Literature DB >> 26136452

Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice.

Andreas Sutter, Anna K Lindholm.   

Abstract

Female multiple mating (polyandry) is widespread across many animal taxa and indirect genetic benefits are a major evolutionary force favouring polyandry. An incentive for polyandry arises when multiple mating leads to sperm competition that disadvantages sperm from genetically inferior mates. A reduction in genetic quality is associated with costly selfish genetic elements (SGEs), and studies in invertebrates have shown that males bearing sex ratio distorting SGEs are worse sperm competitors than wild-type males.We used a vertebrate model species to test whether females can avoid an autosomal SGE, the t haplotype, through polyandry. The t haplotype inhouse mice exhibits strong drive in t heterozygous males by affecting spermatogenesis and is associated with homozygous in utero lethality. We used controlled matings to test the effect of the t haplotype on sperm competitiveness. Regardless of mating order, t heterozygous males sired only 11% of zygotes when competing against wild-type males, suggesting a very strong effect of the t haplotype on sperm quality. We provide, to our knowledge,the first substantial evidence that polyandry ameliorates the harmful effects of an autosomal SGE arising through genetic incompatibility. We discuss potential mechanisms in our study species and the broader implications for the benefits of polyandry.

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Year:  2015        PMID: 26136452      PMCID: PMC4528557          DOI: 10.1098/rspb.2015.0974

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


  41 in total

1.  Meiotic Drive in Natural Populations of Drosophila Melanogaster. I. the Cytogenetic Basis of Segregation-Distortion.

Authors:  L Sandler; Y Hiraizumi; I Sandler
Journal:  Genetics       Date:  1959-03       Impact factor: 4.562

2.  The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus).

Authors:  M D Dean; K G Ardlie; M W Nachman
Journal:  Mol Ecol       Date:  2006-11       Impact factor: 6.185

3.  Coevolutionary dynamics of polyandry and sex-linked meiotic drive.

Authors:  Luke Holman; Thomas A R Price; Nina Wedell; Hanna Kokko
Journal:  Evolution       Date:  2015-02-05       Impact factor: 3.694

4.  Genome scans for transmission ratio distortion regions in mice.

Authors:  Joaquim Casellas; Rodrigo J Gularte; Charles R Farber; Luis Varona; Margarete Mehrabian; Eric E Schadt; Aldon J Lusis; Alan D Attie; Brian S Yandell; Juan F Medrano
Journal:  Genetics       Date:  2012-02-23       Impact factor: 4.562

5.  The polyandry revolution.

Authors:  Tommaso Pizzari; Nina Wedell
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2013-01-21       Impact factor: 6.237

6.  Male sterility of the mouse t-complex is due to homozygosity of the distorter genes.

Authors:  M F Lyon
Journal:  Cell       Date:  1986-01-31       Impact factor: 41.582

Review 7.  Mouse t haplotypes.

Authors:  L M Silver
Journal:  Annu Rev Genet       Date:  1985       Impact factor: 16.830

8.  Wolbachia infection reduces sperm competitive ability in an insect.

Authors:  Fleur E Champion de Crespigny; Nina Wedell
Journal:  Proc Biol Sci       Date:  2006-06-22       Impact factor: 5.349

9.  Fitness effects of a selfish gene (the Mus t complex) are revealed in an ecological context.

Authors:  Lara S Carroll; Shawn Meagher; Linda Morrison; Dustin J Penn; Wayne K Potts
Journal:  Evolution       Date:  2004-06       Impact factor: 3.694

10.  Polyandry and the decrease of a selfish genetic element in a wild house mouse population.

Authors:  Andri Manser; Anna K Lindholm; Barbara König; Homayoun C Bagheri
Journal:  Evolution       Date:  2011-05-28       Impact factor: 3.694

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  27 in total

1.  A reduced propensity to cooperate under enhanced exploitation risk in a social mammal.

Authors:  Manuela Ferrari; Anna K Lindholm; Barbara König
Journal:  Proc Biol Sci       Date:  2016-05-11       Impact factor: 5.349

2.  Rodent gene drives for conservation: opportunities and data needs.

Authors:  John Godwin; Megan Serr; S Kathleen Barnhill-Dilling; Dimitri V Blondel; Peter R Brown; Karl Campbell; Jason Delborne; Alun L Lloyd; Kevin P Oh; Thomas A A Prowse; Royden Saah; Paul Thomas
Journal:  Proc Biol Sci       Date:  2019-11-06       Impact factor: 5.349

Review 3.  Selfish genetic elements and male fertility.

Authors:  Rudi L Verspoor; Tom A R Price; Nina Wedell
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-10-19       Impact factor: 6.237

4.  Baculum shape and paternity success in house mice: evidence for genital coevolution.

Authors:  Goncalo I André; Renée C Firman; Leigh W Simmons
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-10-19       Impact factor: 6.237

Review 5.  Of mice and women: advances in mammalian sperm competition with a focus on the female perspective.

Authors:  Renée C Firman
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-10-19       Impact factor: 6.237

6.  An X-linked meiotic drive allele has strong, recessive fitness costs in female Drosophila pseudoobscura.

Authors:  William Larner; Tom Price; Luke Holman; Nina Wedell
Journal:  Proc Biol Sci       Date:  2019-11-27       Impact factor: 5.349

Review 7.  Genetic Villains: Killer Meiotic Drivers.

Authors:  María Angélica Bravo Núñez; Nicole L Nuckolls; Sarah E Zanders
Journal:  Trends Genet       Date:  2018-02-27       Impact factor: 11.639

Review 8.  Fertility Costs of Meiotic Drivers.

Authors:  Sarah E Zanders; Robert L Unckless
Journal:  Curr Biol       Date:  2019-06-03       Impact factor: 10.834

9.  Carrying a selfish genetic element predicts increased migration propensity in free-living wild house mice.

Authors:  Jan-Niklas Runge; Anna K Lindholm
Journal:  Proc Biol Sci       Date:  2018-10-03       Impact factor: 5.349

Review 10.  Resistance to natural and synthetic gene drive systems.

Authors:  Tom A R Price; Nikolai Windbichler; Robert L Unckless; Andreas Sutter; Jan-Niklas Runge; Perran A Ross; Andrew Pomiankowski; Nicole L Nuckolls; Catherine Montchamp-Moreau; Nicole Mideo; Oliver Y Martin; Andri Manser; Mathieu Legros; Amanda M Larracuente; Luke Holman; John Godwin; Neil Gemmell; Cécile Courret; Anna Buchman; Luke G Barrett; Anna K Lindholm
Journal:  J Evol Biol       Date:  2020-09-24       Impact factor: 2.411

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