{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T22:36:41Z","timestamp":1792276601425,"version":"4.4.0"},"reference-count":50,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T00:00:00Z","timestamp":1759881600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,12,16]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Selective breeding in laying hens has resulted in a laying rate of approximately one egg per day during their first year. Due to variability within a flock, egg-laying rates decline after the first year, leading producers to cull hens. The aim of this study was to identify physiological and molecular differences between persistent (PL, egg-laying rate\u2009=\u2009100%) and non-persistent layers (NPL, egg-laying rate \u226482%) after the first year. Forty laying hens were reared from 16 to 76\u00a0weeks of age and a subset was maintained until 96\u00a0weeks. Throughout the study, egg-laying data were recorded daily, and plasma samples and body weights were collected once to twice monthly. At 76\u00a0weeks, PL (n\u2009=\u20097) and NPL (n\u2009=\u20096) hens were identified. PL hens were heavier than NPL hens starting at 36\u00a0weeks and triiodothyronine levels decreased in PL hens from 26 to 76\u00a0weeks. At 76\u00a0weeks, ovarian tissue was collected from PL (n\u2009=\u20093) and NPL (n\u2009=\u20094) hens for follicle counts, gene expression analysis, and histological analysis. PL hens had significantly more 3\u20135 and &amp;gt;12\u00a0mm follicles, higher anti-Mullerian hormone and bone morphogenic protein 15 mRNA expression, and lower atresia rates in follicles &amp;lt;100\u00a0\u03bcm, suggesting a larger remaining ovarian reserve than NPL hens. Ovarian RNA-sequencing analysis revealed 279 differentially expressed genes between PL and NPL hens and analysis predicted the estrogen receptor as an upstream regulator. A greater understanding of the physiology and molecular patterns of persistent hens could provide insights into ovarian aging and enhance production efficiency.<\/jats:p>","DOI":"10.1093\/biolre\/ioaf227","type":"journal-article","created":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T12:15:25Z","timestamp":1759925725000},"page":"1433-1443","source":"Crossref","is-referenced-by-count":4,"title":["Characterization of persistency of lay in laying hens"],"prefix":"10.1093","volume":"113","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7675-2944","authenticated-orcid":false,"given":"Laurie","family":"Francoeur","sequence":"first","affiliation":[{"name":"Department of Animal Science, College of Agriculture and Life Sciences, Cornell University , Ithaca, NY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1812-8753","authenticated-orcid":false,"given":"Deena M","family":"Scoville","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture and Life Sciences, Cornell University , Ithaca, NY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaclyn G","family":"Ahern","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture and Life Sciences, Cornell University , Ithaca, NY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9432-8039","authenticated-orcid":false,"given":"Patricia A","family":"Johnson","sequence":"additional","affiliation":[{"name":"Department of Animal Science, College of Agriculture and Life Sciences, Cornell University , Ithaca, NY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,10,8]]},"reference":[{"key":"2025121605121220100_ref1","volume-title":"Poultry - Production and Value 2023 Summary","author":"U.S. Department of Agriculture","year":"2024"},{"key":"2025121605121220100_ref2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1080\/00071669208417478","article-title":"Follicle stimulating hormone increases serum oestradial-17\u00df concentrations, number of growing follicles and yolk deposition in aging hens (Gallus gallus domesticus) with decreased egg production","volume":"33","author":"Palmer","year":"1992","journal-title":"Br Poultry Sci"},{"key":"2025121605121220100_ref3","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1080\/00071667808416490","article-title":"Ovarian morphology and rates of ovarian follicular development in laying broiler breeders and commercial egg-producing hens","volume":"19","author":"Williams","year":"1978","journal-title":"Br Poultry Sci"},{"key":"2025121605121220100_ref6","first-page":"513","article-title":"The population of germ cells in the developing female Chick","volume":"11","author":"Hughes","year":"1963","journal-title":"J Embryol Exp Morph"},{"key":"2025121605121220100_ref7","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1111\/j.1439-0531.2012.02087.x","article-title":"Follicle