Dynamics of Hybrid Incompatibility in Gene Networks in a Constant Environment

Palmer, Michael E.; Feldman, Marcus W.

doi:10.1111/j.1558-5646.2008.00577.x

Cited by 59 publications

(74 citation statements)

References 52 publications

(63 reference statements)

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“…For example, Barton's model assumes that adaptation occurred entirely from new mutations of which an infinite variety is available. Yet, the number of advantageous mutations for a given trait may be restricted, with the result that the same mutations occur and fix repeatedly under parallel selection (39,40), preventing divergence. The same is expected if populations adapt from the same standing genetic variation (41,42) and if there is gene flow between separate populations evolving under parallel selection (43).…”

Section: Divergent Selection and Postzygotic Isolationmentioning

confidence: 99%

Genetics and ecological speciation

Schluter

Conte

2009

Proc. Natl. Acad. Sci. U.S.A.

534

601

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Species originate frequently by natural selection. A general mechanism by which this occurs is ecological speciation, defined as the evolution of reproductive isolation between populations as a result of ecologically-based divergent natural selection. The alternative mechanism is mutation-order speciation in which populations fix different mutations as they adapt to similar selection pressures. Although numerous cases now indicate the importance of ecological speciation in nature, very little is known about the genetics of the process. Here, we summarize the genetics of premating and postzygotic isolation and the role of standing genetic variation in ecological speciation. We discuss the role of selection from standing genetic variation in threespine stickleback (Gasterosteus aculeatus), a complex of species whose ancestral marine form repeatedly colonized and adapted to freshwater environments. We propose that ecological speciation has occurred multiple times in parallel in this group via a ''transporter'' process in which selection in freshwater environments repeatedly acts on standing genetic variation that is maintained in marine populations by export of freshwater-adapted alleles from elsewhere in the range. Selection from standing genetic variation is likely to play a large role in ecological speciation, which may partly account for its rapidity.reproductive isolation ͉ stickleback ͉ standing genetic variation ͉ transporter hypothesis O ne of Darwin's greatest ideas was that new species originate by natural selection (1). It has taken evolutionary biologists almost until now to realize that he was probably correct. Darwin looked at species mainly as sets of individuals closely resembling each other (1), in which case adaptive divergence in phenotype eventually leads to speciation almost by definition. Later, Dobzhansky (2) and Mayr (3) defined species and speciation by the criterion of reproductive isolation instead. Recent evidence indicates that reproductive isolation also evolves frequently by natural selection (4-7).Speciation by natural selection occurs by 2 general mechanisms (4, 7). The first of these is ecological speciation, defined as the evolution of reproductive isolation between populations, or subsets of a single population, as a result of ecologically-based divergent natural selection (6,(8)(9)(10). Under this process natural selection acts in contrasting directions between environments, which drives the fixation of different alleles each advantageous in one environment but not in the other (Fig. 1). In contrast, under mutation-order speciation (7, 11), populations diverge as they accumulate a different series of mutations under similar selection pressures (Fig. 1). Natural selection drives alleles to fixation in both speciation mechanisms, but selection favors divergence only under ecological speciation. Divergence occurs by chance under the mutation-order process.There is growing evidence in support of both ecological and mutation-order speciation in nature (4, 7), yet numerous aspects of ...

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Section: Divergent Selection and Postzygotic Isolationmentioning

confidence: 99%

Genetics and ecological speciation

Schluter

Conte

2009

Proc. Natl. Acad. Sci. U.S.A.

