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Haploid selection within a single ejaculate increases offspring fitness
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
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2017 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, no 30, p. 8053-8058Article in journal (Refereed) Published
Abstract [en]

An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid phases. The occurrence of selection during the haploid phase can have far-reaching consequences for fundamental evolutionary processes including the rate of adaptation, the extent of inbreeding depression, and the load of deleterious mutations, as well as for applied research into fertilization technology. Although haploid selection is well established in plants, current dogma assumes that in animals, intact fertile sperm within a single ejaculate are equivalent at siring viable offspring. Using the zebrafish Danio rerio, we show that selection on phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness. Longer-lived sperm sired embryos with increased survival and a reduced number of apoptotic cells, and adult male offspring exhibited higher fitness. The effect on embryo viability was carried over into the second generation without further selection and was equally strong in both sexes. Sperm pools selected by motile phenotypes differed genetically at numerous sites throughout the genome. Our findings clearly link within-ejaculate variation in sperm phenotype to offspring fitness and sperm genotype in a vertebrate and have major implications for adaptive evolution.

Place, publisher, year, edition, pages
2017. no 30, p. 8053-8058
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-320335DOI: 10.1073/pnas.1705601114ISI: 000406189900080PubMedID: 28698378OAI: oai:DiVA.org:uu-320335DiVA, id: diva2:1089269
Funder
Swedish Research CouncilEU, European Research CouncilAvailable from: 2017-04-19 Created: 2017-04-19 Last updated: 2018-05-07Bibliographically approved
In thesis
1. Selection in sperm and its consequences: Exploring haploid selection, ageing and epigenetic effects in sperm
Open this publication in new window or tab >>Selection in sperm and its consequences: Exploring haploid selection, ageing and epigenetic effects in sperm
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Sexually reproducing eukaryotes are typically going through a biphasic life cycle with a diploid and a haploid phase. Unlike in plants where selection on haploid pollen genotypes is well established, the possibility of selection occurring in animal sperm is currently not known. One of the main reasons for this lack of knowledge is the general assumption that due to the shortness and the apparent absence of gene expression in haploid sperm, selection during that phase is unlikely to occur. The aim of this thesis was to fill this gap and address some of the main fundamental questions. I investigated the interaction between sperm phenotype and offspring phenotype with a focus on the trans-generational effects of (i) selection on the haploid sperm genotype, (ii) sperm ageing and (iii) sperm-mediated epigenetic effects. For one, we performed several experimental studies to investigate how selection on the sperm phenotype affects offspring performance in two externally fertilizing fishes, Atlantic salmon and zebrafish. We found that in Atlantic salmon, sperm of intermediate post-activation longevity sire offspring that hatch earlier. In zebrafish, longer living sperm sire more viable offspring with a higher fitness than their short-lived sibling sperm. We explored the mechanisms of these trans-generational effects and found that neither intrinsic post-ejaculation sperm ageing (Atlantic salmon and zebrafish) nor pre-ejaculation sperm ageing (zebrafish) affect offspring performance. However, we identified genetic differences between sperm pools that were obtained by selecting different phenotypes within ejaculates of zebrafish males. These results suggest a genetic basis for intra-ejaculate sperm phenotype variation and show that there is potential for haploid selection in sperm. In a separate experiment, we explored the role of sexual selection in shaping sperm-mediated epigenetic effects, and found that short-time changes in male-male competition affect offspring hatching time and survival. In conclusion, this thesis provides evidence that sperm phenotype affects offspring phenotype, and that sperm phenotype is affected by both epigenetic changes influenced by the male environment and differences in the haploid genome of sperm.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. p. 57
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1518
Keywords
sperm, evolution, selection, haploid selection, epigenetics, sperm-mediated effects, trans-generational effects, sperm ageing, sperm senescence
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320437 (URN)978-91-554-9918-1 (ISBN)
Public defence
2017-06-09, Lindahlsalen, Evolutionary Biology Centre, EBC, Norbyvägen 14, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2017-05-18 Created: 2017-04-20 Last updated: 2017-06-07
2. 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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