selection in the avian ovary","volume":"47","author":"Johnson","year":"2012","journal-title":"Reprod Domest Anim"},{"key":"2025121605121220100_ref8","first-page":"243","volume-title":"Reproductive Biology and Phylogeny of Birds","author":"Johnson","year":"2007"},{"key":"2025121605121220100_ref9","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/0016-6480(85)90122-4","article-title":"Evidence for a positive feedback interaction between progesterone and luteinizing hormone in the induction of ovulation in the hen, Gallus domesticus","volume":"58","author":"Johnson","year":"1985","journal-title":"Gen Comp Endocrinol"},{"key":"2025121605121220100_ref10","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1210\/endo-96-4-962","article-title":"Steroid levels in follicles and the plasma of hens during the ovulatory cycle","volume":"96","author":"Shahabi","year":"1975","journal-title":"Endocrinology"},{"key":"2025121605121220100_ref11","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1677\/joe.0.0710087","article-title":"Induction of luteinizing hormone release by gonadal steroids in the ovariectomized domestic hen","volume":"71","author":"Wilson","year":"1976","journal-title":"J Endocrinol"},{"key":"2025121605121220100_ref12","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1530\/jrf.0.0740399","article-title":"Follicular growth and atresia in the ovaries of hens (Gallus domesticus) with diminished egg production rates","volume":"74","author":"Waddington","year":"1985","journal-title":"Reproduction"},{"key":"2025121605121220100_ref13","doi-asserted-by":"crossref","first-page":"3426","DOI":"10.1210\/en.2006-1383","article-title":"Epidermal growth factor (EGF) receptor ligands in the chicken ovary: I. Evidence for heparin-binding EGF-like growth factor (HB-EGF) as a potential oocyte-derived signal to control granulosa cell proliferation and HB-EGF and kit ligand expression","volume":"148","author":"Wang","year":"2007","journal-title":"Endocrinology"},{"key":"2025121605121220100_ref14","first-page":"66","article-title":"Histology of the ovary of the laying hen (Gallus domesticus)","volume":"4","author":"Apperson","year":"2017","journal-title":"Vet Sci"},{"key":"2025121605121220100_ref15","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/sj.cr.7290234","article-title":"Apoptosis in granulosa cells during follicular atresia: relationship with steroids and insulin-like growth factors","volume":"14","author":"Yu","year":"2004","journal-title":"Cell Res"},{"key":"2025121605121220100_ref16","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.ygcen.2016.06.027","article-title":"Bone morphogenetic protein 15 may promote follicle selection in the hen","volume":"235","author":"Stephens","year":"2016","journal-title":"Gen Comp Endocrinol"},{"key":"2025121605121220100_ref17","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1093\/biolre\/ioac013","article-title":"Feeding level is associated with altered liver transcriptome and follicle selection in the hen","volume":"106","author":"Stephens","year":"2022","journal-title":"Biol Reprod"},{"key":"2025121605121220100_ref18","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"2025121605121220100_ref19","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.1093\/bioinformatics\/btz931","article-title":"ShinyGO: a graphical gene-set enrichment tool for animals and plants","volume":"36","author":"Ge","year":"2020","journal-title":"Bioinformatics"},{"key":"2025121605121220100_ref20","volume-title":"QIAGEN IPA"},{"key":"2025121605121220100_ref19a","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1093\/bioinformatics\/btt703","article-title":"Causal analysis approaches in Ingenuity Pathway Analysis","volume":"30","author":"Kr\u00e4mer","year":"2014","journal-title":"Bioinformatics"},{"key":"2025121605121220100_ref21","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1095\/biolreprod.107.061879","article-title":"Expression and regulation of anti-Mullerian hormone in an oviparous species, the hen","volume":"78","author":"Johnson","year":"2008","journal-title":"Biol Reprod"},{"key":"2025121605121220100_ref22","doi-asserted-by":"crossref","first-page":"4951","DOI":"10.1210\/endo.136.11.7588229","article-title":"Anti-M\u00fcllerian hormone and anti-M\u00fcllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth","volume":"136","author":"Baarends","year":"1995","journal-title":"Endocrinology"},{"key":"2025121605121220100_ref23","doi-asserted-by":"crossref","first-page":"3228","DOI":"10.1210\/en.2005-1588","article-title":"Serum anti-M\u00fcllerian hormone levels reflect the size of