Major regulatory factors for reproductive performances of female chickens

Abstract

The reproductive performance of female chickens is critical for determining the efficiency of production and productivity and thus profitability. Studies have shown that the reproductive performance of female chickens is mainly regulated by the feed, hormones, genes, and light conditions. Herein, we review the major factors regulating female chicken reproductive performance and assess the reproductive organs and their functions. In the current review, we highlight how the interconnections of hormones, candidate genes, and photo-stimulation regulate female chicken reproductive hormones and thus regulate the reproductive organ performance. In this regard, the roles of main hormones [gonadotropinreleasing hormone (GnRH) and genes (GnRH-I)] in regulating sexual maturation and ovarian development and maintenance by influencing the survival and function of follicular granulosa cells were also reviewed. In addition, the current review also highlights how feeding female chickens with diets and artificial light-emitting diodes (LEDs) support the effective functioning of their reproductive capacity through the stimulation of sexual maturity at an appropriate age and regeneration of aged reproductive organs.

Keywords

Chicken reproduction / Gonadotropins / GnRH-I gene / Light emitting diodes

Conflict of interest statement

The authors declare no conflict of interest.

Funding

This work was supported by Jiangsu Provincial Seed Industry Revitalization Project [JBGS (2021)108].

Authors’ contributions

Debela Bayu Derese conceived the study, conducted the literature search, and drafted the figures. Fangxiong Shi reviewed and edited the concept and design of the study. Lizhi Lu reviewed the concept and design of the study. All authors have read and approved the final version of the manuscript.

Publisher’s Note

The Publisher of the Journal remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

[1] Desta TT. Indigenous village chicken production: A tool for poverty alleviation, the empowerment of women, and rural development. Trop Anim Health Prod 2021; 53(1):1.

[2] United Nations, Department of Economic and Social Affairs, Population Division. World urbanization prospects: The 2018 revision. New York: United Nations; 2019.

[3] Henchion M, Moloney AP, Hyland J, Zimmermann J, McCarthy S. Review: Trends for meat, milk and egg consumption for the next decades and the role played by livestock systems in the global production of proteins. Animal 2021; 15:100287.

[4] Steenson S, Buttriss JL. Healthier and more sustainable diets: What changes are needed in high‐income countries? Nutr Bull 2021; 46(3):279-309.

[5] Hannah HE, Zantena V, Martin K, Ittersumb V, De Boer IJM. The role of farm animals in a circular food system. Glob Food Secur 2019; 21:18-22.

[6] Kleyn FJ, Ciacciariello M. Future demands of the poultry industry: Will we meet our commitments sustainably in developed and developing economies? Worlds Poult Sci J 2021; 77(2):267-278.

[7] Du Y, Liu L, He Y, Dou T, Jia J, Ge C. Endocrine and genetic factors affecting egg laying performance in chickens: A review. Br Poult Sci 2020; 61(5):538-549.

[8] Pereira CG, Rabello CBV, Barros MR, Manso HECCC, Santos MJBD, Faria AG, et al. Zinc, manganese and copper amino acid complexed in laying hens’ diets affect performance, blood parameters and reproductive organs development. PLoS One 2020; 15(11):e0239229.

[9] Shen M, Li T, Lu J, Wang K, Qu L, Hou Q, et al. Effect of dietary supplementation with mulberry and moringa leaves on the chicken reproductive performance. Czech J Anim Sci 2022; 67(8):339-347.

[10] Uyanga VA, Xin Q, Sun M, Zhao J, Wang X, Jiao H, et al. Research note: Effects of dietary L-arginine on the production performance and gene expression of reproductive hormones in laying hens fed low crude protein diets. Poult Sci 2022; 101(5):101816.

[11] Yin L, Chen Q, Huang Q, Wang X, Zhang D, Lin Z, et al. Physiological role of dietary energy in the sexual maturity: Clues of body size, gonad development, and serum biochemical parameters of Chinese indigenous chicken. Poult Sci 2023; 102(12):103157.

[12] Oso OM, Metowogo K, Oke OE, Tona K. Influence of LED bulb on reproductive and production performance of different poultry species: A review. Worlds Poult Sci J 2022; 78(2):515-529.

