Intrinsic post-ejaculation sperm ageing does not affect offspring fitness in Atlantic salmon.
external fertilization
gametic selection
nongenetic effects
post-meiotic sperm senescence
reproduction
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
26
09
2019
revised:
07
01
2020
accepted:
10
01
2020
pubmed:
22
1
2020
medline:
3
7
2021
entrez:
22
1
2020
Statut:
ppublish
Résumé
Post-meiotic sperm ageing, both before ejaculation and after ejaculation, has been shown to negatively affect offspring fitness by lowering the rate of embryonic development, reducing embryonic viability and decreasing offspring condition. These negative effects are thought to be caused by intrinsic factors such as oxidative stress and ATP depletion or extrinsic factors such as temperature and osmosis. Effects of post-ejaculation sperm ageing on offspring fitness have so far almost exclusively been tested in internal fertilizers. Here, we tested whether intrinsic post-ejaculation sperm ageing affects offspring performance in an external fertilizer, the Atlantic salmon Salmo salar. We performed in vitro fertilizations with a split-clutch design where sperm were subjected to four post-ejaculation ageing treatments. We varied the duration between sperm activation and fertilization while minimizing extrinsic stress factors and tested how this affected offspring fitness. We found no evidence for an effect of our treatments on embryo survival, hatching time, larval standard length, early larval survival or larval growth rate, indicating that intrinsic post-ejaculation sperm ageing may not occur in Atlantic salmon. One reason may be the short life span of salmon sperm after ejaculation. Whether our findings are true in other external fertilizers with extended sperm activity remains to be tested.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
576-583Informations de copyright
© 2020 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2020 European Society For Evolutionary Biology.
Références
Aitken, R. J., Jones, K. T., & Robertson, S. A. (2012). Reactive oxygen species and sperm function-In sickness and in health. Journal of Andrology, 33, 1096-1106. https://doi.org/10.2164/jandrol.112.016535
Alavi, S., & Cosson, J. (2006). Sperm motility in fishes. (II) Effects of ions and osmolality: A review. Cell Biology International, 30, 1-14. https://doi.org/10.1016/j.cellbi.2005.06.004
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48.
Cabrita, E., Martínez-Páramo, S., Gavaia, P. J., Riesco, M. F., Valcarce, D. G., Sarasquete, C., … Robles, V. (2014). Factors enhancing fish sperm quality and emerging tools for sperm analysis. Aquaculture, 432, 389-401. https://doi.org/10.1016/j.aquaculture.2014.04.034
de La Rochebrochard, E., & Thonneau, P. (2002). Paternal age and maternal age are risk factors for miscarriage; results of a multicentre European study. Human Reproduction, 17, 1649-1656. https://doi.org/10.1093/humrep/17.6.1649
den Boer, S. P. A., Baer, B., Dreier, S., Aron, S., Nash, D. R., & Boomsma, J. J. (2009). Prudent sperm use by leaf-cutter ant queens. Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 3945-3953. https://doi.org/10.1098/rspb.2009.1184
Firman, R. C., Young, F. J., Rowe, D. C., Duong, H. T., & Gasparini, C. (2015). Sexual rest and post-meiotic sperm ageing in house mice. Journal of Evolutionary Biology, 28, 1373-1382. https://doi.org/10.1111/jeb.12661
Ford, W. C. L. (2000). Increasing paternal age is associated with delayed conception in a large population of fertile couples: Evidence for declining fecundity in older men. Human Reproduction, 15, 1703-1708. https://doi.org/10.1093/humrep/15.8.1703
Fox, J., & Weisberg, S. (2011). An R companion to applied regression (2nd ed.). Thousand Oaks, CA: Sage.
Frantsi, C., & Withey, K. G. (1972). A procedure for disinfecting Atlantic salmon Salmo salar eggs using a poly vinyl pyrrolidone iodine solution. Canadian Fisheries and Marine Survey and Research Development Branch Halifax Progress Report, 6, 1-8.
Han, X. (2014). The evolutionary consequences of sperm senescence in Drosophila melanogaster. Ph.D. Thesis, Queen’s University, Kingston.
Johnson, S. L., & Gemmell, N. J. (2012). Are old males still good males and can females tell the difference?: Do hidden advantages of mating with old males off-set costs related to fertility, or are we missing something else? BioEssays, 34, 609-619. https://doi.org/10.1002/bies.201100157
Kidd, S. A., Eskenazi, B., & Wyrobek, A. J. (2001). Effects of male age on semen quality and fertility: A review of the literature. Fertility and Sterility, 75, 237-248. https://doi.org/10.1016/S0015-0282(00)01679-4
Kuhnert, B. (2004). Reproductive functions of the ageing male. Human Reproduction Update, 10, 327-339. https://doi.org/10.1093/humupd/dmh030
Lewis, S. E. M., & Aitken, R. J. (2005). DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell and Tissue Research, 322, 33-41. https://doi.org/10.1007/s00441-005-1097-5
Pizzari, T., Dean, R., Pacey, A., Moore, H. D., & Bonsall, M. B. (2008). The evolutionary ecology of pre-and post-meiotic sperm senescence. Trends in Ecology and Evolution, 23, 131-140. https://doi.org/10.1016/j.tree.2007.12.003
R Development Core Team (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Reinhardt, K. (2007). Evolutionary consequences of sperm cell aging. The Quarterly Review of Biology, 82, 375-393. https://doi.org/10.1086/522811
Reinhardt, K., & Siva-Jothy, M. T. (2005). An advantage for young sperm in the house cricket Acheta domesticus. American Naturalist, 165, 718-723.
Velando, A., Noguera, J. C., Drummond, H., & Torres, R. (2011). Senescent males carry premutagenic lesions in sperm: Senescent males carry damaged germ line. Journal of Evolutionary Biology, 24, 693-697. https://doi.org/10.1111/j.1420-9101.2010.02201.x
Vladic, T. V., & Petersson, E. (2016). Evolutionary biology of the Atlantic salmon. Boca Raton, FL: CRC Press.
Wagner, R. H., Helfenstein, F., & Danchin, E. (2004). Female choice of young sperm in a genetically monogamous bird. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271(suppl_4), S134-S137. https://doi.org/10.1098/rsbl.2003.0142
White, J., Wagner, R. H., Helfenstein, F., Hatch, S. A., Mulard, H., Naves, L. C., & Danchin, E. (2008). Multiple deleterious effects of experimentally aged sperm in a monogamous bird. Proceedings of the National Academy of Sciences of the United States of America, 105, 13947-13952. https://doi.org/10.1073/pnas.0803067105
Yeates, S. E. (2005). Fertilisation dynamics in Atlantic salmon. Norwich, UK: University of East Anglia.
Zhu, J. L., Madsen, K. M., Vestergaard, M., Olesen, A. V., Basso, O., & Olsen, J. (2005). Paternal age and congenital malformations. Human Reproduction, 20, 3173-3177. https://doi.org/10.1093/humrep/dei186
Zubkova, E. V., & Robaire, B. (2006). Effects of ageing on spermatozoal chromatin and its sensitivity to in vivo and in vitro oxidative challenge in the Brown Norway rat. Human Reproduction, 21, 2901-2910. https://doi.org/10.1093/humrep/del193