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Publications (10 of 27) Show all publications
Alavioon, G., Garcia, A. C., LeChatelier, M., Maklakov, A. A. & Immler, S. (2019). Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring. EVOLUTION LETTERS, 3(2), 198-206
Open this publication in new window or tab >>Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring
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2019 (English)In: EVOLUTION LETTERS, ISSN 2056-3744, Vol. 3, no 2, p. 198-206Article in journal (Refereed) Published
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.

Keywords
Ageing, reproductive success, sperm selection, sperm competition, senescence
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-382654 (URN)10.1002/evl3.101 (DOI)000463987900008 ()
Funder
EU, European Research Council, HapSelA 336633Knut and Alice Wallenberg Foundation
Available from: 2019-04-29 Created: 2019-04-29 Last updated: 2019-04-29Bibliographically approved
Silva, W. T. A., Sáez-Espinosa, P., Torrijo-Boix, S., Romero, A., Devaux, C., Durieux, M., . . . Immler, S. (2019). The effects of male social environment on sperm phenotype and genome integrity. Journal of Evolutionary Biology, 32(6), 535-544
Open this publication in new window or tab >>The effects of male social environment on sperm phenotype and genome integrity
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2019 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 32, no 6, p. 535-544Article in journal (Refereed) Published
Abstract [en]

Sperm function and quality are primary determinants of male reproductive performance and hence fitness. The presence of rival males has been shown to affect ejaculate and sperm traits in a wide range of taxa. However, male physiological conditions may not only affect sperm phenotypic traits but also their genetic and epigenetic signatures, affecting the fitness of the resulting offspring. We investigated the effects of male-male competition on sperm quality using TUNEL assays and geometric morphometrics in the zebrafish, Danio rerio. We found that the sperm produced by males exposed to high male-male competition had smaller heads but larger midpiece and flagellum than sperm produced by males under low competition. Head and flagella also appeared less sensitive to the osmotic stress induced by activation with water. In addition, more sperm showed signals of DNA damage in ejaculates of males under high competition. These findings suggest that the presence of a rival male may have positive effects on sperm phenotypic traits but negative effects on sperm DNA integrity. Overall, males facing the presence of rival males may produce faster swimming and more competitive sperm but this may come at a cost for the next generation.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
Keywords
DNA damage, sexual selection, sperm competition, trade‐offs
National Category
Evolutionary Biology Zoology Genetics
Identifiers
urn:nbn:se:uu:diva-359415 (URN)10.1111/jeb.13435 (DOI)000472662300002 ()30817032 (PubMedID)
Funder
EU, European Research Council, HapSelA-336633Knut and Alice Wallenberg Foundation
Available from: 2018-09-01 Created: 2018-09-01 Last updated: 2019-08-13Bibliographically approved
Maklakov, A. A., Carlsson, H., Denbaum, P., Lind, M. I., Mautz, B., Hinas, A. & Immler, S. (2017). Antagonistically pleiotropic allele increases lifespan and late-life reproduction at the cost of early-life reproduction and individual fitness. Proceedings of the Royal Society of London. Biological Sciences, 284(1856), Article ID 20170376.
Open this publication in new window or tab >>Antagonistically pleiotropic allele increases lifespan and late-life reproduction at the cost of early-life reproduction and individual fitness
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2017 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1856, article id 20170376Article in journal (Refereed) Published
Abstract [en]

Evolutionary theory of ageing maintains that increased allocation to early-life reproduction results in reduced somatic maintenance, which is predicted to compromise longevity and late-life reproduction. This prediction has been challenged by the discovery of long-lived mutants with no loss of fecundity. The first such long-lived mutant was found in the nematode worm Caenorhabditis elegans. Specifically, partial loss-of-function mutation in the age-1 gene, involved in the nutrient-sensing insulin/insulin-like growth factor signalling pathway, confers longevity, as well as increased resistance to pathogens and to temperature stress without appreciable fitness detriment. Here, we show that the long-lived age-1(hx546) mutant has reduced fecundity and offspring production in early-life, but increased fecundity, hatching success, and offspring production in late-life compared with wild-type worms under standard conditions. However, reduced early-life performance of long-lived mutant animals was not fully compensated by improved performance in late-life and resulted in reduced individual fitness. These results suggest that the age-1(hx546) allele has opposing effects on early-life versus late-life fitness in accordance with antagonistic pleiotropy (AP) and disposable soma theories of ageing. These findings support the theoretical conjecture that experimental studies based on standing genetic variation underestimate the importance of AP in the evolution of ageing.

