Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Cryptic male choice: experimental evidence of sperm sex ratio and seminal fluid adjustment in relation to coital rate

A. M. Edwards A B and E. Z. Cameron A

A School of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.

B Corresponding author. Email: amy.edwards@utas.edu.au

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16123
Submitted: 18 March 2016  Accepted: 16 May 2016   Published online: 30 May 2016

Abstract

The differential allocation hypothesis suggests that a mother should adjust the sex of offspring in relation to her mate’s attractiveness, thereby increasing future reproductive fitness when her sons inherit the attractive traits. More attractive males have been shown to sire more sons, but it is possible that the sex ratio skew could be a result of paternal rather than maternal manipulation, which would be a more parsimonious explanation. We manipulated coital rate (an indicator of attractiveness) in laboratory mice and showed that males that mate more often have higher levels of glucose in their semen despite lower blood glucose levels. Since peri-conceptual glucose levels in utero increase male conceptus survival, this could result in male-biased sex ratios. The males that mated most also had more remaining X-chromosome-bearing-spermatozoa, suggesting depletion of Y-chromosome-bearing-spermatozoa during mating. We hypothesise that males may alter both seminal fluids and X : Y ratios in an ejaculate to influence subsequent sex ratios. Our results further support a paternal role in sex allocation.

Additional keywords: attractiveness, differential allocation, paternal, sex allocation.


References

Andersson, S. (1986). Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution Int. J. Org. Evolution 40, 804–816.
Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences.CrossRef | open url image1

Burley, N. (1981). Sex ratio manipulation and selection for attractiveness. Science 211, 721–722.
Sex ratio manipulation and selection for attractiveness.CrossRef | 1:STN:280:DC%2BC3cvivFeqtQ%3D%3D&md5=512335a1f48c0c31d7e04375c216c02bCAS | 17776654PubMed | open url image1

Burley, N. (1986). Sexual selection for aesthetic traits in species with biparental care. Am. Nat. 127, 415–445.
Sexual selection for aesthetic traits in species with biparental care.CrossRef | open url image1

Cameron, E. Z. (2004). Facultative adjustment of mammalian sex ratios in support of the Trivers–Willard hypothesis: evidence for a mechanism. Proc. Biol. Sci. 271, 1723–1728.
Facultative adjustment of mammalian sex ratios in support of the Trivers–Willard hypothesis: evidence for a mechanism.CrossRef | 15306293PubMed | open url image1

Cameron, E. Z., Lemons, P. R., Bateman, P. W., and Bennett, N. C. (2008). Experimental alteration of litter sex ratios in a mammal. Proc. Biol. Sci. 275, 323–327.
Experimental alteration of litter sex ratios in a mammal.CrossRef | 18048284PubMed | open url image1

Carvalho, J. O., Silva, L. P., Sartori, R., and Dode, M. A. N. (2013). Nanoscale differences in the shape and size of X and Y chromosome-bearing bovine heads assessed by atomic force microscopy. PLoS One 8, e59387.
Nanoscale differences in the shape and size of X and Y chromosome-bearing bovine heads assessed by atomic force microscopy.CrossRef | 1:CAS:528:DC%2BC3sXltFykurs%3D&md5=13d346b068c0446465bd006f753fd184CAS | 23527178PubMed | open url image1

Check, J. H., and Katsoff, D. (1993). A prospective study to evaluate the efficacy of modified swim-up preparation for male sex selection. Hum. Reprod. 8, 211–214.
| 1:STN:280:DyaK3s3jt1Wrsg%3D%3D&md5=71242e5e90d449df9be0dabe755b463cCAS | 8473421PubMed | open url image1

Cornwallis, C. K., and O’Connor, E. A. (2009). Sperm: seminal fluid interactions and the adjustment of sperm quality in relation to female attractiveness. Proc. Biol. Sci. 276, 3467–3475.
Sperm: seminal fluid interactions and the adjustment of sperm quality in relation to female attractiveness.CrossRef | 19586951PubMed | open url image1

D’Amato, C., Hagen, D., and Dzuik, P. J. (1979). The lack of effect of ejaculate sequence on sex ratio in rabbits. J. Reprod. Fertil. 56, 193–194.
The lack of effect of ejaculate sequence on sex ratio in rabbits.CrossRef | 1:STN:280:DyaE1M3ktFOlsw%3D%3D&md5=48bd5e6e8b34f2247399d826de9fc90aCAS | 469841PubMed | open url image1

Dewsbury, D. A., and Sawrey, D. K. (1984). Male capacity as related to sperm production, pregnancy initiation, and sperm competition in deer mice (Peromyscus maniculatus). Behav. Ecol. Sociobiol. 16, 37–47.
Male capacity as related to sperm production, pregnancy initiation, and sperm competition in deer mice (Peromyscus maniculatus).CrossRef | open url image1

Edwards, A. M., and Cameron, E. Z. (2014). Forgotten fathers: paternal influences on mammalian sex allocation. Trends Ecol. Evol. 29, 158–164.
Forgotten fathers: paternal influences on mammalian sex allocation.CrossRef | 24388760PubMed | open url image1

Edwards, A. M., Cameron, E. Z., Pereira, J. C., and Ferguson-Smith, M. A. (2016a). Paternal sex allocation: how variable is the sperm sex ratio? J. Zool. 299, 37–41.
Paternal sex allocation: how variable is the sperm sex ratio?CrossRef | open url image1

