Experimental Hybridization Studies Suggest That Pleiotropic Alleles Commonly Underlie Adaptive Divergence between Natural Populations

Thompson, Ken

doi:10.1086/708722

Cited by 15 publications

(16 citation statements)

References 52 publications

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“…Decades of empirical and theoretical work have indicated that Dobzhansky-Muller hybrid incompatibilities (DMIs), or incompatible interactions between mutations that are derived in each of the parental species, are a common cause of inviability and infertility in hybrids [21][22][23][24]. Hybrids can also suffer from the effects of intermediate or transgressive traits that place them far from the phenotypic optimum for either parental species [25][26][27][28]. In both of these scenarios, selection is generally expected to act against alleles derived from the "minor" parent species, or the species that contributed less to the genome of the hybrids.…”

Section: Introductionmentioning

confidence: 99%

Predictability and parallelism in the contemporary evolution of hybrid genomes

Langdon

Powell

Kim

et al. 2021

Preprint

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Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni × X. cortezi and X. birchmanni × X. malinche. We find surprisingly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X. birchmanni × X. cortezi and X. birchmanni × X. malinche hybrid populations.

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Section: Introductionmentioning

confidence: 99%

Predictability and parallelism in the contemporary evolution of hybrid genomes

Langdon

Powell

Kim

et al. 2021

Preprint

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“…However, our study demonstrates that reliably predicting hybrid fitness and transgression is not straightforward, especially not across large evolutionary distances and under changing environmental conditions (Gompert et al 2017). In natural populations with standing genetic variation, transgressive segregation in hybrid offspring may be further obscured by large-effect pleiotropic alleles and compensatory mutations in other traits that are fixed during the adaptive divergence of the parents (Thompson 2020). To understand if there are any generalizable patterns in hybrid fitness beyond the idiosyncrasies caused by the specific genomic background of the cross, we need more research on the targets of selection in hybrid genomes, the genetic architecture of these traits, and their interactions with the environment.…”

Section: Discussionmentioning

confidence: 82%

“…The number of transgressive F2 hybrids in our experiment varied significantly among environments, cross backgrounds, and their interactions (Figure 7), suggesting that the outcome of hybridization events is highly context-specific with strong genomic and environmental contingencies, even when hybrid crosses were made from the same two parents. Transgression has been previously described to vary among phenotypic traits (Albertson and Kocher 2005;Thompson 2020) and experimental environments (Stelkens et al 2014;Zhang et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Hybridization Outcomes Have Strong Genomic and Environmental Contingencies

Brice

Zhang

Bendixsen

et al. 2021

The American Naturalist

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Extreme F2 phenotypes known as transgressive segregants can cause increased or decreased fitness in hybrids beyond the ranges seen in parental populations. Despite the usefulness of transgression for plant and animal breeding, and its potential role in hybrid speciation, the genetic mechanisms and predictors of transgressive segregation remain largely untested. We generated seven hybrid crosses between five widely divergent Saccharomyces yeast species and measured the fitness of the parents, and their viable F1 and F2 hybrids in seven stressful environments. We found that on average 16.6% of all replicate F2 hybrids had higher fitness than both parents. Against our predictions, transgression frequency was not a function of parental genetic and phenotypic distances across test environments. Within environments, some relationships were significant but not in the predicted direction, e.g. genetic distance was negatively related to transgression in ethanol and hydrogen peroxide. Significant effects of hybrid cross, test environment, and cross x environment interactions suggest that the amount of transgression produced in a hybrid cross is highly context-specific, and that outcomes of hybridization differ even among crosses made from the same two parents. If the goal is to reliably predict hybrid fitness and forecast the evolutionary potential of admixed populations, we need more efforts to identify patterns beyond the idiosyncrasies caused by specific genomic or environmental contexts.

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“…Simple simulations (included in archived R scripts) illustrate that the strength of selection necessary to generate 3 % excess ancestry heterozygosity in a population of F 2 hybrids (similar to that observed in the present study) can vary by orders of magnitude depending on assumptions about the genetic architecture of selection. Because the expression of maladaptive trait combinations is predicted to increase with the magnitude of divergence between parent populations (Barton, 2001;Chhina et al, 2021;Thompson, 2020), we may predict that the strength of selection against ecological incompatibilities will increase with the magnitude of divergence between parents. However, quantifying the ecological basis of incompatibilities and their genetic structure will remain technically challenging.…”

Section: P R E -P R I N Tmentioning

confidence: 99%

Genetic evidence for environment-dependent hybrid incompatibilities in threespine stickleback

et al. 2021

Preprint

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Hybrid incompatibilities occur when interactions between opposite-ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are 'intrinsic', meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci—a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

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Experimental Hybridization Studies Suggest That Pleiotropic Alleles Commonly Underlie Adaptive Divergence between Natural Populations

Cited by 15 publications

References 52 publications

Predictability and parallelism in the contemporary evolution of hybrid genomes

Predictability and parallelism in the contemporary evolution of hybrid genomes

Hybridization Outcomes Have Strong Genomic and Environmental Contingencies

Genetic evidence for environment-dependent hybrid incompatibilities in threespine stickleback

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