Pre-fertilization gamete thermal environment influences reproductive success, unmasking opposing sex-specific responses in Atlantic salmon (Salmo salar)

Graziano, Marco, Solberg, Monica F., Glover, Kevin A., Vasudeva, Ramakrishnan ORCID: https://orcid.org/0000-0002-3831-0384, Dyrhovden, Lise, Murray, David ORCID: https://orcid.org/0000-0003-4764-1641, Immler, Simone and Gage, Matthew J. G. (2023) Pre-fertilization gamete thermal environment influences reproductive success, unmasking opposing sex-specific responses in Atlantic salmon (Salmo salar). Royal Society Open Science, 10 (12). ISSN 2054-5703

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Abstract

The environment gametes perform in just before fertilization is increasingly recognized to affect offspring fitness, yet the contributions of male and female gametes and their adaptive significance remain largely unexplored. Here, we investigated gametic thermal plasticity and its effects on hatching success and embryo performance in Atlantic salmon (Salmo salar). Eggs and sperm were incubated overnight at 2°C or 8°C, temperatures within the optimal thermal range of this species. Crosses between warm- and cold-incubated gametes were compared using a full-factorial design, with half of each clutch reared in cold temperatures and the other in warm temperatures. This allowed disentangling single-sex interaction effects when pre-fertilization temperature of gametes mismatched embryonic conditions. Pre-fertilization temperature influenced hatch timing and synchrony, and matching sperm and embryo temperatures resulted in earlier hatching. Warm incubation benefited eggs but harmed sperm, reducing the hatching success and, overall, gametic thermal plasticity did not enhance offspring fitness, indicating vulnerability to thermal changes. We highlight the sensitivity of male gametes to higher temperatures, and that gamete acclimation may not effectively buffer against deleterious effects of thermal fluctuations. From an applied angle, we propose the differential storage of male and female gametes as a tool to enhance sustainability within the hatcheries.

Item Type:	Article
Additional Information:	Data accessibility statement: All the material, the raw data files and the script have been uploaded on Dryad: https://doi.org/10.5061/dryad.wstqjq2s9 [99]. A version of the Rscript has been made available on the Dryad repository. Funding information: This research was supported by grants available to M.J.G.G. from the UK Research and Innovation Biotechnology and Biological Sciences Research Council and by grants available to K.A.G. and M.F.S. and financed by the Norwegian Department for Industry and Fisheries. The Open Access funding was provided by the University of East Anglia.
Uncontrolled Keywords:	salmo salar,thermal stress,experimental biology,evolution,gametes,fertilization
Faculty \ School:	Faculty of Science > School of Biological Sciences Faculty of Science > School of Environmental Sciences
UEA Research Groups:	Faculty of Science > Research Groups > Organisms and the Environment Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
Depositing User:	LivePure Connector
Date Deposited:	14 Jun 2024 08:30
Last Modified:	09 Oct 2024 13:40
URI:	https://ueaeprints.uea.ac.uk/id/eprint/95612
DOI:	10.1098/rsos.231427

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