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Creation of synthetic A. suecica allotetraploids and backcross progeny. A. thaliana is typically diploid, with a haploid complement of five chromosomes. C. arenosa is a natural tetraploid with a haploid complement of eight chromosomes. Tetraploid A. thaliana was used as the maternal parent in a cross with C. arenosa, yielding SAS plants. SAS F2 progeny were obtained from self-pollinated flowers. Alternatively, flowers were emasculated and manually pollinated with tetraploid A. thaliana or C. arenosa pollen. Thus progeny with 3:1, 2:2 (F2), or 1:3 A. thaliana to C. arenosa genome complements were obtained from the same mother plant.
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Nucleolar dominance is an epigenetic phenomenon in which one parental set of ribosomal RNA (rRNA) genes is silenced in an interspecific hybrid. In natural Arabidopsis suecica, an allotetraploid (amphidiploid) hybrid of Arabidopsis thaliana and Cardaminopsis arenosa, the A. thaliana rRNA genes are repressed. Interestingly, A. thaliana rRNA gene sile...
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... races tested are tetraploid (L.C. et al., unpublished work), most likely autotet- raploids, because only one type of rRNA gene was detected on sequencing multiple PCR clones (Z.J.C., unpublished work). Autotetraploid A. thaliana were generated by colchicine treat- ment and crossed with C. arenosa to recreate synthetic allotet- raploid A. suecica (Fig. 2). Four self-fertile SAS plants were obtained, designated SAS-1 through SAS-4. C. arenosa tran- scripts were detected in all SAS plants (Fig. 3, lanes 5, 6, 11, 12) at levels similar to the C. arenosa control (lane 7). In contrast, expression of A. thaliana rRNA genes was variable. In SAS-2 and SAS-4, only trace amounts of A. thaliana ...
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... using C. arenosa- (lanes 1-7) or A. thaliana-specific (lanes 8-14) S1 probes. (B) F2 progeny of SAS-2 were analyzed in the same way. effects on nucleolar dominance, SAS plants were backcrossed to C. arenosa or tetraploid A. thaliana. In five siblings derived from SAS-2 backcrossed to A. thaliana, A. thaliana transcripts were detected at levels (Fig. 5A, lanes 2-6, top autoradiogram) comparable to the A. thaliana control (lane 1, top), whereas in five siblings from a backcross to C. arenosa, A. thaliana transcripts were not detected (lanes 7-11, top; the weak signal in lane 7 does not correspond to the A. thaliana start site and was because of incomplete probe digestion). Examination of C. arenosa rRNA gene ...
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... of C. arenosa rRNA gene expression in the SAS-2 A. thaliana backcross progeny yielded interesting results (Fig. 5A, bottom left autoradiogram). Only trace amounts of C. arenosa tran- scripts were detected in sibs a and d (lanes 2 and 5). C. arenosa transcripts were detected at low levels in sibs c and e (lanes 4 and 6). ...
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... cytosine methylation (with aza-dC) or histone deacetylation (with trichostatin A or so- dium butyrate) derepressed silenced rRNA genes subjected to nucleolar dominance (33). In agreement with these results, A. thaliana rRNA transcripts were induced to 40% or 100% of control levels in natural A. suecica plants germinated on media containing aza-dC (Fig. 7, compare lanes 4 and 5 to lane 2). C. arenosa transcripts were also up-regulated 2-to 3-fold at the highest level of aza-dC (compare lane 8 to lanes 1 and 6). These results do not provide mechanistic insights beyond our previ- ous study but confirm that A. thaliana genes in A. suecica are not defective, but are ...
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... However, other studies documented caveats in the particular hypotheses (e.g. Chen et al., 1998;Chandrasekhara et al., 2016), suggesting that neither of the hypotheses is generally applicable. In particular, evidence from studies on Arabidopsis indicates that ND is enforced independently of both transcription factor availability and binding affinity (Chen et al., 1998). ...
... Chen et al., 1998;Chandrasekhara et al., 2016), suggesting that neither of the hypotheses is generally applicable. In particular, evidence from studies on Arabidopsis indicates that ND is enforced independently of both transcription factor availability and binding affinity (Chen et al., 1998). In F 1 hybrids, silencing of alleles from the submissive genome is highly variable, with two generations needed to establish ND in some lines. ...
