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Oxidative stress in vertebrate semen: causes and consequences for male reproductive tactics

English title Oxidative stress in vertebrate semen: causes and consequences for male reproductive tactics
Applicant Helfenstein Fabrice
Number 165840
Funding scheme SNSF Professorships
Research institution Institut de Biologie Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Ecology
Start/End 01.09.2016 - 31.08.2018
Approved amount 870'811.00
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All Disciplines (2)

Discipline
Ecology
Zoology

Keywords (13)

oxidative stress; birds; reproductive tactics; life-history trade-offs; sperm competition; social hierarchy; sperm quality; resource allocation; alternative reproductive tactics; post-copulatory sexual selection; male fertility; antioxidants; mammals

Lay Summary (French)

Lead
La capacité d'un mâle à surmonter un stress oxydant est un déterminant important de sa fertilité. Le but de ce projet est de comprendre quel rôle le stress oxydant a joué dans l’évolution des stratégies de reproduction des mâles.
Lay summary

Contexte

Le stress oxydant est le résultat de dégâts infligés aux cellules par des radicaux oxygénés. C’est une cause importante d'infertilité chez les mâles. Chez les espèces où les femelles s’accouplent avec plusieurs mâles, le succès reproducteur de ces derniers dépend de la qualité de leur sperme. En outre, des modèles théoriques prédisent que les mâles ayant peu les faveurs des femelles, tels que les mâles subordonnés ou « satellites », devraient investir davantage de ressources dans la production de « bon » sperme. Les mâles ayant peu les faveurs des femelles devraient donc allouer davantage de ressources antioxydantes à la protection de leur sperme afin d’en maximiser la qualité. Une série d'expériences chez le moineau domestique a déjà montré que, à la suite d’un changement de statut social, les mâles peuvent modifier leur investissement dans le système antioxydant de leurs spermatozoïdes et ainsi ajuster la qualité de ceux-ci. Ainsi, les mâles dominants produisent des spermatozoïdes plus oxydés et donc moins mobiles que les mâles subdominants. Cependant, nous avons constaté que les mâles totalement subordonnés produisent les spermatozoïdes les plus oxydés et les moins bons. Chez la chauve-souris Fer-de-lance à lunette, les mâles « satellites » produisent de meilleurs spermatozoïdes que les mâles ayant un harem. Cependant, les mâles semblent incapables d'ajuster la qualité de leur sperme à leur nouveau statut - par exemple en passant de mâle harem à mâle « satellite ». Cela suggère que, chez cette espèce, les tactiques de reproduction sont soit génétiquement déterminées, soit déterminées tôt dans la vie d’un individu.

Buts

Ce projet vise à étudier à quelle point l'acquisition et la gestion physiologique de ressources antioxydantes lors de la croissance juvénile ou à l'âge adulte affectent la capacité des mâles à acquérir un statut social donné ainsi que leur capacité à produire des spermatozoïdes de bonne qualité.

Direct link to Lay Summary Last update: 22.09.2016

Responsible applicant and co-applicants

Employees

Publications

Publication
Sperm collection in Black-legged Kittiwakes and characterization of sperm velocity and morphology
Humann-Guilleminot Ségolène, Blévin Pierre, Azou-Barré Antonin, Yacoumas Agathe, Gabrielsen Geir Wing, Chastel Olivier, Helfenstein Fabrice (2018), Sperm collection in Black-legged Kittiwakes and characterization of sperm velocity and morphology, in Avian Research, 9(1), 24-24.
Is sperm morphology functionally related to sperm swimming ability? A case study in a wild passerine bird with male hierarchies
Rojas Mora Alfonso, Meniri Magali, Ciprietti Sabrina, Helfenstein Fabrice (2018), Is sperm morphology functionally related to sperm swimming ability? A case study in a wild passerine bird with male hierarchies, in BMC Evolutionary Biology, 18(1), 142-142.
Relationships between sperm morphological traits and sperm swimming performance in wild Great Tits (Parus major)
Losdat Sylvain, Helfenstein Fabrice (2018), Relationships between sperm morphological traits and sperm swimming performance in wild Great Tits (Parus major), in Journal of Ornithology, 159(3), 805-814.
Effects of an early-life paraquat exposure on adult resistance to oxidative stress, plumage colour and sperm performance in a wild bird
Losdat Sylvain, Blount Jonathan D., Marri Viviana, Maronde Lea, Richner Heinz, Helfenstein Fabrice (2018), Effects of an early-life paraquat exposure on adult resistance to oxidative stress, plumage colour and sperm performance in a wild bird, in Journal of Animal Ecology, 87(4), 1137-1148.
Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long-lived bird
Merkling Thomas, Blanchard Pierrick, Chastel Olivier, Glauser Gaëtan, Vallat-Michel Armelle, Hatch Scott A., Danchin Etienne, Helfenstein Fabrice (2017), Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long-lived bird, in Functional Ecology, 31(6), 1201-1209.
Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat)
Fasel Nicolas Jean, Wesseling Charlotte, Fernandez Ahana Aurora, Vallat Armelle, Glauser Gaétan, Helfenstein Fabrice, Richner Heinz (2017), Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat), in Behavioral Ecology and Sociobiology, 71(1), 11-11.
Antioxidant allocation modulates sperm quality across changing social environments.
Rojas Mora Alfonso, Meniri Magali, Gning Ophélie, Glauser Gaétan, Vallat Armelle, Helfenstein Fabrice (2017), Antioxidant allocation modulates sperm quality across changing social environments., in PLoS ONE, 12(5), e0176385.
Editorial: Oxidative Stress and Signal Honesty
Costantini David, Helfenstein Fabrice (2017), Editorial: Oxidative Stress and Signal Honesty, in Frontiers in Ecology and Evolution, 5, 32-33.
Oxidative stress affects sperm performance and ejaculate redox status in subordinate House Sparrows.
Rojas Mora Alfonso, Firth Alexandra, Blareau Sophie, Vallat Armelle, Helfenstein Fabrice (2017), Oxidative stress affects sperm performance and ejaculate redox status in subordinate House Sparrows., in Journal of Experimental Biology, 220, 2577-2588.
Sensitive and selective quantification of free and total malondialdehyde in plasma using UHPLC-HRMS
Mendonça Rute, Gning Ophélie, Di Cesaré Claudia, Lachat Laurence, Bennett Nigel C, Helfenstein Fabrice, Glauser Gaétan (2017), Sensitive and selective quantification of free and total malondialdehyde in plasma using UHPLC-HRMS, in Journal of Lipid Research, 58(9), 1924-1931.
Social dominance explains within-ejaculate variation in sperm design in a passerine bird.
Rojas Mora Alfonso, Meniri Magali, Ciprietti Sabrina, Helfenstein Fabrice (2017), Social dominance explains within-ejaculate variation in sperm design in a passerine bird., in BMC Evolutionary Biology, 17(1), 66.

