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Open Access Research article

Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve

Jeff S Piotrowski13, Saisubramanian Nagarajan23, Evgueny Kroll3, Alison Stanbery3, Kami E Chiotti3, Arthur L Kruckeberg4, Barbara Dunn5, Gavin Sherlock5 and Frank Rosenzweig3*

Author Affiliations

1 Chemical Genomics Research Group, RIKEN Advance Science Institute, Wako, Wako, Japan

2 School of Chemical and Biotechnology, SASTRA University, Tirumalaisamudram Thanjavur- 613401, Tamil Nadu, India

3 Division of Biological Sciences, The University of Montana, Missoula MT 59812, USA

4 DuPont Corporation, Wilmington DE 19880, USA

5 Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305-5120, USA

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BMC Evolutionary Biology 2012, 12:46  doi:10.1186/1471-2148-12-46

Published: 2 April 2012

Abstract

Background

Interspecific hybridization occurs in every eukaryotic kingdom. While hybrid progeny are frequently at a selective disadvantage, in some instances their increased genome size and complexity may result in greater stress resistance than their ancestors, which can be adaptively advantageous at the edges of their ancestors' ranges. While this phenomenon has been repeatedly documented in the field, the response of hybrid populations to long-term selection has not often been explored in the lab. To fill this knowledge gap we crossed the two most distantly related members of the Saccharomyces sensu stricto group, S. cerevisiae and S. uvarum, and established a mixed population of homoploid and aneuploid hybrids to study how different types of selection impact hybrid genome structure.

Results

As temperature was raised incrementally from 31°C to 46.5°C over 500 generations of continuous culture, selection favored loss of the S. uvarum genome, although the kinetics of genome loss differed among independent replicates. Temperature-selected isolates exhibited greater inherent and induced thermal tolerance than parental species and founding hybrids, and also exhibited ethanol resistance. In contrast, as exogenous ethanol was increased from 0% to 14% over 500 generations of continuous culture, selection favored euploid S. cerevisiae x S. uvarum hybrids. Ethanol-selected isolates were more ethanol tolerant than S. uvarum and one of the founding hybrids, but did not exhibit resistance to temperature stress. Relative to parental and founding hybrids, temperature-selected strains showed heritable differences in cell wall structure in the forms of increased resistance to zymolyase digestion and Micafungin, which targets cell wall biosynthesis.

Conclusions

This is the first study to show experimentally that the genomic fate of newly-formed interspecific hybrids depends on the type of selection they encounter during the course of evolution, underscoring the importance of the ecological theatre in determining the outcome of the evolutionary play.