Maternal cortisol level around conception is associated with offspring sex ratio in captive European wild rabbit (Oryctolagus cuniculus)
DOI:
https://doi.org/10.31914/aak.2793Keywords:
sex allocation, stress, progesterone, glucocorticoids, faecal cortisolAbstract
The sex ratio of the offspring at birth is usually 1: 1 established by natural selection. The sex allocation model predicts that if parents have adequate resources, they would benefit from differentially allocating maternal investment to that sex having higher fittness under the particular environmental conditions. However, little is known about what mechanisms would result in biased sex ratio. One such mechanism could be the interaction of of stress reactivity and progesterone levels in the mothers around conception. In the present investigation the fecal cortisol and progesterone levels at the day of conception were measured in fifteen European wild rabbit does kept in cages. The does were clustered to low and high cortisol response groups and the sex ratio of their progeny was determined. We found a significant correlation between the progesterone levels of mothers and their stress status measured at the mating. This correlation was also reflected in the sex ratio bias in their litters. Even though the litter size was not different, we found higher progesterone levels and more female offspring in the does with higher cortisol levels indicating that maternal status around conception may affect the litter sex ratio.
References
Albrecht, E. D., Nightingale, M. S., Townsley, J. D. (1978). Stress-induced decreases in the serum con-centration of progesterone in the pregnant baboon. J Endocrino., 77(3), 425–426. DOI: https://doi.org/10.1677/joe.0.0770425
Bánszegi, O., Altbäcker, V., Bilkó, Á. (2009). Intrauterine position influences anatomy and behavior in domestic rabbits. Physiol Behav., 98(3), 258–262. DOI: https://doi.org/10.1016/j.physbeh.2009.05.016
Beaulieu-McCoy, N.E., Sherman, K. K., Trego, M. L., Crocker, D.E., Kellar, N.M., (2017). Initial validation of blubber cortisol and progesterone as indicators of stress response and maturity in an otariid; the California sea lion (Zalophus californianus). Gen Comp Endocr.; 252, 1–11. DOI: https://doi.org/10.1016/j.ygcen.2017.07.003
Benedek, I., Altbӓcker, V., Molnár, T. (2021). Stress reactivity near birth affects nest building timing and offspring number and survival in the European rabbit (Oryctolagus cuniculus). Plos one, 16(1), e0246258. DOI: https://doi.org/10.1371/journal.pone.0246258
Bilkó, Á.; Altbäcker V.(2000). Regular handling early in the nursing period eliminates fear responses toward human beings in wild and domestic rabbits. Dev. Psychobiol., 36, 78–87. DOI: https://doi.org/10.1002/(SICI)1098-2302(200001)36:1<78::AID-DEV8>3.0.CO;2-5
Breazile, J. E. (1988). The physiology of stress and its relationship to mechanisms of disease and therapeutics. Vet Clin N A.-Food A., 4(3), 441–480. DOI: https://doi.org/10.1016/S0749-0720(15)31025-2
Cabezas S, Blas J, Marchant T.A, Moreno S. (2007). Physiological stress levels predict survival proba-bilities in wild rabbits. Horm Behav. 51(3), 313–320. DOI: https://doi.org/10.1016/j.yhbeh.2006.11.004
Cameron, E. Z. (2004). Facultative adjustment of mammalian sex ratios in support of the Trivers–Willard hypothesis: evidence for a mechanism. ProcRoyal SocB: Biol Sci, 271(1549), 1723–1728. DOI: https://doi.org/10.1098/rspb.2004.2773
Chandler, J. E., Canal, A. M., Paul, J. B., Moser, E. B. (2002). Collection frequency affects percent Y-chromosome bearing sperm, sperm head area and quality of bovine ejaculates. Theriogenology, 57(4), 1327–1346. DOI: https://doi.org/10.1016/s0093-691x(01)00721-x
Charnov, E.L. (1983) The theory of sex allocation. Princeton University Press, Princeton. DOI: https://doi.org/10.1515/9780691210056
Clutton-Brock, T. H., Albon, S. D., Guinness, F. E. (1984). Maternal dominance, breeding success and birth sex ratios in red deer. Nature, 308(5957), 358–360. DOI: https://doi.org/10.1038/308358a0
Clutton-Brock, T. H., Guinness, F. E., & Albon, S. D. (1982). Red deer: behavior and ecology of two sexes. University of Chicago press, Chicago.
