Abstract
In captive giant pandas (Ailuropoda melanoleuca), both urinary estrogen and progesterone levels have been dynamically measured and routinely involved in the assisted reproduction. Yet the genetic contribution to phenotypic variability on these reproductive hormone levels remains largely unknown, which may be helpful for understanding the influence of mating system on reproduction. In this study, we used the longitudinal measures of urinary estrogen and progesterone levels, which were collected on 59 female giant pandas from 2007 to 2021, for estimating the heritability and genetic correlations of 3 estrus-related indicators, including estrus length (EL), estrogen concentration (EC), and progesterone concentration (Pg). The genetic relationship matrix was derived from pedigree records, and variance components were estimated by a three-trait animal model. Our results revealed that EC had the highest heritability (± SE) of 0.47 ± 0.08, which was followed by Pg of 0.38 ± 0.10 and EL of 0.19 ± 0.08. Weak positive genetic correlations (± SE) were observed between EL and EC (0.47 ± 0.32), and between EC and Pg (0.31 ± 0.26). To our best knowledge, this is the first study to estimate heritability and genetic correlation for estrus-related indicators in captive giant pandas, which could be taken into consideration to optimize the reproduction management of this vulnerable species.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Aitken-Palmer C, Hou R, Burrell C, Zhang Z, Wang C, Spindler R, Wildt DE, Ottinger MA, Howard J (2012) Protracted reproductive seasonality in the male giant panda (Ailuropoda melanoleuca) reflected by patterns in androgen profiles, ejaculate characteristics, and selected behaviors. Biol Reprod 86:195
Cai KL, Yie SM, Zhang ZH, Wang J, Cai ZG, Luo L, Liu YL, Wang HR, Huang H, Wang CD, Huang XM, Lan JC, Hou R (2017) Urinary profiles of luteinizing hormone, estrogen and progestagen during the estrous and gestational periods in giant pandas (Ailuropoda melanoleuca). Sci Rep 7:40749
Gocinski BL, Knott KK, Roberts BM, Brown JL, Vance CK, Kouba AJ (2018) Changes in urinary androgen concentration indicate that male giant pandas (Ailuropoda melanoleuca) respond to impending female oestrus during and outside the typical spring breeding season. Reprod Fertil Dev 30:399–408
Goncalves AR, Gama LT, Antunes L, Guimarães H, Bliebernicht M, Duarte JC, Cosinha C, Rego BD, Costa PF, Guimarães T, Rocha A, Bettencourt E (2023) Impact of inbreeding and genetic parameter estimates for seminal traits in Lusitano horses. Theriogenology 208:43–51
Grigoletto L, Santana MHA, Bressan FF, Eler JP, Nogueira MFG, Kadarmideen HN, Baruselli PS, Ferraz JBS, Brito LF (2020) Genetic parameters and genome-wide association studies for anti-müllerian hormone levels and antral follicle populations measured after estrus synchronization in Nellore cattle. Animals (Basel) 10:1185
Hama N, Kanemitsu H, Sakamoto K, Oyama Y, Acosta TJ, Ishikawa O, Pengyan W, Okuda K (2008) Development and evaluation of a rapid enzyme-immunoassay system for measurement of the urinary concentration of estrone-3-glucuronide in a female giant panda (Ailuropoda melanoleuca). J Reprod Dev 54:281–285
Howard JG, Huang Y, Wang P, Li D, Zhang G, Hou R, Zhang Z, Durrant BS, Spindler RE, Zhang H, Zhang A, Wildt DE (2006) Role and efficiency of artificial insemination and genome resource banking. In: Wildt DE, Zhang A, Zhang H, Janssen DL, Ellis S (eds) Giant pandas: biology, veterinary medicine, and management. Cambridge University Press, Cambridge, pp 198–230
Hu C, Zhen Y, Pang B, Lin XY, Yi HF (2019) Myeloid-derived suppressor cells are regulated by estradiol and are a predictive marker for IVF outcome. Front Endocrinol 10:521
Huang Y, Zhang HM, Li DS, Zhang GQ, Wei RP, Huang Z, Zhou YM, Zhou Q, Liu Y, Wildt DE, Hull V (2012) Relationship of the estrogen surge and multiple mates to cub paternity in the giant panda (Ailuropoda melanoleuca): implications for optimal timing of copulation or artificial insemination. Biol Reprod 87:112
Karasu T, Marczylo TH, Maccarrone M, Konje JC (2011) The role of sex steroid hormones, cytokines and the endocannabinoid system in female fertility. Hum Reprod Update 17(3):347–361
