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MBE Advance Access published online on November 17, 2007

Molecular Biology and Evolution, doi:10.1093/molbev/msm253
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

RESEARCH ARTICLE

The Evolution of the Pheromonal Signal System and Its Potential Role for Reproductive Isolation in Heterothallic Neurospora

Magnus Karlsson1,2, Kristiina Nygren1 and Hanna Johannesson1

1 Uppsala University, Evolutionary Biology Centre, Department of Evolutionary Biology, Norbyvägen 18D, SE-752 36 Uppsala Uppsala, Sweden
2 Current address: Swedish University of Agricultural Sciences, Department of Forest Mycology and Pathology, Ulls väg 26, SE-750 07 Uppsala, Sweden

Corresponding author: Hanna Johannesson, Uppsala University, Evolutionary Biology Centre, Department of Evolutionary Biology, Norbyvägen 18D, SE-752 36 Uppsala Uppsala, Sweden, e-mail: Hanna.Johannesson{at}ebc.uu.se, phone: +46 18 471 66 62, fax: +46 18 471 63 10

Received for publication October 1, 2007. Accepted for publication October 26, 2007.

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 N. crassa and N. 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 evolve 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 while 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 post-fertilization stages. Taken together, our data indicate that pheromones and receptors are important key players during reproductive isolation between Neurospora species, and this study provide a general framework for future studies on the role of reproductive proteins for reproductive isolation.

Key Words: Neurospora • pheromone • pheromone receptor • reproductive protein • speciation • reinforcement


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