... One may speculate that ND of the Lolium genome is conditioned by the prevalence of Lolium-type rDNA loci (dosage effect, Chen et al., 1998). Indeed, none of the genotypes showed an equal number of rDNA loci or a prevalence of Festuca-type loci. ...
Genome or genomic dominance (GD) is a phenomenon observed in hybrids when one parental genome becomes dominant over the other. It is manifested by the replacement of chromatin of the submissive genome by that of the dominant genome and by biased gene expression. Nucleolar dominance (ND) – the functional expression of only one parental set of ribosomal genes in hybrids – is another example of an intragenomic competitive process which, however, concerns ribosomal DNA only. Although GD and ND are relatively well understood, the nature and extent of their potential interdependence is mostly unknown. Here, we ask whether hybrids showing GD also exhibit ND and, if so, whether the dominant genome is the same. To test this, we used hybrids between Festuca and Lolium grasses (Festulolium), and between two Festuca species in which GD has been observed (with Lolium as the dominant genome in Festulolium and F. pratensis in interspecific Festuca hybrids). Using amplicon sequencing of ITS1 and ITS2 of the 45S ribosomal DNA (rDNA) cluster and molecular cytogenetics, we studied the organization and expression of rDNA in leaf tissue in five hybrid combinations, four generations and 31 genotypes [F. pratensis × L. multiflorum (F1, F2, F3, BC1), L. multiflorum × F. pratensis (F1), L. multiflorum × F. glaucescens (F2), L. perenne × F. pratensis (F1), F. glaucescens × F. pratensis (F1)]. We have found that instant ND occurs in Festulolium, where expression of Lolium-type rDNA reached nearly 100% in all F1 hybrids and was maintained through subsequent generations. Therefore, ND and GD in Festulolium are manifested by the same dominant genome (Lolium). We also confirmed the concordance between GD and ND in an interspecific cross between two Festuca species.
... In analysis of 400 and 350 proteins with homoeolog-specific expression in A. suecica and Allo738, respectively, we did not observe any significant differences in aggregation propensity of the homoeologs. This result is consistent with overall balanced expression among subgenomes (Jiang et al., 2021), despite expression bias can occur to rRNA genes and other proteincoding genes due to epigenetic changes (Chen et al., 1998;Lee and Chen, 2001). ...
Hybrid vigor or heterosis has been widely applied in agriculture and extensively studied using genetic and gene expression approaches. However, the biochemical mechanism underlying heterosis remains elusive. One theory suggests that a decrease in protein aggregation may occur in hybrids due to the presence of protein variants between parental alleles, but it has not been experimentally tested. Here, we report comparative analysis of soluble and insoluble proteomes in Arabidopsis intraspecific and interspecific hybrids or allotetraploids formed between A. thaliana and A. arenosa. Both allotetraploids and intraspecific hybrids displayed nonadditive expression (unequal to the sum of the two parents) of the proteins, most of which were involved in biotic and abiotic stress responses. In the allotetraploids, homoeolog-expression bias was not observed among all proteins examined but accounted for 17-20% of the nonadditively expressed proteins, consistent with the transcriptome results. Among expression-biased homoeologs, there were more A. thaliana-biased than A. arenosa-biased homoeologs. Analysis of the insoluble and soluble proteomes revealed more soluble proteins in the hybrids than their parents but not in the allotetraploids. Most proteins in ribosomal biosynthesis and in the thylakoid lumen, membrane, and stroma were in the soluble fractions, indicating a role of protein stability in photosynthetic activities for promoting growth. Thus, nonadditive expression of stress-responsive proteins and increased solubility of photosynthetic proteins may contribute to heterosis in Arabidopsis hybrids and allotetraploids and possibly hybrid crops.
