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How Do Freshwater Fish Sperm Find the Egg? the Physicochemical Factors Guiding the Gamete Encounters of Externally Fertilizing Freshwater Fish

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How Do Freshwater Fish Sperm Find the Egg? the Physicochemical Factors Guiding the Gamete Encounters of Externally Fertilizing Freshwater Fish View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Explore Bristol Research Kholodnyy, V., Gadêlha, H., Cosson, J., & Boryshpolets, S. (2019). How do freshwater fish sperm find the egg? The physicochemical factors guiding the gamete encounters of externally fertilizing freshwater fish. Reviews in Aquaculture. https://doi.org/10.1111/raq.12378 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1111/raq.12378 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Wiley at https://doi.org/10.1111/raq.12378 . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/pure/about/ebr-terms Reviews in Aquaculture, 1–28 doi: 10.1111/raq.12378 How do freshwater fish sperm find the egg? The physicochemical factors guiding the gamete encounters of externally fertilizing freshwater fish Vitaliy Kholodnyy1 , Hermes Gadelha^ 1,2, Jacky Cosson1 and Sergii Boryshpolets1 1 Laboratory of Reproductive Physiology, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, University of South Bohemia in Cesk e Budejovice, Vodnany, Czech Republic 2 Department of Engineering Mathematics, University of Bristol, Bristol, UK Correspondence Abstract Vitaliy Kholodnyy, Laboratory of Reproductive Physiology, Faculty of Fisheries and Protection The lifespan of spermatozoa from externally fertilizing freshwater fish ranges from of Waters, South Bohemian Research Center a few seconds to several minutes, depending on the species. External factors, such of Aquaculture and Biodiversity of as temperature, background flows and ion composition, play an important role in Hydrocenoses, Research Institute of Fish fertilization success. Specific mechanisms guiding spermatozoa appear to be Culture and Hydrobiology, University of South essential to maximize the sperm–egg encounter under these strenuous conditions. Bohemia in Cesk e Budejovice, Zati sı 728/II, 389 Although some existing data support the hypothesis that both the ovarian fluid 25 Vodnany, Czech Republic. Email: [email protected] and the eggs may release chemoattractants that significantly affect spermatozoa behaviour and the fertilization outcome, this hypothesis is still open to debate, as Received 5 March 2019; accepted 22 July the existence of freshwater fish spermatozoa chemotaxis has yet to be demon- 2019. strated; in addition, specific mechanisms supporting spermatozoa guidance and gamete selection have not been elucidated. Is the natural selection of gametes determined by a combination of different physicochemical phenomena? Alterna- tively, is the natural selection of species-specific gametes biased towards the spe- cies-specific guidance mechanisms of their natural landscape? These questions have received more attention as new studies have revealed potential, distinct guid- ance mechanisms in freshwater fish reproduction. In this review, we discuss the empirical studies supporting different hypotheses about freshwater fish gamete guidance and highlight the synergistic combination of experiments and biomathe- matical modelling to explore these questions. Finally, we discuss the challenges in understanding the mechanisms behind sperm guidance in freshwater fish species, and we suppose that knowledge about the mechanisms that underlie spermatozoa selection and guidance in freshwater fish species may elucidate the impact of the traditional aquaculture practice of artificial fertilization on progeny quality and species sustainability. Key words: egg, flagellar dynamics, freshwater fish, guidance, ovarian fluid, spermatozoa. selection takes place even before the gametes meet. Among Introduction the different species of fish, for example, some are adapted Darwinian evolution permeates all life forms on our planet. to fertilize eggs either internally or externally. The exact For most species from Animalia, natural selection begins evolutionary pressures for particular adaptations resulting with the successful swapping of genetic material following in the existence of these two modes of fertilization are fertilization, where an embryo is formed and developed, unknown thus far. Nevertheless, the selective pressure for and if the embryo is sufficiently healthy, it grows and external fertilizers is undeniably higher for both gametes; reaches maturity to reproduce before dying (Pelegri et al. and they pass through convoluted processes and challenges 2017). This selection is perhaps one of the most fundamen- in a harsh and uncharted territory outside the body. Suc- tal components of life. The very first stage of natural cessful fertilization results from the sum of strict step-by- © 2019 The Authors. Reviews in Aquaculture published by John Wiley & Sons Australia, Ltd. 