Gene expression bias between the subgenomes of allopolyploid hybrids is an emergent property of the kinetics of expression

Hybridization coupled to polyploidy, or allopolyploidy, has dramatically shaped the evolution of flowering plants, teleost fishes, and other lineages. Studies of recently formed allopolyploid plants have shown that the two subgenomes that merged to form that new allopolyploid do not generally express their genes equally. Instead, one of the two subgenomes expresses its paralogs more highly on average. Meanwhile, older allopolyploidy events tend to show biases in duplicate losses, with one of the two subgenomes retaining more genes than the other. Since reduced expression is a pathway to duplicate loss, understanding the origins of expression biases may help explain the origins of biased losses. Because we expect gene expression levels to experience stabilizing selection, our conceptual frameworks for how allopolyploid organisms form tend to assume that the new allopolyploid will show balanced expression between its subgenomes. It is then necessary to invoke phenomena such as differences in the suppression of repetitive elements to explain the observed expression imbalances. Here we show that, even for phenotypically identical diploid progenitors, the inherent kinetics of gene expression give rise to biases between the expression levels of the progenitor genes in the hybrid. Some of these biases are expected to be gene-specific and not give rise to global differences in progenitor gene expression. However, particularly in the case of allopolyploids formed from progenitors with different genome sizes, global expression biases favoring one subgenome are expected immediately on formation. Hence, expression biases are arguably the expectation upon allopolyploid formation rather than a phenomenon needing explanation. In the future, a deeper understanding of the kinetics of allopolyploidy may allow us to better understand both biases in duplicate losses and hybrid vigor. Allopolyploidy, or polyploidy through hybridization, is common across the eukaryotes. In newly formed allopolyploids, one of the contributing progenitor subgenomes generally expresses its genes at higher levels than does the subgenome from the other progenitor. It is believed that, as allopolyploids age, these expression differences drive differential duplicate gene losses between the subgenomes, as most older polyploidies show such biases in their gene losses. However, why the expression biases appear in the first place has been debated. Here, we use simple models of gene expression to show that the merging of distinct progenitor genomes through allopolyploidy will almost always yield expression biases due to the nonlinear kinetics of transcription. We argue that expression biases are hence the expectation for most allopolyploidies without a need for more complex explanations.