Coubrough, R. I. (1985). Stress and fertility. Onderstepoort J Vet., 52, 153–156. URI: http://hdl.handle.net/2263/44393
Desfor, K. B., Boomsma, J. J., Sunde, P. (2007). Tawny owls Strix aluco with reliable food supply pro-duce male‐biased broods. Ibis, 149(1), 98–105. DOI: https://doi.org/10.1111/j.1474-919x.2006.00617.x
Edwards, A. M., Cameron, E. Z. (2014). Forgotten fathers: paternal influences on mammalian sex allocation. Trends Ecol Evol., 29(3), 158-164. DOI: https://doi.org/10.1016/j.tree.2013.12.003
Emlen, S. T., Emlen, J. M., Levin, S. A. (1986). Sex-ratio selection in species with helpers-at-the-nest. Am Nat., 127, 1-8.
Fajer, A. B., Holzbauer, M., Newport, H. M. (1971). The contribution of the adrenal gland to the total amount of progesterone produced in the female rat. J Physiol., 214(1), 115–126. DOI: https://doi.org/10.1113/jphysiol.1971.sp009422
Fisher, R. A. (1930): 117ze Genetical Theory of Natural Selection. Clarendon Press, Oxford.
Grant, V. J. (2007). Could maternal testosterone levels govern mammalian sex ratio deviations?. J Theor Biol., 246(4), 708–719. DOI: https://doi.org/10.1016/j.jtbi.2007.02.005
Grant, V. J., Irwin, R. J. (2005). Follicular fluid steroid levels and subsequent sex of bovine embryos. J Exp Zool Part A., 303(12), 1120–1125. DOI: https://doi.org/10.1002/jez.a.233
Gutiérrez‐Adán, A., Perez‐Crespo, M., Fernandez‐Gonzalez, R., Ramirez, M. A., Moreira, P., Pintado, B., Rizos, D. (2006). Developmental consequences of sexual dimorphism during pre‐implantation embryonic development. Reprod Domest Anim., 41, 54–62. DOI: https://doi.org/10.1111/j.1439-0531.2006.00769.x
Hamilton, W. D. (1967). Extraordinary Sex Ratios: A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science, 156, 477–488.
Henriksen, T. B., Wilcox, A. J., Hedegaard, M., Secher, N. J. (1995). Bias in studies of preterm and post-term delivery due to ultrasound assessment of gestational age. Epidemiology, 6(5), 533-537. DOI: https://doi.org/10.1097/00001648-199509000-00012
Howe, H. F. (1977). Sex-ratio adjustment in the common grackle. Science, 198 (4318), 744–746. DOI: https://doi.org/10.1126/science.198.4318.744
James, W. H. (2004). Further evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. Hum Reprod., 19(6), 1250–1256. DOI: https://doi.org/10.1093/humrep/deh245
James, W. H. (2006). Possible constraints on adaptive variation in sex ratio at birth in humans and other primates. J Theor Biol., 238(2), 383–394. DOI: https://doi.org/10.1016/j.jtbi.2005.05.022
Jongbloet, P. H. (2004). The ovopathy concept for explaining the secondary sex ratio. Hum Reprod., 19(4), 1036–1037. DOI: https://doi.org/10.1093/humrep/deh140
Komdeur, J. (2004). Sex-ratio manipulation. Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, 102-116.
Komdeur, J. (2012). Sex allocation. The evolution of parental care, In: N J. Royle, PT. Smiseth, MKölli-ker (Eds.), Oxford University Press, Oxford, UK, 171-188.