[13] Shi L, Sun Y, Xu H, Liu Y, Li Y, Huang Z, et al. Effect of age at photostimulation on sexual maturation and egg-laying performance of layer breeders. Poult Sci 2020; 99(2):812-819.

[14] Habashy WS, Adomako K. The relationship between egg production, reproductive hormones, and the GDF9 gene in three different chicken strains. Anim Gene 2023; 27:200147.

[15] Li J, Li C, Li Q, Li G, Li W, Li H, et al. Novel regulatory factors in the hypothalamic-pituitary-ovarian axis of hens at four developmental stages. Front Genet 2020; 11:591672.

[16] Zhang J, Duan Z, Wang X, Li F, Chen J, Lai X, et al. Screening and validation of candidate genes involved in the regulation of egg yolk deposition in chicken. Poult Sci 2021; 100(6):101077.

[17] Chen Q, Duan J, Wu H, Li J, Jiang Y, Tang H, et al. Expression dynamics of gonadotropin-releasing hormone-Iand its mutual regulation with luteinizing hormone in chicken ovary and follicles. Gen Comp Endocrinol 2019; 270:96-102.

[18] Dong J, Guo C, Yang Z, Wu Y, Zhang C. Follicle-stimulating hormone alleviates ovarian aging by modulating mitophagy-and glycophagybased energy metabolism in hens. Cells 2022; 11(20):3270.

[19] Li C, Cao Y, Ren Y, Zhao Y, Wu X, Si S, et al. The adiponectin receptor agonist, AdipoRon, promotes reproductive hormone secretion and gonadal development via the hypothalamic-pituitary-gonadal axis in chickens. Poult Sci 2023; 102(2):102319.

[20] Nateghi R, Alizadeh A, Jafari Ahangari Y, Fathi R, Akhlaghi A. Stimulatory effects of fish oil and vitamin E on ovarian function of laying hen. Ital J Anim Sci 2019; 18(1):636-645.

[21] Cerrate S, Halley JT, Corzo A, Fancher BI. Effect of dietary amino acid density on broiler breeder reproductive performance. Poult Sci 2019; 98(5):2072-2079.

[22] Guler S, Asmaz E, Saricetin A, Cengiz S, Odabasi Erbay F, Demirkan E. Effects of calcium, available phosphorus and microbial phytase on ovarian FSHR and LHR expression in laying hens: Microbial phytase effect on FSHR and LHR. J Hell Vet Med Soc 2023; 74(3):6135-6142.

[23] Amevor FK, Cui Z, Du X, Ning Z, Shu G, Jin N, et al. Combination of quercetin and vitamin E supplementation promotes yolk precursor synthesis and follicle development in aging breeder hens via liver-blood- ovary signal axis. Animals 2021; 11(7):1915.

[24] Tang Y, Yin L, Liu L, Chen Q, Lin Z, Zhang D, et al. Comparative analysis of different proteins and metabolites in the liver and ovary of local breeds of chicken and commercial chickens in the later laying period. Int J Mol Sci 2023; 24(18):14394.

[25] Haryuni N, Hartutik H, Widodo E, Wahjuningsih S. Interaction effect of vitamin E-selenium supplementation and metabolic energy on reproductive performance of Joper breeders. J Ilmu Ternak Dan Vet 2021; 26(3):124.

[26] Mishra B, Jha R. Oxidative stress in the poultry gut: Potential challenges and interventions. Front Vet Sci 2019; 6:60.

[27] Amevor FK, Cui Z, Du X, Ning Z, Deng X, Xu D, et al. Synergy between dietary quercetin and vitamin E supplementation in aged hen’s diet improves hatching traits, embryo quality, and antioxidant capacity of chicks hatched from eggs subjected to prolonged storage. Front Physiol 2022; 13:873551.

[28] Yaripour M, Seidavi A, Dadashbeiki M, Laudadio V, Tufarelli V, Ragni M, et al. Impact of dietary supra-nutritional levels of vitamins A and E on fertility traits of broiler breeder hens in late production phase. Agriculture 2018; 8(10):149.

