Coadapted genomes and selection on hybrids: Fisher’s geometric model explains a variety of empirical patterns

Simon, Alexis; Bierne, Nicolas; Welch, John J.

doi:10.1101/237925

Cited by 5 publications

(3 citation statements)

References 79 publications

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“…The model we work with describes a continuum of possible systems, parameterized by continuous coefficient matrices. The arguments we make (e.g., Figure 4) are often geometric in nature, and so it would be interesting to ask whether Fisher’s geometric model might provide more quantitative, generalizable predictions, as in for instance Fraïsse et al [2016], Simon et al [2017]. Martin [2014] argued that such an approximation would be often fruitful.…”

Section: Discussionmentioning

confidence: 99%

“…Fisher's geometric model There has been substantial work on models of quadratic stabilizing selection around a single optimum -i.e., Fisher's geometric model [e.g. Simon et al, 2017]. Our model would have this form if viewed only in phenotype space, where there is a single optimum -but differs by explicitly considering evolutionary dynamics of underlying genotype-derived regulatory matrices.…”

Section: Discussionmentioning

confidence: 99%

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System drift and speciation

Schiffman

Ralph

2017

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Even if a species' phenotype does not change over evolutionary time, the underlying mechanism may change, as distinct molecular pathways can realize identical phenotypes. Here we use quantitative genetics and linear system theory to study how a gene network underlying a conserved phenotype evolves, as the genetic drift of small changes to these molecular pathways cause a population to explore the set of mechanisms with identical phenotypes. To do this, we model an organism's internal state as a linear system of differential equations for which the environment provides input and the phenotype is the output, in which context there exists an exact characterization of the set of all mechanisms that give the same input-output relationship. This characterization implies that selectively neutral directions in genotype space should be common and that the evolutionary exploration of these distinct but equivalent mechanisms can lead to the reproductive incompatibility of independently evolving populations. This evolutionary exploration, or system drift, proceeds at a rate proportional to the amount of intrapopulation genetic variation divided by the effective population size (Ne). At biologically reasonable parameter values this process can lead to substantial interpopulation incompatibility, and thus speciation, in fewer than Ne generations. This model also naturally predicts Haldane's rule, thus providing another possible explanation of why heterogametic hybrids tend to be disrupted more often than homogametes during the early stages of speciation.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

System drift and speciation

Schiffman

Ralph

2017

Preprint

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“…Mismatch results from interactions among divergent loci, either via dominance or segregation, and accordingly selection against mismatched trait combinations shares this feature with ‘intrinsic’ incompatibilities. Predictions of genetically-explicit hybrid incompatibility models (Chevin et al, 2014; Simon et al, 2018) can readily be interpreted via lenses of both genetic or phenotypic mismatches, and both types of incompatibilities result in selection against opposite ancestry combinations at incompatible loci. There are some important differences between ‘intrinsic’ and ‘extrinsic’ incompatibilities, however.…”

Section: Discussionmentioning

confidence: 99%

Adaptive divergence and the evolution of hybrid trait mismatch in threespine stickleback

Chhina¹,

Thompson²,

Schluter³

2020

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The fitness of hybrids is a critical determinant of gene flow between hybridizing populations. If hybrid phenotypes change predictably as parental populations become increasingly divergent, this could provide insight into general mechanisms linking ecological divergence with reproductive isolation. In this study, we used threespine stickleback fish (Gasterosteus aculeatus L.) to examine how phenotypic divergence between populations drives the evolution of dominance, phenotypic variation, and trait ‘mismatch’ in hybrids. We generated F1 and F2 hybrids between 12 freshwater populations—which ranged from highly planktivorous to highly benthic-feeding—and an anadromous population that is highly planktivorous and resembles the ancestral state of derived freshwater populations. We measured 16 phenotypic traits in hybrids and pure parental individuals raised under common conditions. We found that dominance varied markedly among traits. By contrast, dominance for a given trait was typically consistent among populations except for two traits where dominance was predicted by the phenotype of the freshwater parent. We find that multivariate phenotypic variation is greater in hybrids between more divergent parents. Finally, we demonstrate that the extent to which parental traits are ‘mismatched’ in both F1 and F2 hybrids increases with the phenotypic distance between the parent populations. Critically, this relationship was clearer in F1 hybrids than in F2s—largely due to traits having different dominance coefficients and F1s having relatively little phenotypic variation. Our results demonstrate that some aspects of hybrid phenotypes evolve predictably as parental populations diverge. We also find evidence for a possible general mechanistic link between ecological divergence and reproductive isolation—that more divergent parent populations tend to produce hybrids with novel and potentially deleterious multivariate phenotypes.

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The divergence history of European blue mussel species reconstructed from Approximate Bayesian Computation: the effects of sequencing techniques and sampling strategies

Fraïssé

Roux

Gagnaire

et al. 2018

Preprint

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Genome-scale diversity data are increasingly available in a variety of biological systems, and can be used to reconstruct the past evolutionary history of species divergence. However, extracting the full demographic information from these data is not trivial and requires inferential methods that account for the diversity of coalescent histories throughout the genome. Here, we evaluate the potential and limitations of one such approach. We reexamine a well-known system of mussel sister species, using the coding joint site frequency spectrum (jSFS), in an approximate Bayesian computation (ABC) framework. We first assess the best sampling strategy (number of: individuals, loci, and classes in the jSFS), and show that the number of individuals and loci have little effect on model selection. In contrast, different decompositions of the joint site frequency spectrum strongly affect the results: including classes of low and high frequency shared polymorphisms can more effectively reveal recent migration events. We then take advantage of the flexibility of the ABC to compare more realistic models of speciation including variation in migration rates through time (i.e. periodic connectivity) and across genes (i.e. genome-wide heterogeneity in migration rates). We show that these models consistently outperform the simpler alternatives. This argues that methods that are restricted to simpler models may fail to reconstruct the true speciation history.

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Coadapted genomes and selection on hybrids: Fisher’s geometric model explains a variety of empirical patterns

Cited by 5 publications

References 79 publications

System drift and speciation

System drift and speciation

Adaptive divergence and the evolution of hybrid trait mismatch in threespine stickleback

The divergence history of European blue mussel species reconstructed from Approximate Bayesian Computation: the effects of sequencing techniques and sampling strategies

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