Collaboration

Group / person Country
Types of collaboration
University of Pretoria, Austin Roberts Chair of Mammalogy South Africa (Africa)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
International Ornithological Congress Poster Sublethal effects of the neonicotinoid insecticide acetamiprid on stress physiology and sperm quality in a songbird 19.08.2018 Vancouver, Canada Helfenstein Fabrice;
Behaviour 2017 Poster Physiological and morphological consequences of a bad start in Seba's short tailed bats 30.07.2017 Estoril, Portugal Helfenstein Fabrice; Meniri Magali;
Behaviour 2017 Poster Effect of adverse conditions in early life on exploratory behaviour of Seba’s short tailed bat 30.07.2017 Estoril, Portugal Meniri Magali; Helfenstein Fabrice;
Behaviour 2017 Poster Physiological costs of cooperative behaviour in Damaraland mole rats 30.07.2017 Estoril, Portugal Mendonça Rute; Helfenstein Fabrice;


Communication with the public

Communication Title Media Place Year
Talks/events/exhibitions La compétition spermatique Western Switzerland 2018
Media relations: radio, television "Moineaux dominés, semence de meilleure bonne qualité" RTS La Première Western Switzerland 2016

Associated projects

Number Title Start Funding scheme
139011 Oxidative stress in avian semen: causes and consequences for male reproductive tactics 01.09.2012 SNSF Professorships

Abstract

Oxidative stress (OS) is the result of random cellular damage caused by oxygen radicals that leads to cell death, ageing, or illness. OS has been identified as a major cause of infertility. In promiscuous species, the fertilizing ability of the ejaculate partly determines the reproductive success of males. Moreover, theory predicts that males with lower access to fertile females such as subdominant or sneaker males should be selected to invest more resources into enhancing their ejaculate quality. We therefore hypothesized that sub-dominant (in species with linear social hierarchy) or sneaker males (in species with alternative reproductive tactics) should prioritize antioxidant allocation to their sperm in order to protect their sperm from OS and thus produce higher quality sperm. We put this hypothesis to the test in a bird species in which social hierarchy correlates with mating success, and in a fruit bat which exhibits two alternative tactics, mate-guarding, harem males and sneaker males. In house sparrows, we found that ejaculate quality correlates with OS level in sperm, and that dominant males produce more oxidized and lower quality ejaculates. After experimentally manipulating the social environment, males matched their ejaculate quality to their new rank, while increases in antioxidant investment into ejaculates paralleled increases in ejaculate quality. Noticeably though, we also found that males at the bottom of the hierarchy were constrained in their resource allocation pattern and, contrary to theoretical expectations, were unable to produce high quality sperm with little oxidative damage. In the Seba's short-tailed bat, we also found that satellite males produced better sperm than harem males. However, when experimentally manipulated to acquire a new status - males switched harem/sneaker, sneaker/harem roles - males did not match the quality of their sperm to their new status. This suggests that reproductive tactics are either genetically determined or determined early in the life of individuals.This new project aims at addressing the new questions, which arose from our recent research. With this project we will investigate whether and how physiological constraints in resource acquisition and/or availability may affect resource allocation patterns and sperm quality under varying risks and intensity of sperm competition. We will also experimentally test whether energy as a whole or more specifically antioxidant resources constrain subordinate males in the house sparrow. Lastly, we will experimentally test whether increased antioxidant availability during early growth (from birth to weaning) determines reproductive tactics and antioxidant resource allocation patterns at adulthood in the Seba's short-tailed bat.
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