Cargando…

Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?

BACKGROUND: With female multiple mating (polyandry), male-male competition extends to after copulation (sperm competition). Males respond to this selective pressure through physiological, morphological and behavioural adaptations. Sperm competitiveness is commonly decreased in heterozygote carriers...

Descripción completa

Detalles Bibliográficos
Autores principales: Sutter, Andreas, Lindholm, Anna K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915163/
https://www.ncbi.nlm.nih.gov/pubmed/27328665
http://dx.doi.org/10.1186/s12862-016-0710-4
_version_ 1782438657999765504
author Sutter, Andreas
Lindholm, Anna K.
author_facet Sutter, Andreas
Lindholm, Anna K.
author_sort Sutter, Andreas
collection PubMed
description BACKGROUND: With female multiple mating (polyandry), male-male competition extends to after copulation (sperm competition). Males respond to this selective pressure through physiological, morphological and behavioural adaptations. Sperm competitiveness is commonly decreased in heterozygote carriers of male meiotic drivers, selfish genetic elements that manipulate the production of gametes in males. This might give carriers an evolutionary incentive to reduce the risk of sperm competition. Here, we explore this possibility in house mice. Natural populations frequently harbour a well-characterised male driver (t haplotype), which is transmitted to 90 % of heterozygous (+/t) males’ offspring. Previous research demonstrated strong detrimental effects on sperm competitiveness, and suggested that +/t males are particularly disadvantaged against wild type males when first-to-mate. Low paternity success in the first-to-mate role is expected to favour male adaptations that decrease the risk of sperm competition by preventing female remating. Genotype-specific paternity patterns (sperm precedence) could lead to genetically determined alternative reproductive tactics that can spread through gene level selection. Here, we seek confirmation that +/t males are generally disadvantaged when first-to-mate and address whether males of different genotypes differ in reproductive tactics (copulatory and morphological) to maximise individual or driver fitness. Finally, we attempt to explain the mechanistic basis for alternative sperm precedence patterns in this species. RESULTS: We confirmed that +/t males are weak sperm competitors when first to mate. When two +/t males competed, the second-to-mate was more successful, which contrasts with first male sperm precedence when wild type males competed. However, we found no differences between male genotypes in reproductive behaviour or morphology that were consistent with alternative reproductive tactics. Sperm of +/+ and +/t males differed with respect to in vitro sperm features. Premature hypermotility in +/t males’ sperm can potentially explain why +/t males are very weak sperm competitors when first-to-mate. CONCLUSIONS: Our results demonstrate that meiotic drivers can have strong effects on sperm precedence patterns, and may provide a heritable basis for alternative reproductive tactics motivated by reduced sperm competitiveness. We discuss how experimental and evolutionary constraints may help explain why male genotypes did not show the predicted differences. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0710-4) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4915163
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-49151632016-06-22 Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics? Sutter, Andreas Lindholm, Anna K. BMC Evol Biol Research Article BACKGROUND: With female multiple mating (polyandry), male-male competition extends to after copulation (sperm competition). Males respond to this selective pressure through physiological, morphological and behavioural adaptations. Sperm competitiveness is commonly decreased in heterozygote carriers of male meiotic drivers, selfish genetic elements that manipulate the production of gametes in males. This might give carriers an evolutionary incentive to reduce the risk of sperm competition. Here, we explore this possibility in house mice. Natural populations frequently harbour a well-characterised male driver (t haplotype), which is transmitted to 90 % of heterozygous (+/t) males’ offspring. Previous research demonstrated strong detrimental effects on sperm competitiveness, and suggested that +/t males are particularly disadvantaged against wild type males when first-to-mate. Low paternity success in the first-to-mate role is expected to favour male adaptations that decrease the risk of sperm competition by preventing female remating. Genotype-specific paternity patterns (sperm precedence) could lead to genetically determined alternative reproductive tactics that can spread through gene level selection. Here, we seek confirmation that +/t males are generally disadvantaged when first-to-mate and address whether males of different genotypes differ in reproductive tactics (copulatory and morphological) to maximise individual or driver fitness. Finally, we attempt to explain the mechanistic basis for alternative sperm precedence patterns in this species. RESULTS: We confirmed that +/t males are weak sperm competitors when first to mate. When two +/t males competed, the second-to-mate was more successful, which contrasts with first male sperm precedence when wild type males competed. However, we found no differences between male genotypes in reproductive behaviour or morphology that were consistent with alternative reproductive tactics. Sperm of +/+ and +/t males differed with respect to in vitro sperm features. Premature hypermotility in +/t males’ sperm can potentially explain why +/t males are very weak sperm competitors when first-to-mate. CONCLUSIONS: Our results demonstrate that meiotic drivers can have strong effects on sperm precedence patterns, and may provide a heritable basis for alternative reproductive tactics motivated by reduced sperm competitiveness. We discuss how experimental and evolutionary constraints may help explain why male genotypes did not show the predicted differences. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0710-4) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-21 /pmc/articles/PMC4915163/ /pubmed/27328665 http://dx.doi.org/10.1186/s12862-016-0710-4 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sutter, Andreas
Lindholm, Anna K.
Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title_full Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title_fullStr Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title_full_unstemmed Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title_short Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
title_sort meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics?
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915163/
https://www.ncbi.nlm.nih.gov/pubmed/27328665
http://dx.doi.org/10.1186/s12862-016-0710-4
work_keys_str_mv AT sutterandreas meioticdrivechangesspermprecedencepatternsinhousemicepotentialformalealternativematingtactics
AT lindholmannak meioticdrivechangesspermprecedencepatternsinhousemicepotentialformalealternativematingtactics