quantitative assessment of collagen in tissue sections","volume":"65","author":"Wegner","year":"2017","journal-title":"J Histochem Cytochem"},{"key":"2021103112031460500_ref31","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.1002128","article-title":"Beyond bar and line graphs: Time for a new data presentation paradigm","volume":"13","author":"Weissgerber","year":"2015","journal-title":"PLoS Biol"},{"key":"2021103112031460500_ref32","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511721946.003","volume-title":"Sexual selection by cryptic female choice in insects and arachnids","author":"Eberhard","year":"1997"},{"key":"2021103112031460500_ref33","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1111\/j.1469-185X.2010.00140.x","article-title":"Sperm competition and ejaculate economics","volume":"85","author":"Parker","year":"2010","journal-title":"Biol Rev Camb Philos Soc"},{"key":"2021103112031460500_ref34","doi-asserted-by":"crossref","DOI":"10.1515\/9781400850600","volume-title":"Sexual Conflict","author":"Arnqvist","year":"2005"},{"key":"2021103112031460500_ref35","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1093\/icb\/17.1.225","article-title":"Social signals and behaviours of adult alligators and crocodiles","volume":"17","author":"Garrick","year":"1977","journal-title":"Am Zool"},{"key":"2021103112031460500_ref36","first-page":"75","article-title":"Social behavior in captive Cuban crocodiles (Crocodylus rhombifer) at the Smithsonian\u2019s National Zoological Park","volume":"48","author":"Augustine","year":"2017","journal-title":"Herpetol Rev"},{"key":"2021103112031460500_ref37","doi-asserted-by":"crossref","DOI":"10.1353\/book.72661","volume-title":"Alligators: The Illustrated Guide to Their Biology, Behavior, and Conservation","author":"Vliet","year":"2020"},{"key":"2021103112031460500_ref38","first-page":"398","article-title":"Mating behavior in three Australian Chelid turtles","volume":"34","author":"Murphy","year":"2013","journal-title":"Herpetologica"},{"key":"2021103112031460500_ref39","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1163\/156853808784124901","article-title":"An analysis of courtship behaviour in the four-eyed spotted turtle, Sacalia quadriocellata (Reptilia: Testudines: Geoemydidae)","volume":"29","author":"Fu","year":"2008","journal-title":"Amphibia-Reptilia"},{"key":"2021103112031460500_ref40","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1098\/rsbl.2012.0361","article-title":"Caught in the act: The first record of copulating fossil vertebrates","volume":"8","author":"Joyce","year":"2012","journal-title":"Biol Lett"},{"key":"2021103112031460500_ref41","first-page":"169","article-title":"The genus Emydura (Testudines: Chelidae) in new Guinea with notes on the penial morphology of Pleurodira. Advances in herpetology and evolutionary biology. Cambridge, MA: Museum of Comparative","author":"McDowell","year":"1983","journal-title":"Fortschr Zool"},{"key":"2021103112031460500_ref42","first-page":"499","article-title":"Reproductive biology of captive green sea turtles Chelonia mydas","volume":"20","author":"Wood","year":"1980","journal-title":"Integr Comp Biol"},{"key":"2021103112031460500_ref43","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.aquaculture.2017.10.026","article-title":"Digital massage for semen collection, evaluation and extension in Malaysian estuarine crocodile (Crocodylus porosus)","volume":"483","author":"Fitri","year":"2018","journal-title":"Aquaculture"},{"key":"2021103112031460500_ref44","doi-asserted-by":"crossref","first-page":"631","DOI":"10.3382\/ps.2007-00527","article-title":"Morphology of the Turkey vagina with and without an egg mass in the uterus","volume":"88","author":"Bakst","year":"2009","journal-title":"Poult Sci"},{"key":"2021103112031460500_ref45","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0150245","article-title":"Multiple paternity in a reintroduced population of the Orinoco crocodile (Crocodylus intermedius) at the El Fr\u00edo Biological Station, Venezuela","volume":"11","author":"Rossi Lafferriere","year":"2016","journal-title":"PLoS One"},{"key":"2021103112031460500_ref46","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1046\/j.1365-294X.2001.01241.x","article-title":"Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis","volume":"10","author":"Davis","year":"2001","journal-title":"Mol Ecol"},{"key":"2021103112031460500_ref47","doi-asserted-by":"crossref","first-page":"4508","DOI":"10.1111\/j.1365-294X.2009.04373.x","article-title":"Multiyear multiple paternity and mate fidelity in the American alligator, Alligator mississippiensis","volume":"18","author":"Lance","year":"2009","journal-title":"Mol Ecol"},{"key":"2021103112031460500_ref48","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1002\/jez.500","article-title":"Evidence of multiple paternity in Morelet\u2019s crocodile (Crocodylus moreletii ) in Belize, CA, inferred from microsatellite markers","volume":"309A","author":"McVay","year":"2008","journal-title":"J Exp Zool Part A Ecol Genet Physiol"},{"key":"2021103112031460500_ref49","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.ygcen.2018.10.003","article-title":"The external genitalia in juvenile Caiman latirostris differ in hormone sex determinate-female from temperature sex determinate-female","volume":"273","author":"Tavalieri","year":"2019","journal-title":"Gen Comp Endocrinol"},{"key":"2021103112031460500_ref50","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/j.tree.2017.08.009","article-title":"Cryptic female choice revisited: A response to Firman et\u00a0al","volume":"32","author":"Eberhard","year":"2017","journal-title":"Trends Ecol Evol"},{"key":"2021103112031460500_ref51","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1002\/jmor.10714","article-title":"Seasonal variation of the oviduct of the american alligator, Alligator mississippiensis (Reptilia: Crocodylia)","volume":"270","author":"Bagwill","year":"2009","journal-title":"J Morphol"},{"key":"2021103112031460500_ref52","first-page":"115","volume-title":"Reproductive Biology and Phylogeny of Birds. Part A:Phylogeny, Morphology, Hormones and Fertilization","author":"Montgomerie","year":"2007"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioaa197\/35280773\/ioaa197.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/104\/2\/374\/36234212\/ioaa197.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/104\/2\/374\/36234212\/ioaa197.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,16]],"date-time":"2024-08-16T15:00:52Z","timestamp":1723820452000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/104\/2\/374\/5941977"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,28]]},"references-count":52,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,10,28]]},"published-print":{"date-parts":[[2021,2,11]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioaa197","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,2]]},"published":{"date-parts":[[2020,10,28]]}}}