Place, publisher, year, edition, pages
ROYAL SOC, 2017
Keywords
ageing, senescence, life history
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-331255 (URN)10.1098/rspb.2017.0376 (DOI)000405955300010 ()
Funder
EU, European Research Council, AGINGSEXDIFF 260885, HAPSELA 336633Swedish Research Council, 2013-04828
Available from: 2017-10-24 Created: 2017-10-24 Last updated: 2017-10-24Bibliographically approved
Alavioon, G., Hotzy, C., Nakhro, K., Rudolf, S., Scofield, D., Zajitschek, S., . . . Immler, S. (2017). Haploid selection within a single ejaculate increases offspring fitness. Proceedings of the National Academy of Sciences of the United States of America (30), 8053-8058
Open this publication in new window or tab >>Haploid selection within a single ejaculate increases offspring fitness
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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.

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
Promerová, M., Alavioon, G., Tusso, S., Burri, R. & Immler, S. (2017). No evidence for MHC class II-based non-random mating at the gametic haplotype in Atlantic salmon. Heredity, 118(6), 563-567
Open this publication in new window or tab >>No evidence for MHC class II-based non-random mating at the gametic haplotype in Atlantic salmon
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2017 (English)In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 118, no 6, p. 563-567Article in journal (Refereed) Published
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.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-390738 (URN)10.1038/hdy.2016.129 (DOI)000401023700007 ()28098849 (PubMedID)
Funder
Swedish Research CouncilEU, European Research Council
Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-12-16Bibliographically approved
Zajitschek, S., Herbert-Read, J. E., Abbasi, N. M., Zajitschek, F. & Immler, S. (2017). Paternal personality and social status influence offspring activity in zebrafish. BMC Evolutionary Biology, 17, Article ID 157.
Open this publication in new window or tab >>Paternal personality and social status influence offspring activity in zebrafish
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2017 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, article id 157Article in journal (Refereed) Published
Abstract [en]

Background: Evidence for the transmission of non-genetic information from father to offspring is rapidly accumulating. While the impact of chemical and physical factors such as toxins or diet on the fitness of the parents and their offspring have been studied extensively, the importance of behavioural and social circumstances has only recently been recognised. Behavioural traits such as personality characteristics can be relatively stable, and partly comprise a genetic component but we know little about the non-genetic transmission of plastic behavioural traits from parents to offspring. We investigated the relative effect of personality and of social dominance as indicators at the opposite ends of the plasticity range on offspring behaviour in the zebrafish (Danio rerio). We assessed male boldness, a behavioural trait that has previously been shown previously to possess genetic underpinnings, and experimentally manipulated male social status to assess the association between the two types of behaviour and their correlation with offspring activity. Results: We found a clear interaction between the relatively stable and putative genetic effects based on inherited differences in personality and the experimentally induced epigenetic effects from changes in the social status of the father on offspring activity. Conclusions: Our study shows that offspring behaviour is determined by a combination of paternal personality traits and on-genetic effects derived from the social status of the father.

Keywords
Behavioural syndrome, Boldness, Context-dependence, Dominance, Sperm trait, Transgenerational effects
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-330000 (URN)10.1186/s12862-017-1005-0 (DOI)000404926600003 ()
Funder
Knut and Alice Wallenberg Foundation, 102 2013.0072Swedish Research CouncilWenner-Gren FoundationsEU, European Research Council
Available from: 2017-10-13 Created: 2017-10-13 Last updated: 2017-11-29Bibliographically approved
Nieuwenhuis, B. P. S. & Immler, S. (2016). The evolution of mating-type switching for reproductive assurance. Bioessays, 38(11), 1141-1149
Open this publication in new window or tab >>The evolution of mating-type switching for reproductive assurance
2016 (English)In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 38, no 11, p. 1141-1149Article, review/survey (Refereed) Published
Abstract [en]

Alternative ways to ensure mate compatibility, such as hermaphroditism and the breakdown of self-incompatibility, evolved repeatedly when finding a mating partner is difficult. In a variety of microorganisms where compatibility is determined by mating-types, a highly regulated form of universal compatibility system called mating-type switching has evolved several times. This sophisticated system allows for the genetic adjustment of the mating type during asexual growth, and it most likely evolved for reproductive assurance of immotile species under low densities. In this review, we compare the switching strategy to other universal compatibility systems such as unisexual mating and homothallism. We identify the costs of switching, including genome instability, and mechanistic costs, as well as the benefits, mainly the maintenance of important mating-type functions. Given the potential benefits of mating-type switching, we speculate that switching is likely to have evolved many times independently, and may be more common in groups where genetic mating types regulate mate compatibility than assumed so far.

