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The genetic architecture of sexual dimorphism
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Phenotypic differences between the sexes evolve largely because selection favours a different complement of traits in either sex. Theory suggests that, despite its frequency, sexual dimorphism should be generally constrained from evolving because the sexes share much of their genome. While selection can lead to adaptation in one sex, correlated responses to selection can be maladaptive in the other. In this thesis I use Drosophila to examine the extent to which the shared genome constrains the evolution of sexual dimorphism and whether the sex chromosomes might play a special role in resolving intralocus sexual conflict.

Gene expression data shows that intersexual genetic correlations are generally high, suggesting that genes often affect both sexes. The intersexual genetic correlation is negatively associated with sex-bias in expression in D. melanogaster, and the rate of change in sex-bias between D. melanogaster and six closely related species, showing that a sex-specific genetic architecture is a prerequisite for the evolution of sex difference. In further studies I find that genetic variance affecting lifespan is found in the male-limited Y chromosome within a population, which could offer a route to the evolution of further sexual dimorphism in lifespan, though the amount of variance was small suggesting adaptive potential from standing genetic variance is limited. Genetic variance on the X chromosome is also expected to be depleted once the sex chromosomes evolve, but here I find no evidence of depletion in either sex. Dosage compensation does not appear to double the male X-linked genetic variance, but this effect may be complex to detect. Finally, the X chromosome appears to be enriched for sex-specific genetic variance, and the consequences of this are explored using a variety of analytical methods to test biologically meaningful aspects of G-matrix structure.

In summary, this thesis suggests that the evolution of sexual dimorphism is generally constrained by the shared genome, but intralocus sexual conflict could be resolved by novel mutations on the Y chromosomes, and by standing sex-specific genetic variance on the X chromosome. It highlights a special role for the X chromosome in the evolution of sexual dimorphism.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 56 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1264
Keyword [en]
Drosophila melanogaster, evolution, intralocus sexual conflict, sex chromosomes, sexually antagonistic selection, sexual dimorphism
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-258986ISBN: 978-91-554-9278-6 (print)OAI: oai:DiVA.org:uu-258986DiVA: diva2:842941
Public defence
2015-09-18, Lindahlsalen, Evolutionary Biology Centre, Norbyvägen 18, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2015-08-28 Created: 2015-07-23 Last updated: 2015-10-01
List of papers
1. The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression
Open this publication in new window or tab >>The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression
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2013 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 30, no 9, 2168-2176 p.Article in journal (Refereed) Published
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.

Keyword
sexual dimorphism, genetic constraint, sex-biased gene expression
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-208062 (URN)10.1093/molbev/mst121 (DOI)000323616600015 ()
Available from: 2013-09-24 Created: 2013-09-23 Last updated: 2017-12-06Bibliographically approved
2. Within-population Y-linked genetic variation for lifespan in Drosophila melanogaster
Open this publication in new window or tab >>Within-population Y-linked genetic variation for lifespan in Drosophila melanogaster
2015 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 28, no 11, 1940-1947 p.Article in journal (Other academic) Published
Abstract [en]

The view that the Y chromosome is of little importance for phenotypic evolution stems from early studies of Drosophila melanogaster. This species’ Y chromosome contains only 13 protein coding genes, is almost entirely heterochromatic, and is not necessary for male viability. Population genetic theory further suggests that non-neutral variation can only be maintained at the Y chromosome under special circumstances. Yet, recent studies suggest that the D. melanogaster Y chromosome trans-regulates hundreds to thousands of X and autosomal genes. This finding suggests that the Y chromosome may play a far more active role in adaptive evolution than has previously been assumed. To evaluate the potential for the Y chromosome to contribute to phenotypic evolution from standing genetic variation, we test for Y-linked variation in lifespan within a population of D. melanogaster. Assessing variation for lifespan provides a powerful test because lifespan i) shows sexual dimorphism, which the Y is primarily predicted to contribute to, ii) is influenced by many genes, which provides the Y with many potential regulatory targets, and iii) is sensitive to heterochromatin remodelling, a mechanism through which the Y chromosome is believed to regulate gene expression. Our results show a small but significant effect of the Y chromosome, and thus suggest that the Y chromosome has the potential to respond to selection from standing genetic variation. Despite its small effect size, Y-linked variation may still be important, in particular when evolution of sexual dimorphism is genetically constrained elsewhere in the genome.

Keyword
intralocus sexual conflict, longevity, sex chromosomes, sexual dimorphism, Y chromosome
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-258982 (URN)10.1111/jeb.12708 (DOI)000364641900003 ()26230387 (PubMedID)
Funder
Swedish Foundation for Strategic Research Carl Tryggers foundation Swedish Research CouncilGerman Research Foundation (DFG), SCHI 1188/1-1
Available from: 2015-07-23 Created: 2015-07-23 Last updated: 2017-12-04Bibliographically approved
3. Autosomal and X-linked additive genetic variation for lifespan and ageing: comparisons within and between the sexes in Drosophila melanogaster
Open this publication in new window or tab >>Autosomal and X-linked additive genetic variation for lifespan and ageing: comparisons within and between the sexes in Drosophila melanogaster
(English)Article in journal (Other academic) Submitted
Keyword
dosage compensation, faster X, heritability, intersexual genetic correlation, longevity, sexual dimorphism, X chromosome
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-258983 (URN)
Available from: 2015-07-23 Created: 2015-07-23 Last updated: 2015-08-28
4. Adaptation across the genome: multivariate decomposition indicates different roles for the X and autosomes
Open this publication in new window or tab >>Adaptation across the genome: multivariate decomposition indicates different roles for the X and autosomes
(English)Manuscript (preprint) (Other academic)
Keyword
Drosophila melanogaster, G-matrix, genetic covariance matrix, intralocus sexual conflict, sex chromosomes, sexual dimorphism
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-258984 (URN)
Available from: 2015-07-23 Created: 2015-07-23 Last updated: 2015-08-28

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