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      The effects of male social environment on sperm phenotype and genome integrity

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          Abstract

          Sperm function and quality are primary determinants of male reproductive performance and hence fitness. The presence of rival males has been shown to affect ejaculate and sperm traits in a wide range of taxa. However, male physiological conditions may not only affect sperm phenotypic traits but also their genetic and epigenetic signatures, affecting the fitness of the resulting offspring. We investigated the effects of male‐male competition on sperm quality using TUNEL assays and geometric morphometrics in the zebrafish, Danio rerio. We found that the sperm produced by males exposed to high male–male competition had smaller heads but larger midpiece and flagellum than sperm produced by males under low competition. Head and flagella also appeared less sensitive to the osmotic stress induced by activation with water. In addition, more sperm showed signals of DNA damage in ejaculates of males under high competition. These findings suggest that the presence of a rival male may have positive effects on sperm phenotypic traits but negative effects on sperm DNA integrity. Overall, males facing the presence of rival males may produce faster swimming and more competitive sperm but this may come at a cost for the next generation.

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          Most cited references64

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          SPERM COMPETITION AND ITS EVOLUTIONARY CONSEQUENCES IN THE INSECTS

          Biological Reviews, 45(4), 525-567
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            The behaviour and ecology of the zebrafish, Danio rerio.

            The zebrafish Danio rerio, is an important model organism in developmental genetics, neurophysiology and biomedicine, but little is known about its natural ecology and behaviour. It is a small, shoaling cyprinid, native to the flood-plains of the Indian subcontinent, where it is found in shallow, slow-flowing waters. Zebrafish are group spawners and egg scatterers, although females are choosy with respect to sites for oviposition and males defend territories around such sites. Laboratory studies of zebrafish behaviour have encompassed shoaling, foraging, reproduction, sensory perception and learning. These studies are reviewed in relation to the suitability of the zebrafish as a model for studies on cognition and learning, development, behavioural and evolutionary ecology, and behavioural genetics.
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              Reproduction and resistance to stress: when and how.

              Environmental and social stresses have deleterious effects on reproductive function in vertebrates. Global climate change, human disturbance and endocrine disruption from pollutants are increasingly likely to pose additional stresses that could have a major impact on human society. Nonetheless, some populations of vertebrates (from fish to mammals) are able to temporarily resist environmental and social stresses, and breed successfully. A classical trade-off of reproductive success for potential survival is involved. We define five examples. (i) Aged individuals with minimal future reproductive success that should attempt to breed despite potential acute stressors. (ii) Seasonal breeders when time for actual breeding is so short that acute stress should be resisted in favour of reproductive success. (iii) If both members of a breeding pair provide parental care, then loss of a mate should be compensated for by the remaining individual. (iv) Semelparous species in which there is only one breeding period followed by programmed death. (v) Species where, because of the transience of dominance status in a social group, individuals may only have a short window of opportunity for mating. We suggest four mechanisms underlying resistance of the gonadal axis to stress. (i) Blockade at the central nervous system level, i.e. an individual no longer perceives the perturbation as stressful. (ii) Blockade at the level of the hypothalamic-pituitary-adrenal axis (i.e. failure to increase secretion of glucocorticosteroids). (iii) Blockade at the level of the hypothalamic-pituitary-gonad axis (i.e. resistance of the reproductive system to the actions of glucocorticosteroids). (iv) Compensatory stimulation of the gonadal axis to counteract inhibitory glucocorticosteroid actions. Although these mechanisms are likely genetically determined, their expression may depend upon a complex interaction with environmental factors. Future research will provide valuable information on the biology of stress and how organisms cope. Such mechanisms would be particularly insightful as the spectre of global change continues to unfold.
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                Author and article information

                Contributors
                willian.silva@evobiolab.com
                paula.saez08@gmail.com
                s.immler@uea.ac.uk
                Journal
                J Evol Biol
                J. Evol. Biol
                10.1111/(ISSN)1420-9101
                JEB
                Journal of Evolutionary Biology
                John Wiley and Sons Inc. (Hoboken )
                1010-061X
                1420-9101
                25 March 2019
                June 2019
                : 32
                : 6 ( doiID: 10.1111/jeb.2019.32.issue-6 )
                : 535-544
                Affiliations
                [ 1 ] Department of Evolutionary Biology Uppsala University Uppsala Sweden
                [ 2 ] Department of Biotechnology University of Alicante Alicante Spain
                [ 3 ] School of Biological Sciences University of East Anglia Norwich UK
                [ 4 ] Cátedra Human Fertility University of Alicante Alicante Spain
                Author notes
                [*] [* ] Correspondence

                Willian T. A. F. Silva and Simone Immler, Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden.

                Emails: willian.silva@ 123456evobiolab.com (W. T. A. F. S.); paula.saez08@ 123456gmail.com (P. S.‐E.); s.immler@ 123456uea.ac.uk (S. I.)

                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-9517-485X
                https://orcid.org/0000-0002-6840-8788
                https://orcid.org/0000-0002-5743-0613
                https://orcid.org/0000-0003-2384-8154
                https://orcid.org/0000-0003-1234-935X
                Article
                JEB13435
                10.1111/jeb.13435
                6850410
                30817032
                d2163e72-f46d-4c46-bc88-debb8080655a
                © 2019 Uppsala University and University of East Anglia. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 February 2019
                : 26 February 2019
                Page count
                Figures: 2, Tables: 0, Pages: 11, Words: 7932
                Categories
                Research Paper
                Research Papers
                Custom metadata
                2.0
                June 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:12.11.2019

                Evolutionary Biology
                dna damage,sexual selection,sperm competition,trade‐offs
                Evolutionary Biology
                dna damage, sexual selection, sperm competition, trade‐offs

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