... The genus Arabidopsis has been widely used for studying evolutionary questions (Koenig and Weigel, 2015;Koch, 2019) including the effects of interspecific hybridization in controlled crossings (Chen et al., 1998;Comai et al., 2000;Nasrallah et al., 2000;Josefsson et al., 2006;Walia et al., 2009;Burkart-Waco et al., 2012;Burkart-Waco et al., 2013;Burkart-Waco et al., 2015;Bjerkan et al., 2020). When diploid A. thaliana is crossed to diploid A. arenosa, the endosperm shows late cellularization and high degree of seed abortion (Josefsson et al., 2006;Bjerkan et al., 2020). ...
Speciation involves reproductive isolation, which can occur by hybridization barriers acting in the endosperm of the developing seed. The nuclear endosperm is a nutrient sink, accumulating sugars from surrounding tissues, and undergoes coordinated cellularization, switching to serve as a nutrient source for the developing embryo. Tight regulation of cellularization is therefore vital for seed and embryonic development. Here we show that hybrid seeds from crosses between Arabidopsis thaliana as maternal contributor and A. arenosa or A. lyrata as pollen donors result in an endosperm based post-zygotic hybridization barrier that gives rise to a reduced seed germination rate. Hybrid seeds display opposite endosperm cellularization phenotypes, with late cellularization in crosses with A. arenosa and early cellularization in crosses with A. lyrata. Stage specific endosperm reporters display temporally ectopic expression in developing hybrid endosperm, in accordance with the early and late cellularization phenotypes, confirming a disturbance of the source-sink endosperm phase change. We demonstrate that the hybrid barrier is under the influence of abiotic factors, and show that a temperature gradient leads to diametrically opposed cellularization phenotype responses in hybrid endosperm with A. arenosa or A. lyrata as pollen donors. Furthermore, different A. thaliana accession genotypes also enhance or diminish seed viability in the two hybrid cross-types, emphasizing that both genetic and environmental cues control the hybridization barrier. We have identified an A. thaliana MADS-BOX type I family single locus that is required for diametrically opposed cellularization phenotype responses in hybrid endosperm. Loss of AGAMOUS-LIKE 35 significantly affects the germination rate of hybrid seeds in opposite directions when transmitted through the A. thaliana endosperm, and is suggested to be a locus that promotes cellularization as part of an endosperm based mechanism involved in post-zygotic hybrid barriers. The role of temperature in hybrid speciation and the identification of distinct loci in control of hybrid failure have great potential to aid the introduction of advantageous traits in breeding research and to support models to predict hybrid admixture in a changing global climate.
... Factors such as the copy number of rRNA genes, the length of intergenic spacer (IGS) regions, and the affinity of IGS binding to transcription factors may affect transcription of rRNA genes (Dammann et al., 1995;Guo & Han, 2014;Jones & Baylin, 2002;Saez-Vasquez & Pikaard, 1997). The IGS, which may include promoters, CpG dinucleotides, and other sequences that affect gene transcription, can play an important role in gene transcription (Chen et al., 1998;Chen & Pikaard, 1997b). For example, in hexaploid common wheat, the NOR locus on chromosome 1B with low copy number forms larger nucleoli, while the one on chromosome 6B with high copy number forms smaller nucleoli. ...
... This may be due to the longer length of the NOR sequence on chromosome 1B, which contains more repetitive sequences and may be more likely to bind transcription factors and facilitate the transcription of downstream genes (Saez-Vasquez & Pikaard, 1997). However, there are exceptions to this pattern, as NORs with long IGSs are not transcribed preferentially in other species, such as Brassica and Arabidopsis (Chen et al., 1998, Chen & Pikaard, 1997b. Furthermore, ND may also be affected by chromosomal position. ...
... Moreover, while cloning experiments revealed a hierarchy of IGS lengths (Ae. tauschii, DD > G genome, GG > T. monococcum, AA) ( Figure S4b), there was poor correlation between underlying DNA sequence and ND in allopolyploids (Chen et al., 1998;Chen & Pikaard, 1997b). Thus, the complex nature of ND suggests that multiple factors likely contribute to its establishment and maintenance, and further research is needed to fully elucidate these mechanisms. ...