534

601

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“…In addition to diversification of cis-regulatory regions (Wray 2007), evidence that affects affinity for DNA binding sites is emerging from comparisons within and among TF gene families of sequence evolution (Jovelin 2009;Nakagawa et al 2013). Because phenotypic divergence often occurs under selection (Schluter 2009;Sobel et al 2010), it is influenced by the adaptive landscape of the genes involved, including how those genes interact to produce the phenotype (Hansen and Wagner 2001;Gavrilets 2004;Palmer and Feldman 2009). The outcomes of those interactions, at the molecular level, are determined in turn by their local bioenergetic milieu.…”

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confidence: 99%

“…Under directional selection, a steeper slope near the derived parental phenotype resulted in higher median HI because fewer incompatible positions are needed to produce a given level of misregulation in the hybrid (Figure 3). Likewise, if parent populations evolved toward a highly robust TF-binding site interaction, the result was less HI, because the interaction is also robust to incompatibilities in the hybrid.The observation that hybrid misregulation occurs in conserved traits (True and Haag 2001) suggests that HI is possible under stabilizing selection (see also Palmer and Feldman 2009;Fierst and Hansen 2010), although it may be less likely (Gavrilets 2004;Schluter 2009). Under stabilizing selection, we found that the amount of HI was determined primarily by the slopes of the G-P map and fitness landscape near the conserved phenotype and by population size (Figure 3).…”

mentioning

confidence: 99%

“…This is because divergence of parental genotypes under stabilizing selection depends on compensatory evolution, which is less likely to occur when the average fitness effect of a mutation is high; such mutations are eliminated by selection before a compensatory mutation can arise (Haag 2007;Fierst and Hansen 2010). Low population size reduces the efficiency of selection (Wright 1931), increasing the parameter range under which compensatory evolution can occur (Lynch 2007).Dependence of compensatory evolution on the shape of the fitness landscape is also found in multilocus models where the shape is determined by the strength of epistasis among loci (Palmer and Feldman 2009;Fierst and Hansen 2010). In general, a flatter plateau of near neutrality around a conserved phenotype is expected to increase divergence at the underlying loci (Haag 2007;Palmer and Feldman 2009), which produced HI in our results if the hybrid genotype fell outside of the nearly neutral plateau.…”

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Hybrid Incompatibility Arises in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

et al. 2014

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Postzygotic isolation between incipient species results from the accumulation of incompatibilities that arise as a consequence of genetic divergence. When phenotypes are determined by regulatory interactions, hybrid incompatibility can evolve even as a consequence of parallel adaptation in parental populations because interacting genes can produce the same phenotype through incompatible allelic combinations. We explore the evolutionary conditions that promote and constrain hybrid incompatibility in regulatory networks using a bioenergetic model (combining thermodynamics and kinetics) of transcriptional regulation, considering the bioenergetic basis of molecular interactions between transcription factors (TFs) and their binding sites. The bioenergetic parameters consider the free energy of formation of the bond between the TF and its binding site and the availability of TFs in the intracellular environment. Together these determine fractional occupancy of the TF on the promoter site, the degree of subsequent gene expression and in diploids, and the degree of dominance among allelic interactions. This results in a sigmoid genotype-phenotype map and fitness landscape, with the details of the shape determining the degree of bioenergetic evolutionary constraint on hybrid incompatibility. Using individual-based simulations, we subjected two allopatric populations to parallel directional or stabilizing selection. Misregulation of hybrid gene expression occurred under either type of selection, although it evolved faster under directional selection. Under directional selection, the extent of hybrid incompatibility increased with the slope of the genotype-phenotype map near the derived parental expression level. Under stabilizing selection, hybrid incompatibility arose from compensatory mutations and was greater when the bioenergetic properties of the interaction caused the space of nearly neutral genotypes around the stable expression level to be wide. F 2 's showed higher hybrid incompatibility than F 1 's to the extent that the bioenergetic properties favored dominant regulatory interactions. The present model is a mechanistically explicit case of the Bateson-Dobzhansky-Muller model, connecting environmental selective pressure to hybrid incompatibility through the molecular mechanism of regulatory divergence. The bioenergetic parameters that determine expression represent measurable properties of transcriptional regulation, providing a predictive framework for empirical studies of how phenotypic evolution results in epistatic incompatibility at the molecular level in hybrids. P OSTZYGOTIC hybrid incompatibility (HI), an important component of reproductive isolation (Coyne and Orr 2004), is usually not due to failure of a single gene, but arises from incompatibilities between interacting genes, as described by the Bateson-Dobzhansky-Muller (BDM) model (Bateson 1909;Dobzhansky 1937;Muller 1942). Recent studies of the genes underlying HI show that this BDM model is well supported and that some form of selection p...

