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Evolutionary Consequences of Reproductive Strategies: Testing Theory on Sex and Reproductive Gene Evolution in the Fungal Model Neurospora
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In this thesis, I used the filamentous ascomycete genus Neurospora as a model to test theoretical predictions on the evolutionary consequences of different reproductive strategies and reproductive gene evolution. The genus Neurospora contains taxa representing a diversity of reproductive strategies, and here I constructed a phylogeny by which I was able to show that several independent transitions in reproductive mode have occurred in the evolutionary history of the genus. This feature makes Neurospora a suitable model for the evolution of reproductive modes. Molecular evolutionary analysis of housekeeping genes revealed an accelerated protein evolution in the highly inbreeding homothallic taxa, in accordance with theory predictions of lower efficiency of selection in asexual and highly inbreeding taxa. Furthermore, self-sterile (heterothallic) taxa capable of asexual propagation was found to be associated with a three-fold higher neutral substitution rate, indicative of a higher mutation accumulation due to elevated number of cell divisions per unit time in these taxa.

Further, I have shown a general pattern of rapid evolution of genes involved in reproduction in Neurospora, thus extending the pattern of general high divergence of reproductive genes previously well known in animals, to fungi. Two rapidly evolving reproductive genes: the pheromone receptor genes pre-1 and pre-2 involved in mate recognition were studied in detail. For the gene pre-1 the rapid divergence was found to be driven by positive selection in both heterothallic and homothallic taxa. The rapid divergence of the pheromone receptor gene pre-2 cannot be explained by positive selection and for this gene a subtle differences in evolutionary constraints between heterothallic and homothallic taxa were found. The general similarity in evolutionary constraints of pre-genes in taxa of both mating-systems indicates that these genes serve other functions beside mate recognition.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2011. , 45 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 839
National Category
Biological Sciences
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-152953ISBN: 978-91-554-8102-5OAI: oai:DiVA.org:uu-152953DiVA: diva2:414572
Public defence
2011-06-10, Zootissalen, Evolutionsmuseet (Museum of Evolution), Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2011-05-19 Created: 2011-05-03 Last updated: 2011-07-01Bibliographically approved
List of papers
1. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi
Open this publication in new window or tab >>A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi
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2011 (English)In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 59, no 3, 649-663 p.Article in journal (Refereed) Published
Abstract [en]

The filamentous ascomycete genus Neurospora encompasses taxa with a wide range of reproductive modes. Sexual reproduction in this genus can be divided into three major modes; heterothallism (self-incompatibility), homothallism (self-compatibility) and pseudohomothallism (partial self-compatibility). In addition to the sexual pathway, most of the heterothallic taxa propagate with morphologically distinct, vegetative dissemination propagules (macroconidia), while this feature is undetected in the majority of the homothallic taxa. In this study, we used sequence information of seven nuclear gene loci from 43 taxa (295 of the possible 301 locus-by-taxon combinations) to create a phylogeny of Neurospora. The results suggest that transitions in reproductive mode have occurred at multiple times within this group of fungi. Although a homothallic ancestor would imply fewer switches in reproductive mode, we argue that the ancestor of Neurospora was likely heterothallic and that homothallism has evolved independently at least six times in the evolutionary history of the genus. Furthermore, the two pseudohomothallic taxa of Neurospora (N. tetrasperma and N. tetraspora) represent two independent origins of pseudohomothallism. Likelihood ratio tests of substitution rates among branches in the phylogeny indicate that reproductive mode is an important factor driving genome evolution in Neurospora. First, an increased level of non-synonymous/synonymous substitutions in branches delineating homothallic taxa was found, suggesting a reduced efficiency of purifying selection in these taxa. Furthermore, elevated nucleotide substitution rates were found in heterothallic, conidia-producing, lineages as compared to the homothallic non-conidiating lineages. The latter finding is likely due to the presence of conidia, i.e., a higher rate of mitotic divisions inducing mutations, and/or that the homothallic taxa have evolved a lower mutation rate to avoid genomic degeneration.

Keyword
Outcrossing, Selfing, Conidia, Mutation rate, dN/dS, Ancestral character state, Dead end theory
National Category
Biological Systematics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-152948 (URN)10.1016/j.ympev.2011.03.023 (DOI)000290609000010 ()21439389 (PubMedID)
Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2016-04-27Bibliographically approved
2. The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic neurospora
Open this publication in new window or tab >>The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic neurospora
2008 (English)In: Molecular biology and evolution, ISSN 0737-4038, Vol. 25, no 1, 168-178 p.Article in journal (Refereed) Published
Abstract [en]

Comparative sequencing studies among a wide range of taxonomic groups, including fungi, provide the overall pattern that reproductive genes evolve more rapidly than other genes, and this divergence is believed to be important in the establishment of reproductive barriers between species. In this study, we investigated the molecular evolution of the pheromone receptor genes pre-1 and pre-2 of strains belonging to 12 and 13 heterothallic taxa, respectively, of the model genus Neurospora. Furthermore, we examined the regulatory pattern of both pheromone precursor and receptor genes during sexual crosses of Neurospora crassa and Neurospora intermedia, for which reinforcement of interspecific reproductive barriers in sympatry previously has been documented. We conclude that the part encoding the C-terminal intracellular domain of pre-1 and pre-2 genes evolves rapidly. Both stochastic and directional processes drive this divergence; both genes contain neutrally evolving codons, and in addition, pre-1 contains codons evolving under positive selection, whereas in pre-2 we found highly variable regions with numerous repeats encoding glycine, threonine, or aspartic acid. In addition, we found regulatory changes of the pheromone and receptor genes during crosses between N. crassa and N. intermedia with different reproductive success. Gene expression levels are higher in the interspecific sympatric crosses with low reproductive success than in their intraspecific and/or allopatric equivalents, both at the stage of initial communication and contact and later at postfertilization stages. Taken together, our data indicate that pheromones and receptors are important key players during reproductive isolation between Neurospora species, and this study provides a general framework for future studies on the role of reproductive proteins for reproductive isolation.

Keyword
Neurospora, pheromone, pheromone receptor, reproductive protein, speciation, reinforcement
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-15328 (URN)10.1093/molbev/msm253 (DOI)000253375900017 ()18024989 (PubMedID)
Available from: 2008-02-11 Created: 2008-02-11 Last updated: 2011-07-01Bibliographically approved
3. Inferring the evolutionary constraints of pheromone receptor genes in self-fertilizing species of the model genus Neurospora
Open this publication in new window or tab >>Inferring the evolutionary constraints of pheromone receptor genes in self-fertilizing species of the model genus Neurospora
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(English)Manuscript (preprint) (Other academic)
National Category
Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-152951 (URN)
Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2011-07-01
4. Evolutionary expressed sequence tag analysis of Neurospora reveals rapid evolution of fungal reproductive genes
Open this publication in new window or tab >>Evolutionary expressed sequence tag analysis of Neurospora reveals rapid evolution of fungal reproductive genes
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(English)Manuscript (preprint) (Other academic)
National Category
Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-152952 (URN)
Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2011-07-01

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