Nucleolar dominance (ND) is a widespread epigenetic phenomenon in hybridizations where nucleolus transcription fails at the nucleolus organizing region (NOR). However, the dynamics of NORs during the formation of Triticum zhukovskyi (GGAu Au Am Am ), another evolutionary branch of allohexaploid wheat, remains poorly understood. Here, we elucidated genetic and epigenetic changes occurring at the NOR loci within the Am , G, and D subgenomes during allopolyploidization by synthesizing hexaploid wheat GGAu Au Am Am and GGAu Au DD. In T. zhukovskyi, Au genome NORs from T. timopheevii (GGAu Au ) were lost, while the second incoming NORs from T. monococcum (Am Am ) were retained. Analysis of the synthesized T. zhukovskyi revealed that rRNA genes from the Am genome were silenced in F1 hybrids (GAu Am ) and remained inactive after genome doubling and subsequent self-pollinations. We observed increased DNA methylation accompanying the inactivation of NORs in the Am genome and found that silencing of NORs in the S1 generation could be reversed by the cytidine methylase inhibitor. Our findings provide insights into the ND process during the evolutionary period of T. zhukovskyi and highlight inactive rDNA units may serve as a "first reserve" in the form of R-loops, contributing to the successful evolution of T. zhukovskyi.
... DNA methylation pattern changes have some epigenetic effects. A series of studies in polyploid plants, such as Brassica [29], wheat [14], Arabidopsis [13,30,31], triticale and rice [32] have demonstrated this. The results of these studies have suggested that DNA methylation could activate mobile elements and silence redundant genes, leading to epigenetic phenomena including nucleolar dominance and dosage compen- Table S1. ...
Hybridization and polyploidization may lead to divergence in adaptation and boost speciation in angiosperms and some lower animals. Epigenetic change plays a significant role in the formation and adaptation of polyploidy. Studies of the effects of methylation on genomic recombination and gene expression in allopolyploid plants have achieved good progress. However, relevant advances in polyploid animals have been relatively slower. In the present study, we used the bisexual, fertile, genetically stable allotetraploid generated by hybridization of Carassius auratus red var. and Cyprinus carpio L. to investigate cytosine methylation level using methylation-sensitive amplification polymorphism (MSAP) analysis. We observed 38.31% of the methylation changes in the allotetraploid compared with the parents at 355 randomly selected CCGG sites. In terms of methylation status, these results indicate that the level of methylation modification in the allotetraploid may have increased relative to that in the parents. We also found that the major methylation changes were hypermethylation on some genomic fragments and genes related to metabolism or cell cycle regulation. These results provide circumstantial evidence that DNA methylation might be related to the gene expression and phenotype variation in allotetraploid hybrids. Our study partly fulfils the need for epigenetic research in polyploid animals, and provides evidence for the epigenetic regulation of allopolyploids. Citation: Xiao J, Song C, Liu S, Tao M, Hu J, et al. (2013) DNA Methylation Analysis of Allotetraploid Hybrids of Red Crucian Carp (Carassius auratus red var.) and Common Carp (Cyprinus carpio L.). PLoS ONE 8(2): e56409.
... In both groups of angiosperms, ND is driven and maintained through epigenetic mechanisms [5,[7][8][9]42]. Early experiments using cytosine methyltransferase (5-azacytidine; 5-azadeoxycytidine) and histone deacetylase (sodium butyrate; trichostatin A) inhibitors reactivated underdominant 35S rRNA genes in some dicots [5,10,43] and monocots [9,31,44]. Indeed, the differential DNA methylation status of active and silenced ancestral rDNA sets has been documented in many allopolyploids, including the allotetraploid grass B. hybridum, in which the silenced 35S rDNA loci of the S-subgenome have significantly higher DNA methylation levels than those of the D-subgenome ( Figure 2) [45]. ...
... Thus, at least in the case of Brassica allopolyploids, it seems that interspecific hybridisation itself is sufficient to induce epigenetic repatterning of the C-subgenome rDNA set and, consequently, triggers uniparental silencing [46]. In newly formed A. suecica F1 hybrids, the silencing of A. thalianaoriginated rDNA was variable, with two generations needed to establish stable ND in some lines [43]. By contrast, in resynthesised wheat, allopolyploidisation constitutes a critical step for the silencing trigger [7]. ...