[29] Brady K, Porter TE, Liu HC, Long JA. Characterization of the hypothalamo-pituitary-gonadal axis in low and high egg producing turkey hens. Poult Sci 2020; 99(2):1163-1173.

[30] Zhang BB, Li XN, Li MX, Sun YY, Shi YX, Ma TH. miR-140-3p promotes follicle granulosa cell proliferation and steroid hormone synthesis via targeting AMH in chickens. Theriogenology 2023; 202:84-92.

[31] Yu S, Wang G, Liao J, Tang M, Chen J. Identification of differentially expressed genes associated with egg production in black-boned chicken. Br Poult Sci 2020; 61(4):350-356.

[32] Guo C, Liu G, Zhao D, Mi Y, Zhang C, Li J. Interaction of follicle-stimulating hormone and stem cell factor to promote primordial follicle assembly in the chicken. Front Endocrinol 2019; 10:91.

[33] Stanić D, Plećaš-Solarović B, Mirković D, Jovanović P, Dronjak S, Marković B, et al. Oxytocin in corticosterone-induced chronic stress model: Focus on adrenal gland function. Psychoneuroendocrinology 2017; 80:137-146.

[34] Nicol B, Estermann MA, Yao HHC, Mellouk N. Becoming female: Ovarian differentiation from an evolutionary perspective. Front Cell Dev Biol 2022; 10:944776.

[35] Grzegorzewska AK, Sechman A, Paczoska-Eliasiewicz HE, Rząsa J. The expression of pituitary FSHβ and LHβ mRNA and gonadal FSH and LH receptor mRNA in the chicken embryo. Reprod Biol 2009; 9(3):253-269.

[36] Prastiya RA, Madyawati SP, Sari SY, Nugroho AP. Effect of follicle-stimulating hormone and luteinizing hormone levels on egg-laying frequency in hens. Vet World 2022; 15(12):2890-2895. doi: 10.14202/vetworld.2022.2890-2895.

[37] Natsir MH, Ciptadi G, Susilawati TI. Egg production, fertility, hatchability and luteinizing hormone profile of progesterone hormone injected to arabic gold chicken (Gallus turcicus). J Worlds Poult Res 2021; 11(1):73-82.

[38] Long H, Zhao Y, Wang T, Ning Z, Xin H. Effect of light-emitting diode vs. fluorescent lighting on laying hens in aviary hen houses: Part 1- Operational characteristics of lights and production traits of hens. Poult Sci 2016; 95(1):1-11.

[39] Akhtar MF, Shafiq M, Ali I. Improving gander reproductive efficacy in the context of globally sustainable goose production. Animals 2021; 12(1):44.

[40] Li P, Zhao Y, Yan S, Song B, Liu Y, Gao M, et al. Soya saponin improves egg-laying performance and immune function of laying hens. J Anim Sci Biotechnol 2021; 12(1):126.

[41] Wang Y, Li Y, Yang H, Wang Z. Effect of photoperiod on the egg production, plasma luteinizing hormone, follicle-stimulating hormone, gonadal hormones, and mRNA levels of LH and FSH in the hypothalamic-pituitary-gonadal axis of pigeons. Braz J Poult Sci 2019; 21(4): eRBCA-2018-0931.

[42] Zhang S, Xia X, Wang L, Li R, Yang M, Wangs S. Associations between forkhead box L2 expression and ovary development in laying hens. Kafkas Univ Vet Fak Derg 2019; 25(3):305-309.

[43] Hsueh AJW, Kawamura K, Cheng Y, Fauser BCJM. Intraovarian control of early folliculogenesis. Endocr Rev 2015; 36(1):1-24.

[44] Yu J, Yan L, Chen Z, Li H, Ying S, Zhu H, et al. Investigating right ovary degeneration in chick embryos by transcriptome sequencing. J Reprod Dev 2017; 63(3):295-303.

[45] Hirst CE, Major AT, Smith CA. Sex determination and gonadal sex differentiation in the chicken model. Int J Dev Biol 2018; 62(1-2-3): 153-166.

[46] Johnson PA. Follicle selection in the avian ovary. Reprod Domest Anim 2012; 47:283-287.

