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  • 1.
    Burgevin, Lorraine
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Intersexual correlation for same-sex sexual behaviour in an insect2013In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 85, no 4, p. 759-762Article in journal (Refereed)
    Abstract [en]

    Same-sex sexual behaviour is widespread across taxa and is particularly common in insects, in which up to 50% of copulation attempts by males are directed towards other males in some species. Research effort has focused on male-male same-sex behaviour and the prevailing theory is that benefits of high mating rate combined with poor sex discrimination explain the high incidence of male-male mounting. However, the evolution of female-female mounting is more enigmatic, since females typically do not mount males in order to mate. Using a full-sib design, we found an intersexual correlation for same-sex mounting in the beetle Callosobruchus maculatus. Variation in male-male mounting across families explained over 20% of variation in female-female mounting. Moreover, we found no evidence that same-sex behaviour was related to general activity level in either sex or carried a fitness cost to females. Taken together, our results suggest that female-female mounting is a relatively low-cost behaviour that may be maintained in the population via selection on males.

  • 2.
    Friberg, Urban
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Genetic variation in male and female reproductive characters associated with sexual conflict in Drosophila melanogaster2005In: Behavior Genetics, Vol. 35, p. 455-462Article in journal (Refereed)
  • 3.
    Friberg, Urban
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Arnqvist, Göran
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females2003In: Journal of Evolutionary Biology, Vol. 16, p. 797-811Article in journal (Refereed)
  • 4.
    Friberg, Urban
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Lew, T A
    Byrne, P G
    Rice, W R
    Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation2005In: Evolution, Vol. 59, p. 1540-1551Article in journal (Refereed)
  • 5.
    Friberg, Urban
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Stewart, Andrew D.
    Rice, William R.
    X- and Y-chromosome linked paternal effects on a life-history trait2012In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 8, no 1, p. 71-73Article in journal (Refereed)
    Abstract [en]

    Males and females usually invest asymmetrically in offspring. In species lacking parental care, females influence offspring in many ways, while males only contribute genetic material via their sperm. For this reason, maternal effects have long been considered an important source of phenotypic variation, while paternal effects have been presumed to be absent or negligible. The recent surge of studies showing trans-generational epigenetic effects questions this assumption, and indicates that paternal effects may be far more important than previously appreciated. Here, we test for sex-linked paternal effects in Drosophila melanogaster on a life-history trait, and find substantial support for both X- and Y-linked effects.

  • 6.
    Griffin, Robert M.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Dean, Rebecca
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Grace, Jaime L.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ryden, Patrik
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression2013In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 30, no 9, p. 2168-2176Article in journal (Refereed)
    Abstract [en]

    Males and females share most of their genomes, and differences between the sexes can therefore not evolve through sequence divergence in protein coding genes. Sexual dimorphism is instead restricted to occur through sex-specific expression and splicing of gene products. Evolution of sexual dimorphism through these mechanisms should, however, also be constrained when the sexes share the genetic architecture for regulation of gene expression. Despite these obstacles, sexual dimorphism is prevalent in the animal kingdom and commonly evolves rapidly. Here, we ask whether the genetic architecture of gene expression is plastic and easily molded by sex-specific selection, or if sexual dimorphism evolves rapidly despite pervasive genetic constraint. To address this question, we explore the relationship between the intersexual genetic correlation for gene expression (r(MF)), which captures how independently genes are regulated in the sexes, and the evolution of sex-biased gene expression. Using transcriptome data from Drosophila melanogaster, we find that most genes have a high r(MF) and that genes currently exposed to sexually antagonistic selection have a higher average r(MF) than other genes. We further show that genes with a high r(MF) have less pronounced sex-biased gene expression than genes with a low r(MF) within D. melanogaster and that the strength of the r(MF) in D. melanogaster predicts the degree to which the sex bias of a gene's expression has changed between D. melanogaster and six other species in the Drosophila genus. In sum, our results show that a shared genome constrains both short- and long-term evolution of sexual dimorphism.

  • 7.
    Lehtovaara, Anne
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Schielzeth, Holger
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Flis, Ilona
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Heritability of Life Span Is Largely Sex Limited in Drosophila2013In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 182, no 5, p. 653-665Article in journal (Refereed)
    Abstract [en]

    Males and females differ with respect to life span and rate of aging in most animal species. Such sexual dimorphism can be associated with a complex genetic architecture, where only part of the genetic variation is shared between the sexes. However, the extent to which this is true for life span and aging is not known, because studies of life span have given contradictory results and aging has not been studied from this perspective. Here we investigate the additive genetic architecture of life span and aging in Drosophila melanogaster. We find substantial amounts of additive genetic variation for both traits, with more than three-quarters of this variation available for sex-specific evolutionary change. This result shows that the sexes have a profoundly different additive genetic basis for these traits, which has several implications. First, it translates into an, on average, three-times-higher heritability of life span within, compared to between, the sexes. Second, it implies that the sexes are relatively free to evolve with respect to these traits. And third, as life span and aging are traits that integrate over all genetic factors that contribute to mortal disease, it also implies that the genetics of heritable disease differs vastly between the sexes.

