Change search
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf
Haploid selection in animals: Exploring the fitness consequences and underlying mechanisms
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics. (Immler)
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 [en]
sperm, evolution, haploid selection, reproductive aging, fitness
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-350192ISBN: 978-91-513-0358-1 (print)OAI: oai:DiVA.org:uu-350192DiVA, id: diva2:1204348
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
List of papers
1. Haploid selection within a single ejaculate increases offspring fitness
Open this publication in new window or tab >>Haploid selection within a single ejaculate increases offspring fitness
Show others...
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.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320335 (URN)10.1073/pnas.1705601114 (DOI)000406189900080 ()28698378 (PubMedID)
Funder
Swedish Research CouncilEU, European Research Council
Available from: 2017-04-19 Created: 2017-04-19 Last updated: 2018-05-07Bibliographically approved
2. Within-ejaculate selection for sperm longevity reduces male reproductive ageing
Open this publication in new window or tab >>Within-ejaculate selection for sperm longevity reduces male reproductive ageing
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Males produce numerous sperm in the single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic variation among sperm in the single ejaculate of a male reflects the phenotype and the genotype of the resulting offspring. Specifically, within-ejaculate sperm selection (WESS) for sperm longevity increased the performance of the resulting offspring in several key life-history traits in early-life. Because increased early-life reproductive performance often correlates with rapid ageing, it is possible that WESS increases early-life fitness at the cost of accelerated senescence. Alternatively, WESS can improve offspring quality throughout the life cycle, including reduced age-specific deterioration. We found that WESS for sperm longevity reduced age-specific deterioration of male fertility and embryo survival, while there is no effect on fertilization success. Remarkably, we found opposing effect of WESS on female fecundity, where selection for sperm longevity resulted in increased early-life performance followed by a slow decline, while unselected controls started low but increased their fecundity with age. Intriguingly, WESS also reduced the age-specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within-ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and have important implications for assisted fertilization programs in livestock and humans. 

Keywords
Ageing, Reproductive Success, Sperm Selection, Sperm Competition, Senescence
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-350186 (URN)
Available from: 2018-05-07 Created: 2018-05-07 Last updated: 2018-05-07
3. The fitness consequences of selection among sperm within an ejaculate across generations
Open this publication in new window or tab >>The fitness consequences of selection among sperm within an ejaculate across generations
(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
Haploid selection, sperm selection, offspring fitness, gene expression
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-350190 (URN)
Available from: 2018-05-07 Created: 2018-05-07 Last updated: 2018-05-07
4. Sperm performance traits exhibit low additive genetic component and strong parental effects in external fertilizer
Open this publication in new window or tab >>Sperm performance traits exhibit low additive genetic component and strong parental effects in external fertilizer
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Despite their key role in determining reproductive success and with that Darwinian fitness, the heritability and underlying additive genetic variance of reproductive traits is still not fully understood. While some traits show relatively high genetic variance, others show very low genetic variance, which is particularly true for complex non-morphological traits. In line with these general patterns, morphological sperm traits show surprisingly high heritability, whereas heritability reported for sperm quality and performance traits generally is lower. A possible explanation for this is the general notion that more fitness related traits show lower levels of additive genetic variance and heritability. We investigated the additive genetic variance and heritability of sperm swimming velocity, the percentage of motile sperm, sperm concentration in the ejaculate and sperm longevity in the externally fertilizing zebrafish Danio rerio. All sperm traits showed low but significant additive genetic variance and high parental components. While the additive genetic variance was significant it was lower than reported in many other studies. A possible explanation for this is that in externally fertilizing species, sperm traits are the prime determinant of fertilization success and high plasticity is crucial for swift adaptations to changes in the environmental conditions such as competition but also water temperature and currents. Given that this is the first study looking into the heritability of sperm traits in an external fertilizer it will be interesting to understand, whether this is true for other externally fertilizing species and taxa.

Keywords
additive genetic, parental effect, sperm traits, reproduction
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-350191 (URN)
Available from: 2018-05-07 Created: 2018-05-07 Last updated: 2018-06-01

Open Access in DiVA

fulltext(837 kB)55 downloads
File information
File name FULLTEXT01.pdfFile size 837 kBChecksum SHA-512
5a4eee61d279782398c79660f0459e3a36a4e391da2f8fe4f7e0e25d2c463f7173b425798b7402275ea57b71896be7c61abba6cab05436c4d3351b6e19132bb1
Type fulltextMimetype application/pdf
Buy this publication >>

Search in DiVA

By author/editor
Alavioon, Ghazal
By organisation
Department of Ecology and Genetics
Evolutionary Biology

Search outside of DiVA

GoogleGoogle Scholar
Total: 55 downloads
The number of downloads is the sum of all downloads of full texts. It may include eg previous versions that are now no longer available

isbn
urn-nbn

Altmetric score

isbn
urn-nbn
Total: 417 hits
CiteExportLink to record
Permanent link

Direct link
Cite
Citation style
  • apa
  • ieee
  • modern-language-association-8th-edition
  • vancouver
  • Other style
More styles
Language
  • de-DE
  • en-GB
  • en-US
  • fi-FI
  • nn-NO
  • nn-NB
  • sv-SE
  • Other locale
More languages
Output format
  • html
  • text
  • asciidoc
  • rtf