[47] You S, Bridgham JT, Foster DN, Johnson AL. Characterization of the chicken follicle-stimulating hormone receptor (cFSH-R) complementary deoxyribonucleic acid, and expression of cFSH-R messenger ribonucleic acid in the ovary. Biol Reprod 1996; 55(5):1055-1062.

[48] Charlier C, Montfort J, Chabrol O, Brisard D, Nguyen T, Le Cam A, et al. Oocyte-somatic cells interactions, lessons from evolution. BMC Genomics 2012; 13(1):560.

[49] Liu X, Qiao P, Jiang A, Jiang J, Han H, Wang L, et al. Paracrine regulation of steroidogenesis in theca cells by granulosa cells derived from mouse preantral follicles. BioMed Res Int 2015; 2015:925691. doi: 10.1155/2015/925691.

[50] Qiu M, Quan F, Han C, Wu B, Liu J, Yang Z, et al. Effects of granulosa cells on steroidogenesis, proliferation and apoptosis of stromal cells and theca cells derived from the goat ovary. J Steroid Biochem Mol Biol 2013; 138:325-333.

[51] Dougherty DC, Sanders MM. Estrogen action: Revitalization of the chick oviduct model. Trends Endocrinol Metab 2005; 16(9):414-419.

[52] Yin Z, Lian L, Zhu F, Zhang ZH, Hincke M, Yang N, et al. The transcriptome landscapes of ovary and three oviduct segments during chicken (Gallus gallus) egg formation. Genomics 2020; 112(1):243-251.

[53] Luan X, Liu D, Cao Z, Luo L, Liu M, Gao M, et al. Transcriptome profiling identifies differentially expressed genes in Huoyan goose ovaries between the laying period and ceased period. PLoS One 2014; 9(11):e113211.

[54] Hrabia A, Leśniak-Walentyn A, Ocłoń E, Sechman A. Changes in proliferating and apoptotic markers in the oviductal magnum of chickens during sexual maturation. Theriogenology 2016; 85(9):1590-1598.

[55] Yoshimura Y, Barua A. Female reproductive system and immunology. Avian Reprod Behav Mol 2017; 1001:33-57. doi: 10.1007/978-981-103975-1_3.

[56] Hrabia A. Reproduction in the female. Sturkie Avian Physiol 2022; 941-986. doi: 10.1016/B978-0-12-819770-7.00002-5.

[57] Zhang Q, Zhu F, Liu L, Zheng CW, Wang DH, Hou ZC, et al. Integrating transcriptome and genome re-sequencing data to identify key genes and mutations affecting chicken eggshell qualities. PLoS One 2015; 10(5):e0125890.

[58] Wang Z, Kong L, Zhu L, Hu X, Su P, Song Z. The mixed application of organic and inorganic selenium shows better effects on incubation and progeny parameters. Poult Sci 2021; 100(2):1132-1141.

[59] El-Hussein OM, Soliman AZM, El-Sherif HMR, Fouad AM. Influence of dietary vitamin A, zinc and copper on productive and reproductive performance of broiler breeders. Int J Poult Sci 2018; 17(3):140-146.

[60] Yang J, Ding XM, Bai SP, Wang JP, Zeng QF, Peng HW, et al. Effects of dietary vitamin E supplementation on laying performance, hatchability, and antioxidant status in molted broiler breeder hens. J Appl Poult Res 2021; 30(3):100184.

[61] Shi H, Li B, Tong Q, Zheng W, Zeng D, Feng G. Effects of LED light color and intensity on feather pecking and fear responses of layer breeders in natural mating colony cages. Animals 2019; 9(10):814.

[62] Abd El-Hack ME, Mahrose K, Arif M, Chaudhry MT, Saadeldin IM, Saeed M, et al. Alleviating the environmental heat burden on laying hens by feeding on diets enriched with certain antioxidants (vitamin E and selenium) individually or combined. Environ Sci Pollut Res 2017; 24:10708-10717.