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“…Interpopulation divergence in regulatory interactions may be expected to result in hybrid incompatibility due to misregulation of the traits they control Porter 2000, 2001;Landry et al 2007;Ortíz-Barrientos et al 2007;Barbash 2011, 2012). Theoretical studies Porter 2000, 2007;Palmer and Feldman 2009) of the molecular basis of evolving regulatory interactions demonstrate that misregulation in hybrids readily arises as a byproduct of adaptation. Tulchinsky et al (2014) show that the degree of this hybrid incompatibility is determined in large part by the bioenergetic [thermodynamic plus kinetic (Morowitz 1978)] details of the molecular interactions between coevolving transcription factors and the sites to which they bind.…”

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confidence: 99%

Hybrid Incompatibility Despite Pleiotropic Constraint in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

2014

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Hybrid incompatibility can result from gene misregulation produced by divergence in trans-acting regulatory factors and their cis-regulatory targets. However, change in trans-acting factors may be constrained by pleiotropy, which would in turn limit the evolution of incompatibility. We employed a mechanistically explicit bioenergetic model of gene expression wherein parameter combinations (number of transcription factor molecules, energetic properties of binding to the regulatory site, and genomic background size) determine the shape of the genotype-phenotype (G-P) map, and interacting allelic variants of mutable cis and trans sites determine the phenotype along that map. Misregulation occurs when the phenotype differs from its optimal value. We simulated a pleiotropic regulatory pathway involving a positively selected and a conserved trait regulated by a shared transcription factor (TF), with two populations evolving in parallel. Pleiotropic constraints shifted evolution in the positively selected trait to its cis-regulatory locus. We nevertheless found that the TF genotypes often evolved, accompanied by compensatory evolution in the conserved trait, and both traits contributed to hybrid misregulation. Compensatory evolution resulted in "developmental system drift," whereby the regulatory basis of the conserved phenotype changed although the phenotype itself did not. Pleiotropic constraints became stronger and in some cases prohibitive when the bioenergetic properties of the molecular interaction produced a G-P map that was too steep. Likewise, compensatory evolution slowed and hybrid misregulation was not evident when the G-P map was too shallow. A broad pleiotropic "sweet spot" nevertheless existed where evolutionary constraints were moderate to weak, permitting substantial hybrid misregulation in both traits. None of these pleiotropic constraints manifested when the TF contained nonrecombining domains independently regulating the respective traits.A DAPTIVE changes in phenotype often occur through changes in gene regulation (Wray 2007;Carroll 2008). Regulatory networks map an organism's genotype to its phenotype through developmental and physiological processes (Wilkins 2002). Such networks consist of interacting loci that can respond to selection by changing the expression levels of individual genes in space and time. In addition to gene interaction (epistasis) (Phillips 2008), gene networks are also characterized by pleiotropy, where single genetic loci have manifold effects (Gibson 1996;Paaby and Rockman 2013).Gene interactions are pervasive in the evolution of hybrid incompatibility, an important form of reproductive isolation between species (Coyne and Orr 2004). The leading model for the evolution of hybrid incompatibility, the BatesonDobzhansky-Muller (BDM) model, requires interactions between at least two genetic loci (Bateson 1909;Dobzhansky 1937;Muller 1942). Interpopulation divergence in regulatory interactions may be expected to result in hybrid incompatibility due to misregulation of th...

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Dynamics of Hybrid Incompatibility in Gene Networks in a Constant Environment

Cited by 59 publications

References 52 publications

Genetics and ecological speciation

Genetics and ecological speciation

Hybrid Incompatibility Arises in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

Hybrid Incompatibility Despite Pleiotropic Constraint in a Sequence-Based Bioenergetic Model of Transcription Factor Binding

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