... Because ND seems to occur independently of paternal or maternal effects [3,11] and is established either during embryogenesis [53] or early after embryogenesis [51], ancestral rDNA imprinting in the gametes does not appear to be involved. In both dicots and monocots, it is usually the same parental rDNA set chosen for inactivation, implying that ND is not random yet may be dosage dependent, as was shown in Arabidopsis allopolyploids [43]. Also, there seems to be no simple relationship between the number of rDNA units within a locus and the direction of ND, because NORs with fewer genes can be dominant over those with more rRNA genes, as was shown in bread wheat [30,56] and Brassica allopolyploids [3]. ...
Nucleolar dominance (ND) is selective epigenetic silencing of 35-48S rDNA loci. In allopolyploids, it is frequently manifested at the cytogenetic level by the inactivation of nucleolar organiser region(s) (NORs) inherited from one or several evolutionary ancestors. Grasses are ecologically and economically one of the most important land plant groups, which have frequently evolved through hybridisation and polyploidisation events. Here we review common and unique features of ND phenomena in this monocot family from cytogenetic, molecular, and genomic perspectives. We highlight recent advances achieved by using an allotetraploid model grass, Brachypodium hybridum, where ND commonly occurs at a population level, and we cover modern genomic approaches that decipher structural features of core arrays of NORs.
... This chromosomal region was not lost in hybrids but could be reactivated to produce normal nucleoli in hybrids with a different crossing partner. Experiments with epigenetic inhibitors performed in plants towards the end of the last century established that histone deacetylation and DNA methylation pathways interact in a self-reinforcing mechanism, maintaining silencing of partner rDNA units in hybrids (Chen and Pikaard, 1997a;Chen et al., 1988). The VH and AK groups investigated nucleolar dominance from different perspectives, asking questions about the influence of structural features of the 35S IGS, cytosine methylation of rDNA units and developmental stability of nucleolar dominance. ...
The history of rDNA research started almost 90 years ago when the geneticist, Barbara McClintock observed that in interphase nuclei of maize the nucleolus was formed in association with a specific region normally located near the end of a chromosome, which she called the nucleolar organizer region (NOR). Cytologists in the twentieth century recognized the nucleolus as a common structure in all eukaryotic cells, using both light and electron microscopy and biochemical and genetic studies identified ribosomes as the subcellular sites of protein synthesis. In the mid- to late 1960s, the synthesis of nuclear-encoded rRNA was the only system in multicellular organisms where transcripts of known function could be isolated, and their synthesis and processing could be studied. Cytogenetic observations of NOR regions with altered structure in plant interspecific hybrids and detailed knowledge of structure and function of rDNA were prerequisites for studies of nucleolar dominance, epistatic interactions of rDNA loci, and epigenetic silencing. In this article, we focus on the early rDNA research in plants, performed mainly at the dawn of molecular biology in the 60 to 80-ties of the last century which presented a prequel to the modern genomic era. We discuss – from a personal view – the topics such as synthesis of rRNA precursor (35S pre-rRNA in plants), processing, and the organization of 35S and 5S rDNA. Cloning and sequencing led to the observation that the transcribed and processed regions of the rRNA genes vary enormously, even between populations and species, in comparison with the more conserved regions coding for the mature rRNAs. Epigenetic phenomena and the impact of hybridization and allopolyploidy on rDNA expression and homogenization are discussed. This historical view of scientific progress and achievements sets the scene for the other articles highlighting the immense progress in rDNA research published in this special issue of Frontiers in Plant Science on “Molecular organization, evolution, and function of ribosomal DNA.”
... AaROS1-1 expression level was low in all lines tested. This type of allelic expression variation was also observed for CCA1 and FLC homologous loci in allotetraploids 20,59 , which may be controlled by a mechanism similar to nucleolar dominance 19,60 . Consistent with feedback regulation of ROS1 expression by RdDM pathway 58 , expression of several RdDM pathway genes examined was upregulated in A. suecica and neo-allotetraploids (Extended Data Fig. 8a), while CHH methylation levels were higher in the F 1 , Allo733 and Allo738 than in A. thaliana or A. arenosa (Extended Data Fig. 6a,b and Extended Data Fig. 8b). ...
