Remarkably ancient balanced polymorphisms in a multi-locus gene network

Chris Todd Hittinger, Paula Gonçalves, José Paulo Sampaio, Jim Dover, Mark Johnston () and Antonis Rokas
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Chris Todd Hittinger: University of Colorado School of Medicine, Aurora, Colorado 80045, USA
Paula Gonçalves: Centro de Recursos Microbiológicos, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa
José Paulo Sampaio: Centro de Recursos Microbiológicos, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa
Jim Dover: University of Colorado School of Medicine, Aurora, Colorado 80045, USA
Mark Johnston: University of Colorado School of Medicine, Aurora, Colorado 80045, USA
Antonis Rokas: Vanderbilt University, Nashville, Tennessee 37235, USA

Nature, 2010, vol. 464, issue 7285, 54-58

Abstract: Abstract Local adaptations within species are often governed by several interacting genes scattered throughout the genome. Single-locus models of selection cannot explain the maintenance of such complex variation because recombination separates co-adapted alleles. Here we report a previously unrecognized type of intraspecific multi-locus genetic variation that has been maintained over a vast period. The galactose (GAL) utilization gene network of Saccharomyces kudriavzevii, a relative of brewer’s yeast, exists in two distinct states: a functional gene network in Portuguese strains and, in Japanese strains, a non-functional gene network of allelic pseudogenes. Genome sequencing of all available S. kudriavzevii strains revealed that none of the functional GAL genes were acquired from other species. Rather, these polymorphisms have been maintained for nearly the entire history of the species, despite more recent gene flow genome-wide. Experimental evidence suggests that inactivation of the GAL3 and GAL80 regulatory genes facilitated the origin and long-term maintenance of the two gene network states. This striking example of a balanced unlinked gene network polymorphism introduces a remarkable type of intraspecific variation that may be widespread.

Date: 2010
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DOI: 10.1038/nature08791

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