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Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element

Meiotic drive genes cause the degeneration of non-carrier sperm to bias transmission in their favour. Males carrying meiotic drive are expected to suffer reduced fertility due to the loss of sperm and associated harmful side-effects of the mechanisms causing segregation distortion. However, sexual s...

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Autores principales: Meade, Lara C., Dinneen, Deidre, Kad, Ridhima, Lynch, Dominic M., Fowler, Kevin, Pomiankowski, Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781104/
https://www.ncbi.nlm.nih.gov/pubmed/30467401
http://dx.doi.org/10.1038/s41437-018-0166-y
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author Meade, Lara C.
Dinneen, Deidre
Kad, Ridhima
Lynch, Dominic M.
Fowler, Kevin
Pomiankowski, Andrew
author_facet Meade, Lara C.
Dinneen, Deidre
Kad, Ridhima
Lynch, Dominic M.
Fowler, Kevin
Pomiankowski, Andrew
author_sort Meade, Lara C.
collection PubMed
description Meiotic drive genes cause the degeneration of non-carrier sperm to bias transmission in their favour. Males carrying meiotic drive are expected to suffer reduced fertility due to the loss of sperm and associated harmful side-effects of the mechanisms causing segregation distortion. However, sexual selection should promote adaptive compensation to overcome these deleterious effects. We investigate this using SR, an X-linked meiotic drive system in the stalk-eyed fly, Teleopsis dalmanni. Despite sperm destruction caused by drive, we find no evidence that SR males transfer fewer sperm to the female’s spermathecae (long-term storage organs). Likewise, migration from the spermathecae to the ventral receptacle for fertilisation is similar for SR and wildtype male sperm, both over short and long time-frames. In addition, sperm number in storage is similar even after males have mated multiple times. Our study challenges conventional assumptions about the deleterious effects of drive on male fertility. This suggests that SR male ejaculate investment per ejaculate has been adjusted to match sperm delivery by wildtype males. We interpret these results in the light of recent theoretical models that predict how ejaculate strategies evolve when males vary in the resources allocated to reproduction or in sperm fertility. Adaptive compensation is likely in species where meiotic drive has persisted over many generations and predicts a higher stable frequency of drive maintained in wild populations. Future research must determine exactly how drive males compensate for failed spermatogenesis, and how such compensation may trade-off with investment in other fitness traits.
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spelling pubmed-67811042019-10-09 Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element Meade, Lara C. Dinneen, Deidre Kad, Ridhima Lynch, Dominic M. Fowler, Kevin Pomiankowski, Andrew Heredity (Edinb) Article Meiotic drive genes cause the degeneration of non-carrier sperm to bias transmission in their favour. Males carrying meiotic drive are expected to suffer reduced fertility due to the loss of sperm and associated harmful side-effects of the mechanisms causing segregation distortion. However, sexual selection should promote adaptive compensation to overcome these deleterious effects. We investigate this using SR, an X-linked meiotic drive system in the stalk-eyed fly, Teleopsis dalmanni. Despite sperm destruction caused by drive, we find no evidence that SR males transfer fewer sperm to the female’s spermathecae (long-term storage organs). Likewise, migration from the spermathecae to the ventral receptacle for fertilisation is similar for SR and wildtype male sperm, both over short and long time-frames. In addition, sperm number in storage is similar even after males have mated multiple times. Our study challenges conventional assumptions about the deleterious effects of drive on male fertility. This suggests that SR male ejaculate investment per ejaculate has been adjusted to match sperm delivery by wildtype males. We interpret these results in the light of recent theoretical models that predict how ejaculate strategies evolve when males vary in the resources allocated to reproduction or in sperm fertility. Adaptive compensation is likely in species where meiotic drive has persisted over many generations and predicts a higher stable frequency of drive maintained in wild populations. Future research must determine exactly how drive males compensate for failed spermatogenesis, and how such compensation may trade-off with investment in other fitness traits. Springer International Publishing 2018-11-22 2019-06 /pmc/articles/PMC6781104/ /pubmed/30467401 http://dx.doi.org/10.1038/s41437-018-0166-y Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Meade, Lara C.
Dinneen, Deidre
Kad, Ridhima
Lynch, Dominic M.
Fowler, Kevin
Pomiankowski, Andrew
Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title_full Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title_fullStr Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title_full_unstemmed Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title_short Ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
title_sort ejaculate sperm number compensation in stalk-eyed flies carrying a selfish meiotic drive element
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6781104/
https://www.ncbi.nlm.nih.gov/pubmed/30467401
http://dx.doi.org/10.1038/s41437-018-0166-y
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