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. V. Kholodnyy et al. step phenomena leading to the fusion of the male and guidance in freshwater fish species may help elucidate the female gametes. Each individual step triggers the next step, impact of traditional artificial fertilization practices on the and if a step has a weak performance, the fertilization out- quality and sustainability of progeny. come may be dramatically affected. Although several excellent reviews have been compiled In most externally fertilizing freshwater fish species, both covering different aspects of fish reproduction (Hart 1990; males and females spawn synchronously by generating suf- Taborsky 1998; Coward et al. 2002; Cosson 2004; Alavi & ficient muscular contractions to ultimately produce an Cosson 2005, 2006; Yoshida et al. 2008; Bobe & Labbe underwater plume of gametes containing approximately 2010; Schulz et al. 2010; Dzyuba & Cosson 2014; Browne 10 billion spermatozoa and 3 million eggs (Wootton & et al. 2015; Smith & Wootton 2016), there is still a need for Smith 2014). Nevertheless, the short lifespan of either sper- an analysis with a focus on the biophysical and biochemical matozoa or eggs, as well as the environmental conditions aspects of freshwater gamete guidance. In this review, we (e.g. flow), makes the reproductive success quite time-lim- explore the scientific developments thus far covering the ited by sperm availability, and the gametes are under selec- underlying physicochemical factors responsible for sperm– tion for mechanisms that may control sperm–egg egg encounters in the case of externally fertilizing fish spe- encounters. The mechanisms involved in these processes cies. We highlight the gaps present in our understanding of are sophisticated and combine various molecular, chemical freshwater sperm guidance, and thus, the urgent need for and physical factors (Zimmer & Riffell 2011; Zaferani et al. substantial further research. Indeed, to date, empirical evi- 2018). Egg signalling and sperm response could be adapted, dence of the guidance mechanisms in many fish species is for instance, to meet one or many specific environmental lacking, and knowledge on the processes by which sperma- constraints, such as chemical diffusivity, pH, fluid and flow tozoa find the egg in these species is scarce. Most of the properties, surface interactions and other external factors studies on reproduction and the established regularities (Hart 1990; Iwamatsu 2000). Likewise, these external selec- and mechanisms in external fertilizers are traditionally and tive stresses are likely to drive gamete evolution and deter- predominately dealing with marine invertebrates, mainly mine fitness within natural habitats. sea urchins, for example Arbacia punctulata, which may be Freshwater fish species that reproduce externally consti- attributed to their ready availability, relatively convenient tute a group of perfect model organisms for reproduction handling and processing (Kaupp et al. 2008), as well as the studies. In vivo investigations with internally fertilizing spe- simplicity of their internal structure, especially that of their cies often suffer from the unavoidable translation between flagellum (Gibbons & Grimstone 1960). In our review, we natural and in vitro conditions. Freshwater fish species discuss the new directions of investigation needed and allow a close inspection of the selective pressures mediating highlight the synergistic combination of interdisciplinary reproduction and sperm–egg fusion, including the conse- research exploring experimental investigations, advances in quences of changes in the environment, adaptivity or even imaging technology, mathematical data analysis and in-sil- extinction potential given external perturbations. This is ico predictions of virtual sperm–egg meeting models. We particularly relevant now, as external environmental stres- address the future challenges of observational and theoreti- ses are rapidly changing, from global warming and pollu- cal studies in understanding the external selective pressures tion to other detrimental aspects of our industrial society. for sperm–egg encounters in freshwater
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