Kersey DC, Wildt DE, Brown JL, Snyder RJ, Huang Y, Monfort SL (2010) Endocrine milieu of perioestrus in the giant panda (Ailuropoda melanoleuca), as determined by non-invasive hormone measures. Reprod Fertil Dev 22:901–912
Kersey DC, Wildt DE, Brown JL, Snyder RJ, Huang Y, Monfort SL (2011) Rising fecal glucocorticoid concentrations track reproductive activity in the female giant panda (Ailuropoda melanoleuca). Gen Comp Endocrinol 173:364–370
Kersey DC, Aitken-Palmer C, Rivera S, Willis EL, Liang LY, Snyder RJ (2016) The birth of a giant panda: Tracking the biological factors that successfully contribute to conception through to postnatal development. Theriogenology 85:671–677
Kuijper EA, Lambalk CB, Boomsma DI, van der Sluis S, Blankenstein MA, de Geus EJ, Posthuma D (2007) Heritability of reproductive hormones in adult male twins. Hum Reprod 22:2153–2159
Lindburg DG, Czekala NM, Swaisgood RR (2001) Hormonal and behavioral relationships during estrus in the Giant Panda. Zoo Biol 20:537–543
Martin-Wintle MS, Wintle NJP, Díez-León M, Swaisgood RR, Asa CS (2019) Improving the sustainability of ex situ populations with mate choice. Zoo Biol 38:119–132
Mastrangelo S, Tolone M, Di Gerlando R, Fontanesi L, Sardina MT, Portolano B (2016) Genomic inbreeding estimation in small populations: evaluation of runs of homozygosity in three local dairy cattle breeds. Animal 10:746–754
McGeehan L, Li XB, Jackintell L, Huang SQ, Wang AP, Czekala NM (2002) Hormonal and behavioral correlates of estrus in captive giant pandas. Zoo Biol 21:449–466
Meuwissen THE, Sonesson AK, Gebregiwergis G, Woolliams JA (2020) Management of genetic diversity in the era of genomics. Front Genet 11:880
Misztal I, Tsuruta S, Lourenco D, Aguilar I, Legarra A, Vitezica Z (2015) Manual for BLUPF90 family programs. University of Georgia, Athen, USA
Munro CJ, Stabenfeldt GH, Cragun JR, Addiego LA, Overstreet JW, Lasley BL (1991) Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay and radioimmunoassay. Clin Chem 37:838–844
Steinman KJ, Monfort SL, McGeehan L, Kersey DC, Gual-Sil F, Snyder R, Wang P, Nakao T, Czekala N (2006) Endocrinology of the giant panda and application of hormone technology to species management. In: Wildt DE, Zhang A, Zhang H, Janssen DL, Ellis S (eds) Giant pandas: biology, veterinary medicine, and management. Cambridge University Press, Cambridge, pp 198–230
Taussky HH (1954) A microcolorimetric determination of creatine in urine by the Jaffe reaction. J Biol Chem 208:853–861
Villanueva B, Fernández A, Saura M, Caballero A, Fernández J, Morales-González E, Toro MA, Pong-Wong R (2021) The value of genomic relationship matrices to estimate levels of inbreeding. Genet Sel Evol 53:42
Wauters J, Wilson KS, Bouts T, Valentine L, Vanderschueren K, McNeilly A, Girling S, Li R, Li D, Zhang H, Rae MT, Howie F, Andrew R, Duncan WC (2018) Urinary specific gravity as an alternative for the normalisation of endocrine metabolite concentrations in giant panda (Ailuropoda melanoleuca) reproductive monitoring. PLoS ONE 13:e0201420
Acknowledgements
This study was financially supported by Chengdu Research Base of Giant Panda Breeding (2021CPB-B09 and 2022CPB-B09).
Author information
Authors and Affiliations
Contributions
Study conception and design: HH, SYC, and JCL; data collection: YY F, ZJY, RH, YLL, LL, XMH, KJW, and KLC; analysis and interpretation of results: HH, SYC, and JCL; original draft preparation: HH and JCL; writing—review and editing: HH, SYC, JCL, and JA. All authors reviewed the results and approved the final version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethical approval and consent to participate
This study was approved by the Institutional Animal Care and Use Committee of the Chengdu Research Base of Giant Panda Breeding, and was conducted in compliance with China Wildlife Conservation Association’s Principles for the Ethical Treatment of Endangered Species.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling editor: Yoshiyuki Henning.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Huang, H., Chen, S., Feng, Y. et al. Genetic parameter estimates for estrus duration and urinary hormone levels in captive female giant pandas. Mamm Biol 103, 543–548 (2023). https://doi.org/10.1007/s42991-023-00375-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-023-00375-2