... Alternatively, homologous chromosomes from closely related progenitors may pair as in Tragopogon 10 . In A. suecica, sT and sA subgenomes are divergent enough to prevent homologous exchanges and subject to convergent and concerted changes in DNA methylation and gene expression including silencing of uniparental ribosomal DNA (rDNA) loci epigenetically via nucleolar dominance 19,60 . With advanced sequencing and epigenomic technologies, this paradox of rapid genomic reshuffling and genomic stability will be addressed to illuminate our understanding of polyploid genome evolution and to empower our efforts on editing genes and modifying epigenetic landscapes for crop improvement. ...
During evolution successful allopolyploids must overcome ‘genome shock’ between hybridizing species but the underlying process remains elusive. Here, we report concerted genomic and epigenomic changes in resynthesized and natural Arabidopsis suecica (TTAA) allotetraploids derived from A rabidopsis thaliana (TT) and A rabidopsis arenosa (AA). A. suecica shows conserved gene synteny and content with more gene family gain and loss in the A and T subgenomes than respective progenitors, although A. arenosa -derived subgenome has more structural variation and transposon distributions than A. thaliana -derived subgenome. These balanced genomic variations are accompanied by pervasive convergent and concerted changes in DNA methylation and gene expression among allotetraploids. The A subgenome is hypomethylated rapidly from F 1 to resynthesized allotetraploids and convergently to the T-subgenome level in natural A. suecica , despite many other methylated loci being inherited from F 1 to all allotetraploids. These changes in DNA methylation, including small RNAs, in allotetraploids may affect gene expression and phenotypic variation, including flowering, silencing of self-incompatibility and upregulation of meiosis- and mitosis-related genes. In conclusion, concerted genomic and epigenomic changes may improve stability and adaptation during polyploid evolution.
... In inter-specific hybrids it was previously observed that the rDNA of only one parent tended to be involved in nucleolus formation, a phenomenon known as 'nucleolar dominance' [81][82][83][84] . In A. suecica, it was observed that the rDNA clusters inherited from A. thaliana were silenced [81][82][83][84][85][86][87] , and structural changes associated with these clusters were also suggested 88 . ...
Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of ‘genome shock’, such as genome reorganization and subgenome expression dominance. Here we study polyploidization in Arabidopsis suecica , a post-glacial allopolyploid species formed via hybridization of Arabidopsis thaliana and Arabidopsis arenosa . We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica , and the A. arenosa subgenome shows upregulation of cyto-nuclear processes, possibly in response to the new cytoplasmic environment of A. suecica , with plastids maternally inherited from A. thaliana . These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution.
... In fact, two clusters of rRNA genes exist in A. thaliana, with typically only one being transcribed, and there is variation among A. thaliana accessions in the identity of the cluster that is expressed. Nucleolar dominance was shown to evolve rapidly, with only two generations being necessary for one of the two sets of rRNA genes to become silenced in synthetic A. suecica lines newly obtained by experimental crosses in the laboratory (Chen, Comai & Pikaard, 1998). However, Joly et al. (2004) did not observed such rapid evolution of nucleolar dominance in Glycine hybrids. ...
Dominance is a basic property of inheritance systems describing the link between a diploid genotype at a single locus and the resulting phenotype. Models for the evolution of dominance have long been framed as an opposition between the irreconcilable views of Fisher in 1928 supporting the role of largely elusive dominance modifiers and Wright in 1929, who viewed dominance as an emerging property of the structure of enzymatic pathways. Recent theoretical and empirical advances however suggest that these opposing views can be reconciled, notably using models investigating the regulation of gene expression and developmental processes. In this more comprehensive framework, phenotypic dominance emerges from departures from linearity between any levels of integration in the genotype‐to‐phenotype map. Here, we review how these different models illuminate the emergence and evolution of dominance. We then detail recent empirical studies shedding new light on the diversity of molecular and physiological mechanisms underlying dominance and its evolution. By reconciling population genetics and functional biology, we hope our review will facilitate cross‐talk among research fields in the integrative study of dominance evolution.