[63] Emamverdi M, Zare-Shahneh A, Zhandi M, Zaghari M, Minai-Tehrani D, Khodaei-Motlagh M. An improvement in productive and reproductive performance of aged broiler breeder hens by dietary supplementation of organic selenium. Theriogenology 2019; 126:279-285.

[64] El-Tarabany MS, Nassan MA, Salah AS. Royal jelly improves the morphology of the reproductive tract, internal egg quality, and blood biochemical parameters in laying hens at the late stage of production. Animals 2021; 11(7):1861.

[65] He W, Wang H, Tang C, Zhao Q, Zhang J. Dietary supplementation with astaxanthin alleviates ovarian aging in aged laying hens by enhancing antioxidant capacity and increasing reproductive hormones. Poult Sci 2023; 102(1):102258.

[66] Richards MP, Proszkowiec-Weglarz M. Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult Sci 2007; 86(7):1478-1490.

[67] Barbe A, Mellouk N, Ramé C, Grandhaye J, Staub C, Venturi E, et al. A grape seed extract maternal dietary supplementation in reproductive hens reduces oxidative stress associated to modulation of plasma and tissue adipokines expression and improves viability of offsprings. PLoS One 2020; 15(4):e0231131.

[68] Bédécarrats GY, Baxter M, Sparling B. An updated model to describe the neuroendocrine control of reproduction in chickens. Gen Comp Endocrinol 2016; 227:58-63.

[69] Maddineni SR, Ocón-Grove OM, Krzysik-Walker SM, Hendricks GL, Ramachandran R. Gonadotropin-inhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: Potential role of GnIH in follicular maturation. Reproduction 2008; 135(2):267-274.

[70] Stamatiades GA, Carroll RS, Kaiser UB. GnRH-A key regulator of FSH. Endocrinology 2019; 160(1):57-67.

[71] Jonak CR, Lainez NM, Roybal LL, Williamson AD, Coss D. c-JUN dimerization protein 2 (JDP2) is a transcriptional repressor of follicle-stimulating hormone β (FSH β) and is required for preventing premature reproductive senescence in female mice. J Biol Chem 2017; 292(7):26462659.

[72] Han S, Wang Y, Liu L, Li D, Liu Z, Shen X, et al. Influence of three lighting regimes during ten weeks growth phase on laying performance, plasma levels-and tissue specific gene expression- of reproductive hormones in Pengxian yellow pullets. PLoS One 2017; 12(5):e0177358.

[73] Mishra B, Sah N, Wasti S. Genetic and hormonal regulation of egg formation in the oviduct of laying hens. Poultry 2020. doi: 10.5772/intechopen.85011.

[74] Luna M, Martínez-Moreno CG, Ahumada-Solórzano MS, Harvey S, Carranza M, Arámburo C. Extrapituitary growth hormone in the chicken reproductive system. Gen Comp Endocrinol 2014; 203:60-68.

[75] Socha JK, Hrabia A. Response of the chicken ovary to GH treatment during a pause in laying induced by fasting. Domest Anim Endocrinol 2019; 69:84-95.

[76] Hu S, Duggavathi R, Zadworny D. Regulatory mechanisms underlying the expression of prolactin receptor in chicken granulosa cells. PLoS One 2017; 12(1):e0170409.

[77] González-Morán MG, González-Arenas A, Germán-Castelán L, Camacho-Arroyo I. Changes in the content of sex steroid hormone receptors in the growing and regressing ovaries of Gallus domesticus during development. Gen Comp Endocrinol 2013; 189:51-58.

[78] Rangel PL, Sharp PJ, Gutierrez CG. Testosterone antagonist (flutamide) blocks ovulation and preovulatory surges of progesterone, luteinizing hormone and oestradiol in laying hens. Reproduction 2006; 131(6):11091114.

[79] Siopes TD, Millam JR, Steinman MQ. Initiating egg production in turkey breeder hens: Thyroid hormone involvement. Poult Sci 2010; 89(10):2265-2272.

[80] Sechman A. The role of thyroid hormones in regulation of chicken ovarian steroidogenesis. Gen Comp Endocrinol 2013; 190:68-75.

