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The fitness consequences of selection among sperm within an ejaculate across generations
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics. (Simone Immler)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics. (Simone Immler)
Jagiellonian University.
University of East Anglia.
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The evolution of a biphasic life cycle with alternating diploid and haploid phases is a necessary consequence of sexual reproduction in eukaryotes. Selection in each of the phases may have far reaching consequences for many evolutionary processes. While our focus in evolutionary biology lies mainly on selection during the diploid phase, we know relatively little about the role and consequences of selection occurring during the haploid gametic stage. This is particularly true in predominantly diploid animals where the haploid gametic phase is very short. To test the importance of haploid selection in animals, we performed a large-scale selection experiment with selection acting on haploid sperm. We selected on sperm longevity within an ejaculate and tested the effects of such selection over three generation. We performed fitness assays for every generation and found that offspring sired by longer-lived sperm generally exhibit higher fitness from early development into adulthood compared to offspring sired by their shorter-lived sibling sperm in all three generations. These fitness effects were carried over into the second generation without further selection in all three generations. Moreover, using RNA sequencing, we assessed differences in tissue specific gene expression between the offspring sired by the two sperm phenotypes in generation F1 and F3. The transcriptomes in both tissues differed significantly between the two treatments. Many very basic housekeeping genes involved in metabolism and development showed small differences in expression in both tissues. Our study provides solid evidence for the far-reaching consequences of selection on different sperm within a single ejaculate in three consecutive generations, and offers exciting new insights into the possible underlying mechanisms. Our results further highlight the importance of selection at the haploid gametic stages for fundamental evolutionary processes and assisted fertilization technologies.

Keywords [en]
Haploid selection, sperm selection, offspring fitness, gene expression
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-350190OAI: oai:DiVA.org:uu-350190DiVA, id: diva2:1204338
Available from: 2018-05-07 Created: 2018-05-07 Last updated: 2018-05-07
In thesis
1. Haploid selection in animals: Exploring the fitness consequences and underlying mechanisms
Open this publication in new window or tab >>Haploid selection in animals: Exploring the fitness consequences and underlying mechanisms
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

A consequence of sexual reproduction in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid gametic phases. While our focus in evolutionary biology is on selection during the diploid phase, we know relatively little about selection occurring during the haploid gametic stage. This is particularly true in predominantly diploid animals, where gene expression and hence selection have long been thought to be absent in haploid cells like gametes and particularly sperm. During my PhD, I tested the idea of selection during the haploid gametic phase using zebrafish Danio rario as a study species. I combined a large-scale selection experiment over three generations with fitness assays and next-generation sequencing to assess the importance of haploid selection. We measured offspring fitness in all three generations.  In addition, we compared gene expression in brain and testes of F1 and F3 adult male from each treatment by RNA sequencing. We found that offspring sired by longer-lived sperm showed higher survival rate and higher early- and late-life reproductive fitness compared to offspring sired by shorter-lived sperm. We also found differentially expressed genes between the two treatments with functions in metabolic and developmental pathways. These findings suggest that the observed fitness differences to be caused by small expression changes in many basic genes. We also tested for a genetic underpinning of the selected sperm phenotypes and identified allelic differences across the entire genome. Finally, we investigated the additive genetic component and parental effect of different sperm phenotypes. We found generally low additive genetic variation and high parental effects on sperm performance traits. In conclusion, this thesis provides evidence that the phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness throughout life and provides a clear link between sperm phenotype and offspring fitness and between sperm phenotype and sperm genotype.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2018. p. 41
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1681
Keywords
sperm, evolution, haploid selection, reproductive aging, fitness
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-350192 (URN)978-91-513-0358-1 (ISBN)
Public defence
2018-09-14, Lindahlsalen, Norbyvagen 18d, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2018-08-24 Created: 2018-05-07 Last updated: 2018-09-06

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