the primordial follicle pool in mice","volume":"147","author":"Kevenaar","year":"2006","journal-title":"Endocrinology"},{"key":"2025121605121220100_ref24","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0015-0282(01)02993-4","article-title":"Antim\u00fcllerian hormone serum levels: a putative marker for ovarian aging","volume":"77","author":"De Vet","year":"2002","journal-title":"Fertil Steril"},{"key":"2025121605121220100_ref25","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.cca.2014.07.029","article-title":"AMH: an ovarian reserve biomarker in assisted reproduction","volume":"437","author":"Peluso","year":"2014","journal-title":"Clin Chim Acta"},{"key":"2025121605121220100_ref26","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/nrendo.2011.224","article-title":"Anti-M\u00fcllerian hormone: an ovarian reserve marker in primary ovarian insufficiency","volume":"8","author":"Visser","year":"2012","journal-title":"Nat Rev Endocrinol"},{"key":"2025121605121220100_ref27","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.ygcen.2016.06.027","article-title":"Bone morphogenetic protein 15 may promote follicle selection in the hen","volume":"235","author":"Stephens","year":"2016","journal-title":"Gen Comp Endocrinol"},{"key":"2025121605121220100_ref28","doi-asserted-by":"crossref","first-page":"106114","DOI":"10.1016\/j.anireprosci.2019.106114","article-title":"Transcriptome analysis of ovary in relatively greater and lesser egg producing Jinghai yellow chicken","volume":"208","author":"Zhang","year":"2019","journal-title":"Anim Reprod Sci"},{"key":"2025121605121220100_ref29","doi-asserted-by":"crossref","DOI":"10.1530\/rep.0.1240601","article-title":"Regulation of ovarian function: the role of anti-Mullerian hormone","volume":"124","author":"Durlinger","year":"2002","journal-title":"Reproduction"},{"key":"2025121605121220100_ref30","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.mce.2016.05.019","article-title":"Intra-cellular mechanism of anti-M\u00fcllerian hormone (AMH) in regulation of follicular development","volume":"433","author":"Hayes","year":"2016","journal-title":"Mol Cell Endocrinol"},{"key":"2025121605121220100_ref31","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1530\/jrf.0.0530141","article-title":"Age-dependent changes in the hypothalamo\u2013pituitary\u2013ovarian axis of the laying hen","volume":"53","author":"Williams","year":"1978","journal-title":"Reproduction"},{"key":"2025121605121220100_ref32","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1095\/biolreprod35.3.641","article-title":"Decreased granulosa cell luteinizing hormone sensitivity and altered thecal estradiol concentration in the aged hen, Gallus domesticus","volume":"35","author":"Johnson","year":"1986","journal-title":"Biol Reprod"},{"key":"2025121605121220100_ref33","doi-asserted-by":"crossref","first-page":"106432","DOI":"10.1016\/j.domaniend.2019.106432","article-title":"Anti-M\u00fcllerian hormone and its receptor are detected in most gonadotropin-releasing-hormone cell bodies and fibers in heifer brains","volume":"72","author":"Kereilwe","year":"2020","journal-title":"Domest Anim Endocrinol"},{"key":"2025121605121220100_ref34","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.theriogenology.2020.01.011","article-title":"Active immunization against AMH reveals its inhibitory role in the development of pre-ovulatory follicles in Zhedong white geese","volume":"144","author":"Chen","year":"2020","journal-title":"Theriogenology"},{"key":"2025121605121220100_ref35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms10055","article-title":"Novel role for anti-M\u00fcllerian hormone in the regulation of GnRH neuron excitability and hormone secretion","volume":"7","author":"Cimino","year":"2016","journal-title":"Nat Commun"},{"key":"2025121605121220100_ref36","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1530\/REP-16-0129","article-title":"Reproductive age-associated fibrosis in the stroma of the mammalian ovary","volume":"152","author":"Briley","year":"2016","journal-title":"Reproduction"},{"key":"2025121605121220100_ref37","doi-asserted-by":"crossref","first-page":"9686","DOI":"10.18632\/aging.103237","article-title":"Ovulation and ovarian wound healing are impaired with advanced reproductive age","volume":"12","author":"Mara","year":"2020","journal-title":"Aging (Albany NY)"},{"key":"2025121605121220100_ref38","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1038\/nrc3535","article-title":"The hen as a model of ovarian cancer","volume":"13","author":"Johnson","year":"2013","journal-title":"Nat Rev