Differences in Reproductive Performance, Intestinal Tissue Morphology, Ovarian Function and Caecal Microbiota of Broiler Breeders with Different Egg Production Levels

  • YANG Zengqiao ,
  • DING Xuemei ,
  • BAI Shiping ,
  • ZENG Qiufeng ,
  • ZHANG Keying ,
  • WANG Jianping
Expand
  • Sichuan Key Laboratory of Animal Disease-Resistance Nutrition, Key Laboratory for Animal Disease-Resistance Nutrition and Feed, Ministry of Agriculture, Key Laboratory for Animal Disease-Resistance Nutrition, Ministry of Education, Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China

Received date: 2020-06-18

  Online published: 2021-01-18

Abstract

The present study was to compare the differences in reproductive performance, intestinal tissue morphology, ovarian function and caecal microbiota of broiler breeders with different egg production levels. In the experiment, 5 000 Arbor Acres parent broiler breeders of 37 weeks old in the same house were used and recorded the egg laying rate, fertilization rate and hatching rate of each breeding chicken for 2 weeks. Then every 90 broilers with high and average egg production levels were selected and set into 2 groups of average reproductive group [AR group with (79.34±0.49)% egg laying rate] and high reproductive group [HR group with (90.03±0.34)% egg laying rate] with 10 replicates per group and 9 birds per replicate. The trial lasted for 6 weeks after a 2-week adaption. The results showed that, compared with the AR group, the egg laying rate and hatchability of setting eggs were significantly higher (P<0.05), the serum alanine transaminase activity was significantly lower (P<0.05), the villus height in jejunum was significantly lower (P<0.05), the crypt depth in ileum was significantly higher (P<0.05), the apoptosis rate of ovarian cells was extremely significantly lower (P<0.05), the gene expression levels of pro-apoptotic protein as caspase 9 and follicle development related proteins as bone morphogenetic protein receptor 1B (BMPR1B), a novel prolactin-like protein in chickens (PRL-L) and GATA4 in ovary were significantly increased (P<0.05), the relative abundance of Firmicutes and Lactobacillus in cecum was significantly higher (P<0.05), and the relative abundance of Bacteroidetes and Spirochaetes in cecum was significantly lower (P<0.05) of broilers in the HR group. The Bacteroidetes relative abundance in cecum of broiler breeders was significantly negatively correlated with the expression levels of BMPR1B and GATA4 in ovary (P<0.05), the Firmicutes relative abundance in cecum was significantly positively correlated with the expression levels of BMPR1B and GATA4 in ovary (P<0.05), the Lactobacillus relative abundance in cecum was significantly positively correlated with the expression levels of caspase 9, BMPR1B, GATA4 and PRL-L in ovary (P<0.05), and the Helicobacter relative abundance in cecum was extremely significantly positively correlated with the GATA4 expression level in ovary (P<0.01). To sum up, the results indicate that there are significant differences in intestinal tissue morphology, caecal microflora and ovarian function of broiler breeders with different egg production levels, and the relative abundance of Firmicutes and Lactobacillus in cecum is closely related to high reproductive performance.

Cite this article

YANG Zengqiao , DING Xuemei , BAI Shiping , ZENG Qiufeng , ZHANG Keying , WANG Jianping . Differences in Reproductive Performance, Intestinal Tissue Morphology, Ovarian Function and Caecal Microbiota of Broiler Breeders with Different Egg Production Levels[J]. Chinese Journal of Animal Nutrition, 2021 , 33(1) : 270 -284 . DOI: 10.3969/j.issn.1006-267x.2021.01.028

