Literature DB >> 29367392

Evidence that fertility trades off with early offspring fitness as males age.

Sheri L Johnson1,2,3, Sylvia Zellhuber-McMillan2, Joanne Gillum2, Jessica Dunleavy2, Jonathan P Evans4, Shinichi Nakagawa5,6, Neil J Gemmell2,3.   

Abstract

Models of ageing predict that sperm function and fertility should decline with age as sperm are exposed to free radical damage and mutation accumulation. However, theory also suggests that mating with older males should be beneficial for females because survival to old age is a demonstration of a male's high genetic and/or phenotypic quality. Consequently, declines in sperm fitness may be offset by indirect fitness benefits exhibited in offspring. While numerous studies have investigated age-based declines in male fertility, none has taken the integrated approach of studying age-based effects on both male fertility and offspring fitness. Here, using a cohort-based longitudinal study of zebrafish (Danio rerio), we report a decline in male mating success and fertility with male age but also compensating indirect benefits. Using in vitro fertilization, we show that offspring from older males exhibit superior early survival compared to those from their youngest counterparts. These findings suggest that the high offspring fitness observed for the subset of males that survive to an old age (approx. 51% in this study) may represent compensating benefits for declining fertility with age, thus challenging widely held views about the fitness costs of mating with older males.
© 2018 The Author(s).

Entities:  

Keywords:  Danio rerio; mating success; sperm quality; zebrafish

Mesh:

Year:  2018        PMID: 29367392      PMCID: PMC5805930          DOI: 10.1098/rspb.2017.2174

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  56 in total

Review 1.  Why do females mate multiply? A review of the genetic benefits.

Authors:  M D Jennions; M Petrie
Journal:  Biol Rev Camb Philos Soc       Date:  2000-02

Review 2.  Effects of male age on semen quality and fertility: a review of the literature.

Authors:  S A Kidd; B Eskenazi; A J Wyrobek
Journal:  Fertil Steril       Date:  2001-02       Impact factor: 7.329

3.  Sperm viability and sperm competition in insects.

Authors:  F M Hunter; T R Birkhead
Journal:  Curr Biol       Date:  2002-01-22       Impact factor: 10.834

4.  Can older males deliver the good genes?

Authors:  R Brooks; D J. Kemp
Journal:  Trends Ecol Evol       Date:  2001-06-01       Impact factor: 17.712

5.  Human mtDNA haplogroups associated with high or reduced spermatozoa motility.

Authors:  E Ruiz-Pesini; A C Lapeña; C Díez-Sánchez; A Pérez-Martos; J Montoya; E Alvarez; M Díaz; A Urriés; L Montoro; M J López-Pérez; J A Enríquez
Journal:  Am J Hum Genet       Date:  2000-08-09       Impact factor: 11.025

6.  Can mitochondrial DNA mutations cause sperm dysfunction?

Authors:  John Spiropoulos; Douglass M Turnbull; Patrick F Chinnery
Journal:  Mol Hum Reprod       Date:  2002-08       Impact factor: 4.025

7.  Reproductive aging and mating: the ticking of the biological clock in female cockroaches.

Authors:  P J Moore; A J Moore
Journal:  Proc Natl Acad Sci U S A       Date:  2001-07-24       Impact factor: 11.205

8.  Sperm structural and motility changes during aging in the Brown Norway rat.

Authors:  P Syntin; B Robaire
Journal:  J Androl       Date:  2001 Mar-Apr

9.  Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism.

Authors:  J S Armstrong; M Rajasekaran; W Chamulitrat; P Gatti; W J Hellstrom; S C Sikka
Journal:  Free Radic Biol Med       Date:  1999-04       Impact factor: 7.376

10.  Life spans and senescent phenotypes in two strains of Zebrafish (Danio rerio).

Authors:  Glenn S Gerhard; Elizabeth J Kauffman; Xujun Wang; Richard Stewart; Jessica L Moore; Claudia J Kasales; Eugene Demidenko; Keith C Cheng
Journal:  Exp Gerontol       Date:  2002 Aug-Sep       Impact factor: 4.032

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  12 in total

1.  Limited scope for reproductive senescence in wild populations of a short-lived fish.

Authors:  Milan Vrtílek; Jakub Žák; Radim Blažek; Matej Polačik; Alessandro Cellerino; Martin Reichard
Journal:  Naturwissenschaften       Date:  2018-11-22

2.  Post-copulatory sexual selection allows females to alleviate the fitness costs incurred when mating with senescing males.

Authors:  Pauline Vuarin; Alice Bouchard; Loïc Lesobre; Gwènaëlle Levêque; Toni Chalah; Michel Saint Jalme; Frédéric Lacroix; Yves Hingrat; Gabriele Sorci
Journal:  Proc Biol Sci       Date:  2019-10-23       Impact factor: 5.349

3.  An experimental test of the role of male mating history on paternal effects in the livebearer fish Gambusia holbrooki.

Authors:  Upama Aich; Michael D Jennions; Rebecca J Fox
Journal:  Biol Lett       Date:  2020-02-26       Impact factor: 3.703

4.  A synthesis of senescence predictions for indeterminate growth, and support from multiple tests in wild lake trout.

Authors:  Craig F Purchase; Anna C Rooke; Michael J Gaudry; Jason R Treberg; Elizabeth A Mittell; Michael B Morrissey; Michael D Rennie
Journal:  Proc Biol Sci       Date:  2022-01-05       Impact factor: 5.349

5.  Influence of age on sperm characteristics evaluated by light and electron microscopies.

Authors:  Giulia Collodel; Fabio Ferretti; Maurizio Masini; Giacomo Gualtieri; Elena Moretti
Journal:  Sci Rep       Date:  2021-03-02       Impact factor: 4.379

6.  Male age alone predicts paternity success under sperm competition when effects of age and past mating effort are experimentally separated.

Authors:  Upama Aich; Megan L Head; Rebecca J Fox; Michael D Jennions
Journal:  Proc Biol Sci       Date:  2021-07-28       Impact factor: 5.530

7.  Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring.

Authors:  Simon D Lamb; Jolyn H Z Chia; Sheri L Johnson
Journal:  PLoS One       Date:  2020-04-10       Impact factor: 3.240

8.  Differential reproductive plasticity under thermal variability in a freshwater fish (Danio rerio).

Authors:  Melanie D Massey; M Kate Fredericks; David Malloy; Suchinta Arif; Jeffrey A Hutchings
Journal:  Proc Biol Sci       Date:  2022-09-07       Impact factor: 5.530

9.  Paternal hypoxia exposure primes offspring for increased hypoxia resistance.

Authors:  Alexandria Ragsdale; Oscar Ortega-Recalde; Ludovic Dutoit; Anne A Besson; Jolyn H Z Chia; Tania King; Shinichi Nakagawa; Anthony Hickey; Neil J Gemmell; Timothy Hore; Sheri L Johnson
Journal:  BMC Biol       Date:  2022-08-30       Impact factor: 7.364

10.  Effect of age on the mercury sensitivity of zebrafish (Danio rerio) sperm.

Authors:  Tímea Kollár; Ákos Horváth; Bernadett Pataki; Berta Izabella Roberta; Gyöngyi Gazsi; Béla Urbányi
Journal:  Fish Physiol Biochem       Date:  2020-09-17       Impact factor: 2.794

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