Keywords
Allee effect, Baker's Law, density dependence, fungi, self-incompatibility, yeast
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-313664 (URN)10.1002/bies.201600139 (DOI)000387054600014 ()27650253 (PubMedID)
Funder
Carl Tryggers foundation EU, European Research Council
Available from: 2017-01-24 Created: 2017-01-23 Last updated: 2017-11-29Bibliographically approved
Maklakov, A. A. & Immler, S. (2016). The Expensive Germline and the Evolution of Ageing. Current Biology, 26(13), R577-R586
Open this publication in new window or tab >>The Expensive Germline and the Evolution of Ageing
2016 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 26, no 13, p. R577-R586Article, review/survey (Refereed) Published
Abstract [en]

The trade-off between survival and reproduction is the bedrock of the evolutionary theory of ageing. The reproductive system regulates ageing of the soma, and removal of germ cells extends somatic lifespan and increases resistance to a broad variety of abiotic and biotic stresses. The general explanation for this somatic response is that reduced reproduction frees up resources for survival. Remarkably, however, the disruption of molecular signaling pathways that regulate ageing increases lifespan without the obligatory reduction in fecundity, thus challenging the key role of the survival-reproduction trade-off. Here, we review the diverse literature on the costs of lifespan extension and suggest that the current paradigm is overly centered on the trade-off between lifespan and fecundity, often neglecting key aspects of fitness, such as development time, defense against parasites and, in particular, the high costs of germline maintenance. Compromised germline maintenance increases germline mutation rate, which reduces offspring fitness and ultimately can terminate germline proliferation across generations. We propose that future work should incorporate the costs of germline maintenance in the study of ageing evolution, as well as in applied biomedical research, by assessing offspring fitness.

National Category
Biochemistry and Molecular Biology Cell Biology
Identifiers
urn:nbn:se:uu:diva-309838 (URN)10.1016/j.cub.2016.04.012 (DOI)000384799500024 ()27404253 (PubMedID)
Funder
EU, European Research CouncilSwedish Research CouncilKnut and Alice Wallenberg Foundation
Available from: 2016-12-08 Created: 2016-12-07 Last updated: 2017-11-29Bibliographically approved
Otto, S. P., Scott, M. F. & Immler, S. (2015). Evolution of haploid selection in predominantly diploid organisms. Proceedings of the National Academy of Sciences of the United States of America, 112(52), 15952-15957
Open this publication in new window or tab >>Evolution of haploid selection in predominantly diploid organisms
2015 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 112, no 52, p. 15952-15957Article in journal (Refereed) Published
Abstract [en]

Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes. Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the "selective arena" within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids ("ploidally antagonistic selection"), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father's gametes. We discuss the implications of this maternal-paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.

Keywords
pollen competition, antagonistic selection, haploid selection, sperm competition, evolutionary theory
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-274434 (URN)10.1073/pnas.1512004112 (DOI)000367234700061 ()26669442 (PubMedID)
Funder
Swedish Research Council, VR 621-2010-5670EU, European Research Council, 336633-HapSelA
Available from: 2016-01-21 Created: 2016-01-21 Last updated: 2017-11-30Bibliographically approved
Kotrschal, A., Corral-Lopez, A., Zajitschek, S., Immler, S., Maklakov, A. A. & Kolm, N. (2015). Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size. Journal of Evolutionary Biology, 28(4), 841-850
Open this publication in new window or tab >>Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size
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2015 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 28, no 4, p. 841-850Article in journal (Refereed) Published
Abstract [en]

Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade-offs between brain size and sexual traits. Instead, larger-brained males had higher expression of several primary and precopulatory sexual traits - they had longer genitalia, were more colourful and developed longer tails than smaller-brained males. Larger-brained males were also in better body condition when housed in single-sex groups. There was no difference in post-copulatory sexual traits between males from the large- and small-brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.

Keywords
artificial selection, brain size, genetic correlation, guppy, sexual selection, trade-off
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-253074 (URN)10.1111/jeb.12608 (DOI)000353295200009 ()25705852 (PubMedID)
Funder
Carl Tryggers foundation Swedish Research Council
Available from: 2015-06-11 Created: 2015-05-20 Last updated: 2017-12-04Bibliographically approved
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