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  • 1.
    Alavioon, Ghazal
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Haploid selection in animals: Exploring the fitness consequences and underlying mechanisms2018Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
    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.

    Delarbeten
    1. Haploid selection within a single ejaculate increases offspring fitness
    Öppna denna publikation i ny flik eller fönster >>Haploid selection within a single ejaculate increases offspring fitness
    Visa övriga...
    2017 (Engelska)Ingår i: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, nr 30, s. 8053-8058Artikel i tidskrift (Refereegranskat) 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.

    Nationell ämneskategori
    Evolutionsbiologi
    Identifikatorer
    urn:nbn:se:uu:diva-320335 (URN)10.1073/pnas.1705601114 (DOI)000406189900080 ()28698378 (PubMedID)
    Forskningsfinansiär
    VetenskapsrådetEU, Europeiska forskningsrådet
    Tillgänglig från: 2017-04-19 Skapad: 2017-04-19 Senast uppdaterad: 2018-05-07Bibliografiskt granskad
    2. Within-ejaculate selection for sperm longevity reduces male reproductive ageing
    Öppna denna publikation i ny flik eller fönster >>Within-ejaculate selection for sperm longevity reduces male reproductive ageing
    Visa övriga...
    (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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. 

    Nyckelord
    Ageing, Reproductive Success, Sperm Selection, Sperm Competition, Senescence
    Nationell ämneskategori
    Evolutionsbiologi
    Forskningsämne
    Biologi med inriktning mot evolutionär genetik
    Identifikatorer
    urn:nbn:se:uu:diva-350186 (URN)
    Tillgänglig från: 2018-05-07 Skapad: 2018-05-07 Senast uppdaterad: 2018-05-07
    3. The fitness consequences of selection among sperm within an ejaculate across generations
    Öppna denna publikation i ny flik eller fönster >>The fitness consequences of selection among sperm within an ejaculate across generations
    (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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.

    Nyckelord
    Haploid selection, sperm selection, offspring fitness, gene expression
    Nationell ämneskategori
    Evolutionsbiologi
    Forskningsämne
    Biologi med inriktning mot evolutionär genetik
    Identifikatorer
    urn:nbn:se:uu:diva-350190 (URN)
    Tillgänglig från: 2018-05-07 Skapad: 2018-05-07 Senast uppdaterad: 2018-05-07
    4. Sperm performance traits exhibit low additive genetic component and strong parental effects in external fertilizer
    Öppna denna publikation i ny flik eller fönster >>Sperm performance traits exhibit low additive genetic component and strong parental effects in external fertilizer
    (Engelska)Manuskript (preprint) (Övrigt vetenskapligt)
    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.

    Nyckelord
    additive genetic, parental effect, sperm traits, reproduction
    Nationell ämneskategori
    Evolutionsbiologi
    Forskningsämne
    Biologi med inriktning mot evolutionär genetik
    Identifikatorer
    urn:nbn:se:uu:diva-350191 (URN)
    Tillgänglig från: 2018-05-07 Skapad: 2018-05-07 Senast uppdaterad: 2018-06-01
  • 2.
    Alavioon, Ghazal
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Garcia, Andrea Cabrera
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    LeChatelier, Magali
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Maklakov, Alex A.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich, Norfolk, England.
    Immler, Simone
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich, Norfolk, England.
    Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring2019Ingår i: EVOLUTION LETTERS, ISSN 2056-3744, Vol. 3, nr 2, s. 198-206Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within-ejaculate sperm selection 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 within-ejaculate sperm selection increases early-life fitness at the cost of accelerated senescence. Alternatively, within-ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age-specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio. We found that within-ejaculate sperm selection for sperm longevity reduced age-specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within-ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early-life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within-ejaculate sperm selection 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 may have important implications for assisted fertilization programs in livestock and humans.

  • 3.
    Alavioon, Ghazal
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Hotzy, Cosima
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nakhro, Khriezhanuo
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Rudolf, Sandra
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Scofield, Douglas
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Zajitschek, Susanne
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Spanish Natl Res Council, Donana Biol Stn, Seville 41092, Spain.
    Maklakov, Alex A
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi. Univ East Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England.
    Immler, Simone
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Univ East Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England.
    Haploid selection within a single ejaculate increases offspring fitness2017Ingår i: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, nr 30, s. 8053-8058Artikel i tidskrift (Refereegranskat)
    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.