Cancer"},{"key":"2025121605121220100_ref39","doi-asserted-by":"crossref","first-page":"192","DOI":"10.3389\/fendo.2014.00192","article-title":"Estrogen biosynthesis and action in ovarian cancer","volume":"5","author":"Mungenast","year":"2014","journal-title":"Front Endocrinol (Lausanne)"},{"key":"2025121605121220100_ref40","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/gt.2017.69","article-title":"Targeting the CXCR4\/CXCL12 axis in treating epithelial ovarian cancer","volume":"24","author":"Mao","year":"2017","journal-title":"Gene Ther"},{"key":"2025121605121220100_ref41","first-page":"5097","article-title":"CALB1 enhances the interaction between p53 and MDM2, and inhibits the senescence of ovarian cancer cells","volume":"19","author":"Cao","year":"2019","journal-title":"Mol Med Rep"},{"key":"2025121605121220100_ref42","doi-asserted-by":"crossref","first-page":"2175","DOI":"10.1111\/j.1349-7006.2009.01285.x","article-title":"Field methylation silencing of the protocadherin 10 gene in cervical carcinogenesis as a potential specific diagnostic test from cervical scrapings","volume":"100","author":"Wang","year":"2009","journal-title":"Cancer Sci"},{"key":"2025121605121220100_ref43","doi-asserted-by":"crossref","first-page":"3841","DOI":"10.2147\/CMAR.S298072","article-title":"The clinical significance and biological function of PCDH7 in cervical cancer","volume":"13","author":"Zhang","year":"2021","journal-title":"Cancer Manag Res"},{"key":"2025121605121220100_ref44","first-page":"6281","article-title":"Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer","volume":"60","author":"Hough","year":"2000","journal-title":"Cancer Res"},{"key":"2025121605121220100_ref45","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1289\/ehp.877335","article-title":"Ovarian tumors of the hen","volume":"73","author":"Fredrickson","year":"1987","journal-title":"Environ Health Perspect"},{"key":"2025121605121220100_ref46","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1111\/IGC.0b013e3181da2c49","article-title":"The restricted ovulator chicken: a unique animal model for investigating the etiology of ovarian cancer","volume":"20","author":"Giles","year":"2010","journal-title":"Int J Gynecol Cancer"},{"key":"2025121605121220100_ref47","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1158\/1940-6207.CAPR-11-0344","article-title":"Oral contraceptives decrease the prevalence of ovarian cancer in the hen","volume":"5","author":"Trevi\u00f1o","year":"2012","journal-title":"Cancer Prev Res"},{"key":"2025121605121220100_ref48","doi-asserted-by":"crossref","first-page":"382","DOI":"10.3389\/fphys.2021.651491","article-title":"Changes in the control of the hypothalamic-pituitary gonadal axis across three differentially selected strains of laying hens (Gallus gallus domesticus)","volume":"12","author":"Hanlon","year":"2021","journal-title":"Front Physiol"},{"key":"2025121605121220100_ref49","doi-asserted-by":"crossref","first-page":"2706","DOI":"10.3390\/ani11092706","article-title":"Ad libitum feeding in broiler breeder hens alters the transcriptome of granulosa cells of pre-hierarchal follicles","volume":"11","author":"Francoeur","year":"2021","journal-title":"Animals"},{"key":"2025121605121220100_ref50","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.domaniend.2006.04.008","article-title":"Increased food intake stimulates GnRH-I, glycoprotein hormone \u03b1-subunit and follistatin mRNAs, and ovarian follicular numbers in laying broiler breeder hens","volume":"33","author":"Ciccone","year":"2007","journal-title":"Domest Anim Endocrinol"},{"key":"2025121605121220100_ref51","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.ygcen.2013.04.012","article-title":"The role of thyroid hormones in regulation of chicken ovarian steroidogenesis","volume":"190","author":"Sechman","year":"2013","journal-title":"Gen Comp Endocrinol"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioaf227\/64549456\/ioaf227.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/113\/6\/1433\/64549456\/ioaf227.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/113\/6\/1433\/64549456\/ioaf227.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,16]],"date-time":"2025-12-16T10:12:26Z","timestamp":1765879946000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/113\/6\/1433\/8277617"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,8]]},"references-count":50,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2025,10,8]]},"published-print":{"date-parts":[[2025,12,16]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioaf227","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,12]]},"published":{"date-parts":[[2025,10,8]]}}}