References

[1] LEY R E,PETERSON D A,GORDON J I.Ecological and evolutionary forces shaping microbial diversity in the human intestine[J].Cell,2006,124(4):837-848.  
[2] MCKNITE A M,PEREZ-MUNOZ M E,LU L,et al.Murine gut microbiota is defined by host Genetics and modulates variation of metabolic traits[J].PLoS One,2012,7(6):e39191.
[3] OAKLEY B B,LILLEHOJ H S,KOGUT M H,et al.The chicken gastrointestinal microbiome[J].FEMS Microbiology Letters,2015,360(2):100-112.
[4] SHAUFI M A M,SIEO C C,CHONG C W,et al.Deciphering chicken gut microbial dynamics based on high-throughput 16S rRNA metagenomics analyses[J].Gut Pathogens,2015,7(1):4.
[5] WAITE D W,TAYLOR M W.Exploring the avian gut microbiota:current trends and future directions[J].Frontiers in Microbiology,2015,6:673.
[6] CLEMENTE J,URSELL L,PARFREY L W,et al.The impact of the gut microbiota on human health:an integrative view[J].Cell,2012,148(6):1258-1270.  
[7] BÄCKHED F,DING H,WANG T,et al.The gut microbiota as an environmental factor that regulates fat storage[J].Proceeding of the National Academy of Sicences of the Unitied States of America,2004,101(44):15718-15723.
[8] TURNBAUGH P J,LEY R E,MAHOWALD M A,et al.An obesity-associated gut microbiome with increased capacity for energy harvest[J].Nature,2006,444(7122):1027-1031.  
[9] SONNENBURG J L,BÄCKHED F.Diet-microbiota interactions as moderators of human metabolism[J].Nature,2016,535(7610):56-64.  
[10] INSENSER M,MURRI M,DEL CAMPO R,et al.Gut microbiota and the polycystic ovary Syndrome:influence of sex,sex hormones,and obesity[J].The Journal of Clinical Endocrinology & Metabolism,2018,103(7):2552-2562.  
[11] LOMBARDI P,GOLDIN B,BOUTIN E,et al.Metabolism of androgens and estrogens by human fecal microorganisms[J].Journal of Steroid Biochemistry,1978,9(8):795-801.  
[12] DONOVA M V,EGOROVA O V.Microbial steroid transformations:current state and prospects[J].Applied Microbiology and Biotechnology,2012,94(6):1423-1447.  
[13] 张亚楠.蛋鸡肠道微生物菌群结构特征与产蛋水平关联性研究[D].硕士学位论文.郑州:河南农业大学,2016. ZHANG Y N.Association analysis between intestinal microbiota with egg laying levels in hens[D].Master's Thesis.Zhengzhou:Henan Agriculture University,2016.(in Chinese)
[14] 陈娜娜,马莲香,侯川川,等.蛋氨酸锌对蛋鸡生产性能、肠道形态、组织学结构及盲肠微生物菌群的影响[J].中国畜牧杂志,2017,53(9):102-108. CHEN N N,MA L X,HOU C C,et al.Effects of zinc-methionine on performance,intestinal morphology,histological structure and cecal microbial flora of laying hens[J].Chinese Journal of Animal Science,2017,53(9):102-108.(in Chinese)
[15] 熊立根.芦笋秸秆提取物对蛋鸡生产性能及生化指标的调控作用[D].硕士学位论文.南昌:江西农业大学,2013. XIONG L G.Roles of asparagus straw extract in regulation of performance and biochemical indexes to layer[D].Master's Thesis.Nanchang:Jiangxi Agricultrue University,2013.(in Chinese)
[16] APAJALAHTI J,VIENOLA K.Interaction between chicken intestinal microbiota and protein digestion[J].Animal Feed Science and Technology,2016,221:323-330.
[17] LU N S,LI M J,LEI H L,et al.Butyric acid regulates progesterone and estradiol secretion via cAMP signaling pathway in porcine granulosa cells[J].Journal of Steroid Biochemistry and Molecular Biology,2017,172:89-97.
[18] 刘松珍,张雁,张名位,等.肠道短链脂肪酸产生机制及生理功能的研究进展[J].广东农业科学,2013,40(11):99-103. LIU S Z,ZHANG Y,ZHANG M W,et al.Research progress on producing mechanism and physiological functions of intestinal short chain fatty acids[J].Guangdong Agricultural Sciences,2013,40(11):99-103.(in Chinese)
[19] CELI P,VERLHAC V,CALVO E P,et al.Biomarkers of gastrointestinal functionality in animal nutrition and health[J].Animal Feed Science and Technology,2019,250:9-31.
[20] TREMELLEN K,PEARCE K.Dysbiosis of gut microbiota (DOGMA)-a novel theory for the development of polycystic ovarian syndrome[J].Medical Hypotheses,2012,79(1):104-112.  
[21] POLANSKY O,SEKELOVA Z,FALDYNOVA M,et al.Characterisation of the most important metabolic pathways and biological processes expressed in chicken caecal microbiota[J].Applied and Environmental Microbiology,2015,82(5):AEM.03473-15.
[22] STANLEY D,HUGHES R J,MOORE R J.Microbiota of the chicken gastrointestinal tract:influence on health,productivity and disease[J].Applied Microbiology and Biotechnology,2014,98(10):4301-4310.  
