Evolution of dominance in gene expression pattern associated with phenotypic robustness
Abstract Background Mendelian inheritance is a fundamental law of genetics. When we consider two genomes in a diploid cell, a heterozygote’s phenotype is dominated by a particular homozygote according to the law of dominance. Classical Mendelian dominance is concerned with which proteins are dominan...
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| Format: | Article |
| Language: | English |
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BMC
2021-06-01
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| Series: | BMC Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12862-021-01841-6 |
| _version_ | 1819134321369284608 |
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| author | Kenji Okubo Kunihiko Kaneko |
| author_facet | Kenji Okubo Kunihiko Kaneko |
| author_sort | Kenji Okubo |
| collection | DOAJ |
| description | Abstract Background Mendelian inheritance is a fundamental law of genetics. When we consider two genomes in a diploid cell, a heterozygote’s phenotype is dominated by a particular homozygote according to the law of dominance. Classical Mendelian dominance is concerned with which proteins are dominant, and is usually based on simple genotype–phenotype relationship in which one gene regulates one phenotype. However, in reality, some interactions between genes can exist, resulting in deviations from Mendelian dominance. Whether and how Mendelian dominance is generalized to the phenotypes of gene expression determined by gene regulatory networks (GRNs) remains elusive. Results Here, by using the numerical evolution of diploid GRNs, we discuss whether the dominance of phenotype evolves beyond the classical Mendelian case of one-to-one genotype–phenotype relationship. We examine whether complex genotype–phenotype relationship can achieve Mendelian dominance at the expression level by a pair of haplotypes through the evolution of the GRN with interacting genes. This dominance is defined via a pair of haplotypes that differ from each other but have a common phenotype given by the expression of target genes. We numerically evolve the GRN model for a diploid case, in which two GRN matrices are added to give gene expression dynamics and simulate evolution with meiosis and recombination. Our results reveal that group Mendelian dominance evolves even under complex genotype–phenotype relationship. Calculating the degree of dominance shows that it increases through the evolution, correlating closely with the decrease in phenotypic fluctuations and the increase in robustness to initial noise. We also demonstrate that the dominance of gene expression patterns evolves concurrently. This evolution of group Mendelian dominance and pattern dominance is associated with phenotypic robustness against meiosis-induced genome mixing, whereas sexual recombination arising from the mixing of genomes from the parents further enhances dominance and robustness. Due to this dominance, the robustness to genetic differences increases, while optimal fitness is sustained to a significant difference between the two genomes. Conclusion Group Mendelian dominance and gene-expression pattern dominance are achieved associated with the increase in phenotypic robustness to noise. |
| first_indexed | 2024-12-22T10:01:20Z |
| format | Article |
| id | doaj.art-7e8c830adea44d1da9f46d105724340d |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-12-22T10:01:20Z |
| publishDate | 2021-06-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj.art-7e8c830adea44d1da9f46d105724340d2022-12-21T18:30:07ZengBMCBMC Ecology and Evolution2730-71822021-06-0121111410.1186/s12862-021-01841-6Evolution of dominance in gene expression pattern associated with phenotypic robustnessKenji Okubo0Kunihiko Kaneko1Department of Basic Science, Graduate School of Arts and Sciences, University of TokyoDepartment of Basic Science, Graduate School of Arts and Sciences, University of TokyoAbstract Background Mendelian inheritance is a fundamental law of genetics. When we consider two genomes in a diploid cell, a heterozygote’s phenotype is dominated by a particular homozygote according to the law of dominance. Classical Mendelian dominance is concerned with which proteins are dominant, and is usually based on simple genotype–phenotype relationship in which one gene regulates one phenotype. However, in reality, some interactions between genes can exist, resulting in deviations from Mendelian dominance. Whether and how Mendelian dominance is generalized to the phenotypes of gene expression determined by gene regulatory networks (GRNs) remains elusive. Results Here, by using the numerical evolution of diploid GRNs, we discuss whether the dominance of phenotype evolves beyond the classical Mendelian case of one-to-one genotype–phenotype relationship. We examine whether complex genotype–phenotype relationship can achieve Mendelian dominance at the expression level by a pair of haplotypes through the evolution of the GRN with interacting genes. This dominance is defined via a pair of haplotypes that differ from each other but have a common phenotype given by the expression of target genes. We numerically evolve the GRN model for a diploid case, in which two GRN matrices are added to give gene expression dynamics and simulate evolution with meiosis and recombination. Our results reveal that group Mendelian dominance evolves even under complex genotype–phenotype relationship. Calculating the degree of dominance shows that it increases through the evolution, correlating closely with the decrease in phenotypic fluctuations and the increase in robustness to initial noise. We also demonstrate that the dominance of gene expression patterns evolves concurrently. This evolution of group Mendelian dominance and pattern dominance is associated with phenotypic robustness against meiosis-induced genome mixing, whereas sexual recombination arising from the mixing of genomes from the parents further enhances dominance and robustness. Due to this dominance, the robustness to genetic differences increases, while optimal fitness is sustained to a significant difference between the two genomes. Conclusion Group Mendelian dominance and gene-expression pattern dominance are achieved associated with the increase in phenotypic robustness to noise.https://doi.org/10.1186/s12862-021-01841-6Mendelian dominanceGene regulatory networkRobustnessDiploidEvolutionTheoretical model |
| spellingShingle | Kenji Okubo Kunihiko Kaneko Evolution of dominance in gene expression pattern associated with phenotypic robustness BMC Ecology and Evolution Mendelian dominance Gene regulatory network Robustness Diploid Evolution Theoretical model |
| title | Evolution of dominance in gene expression pattern associated with phenotypic robustness |
| title_full | Evolution of dominance in gene expression pattern associated with phenotypic robustness |
| title_fullStr | Evolution of dominance in gene expression pattern associated with phenotypic robustness |
| title_full_unstemmed | Evolution of dominance in gene expression pattern associated with phenotypic robustness |
| title_short | Evolution of dominance in gene expression pattern associated with phenotypic robustness |
| title_sort | evolution of dominance in gene expression pattern associated with phenotypic robustness |
| topic | Mendelian dominance Gene regulatory network Robustness Diploid Evolution Theoretical model |
| url | https://doi.org/10.1186/s12862-021-01841-6 |
| work_keys_str_mv | AT kenjiokubo evolutionofdominanceingeneexpressionpatternassociatedwithphenotypicrobustness AT kunihikokaneko evolutionofdominanceingeneexpressionpatternassociatedwithphenotypicrobustness |