Hybridization and polyploidy are powerful evolutionary forces, inducing a range of phenotypic outcomes, including non-additive expression, subgenome dominance, deviations in genomic dosage, and transcriptome downsizing. The reasons for these patterns and whether they are universal adaptive responses to genome merging and doubling remain debated. To address this, we develop a thermodynamic model of gene expression based on transcription factor (TF)-promoter binding. Applied to hybridization between species with divergent gene expression levels, cell volumes, or euchromatic ratios, this model distinguishes the effects of hybridization from those of polyploidy. Our results align with empirical observations, suggesting that gene regulation patterns in hybrids and polyploids often stem from the constrained interplay between inherited diverged regulatory networks rather than from subsequent adaptive evolution. In addition, occurrence of certain phenotypic traits depend on specific assumptions about promoter-TF coevolution and their distribution within the hybrid's nucleoplasm, offering new research avenues to understand the underlying mechanisms. In summary, our model explains how the legacy of divergent species directly influences the phenotypic traits of hybrids and allopolyploids.

Department of Biology and Ecology Faculty of Natural Sciences University of Ostrava Chittussiho 10 Ostrava Czech Republic

Department of Mathematics Faculty of Science University of South Bohemia in České Budějovice Branišovská 1760 370 05 České Budějovice Czech Republic

Institute of Organic Chemistry and Biochemistry of the CAS 166 10 Prague Czech Republic

Laboratory of Non Mendelian Evolution Institute of Animal Physiology and Genetics of the Czech Aacademy of Sciences Rumburská 89 277 21 Liběchov Czech Republic

University of South Bohemia in České Budějovice Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Zátiší 728 2 389 25 Vodňany Czech Republic

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Veitia, R. A., Bottani, S. & Birchler, J. A. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. PubMed DOI

Yoo, M.-J., Liu, X., Pires, J. C., Soltis, P. S. & Soltis, D. E. Nonadditive gene expression in polyploids. PubMed DOI

Comeault, A. A. & Matute, D. R. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation. PubMed DOI PMC

Stöck, M. et al. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum’. PubMed DOI PMC

Bartoš, O. et al. The legacy of sexual ancestors in phenotypic variability, gene expression, and homoeolog regulation of asexual hybrids and polyploids. PubMed DOI PMC

Li, M., Wang, R., Wu, X. & Wang, J. Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus. PubMed DOI PMC

Gianinetti, A. A criticism of the value of midparent in polyploidization. PubMed DOI

Matos, I., Machado, M. P., Schartl, M. & Coelho, M. M. Gene expression dosage regulation in an allopolyploid fish. PubMed DOI PMC

Zhang, M. et al. Effects of parental genetic divergence on gene expression patterns in interspecific hybrids of Camellia. PubMed DOI PMC

Wang, X., Morton, J. A., Pellicer, J., Leitch, I. J. & Leitch, A. R. Genome downsizing after polyploidy: mechanisms, rates and selection pressures. PubMed DOI

Goncalves, A. et al. Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. PubMed DOI PMC

Hu, G. & Wendel, J. F. Cis–trans controls and regulatory novelty accompanying allopolyploidization. PubMed DOI

Mattioli, K. et al. Cis and trans effects differentially contribute to the evolution of promoters and enhancers. PubMed DOI PMC

Ren, L. et al. The subgenomes show asymmetric expression of alleles in hybrid lineages of Megalobrama amblycephala × Culter alburnus. PubMed DOI PMC

Hollister, J. D. & Gaut, B. S. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. PubMed DOI PMC

Tulchinsky, A. Y., Johnson, N. A., Watt, W. B. & Porter, A. H. Hybrid incompatibility arises in a sequence-based bioenergetic model of transcription factor binding. PubMed DOI PMC

Botet, R. & Keurentjes, J. J. B. The role of transcriptional regulation in hybrid vigor. PubMed DOI PMC

McClintock, B. The significance of responses of the genome to challenge. PubMed DOI

GTEx Consortium et al. Genetic effects on gene expression across human tissues. PubMed DOI PMC

Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Evolutionary changes in cis and trans gene regulation. PubMed DOI

Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Regulatory changes underlying expression differences within and between Drosophila species. PubMed DOI

Tirosh, I., Reikhav, S., Levy, A. A. & Barkai, N. A yeast hybrid provides insight into the evolution of gene expression regulation. PubMed DOI

Emerson, J. J. et al. Natural selection on cis and trans regulation in yeasts. PubMed DOI PMC

Shi, X. et al. Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. PubMed DOI

Osada, N., Miyagi, R. & Takahashi, A. Cis- and trans-regulatory effects on gene expression in a natural population of drosophila melanogaster. PubMed DOI PMC

Chu, D., Zabet, N. R. & Mitavskiy, B. Models of transcription factor binding: sensitivity of activation functions to model assumptions. PubMed DOI

Mueller, F., Stasevich, T. J., Mazza, D. & McNally, J. G. Quantifying transcription factor kinetics: at work or at play? PubMed DOI

Porter, A. H., Johnson, N. A. & Tulchinsky, A. Y. A new mechanism for mendelian dominance in regulatory genetic pathways: competitive binding by transcription factors. PubMed DOI PMC

Okubo, K. & Kaneko, K. Evolution of dominance in gene expression pattern associated with phenotypic robustness. PubMed DOI PMC

Bottani, S., Zabet, N. R., Wendel, J. F. & Veitia, R. A. Gene expression dominance in allopolyploids: hypotheses and models. PubMed DOI

Spivakov, M. Spurious transcription factor binding: non-functional or genetically redundant? PubMed DOI PMC

An, H., Pires, J. C. & Conant, G. C. Gene expression bias between the subgenomes of allopolyploid hybrids is an emergent property of the kinetics of expression. PubMed DOI PMC

Coate, J. E. & Doyle, J. J. Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: an example from a plant allopolyploid. PubMed DOI PMC

Coate, J. E. & Doyle, J. J. Variation in transcriptome size: are we getting the message? PubMed DOI

Yoo, M.-J., Szadkowski, E. & Wendel, J. F. Homoeolog expression bias and expression level dominance in allopolyploid cotton. PubMed DOI PMC

Combes, M.-C. et al. Regulatory divergence between parental alleles determines gene expression patterns in hybrids. PubMed DOI PMC

Bell, G. D. M., Kane, N. C., Rieseberg, L. H. & Adams, K. L. RNA-seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. PubMed DOI PMC

Ren, L. et al. Determination of dosage compensation and comparison of gene expression in a triploid hybrid fish. PubMed DOI PMC

Zhang, X., Fang, B. & Huang, Y.-F. Transcription factor binding sites are frequently under accelerated evolution in primates. PubMed DOI PMC

Wunderlich, Z. & Mirny, L. A. Spatial effects on the speed and reliability of protein-DNA search. PubMed DOI PMC

Stoof, R., Wood, A. & Goñi-Moreno, Á. A model for the spatiotemporal design of gene regulatory circuits †. PubMed DOI

Bottani, S. & Veitia, R. A. Hill function-based models of transcriptional switches: impact of specific, nonspecific, functional and nonfunctional binding. PubMed DOI

Tsong, A. E., Tuch, B. B., Li, H. & Johnson, A. D. Evolution of alternative transcriptional circuits with identical logic. PubMed DOI

Metzger, B. P. H., Wittkopp, P. J. & Coolon Joseph. D. Evolutionary dynamics of regulatory changes underlying gene expression divergence among saccharomyces species. PubMed DOI PMC

Wickham, H.