[81] Bobadilla-Mendez MF, Rojas-Granados CP, Andrade EF, Retes PL, Ferreira LG, Alvarenga RR, et al. Effect of different light sources on reproductive anatomy and physiology of Japanese quail (Coturnix coturnix japonica). Anim Reprod Sci 2016; 168:50-56.

[82] Shi L, Sun Y, Xu H, Liu Y, Li Y, Huang Z, et al. Effect of age at photostimulation on reproductive performance of Beijing-You chicken breeders. Poult Sci 2019; 98(10):4522-4529.

[83] Akyüz HÇ, Onbaşilar EE. Light wavelength on different poultry species. Worlds Poult Sci J 2018; 74(1):79-88.

[84] Geng AL, Zhang Y, Zhang J, Wang HH, Chu Q, Yan ZX, et al. Effects of light regime on circadian rhythmic behavior and reproductive parameters in native laying hens. Poult Sci 2022; 10(5)1: 101808.

[85] El-Emam H, Ateya A, Abou-Ismail U, El-Araby I, Fouda M. Very cool white LED light improves reproductive performance and up-regulates expression of reproductive genes in layers. Ank Üniversitesi Vet Fakültesi Derg 2022; 69(4):401-408.

[86] Lizneva D, Rahimova A, Kim SM, Atabiekov I, Javaid S, Alamoush B. FSH beyond fertility. Front Endocrinol (Lausanne) 2019; 10:136.

[87] Ying W, Yang-bai L, Hai-ming Y, Zhi-yue W. Effect of monochromatic light on plasma and mRNA levels of luteinising hormone, follicle-stimulating hormone, and their receptors in the hypothalamic-pituitary- gonadal axis of pigeons. Avian Biol Res 2018; 11(3):196-203.

[88] Chowdhury VS, Yamamoto K, Ubuka T, Bentley GE, Hattori A, Tsutsui K. Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus. Endocrinology 2010; 151(1):271-280.

[89] Luo W, Gu L, Li J, Gong Y. Transcriptome sequencing revealed that knocking down FOXL2 affected cell proliferation, the cell cycle, and DNA replication in chicken pre-ovulatory follicle cells. PLoS One 2020; 15(7):e0234795.

[90] Geiersbach KB, Jarboe EA, Jahromi MS, Baker CL, Paxton CN, Tripp SR, et al. FOXL2 mutation and large-scale genomic imbalances in adult granulosa cell tumors of the ovary. Cancer Genet 2011; 204(11):596-602.

[91] Shen X, Zhao X, He H, Zhang Y, Zhu Q, Yin H. Transcriptome profiling reveals SLC5A5 regulates chicken ovarian follicle granulosa cell proliferation, apoptosis, and steroid hormone synthesis. Poult Sci 2024; 103(1):103241.

[92] De Vries L, Gat-Yablonski G, Dror N, Singer A, Phillip M. A novel MKRN3 missense mutation causing familial precocious puberty. Hum Reprod 2014; 29(12):2838-2843.

[93] Chen B, Liang G, Zhu X, Tan Y, Xu J, Wu H, et al. Gene expression profiling in ovaries and association analyses reveal HEP21 as a candidate gene for sexual maturity in chickens. Animals 2020; 10(2):181.

[94] Vijayakumar N, Op De Macks Z, Shirtcliff EA, Pfeifer JH. Puberty and the human brain: Insights into adolescent development. Neurosci Biobehav Rev 2018; 92:417-436.

[95] Jin S, Sun D, Xi Q, Dong X, Song D, Fu H, et al. Identification of genes in the hypothalamus-pituitary-gonad axis in the brain of Amur sturgeons (Acipenser schrenckii) by comparative transcriptome analysis in relation to kisspeptin treatment. Gene 2016; 595(1):53-61.

[96] Shen M, Qu L, Ma M, Dou T, Lu J, Guo J, et al. A genome-wide study to identify genes responsible for oviduct development in chickens. PLoS One 2017; 12(12):e0189955.

[97] Liu L, Fan Y, Zhang Z, Yang C, Geng T, Gong D, et al. Analysis of gene expression and regulation implicates C2H9orf152 has an important role in calcium metabolism and chicken reproduction. Anim Reprod Sci 2017; 176:1-10.