  • 8.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lövlie, Hanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Flis, Ilona
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The effect of sexual harassment on lethal mutation rate in female Drosophila melanogaster2013In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 280, no 1750, p. 20121874-Article in journal (Refereed)
    Abstract [en]

    The rate by which new mutations are introduced into a population may have far-reaching implications for processes at the population level. Theory assumes that all individuals within a population have the same mutation rate, but this assumption may not be true. Compared with individuals in high condition, those in poor condition may have fewer resources available to invest in DNA repair, resulting in elevated mutation rates. Alternatively, environmentally induced stress can result in increased investment in DNA repair at the expense of reproduction. Here, we directly test whether sexual harassment by males, known to reduce female condition, affects female capacity to alleviate DNA damage in Drosophila melanogaster fruitflies. Female gametes can repair double-strand DNA breaks in sperm, which allows manipulating mutation rate independently from female condition. We show that male harassment strongly not only reduces female fecundity, but also reduces the yield of dominant lethal mutations, supporting the hypothesis that stressed organisms invest relatively more in repair mechanisms. We discuss our results in the light of previous research and suggest that social effects such as density and courtship can play an important and underappreciated role in mediating condition-dependent mutation rate.

  • 9. Rice, William R.
    et al.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gavrilets, Sergey
    Homosexuality as a Consequence of Epigenetically Canalized Sexual Development2012In: The Quarterly review of biology, ISSN 0033-5770, E-ISSN 1539-7718, Vol. 87, no 4, p. 343-368Article, review/survey (Refereed)
    Abstract [en]

    Male and female homosexuality have substantial prevalence in humans. Pedigree and twin studies indicate that homosexuality has substantial heritability in both sexes, yet concordance between identical twins is low and molecular studies have failed to find associated DNA markers. This paradoxical pattern calls for an explanation. We use published data on fetal androgen signaling and gene regulation via nongenetic changes in DNA packaging (epigenetics) to develop a new model for homosexuality. It is well established that fetal androgen signaling strongly influences sexual development. We show that an unappreciated feature of this process is reduced androgen sensitivity in XX fetuses and enhanced sensitivity in XY fetuses, and that this difference is most feasibly caused by numerous sex-specific epigenetic modifications ("epi-marks") originating in embryonic stem cells. These epi-marks buffer XX fetuses from masculinization due to excess fetal androgen exposure and similarly buffer XY fetuses from androgen underexposure. Extant data indicates that individual epi-marks influence some but not other sexually dimorphic traits, vary in strength across individuals, and are produced during ontogeny and erased between generations. Those that escape erasure will steer development of the sexual phenotypes they influence in a gonad-discordant direction in opposite sex offspring, mosaically feminizing XY offspring and masculinizing XX offspring. Such sex-specific epi-marks are sexually antagonistic (SA-epi-marks) because they canalize sexual development in the parent that produced them, but contribute to gonad-trait discordances in opposite-sex offspring when unerased. In this model, homosexuality occurs when stronger-than-average SA-epi-marks (influencing sexual preference) from an opposite-sex parent escape erasure and are then paired with a weaker-than-average de novo sex-specific epi-marks produced in opposite-sex offspring. Our model predicts that homosexuality is part of a wider phenomenon in which recently evolved androgen-influenced traits commonly display gonad-trait discordances at substantial frequency, and that the molecular feature underlying most homosexuality is not DNA polymorphism(s), but epi-marks that evolved to canalize sexual dimorphic development that sometimes carryover across generations and contribute to gonad-trait discordances in opposite-sex descendants.

  • 10. Rice, William R.
    et al.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gavrilets, Sergey
    Homosexuality via canalized sexual development: A testing protocol for a new epigenetic model2013In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 35, no 9, p. 764-770Article in journal (Refereed)
    Abstract [en]

    We recently synthesized and reinterpreted published studies to advance an epigenetic model for the development of homosexuality (HS). The model is based on epigenetic marks laid down in response to the XX vs. XY karyotype in embryonic stem cells. These marks boost sensitivity to testosterone in XY fetuses and lower it in XX fetuses, thereby canalizing sexual development. Our model predicts that a subset of these canalizing epigenetic marks stochastically carry over across generations and lead to mosaicism for sexual development in opposite-sex offspring - the homosexual phenotype being one such outcome. Here, we begin by outlining why HS has been under-appreciated as a commonplace phenomenon in nature, and how this trend is currently being reversed in the field of neurobiology. We next briefly describe our epigenetic model of HS, develop a set of predictions, and describe how epigenetic profiles of human stem cells can provide for a strong test of the model.

  • 11.
    Zajitschek, Felix
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Zajitschek, Susanne R. K.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Interactive effects of sex, social environment, dietary restriction, and methionine on survival and reproduction in fruit flies2013In: Age (Omaha), ISSN 0161-9152, E-ISSN 1574-4647, Vol. 35, no 4, p. 1193-1204Article in journal (Refereed)
    Abstract [en]

    For the evolution of life histories, the trade-off between survival and reproduction is fundamental. Because sexes optimize fitness in different ways, this trade-off is expected to be resolved differently by males and females. Consequently, the sexes are predicted to respond differently to changes in resource availability. In fruit flies, research on dietary restriction has focused largely on females maintained in the absence of males, thereby neglecting sexual interactions that affect reproductive behavior of both sexes under more natural conditions. Here, we tested for the interactive effects of diet (40, 60, 100, and 300 % of standard yeast concentrations) and social environment (separate-sex vs. mixed-sex groups) on male and female Drosophila melanogaster life histories. Additionally, we evaluated the essential amino acid methionine as an agent that can uncouple the survival-reproduction trade-off. We show sex differences in the effect of social environment on survival patterns, but not on reproductive fitness. In females, yeast had a positive effect on reproduction and a negative effect on survival. In males, yeast had a negative effect on reproduction and the effect on survival depended on the social environment. Methionine reduced survival, but had no effect on reproduction. Our findings highlight the need to include both sexes and to vary social environments in research programs aimed at lifespan extension and call for further evaluation of the fecundity-restoring effect of methionine.

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