Korsten, P., Clutton-Brock, T., Pilkington, J. G., Pemberton, J. M., Kruuk, L. E. (2009). Sexual conflict in twins: male co-twins reduce fitness of female Soay sheep. Biol Letters, 5(5), 663–666. DOI: https://doi.org/10.1098/rsbl.2009.0366
Larson, M. A., Kimura, K., Kubisch, H. M., Roberts, R. M. (2001). Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-τ. Proc Natl Acad Sci-Biol., 98(17), 9677–9682. DOI: https://doi.org/10.1073/pnas.171305398
Lessells, C. M., Avery, M. I. (1987). Sex-ratio selection in species with helpers at the nest: some exten-sions of the repayment model. Am Nat., 129(4), 610–620.
Marcus, M., Kiely, J., Xu, F., McGeehin, M., Jackson, R., Sinks, T. (1998). Changing sex ratio in the United States, 1969–1995. Fertil Steril., 70(2), 270–273. DOI: https://doi.org/10.1016/s0015-0282(98)00149-6
McMillen, M. M. (1979). Differential mortality by sex in fetal and neonatal deaths. Science, 204(4388), 89–91. DOI: https://doi.org/10.1126/science.571144
Obel, C., Henriksen, T. B., Secher, N. J., Eskenazi, B., Hedegaard, M. (2007). Psychological distress during early gestation and offspring sex ratio. Hum Reprod., 22(11), 3009–3012. DOI: https://doi.org/10.1093/humrep/dem274
Palmer, A. R. (2000). Quasi-replication and the contract of error: lessons from sex ratios, heritabili-ties and fluctuating asymmetry. Annu Rev Ecol Syst., 31(1), 441–480. DOI: https://doi.org/10.1146/annurev.ecolsys.31.1.441
Pongrácz, P.; Altbäcker, V.; Fenes, D. (2001). Human handling might interfere with conspecific recog-nition in the European rabbit (Oryctolagus cuniculus). Dev. Psychobiol., 39(1), 53–62. DOI: https://doi.org/10.1002/dev.1028
Pratt, N. C., Lisk, R. D. (1989). Effects of social stress during early pregnancy on litter size and sex ratio in the golden hamster (Mesocricetus auratus). Reproduction, 87(2), 763–769. DOI: https://doi.org/10.1530/jrf.0.0870763
Rivers, J. P. W., Crawford, M. A. (1974). Maternal nutrition and the sex ratio at birth. Nature, 252(5481), 297–298.
Rosenfeld, C. S., Roberts, R. M. (2004). Maternal diet and other factors affecting offspring sex ratio: a review. Biol Reprod., 71(4), 1063–1070. DOI: https://doi.org/10.1095/biolreprod.104.030890
Ryan, C. P., Anderson, W. G., Berkvens, C. N., Hare, J. F. (2014). Maternal gestational cortisol and testosterone are associated with trade-offs in offspring sex and number in a free-living rodent (Urocitellus richardsonii). PloS one, 9(10), e111052. DOI: https://doi.org/10.1371/journal.pone.0111052
Sheldon, B. C., West, S. A. (2004). Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat., 163(1), 40–54. DOI: https://doi.org/10.1086/381003
Teixeira, C. P., De Azevedo, C. S., Mendl, M., Cipreste, C. F., Young, R. J. (2007). Revisiting translocation and reintroduction programmes: the importance of considering stress. Anim Behav., 73(1), 1–13. DOI: https://doi.org/10.1016/j.anbehav.2006.06.002
Trivers, R. L., Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179(4068), 90–92. DOI: https://doi.org/10.1126/science.179.4068.90
Weatherhead, P. J., Robertson, R. J. (1979). Offspring quality and the polygyny threshold:" the sexy son hypothesis". Am Nat., 113(2), 201–208. DOI: https://doi.org/10.1086/283379
West, S. A., Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295(5560), 1685–1688. DOI: https://doi.org/10.1126/science.1069043
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