  • 4.
    Immler, Simone
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Hotzy, Cosima
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Alavioon, Ghazal
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Petersson, Erik
    Arnqvist, Goran
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sperm variation within a single ejaculate affects offspring development in Atlantic salmon2014Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 10, nr 2, s. 20131040-Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    It is generally believed that variation in sperm phenotype within a single ejaculate has no consequences for offspring performance, because sperm phenotypes are thought not to reflect sperm genotypes. We show that variation in individual sperm function within an ejaculate affects the performance of the resulting offspring in the Atlantic salmon Salmo salar. We experimentally manipulated the time between sperm activation and fertilization in order to select for sperm cohorts differing in longevity within single ejaculates of wild caught male salmon. We found that within-ejaculate variation in sperm longevity significantly affected offspring development and hence time until hatching. Whether these effects have a genetic or epigenetic basis needs to be further evaluated. However, our results provide experimental evidence for transgenerational effects of individual sperm function.

  • 5.
    Lind, Martin I.
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Berg, Elena C.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Alavioon, Ghazal
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Maklakov, Alexei A.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Evolution of differential maternal age effects on male and female offspring development and longevity2015Ingår i: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 29, nr 1, s. 104-110Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Maternal age effects on life-history traits, including longevity, are widespread and can be seen as a manifestation of ageing. However, little is known about how maternal life span may influence the maternal age effect. At a given chronological age, a long-lived parent may be at a younger biological age than a short-lived parent and thus has a less severe parental age effect. However, earlier work using experimentally evolved short- and long-lived lines did not support this hypothesis. We scored developmental time and longevity of 14995 individual seed beetles, Callosobruchus maculatus derived from replicate short-lived and long-lived lines created via artificial selection on male life span. Offspring from older mothers had shorter life span, which is consistent with most of the literature. We found support for the hypothesis that detrimental maternal age effects evolve to be weaker under selection for long life span. However, this finding was only apparent in males, suggesting that maternal age affects male and female offspring differently. These results suggest that sex-dependent parental age effects should be incorporated in the studies of longevity and ageing evolution and that selection on one sex can cause evolution of parental age effects in the other sex.

  • 6.
    Promerová, Marta
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, Germany.
    Alavioon, Ghazal
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Tusso, Sergio
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Burri, Reto
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Department of Population Ecology, Friedrich Schiller University Jena, Jena, Germany.
    Immler, Simone
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    No evidence for MHC class II-based non-random mating at the gametic haplotype in Atlantic salmon2017Ingår i: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 118, nr 6, s. 563-567Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Genes of the major histocompatibility complex (MHC) are a likely target of mate choice because of their role in inbreeding avoidance and potential benefits for offspring immunocompetence. Evidence for female choice for complementary MHC alleles among competing males exists both for the pre- and the postmating stages. However, it remains unclear whether the latter may involve non-random fusion of gametes depending on gametic haplotypes resulting in transmission ratio distortion or non-random sequence divergence among fused gametes. We tested whether non-random gametic fusion of MHC-II haplotypes occurs in Atlantic salmon Salmo salar. We performed in vitro fertilizations that excluded interindividual sperm competition using a split family design with large clutch sample sizes to test for a possible role of the gametic haplotype in mate choice. We sequenced two MHC-II loci in 50 embryos per clutch to assess allelic frequencies and sequence divergence. We found no evidence for transmission ratio distortion at two linked MHC-II loci, nor for non-random gamete fusion with respect to MHC-II alleles. Our findings suggest that the gametic MHC-II haplotypes play no role in gamete association in Atlantic salmon and that earlier findings of MHC-based mate choice most likely reflect choice among diploid genotypes. We discuss possible explanations for these findings and how they differ from findings in mammals.

  • 7.
    Silva, Willian T. A. F.
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Jolly, Cécile
    Alavioon, Ghazal
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Kiehl, Berrit
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Immler, Simone
    Social environment of fathers affects gene expression patterns in early offspringManuskript (preprint) (Övrigt vetenskapligt)
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