[23] TURNBAUGH P J,HAMADY M,YATSUNENKO T,et al.A core gut microbiome in obese and lean twins[J].Nature,2008,457(7228):480-484.
[24] JUMPERTZ R,LE D S,TURNBAUGH P J,et al.Energy-balance studies reveal associations between gut microbes,caloric load,and nutrient absorption in humans[J].The American Journal of Clinical Nutrition,2011,94(1):58-65.  
[25] STEPHENS C P,HAMPSON D J.Intestinal spirochete infections of chickens:a review of disease associations,epidemiology and control[J].Animal Health Research Reviews,2001,2(1):83-91.  
[26] DWARS R M,DAVELAAR F G,SMIT H F.Infection of broiler parent hens with avian intestinal spirochaetes:effects on egg production and chick quality[J].Avian Pathology,1993,22(4):693-701.  
[27] RICHARDS M P,POCH S M,COON C N,et al.Feed restriction significantly alters lipogenic gene expression in broiler breeder chickens[J].The Journal of Nutrition,2003,133(3):707-715.  
[28] RICHARDS M P,PROSZKOWIEC-WEGLARZ M.Mechanisms regulating feed intake,energy expenditure,and body weight in poultry[J].Poultry Science,2007,86(7):1478-1490.  
[29] CHEN S E,MCMURTRY J P,WALZEM R L.Overfeeding-induced ovarian dysfunction in broiler breeder hens is associated with lipotoxicity[J].Poultry Science,2006,85(1):70-81.  
[30] WALZEM R L,DAVIS P A,HANSEN R J.Overfeeding increases very low density lipoprotein diameter and causes the appearance of a unique lipoprotein particle in association with failed yolk deposition[J].Journal of Lipid Research,1994,35(8):1354-1366.  
[31] PAN Y E,LIU Z C,CHANG C J,et al.Ceramide accumulation and up-regulation of proinflammatory interleukin-1β exemplify lipotoxicity to mediate declines of reproductive efficacy of broiler hens[J].Domestic Animal Endocrinology,2012,42(3):183-194.  
[32] BILGILI S F,RENDEN J A.Relationship of body fat to fertility in broiler breeder hens[J].Poultry Science,1985,64(7):1394-1396.  
[33] ROSEN V,THIES R S,LYONS K.Signaling pathways in skeletal formation:a role for BMP receptors[J].Annals of the New York Academy of Sciences,2010,785:59-69.
[34] BU G X,WANG C Y,CAI G Q,et al.Molecular characterization of prolactin receptor (cPRLR) gene in chickens:gene structure,tissue expression,promoter analysis,and its interaction with chicken prolactin (cPRL) and prolactin-like protein (cPRL-L)[J].Molecular and Cellular Endocrinology,2013,370(1/2):149-162.
[35] BU G X,LIANG X M,LI J,et al.Extra-pituitary prolactin (PRL) and prolactin-like protein (PRL-L) in chickens and zebrafish[J].General and Comparative Endocrinology,2015,220:143-153.
[36] 王倩倩,朱依敏.转录因子GATA-4在卵泡发育中的调节作用[J].国外医学(计划生育/生殖健康分册),2007,26(6):298-301. WANG Q Q,ZHU Y M.The regulatory role of transcription factor GATA-4 in follicular development[J].Foreign Medical Sciences:Family Planning/Reproductive Health Fascicle,2007,26(6):298-301.(in Chinese)
[37] 苟华.GATA-6过表达和干扰载体的构建及其对鹅颗粒细胞类固醇合成及相关基因的调控研究[D].硕士学文论文.成都:四川农业大学,2015. GOU H.Construction of GATA-6 eukaryotic expression and shRNA interference vectors to characterize its role on steroidogenesis in goose granulosa cells[D].Master's Thesis.Chengdu:Sichuan Agricultural University,2015.(in Chinese)
[38] KWINTKIEWICZ J,CAI Z L,STOCCO C.Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation of Cyp19 expression in rat granulosa cells[J].Molecular Endocrinology,2007,21(4):933-947.  
[39] 李富贵,刘嘉,覃飞,等.蛋鸡育成期与产蛋高峰期部分生殖激素及其受体基因变化规律研究[C]//中国畜牧兽医学会2018年学术年会禽病学分会第十九次学术研讨会论文集.南宁:中国畜牧兽医学会,2018. LI F G,LIU J,QIN F,et al.Study on the variation of partly reproductive hormones and their receptor genes in laying hens during the growth period and egg production peak period[C].Proceedings of the 19th Symposium of the Poultry Disease Branch in the 2018 Annual Academic Conference of The Chinese Association of Animal Science and Veterinary Medicine.Nanning:Chinese Association of Animal Science and Veterinary Medicine,2018.(in Chinese)
[40] JOSEPH E K,LEVINE J D.Caspase signalling in neuropathic and inflammatory pain in the rat[J].European Journal of Neuroscience,2015,20(11):2896-2902.
Outlines

/