Inbreeding depression in male gametic performance

S. Losdat*, S.-M. Chang, J. M. Reid

*Corresponding author for this work

Research output: Contribution to journalReview article

19 Citations (Scopus)

Abstract

One key objective in evolutionary ecology is to understand the magnitude of inbreeding depression expressed across sex-specific components of fitness. One major component of male fitness is fertilization success, which depends on male gametic performance (sperm and pollen performance in animals and plants, respectively). Inbreeding depression in male gametic performance could create sex-specific inbreeding depression in fitness, increase the benefit of inbreeding avoidance and reduce the efficacy of artificial insemination and pollination. However, there has been no assessment of the degree to which inbreeding generally depresses male gametic performance and hence post-copulatory or post-pollination fertilization success. Because inbreeding depression is understood to be a property of diploid entities, it is not clear what degree of inbreeding depression in haploid gametic performance should be expected. Here, we first summarize how inbreeding depression in male gametic performance could potentially arise through gene expression in associated diploid cells and/or reduced genetic diversity among haploid gametes. We then review published studies that estimate the magnitude of inbreeding depression in traits measuring components of sperm or pollen quantity, quality and competitiveness. Across 51 published studies covering 183 study traits, the grand mean inbreeding load was approximately one haploid lethal equivalent, suggesting that inbreeding depresses male gametic performance across diverse systems and traits. However, there was an almost complete lack of explicit estimates from wild populations. Future studies should quantify inbreeding depression in systematic sets of gametic traits under naturally competitive and noncompetitive conditions and quantify the degree to which gamete phenotypes and performance reflect haploid vs. diploid gene expression.

Original languageEnglish
Pages (from-to)992-1011
Number of pages20
JournalJournal of Evolutionary Biology
Volume27
Issue number6
Early online date13 May 2014
DOIs
Publication statusPublished - Jun 2014

Fingerprint

inbreeding depression
haploidy
inbreeding
diploidy
fitness
gamete
fertilization (reproduction)
pollination
sperm
gene expression
germ cells
pollen
spermatozoa
inbreeding avoidance
gender
animal performance
wild population
lethal genes
artificial insemination
competitiveness

Keywords

  • Gamete competition
  • Inbreeding depression
  • Inbreeding load
  • Male reproductive success
  • Meta-analysis
  • Pollen performance
  • Pollination
  • Post-copulatory sexual selection
  • Sperm performance

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

Inbreeding depression in male gametic performance. / Losdat, S.; Chang, S.-M.; Reid, J. M.

In: Journal of Evolutionary Biology, Vol. 27, No. 6, 06.2014, p. 992-1011.

Research output: Contribution to journalReview article

Losdat, S. ; Chang, S.-M. ; Reid, J. M. / Inbreeding depression in male gametic performance. In: Journal of Evolutionary Biology. 2014 ; Vol. 27, No. 6. pp. 992-1011.
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abstract = "One key objective in evolutionary ecology is to understand the magnitude of inbreeding depression expressed across sex-specific components of fitness. One major component of male fitness is fertilization success, which depends on male gametic performance (sperm and pollen performance in animals and plants, respectively). Inbreeding depression in male gametic performance could create sex-specific inbreeding depression in fitness, increase the benefit of inbreeding avoidance and reduce the efficacy of artificial insemination and pollination. However, there has been no assessment of the degree to which inbreeding generally depresses male gametic performance and hence post-copulatory or post-pollination fertilization success. Because inbreeding depression is understood to be a property of diploid entities, it is not clear what degree of inbreeding depression in haploid gametic performance should be expected. Here, we first summarize how inbreeding depression in male gametic performance could potentially arise through gene expression in associated diploid cells and/or reduced genetic diversity among haploid gametes. We then review published studies that estimate the magnitude of inbreeding depression in traits measuring components of sperm or pollen quantity, quality and competitiveness. Across 51 published studies covering 183 study traits, the grand mean inbreeding load was approximately one haploid lethal equivalent, suggesting that inbreeding depresses male gametic performance across diverse systems and traits. However, there was an almost complete lack of explicit estimates from wild populations. Future studies should quantify inbreeding depression in systematic sets of gametic traits under naturally competitive and noncompetitive conditions and quantify the degree to which gamete phenotypes and performance reflect haploid vs. diploid gene expression.",
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note = "Acknowledgments We thank Łukasz Michalczyk, Louise D. Pedersen, Peter van Eldik, Stephen Robinson, Susan W. Margulis, Mar{\'i}a J. Caraba{\~n}o, Giorgina Bernasconi, Arlee Montalvo, Thure P. Hauser and Andrew G. Stephenson for providing raw data or regression parameters associated with their published studies; Aurelio F. Malo, on behalf of the Chicago Zoological Society, for providing unpublished regression values; and Lukas Keller, Pirmin Nietlisbach, Matthew Wolak and Erik Postma for providing helpful comments and ideas. SL was supported by a Swiss National Science Foundation post-doctoral fellowship (PBBEP3_139396), an IEF Marie Curie fellowship and a Philip Leverhulme Prize awarded to JMR. JMR was supported by the UK Royal Society and the European Research Council. SMC was supported by the US National Science Foundation (award 0640881).",
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