Edwards, A. M., Cameron, E. Z., and Wapstra, E. (2016b). Are there physiological constraints on maternal ability to adjust sex ratios in mammals? J. Zool. 299, 1–9.
Are there physiological constraints on maternal ability to adjust sex ratios in mammals?CrossRef | open url image1

Gutiérrez-Adán, A., Granados, J., Pintado, B., and De La Fuente, J. (2001). Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod. Fertil. Dev. 13, 361–365.
Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro.CrossRef | 11833931PubMed | open url image1

Hurd, P. L., Bailey, A. A., Gongal, P. A., Yan, R. H., Greer, J. J., and Pagliardini, S. (2008). Intrauterine position effects on anogenital distance and digit ratio in male and female mice. Arch. Sex. Behav. 37, 9–18.
Intrauterine position effects on anogenital distance and digit ratio in male and female mice.CrossRef | 18080736PubMed | open url image1

Larson, M. A., Kimura, K., Kubisch, H. M., and 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 signalling molecule IFN-t. Proc. Natl. Acad. Sci. USA 98, 9677–9682.
Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signalling molecule IFN-t.CrossRef | 1:CAS:528:DC%2BD3MXmtlCnu7g%3D&md5=c54d0c4c683baa13b358ef5dfe964691CAS | 11481449PubMed | open url image1

Lloyd-Jones, O., and Hays, F. A. (1918). The influence of excessive sexual activity of male rabbits. 1. On the properties of the seminal discharge. J. Exp. Zool. 25, 463–497.
The influence of excessive sexual activity of male rabbits. 1. On the properties of the seminal discharge.CrossRef | open url image1

Malo, A. F., Garde, J. J., Soler, A. J., Garcia, A. J., Gomendio, M., and Roldan, E. R. S. (2005). Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol. Reprod. 72, 822–829.
Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa.CrossRef | 1:CAS:528:DC%2BD2MXis12hsrY%3D&md5=4695581b93967d1c9cc9464f2b331574CAS | 15576823PubMed | open url image1

Mannowetz, N., Wandernoth, P. M., and Wennemuth, G. (2012). Glucose is a pH-dependent motor for sperm beat frequency during early activation. PLoS One 7, e41030.
Glucose is a pH-dependent motor for sperm beat frequency during early activation.CrossRef | 1:CAS:528:DC%2BC38XhtFSkt7rP&md5=fc4af5e8feb1ddde80b81fa6548934fdCAS | 22911736PubMed | open url image1

Oakberg, E. F. (1956). Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am. J. Anat. 99, 507–516.
Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium.CrossRef | 1:STN:280:DyaG2s%2FkvV2luw%3D%3D&md5=423b82a58cf97778c36c7dc0233a81c2CAS | 13402729PubMed | open url image1

Perry, J. C., Sirot, L., and Wigby, S. (2013). The seminal symphony: how to compose an ejaculate. Trends Ecol. Evol. 28, 414–422.
The seminal symphony: how to compose an ejaculate.CrossRef | 23582755PubMed | open url image1

Røed, K. H., Holand, Ø., Mysterud, A., Tverdal, A., Kumpula, J., and Nieminen, M. (2007). Male phenotypic quality influences offspring sex ratio in a polygynous ungulate. Proc. Biol. Sci. 274, 727–733.
Male phenotypic quality influences offspring sex ratio in a polygynous ungulate.CrossRef | 17254998PubMed | open url image1

Rutstein, A. N., Gorman, H. E., Arnold, K. E., Gilbert, L., Orr, K. J., Adam, A., Nagar, R., and Graves, J. A. (2005). Sex allocation in response to paternal attractiveness in the zebra finch. Behav. Ecol. 16, 763–769.
Sex allocation in response to paternal attractiveness in the zebra finch.CrossRef | open url image1

Saragusty, J., Hermes, R., Hofer, H., Bouts, T., Goritz, F., and Hildebrandt, T. B. (2012). Male pygmy hippopotamus influence offspring sex ratio. Nat. Commun. 3, 697.
Male pygmy hippopotamus influence offspring sex ratio.CrossRef | 22426218PubMed | open url image1

Schulte-Hostedde, A. I., Zinner, B., Millar, J. S., and Hickling, G. J. (2005). Restitution of mass-size residuals: validating body condition indices. Ecology 86, 155–163.
Restitution of mass-size residuals: validating body condition indices.CrossRef | open url image1

Weatherhead, P. J., and Robertson, R. J. (1979). Offspring quality and the polygyny threshold: ‘the sexy son hypothesis’. Am. Nat. 113, 201–208.
Offspring quality and the polygyny threshold: ‘the sexy son hypothesis’.CrossRef | open url image1

Whitten, W. K. (1966) ‘Pheromones and Mammalian Reproduction’. (Academic Press: London.)

Windsor, D. P., Evans, G., and White, I. G. (1993). Sex predetermination by separation of X and Y chromosome-bearing sperm: a review. Reprod. Fertil. Dev. 5, 155–171.
Sex predetermination by separation of X and Y chromosome-bearing sperm: a review.CrossRef | 1:STN:280:DyaK2c%2FovF2gsA%3D%3D&md5=7341a8ad2538cfed1106739cd69556a1CAS | 8265800PubMed | open url image1



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