Reproductive isolation of hybrid populations driven by genetic incompatibilities

Schumer, Molly; Cui, Rongfeng; Rosenthal, Gil G.; Andolfatto, Peter

doi:10.1101/007518

Cited by 16 publications

(25 citation statements)

References 61 publications

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“…Detecting candidate regions of DMIs in non‐model organisms is a currently growing body of work mainly investigated in relatively recent hybrid zones (Schumer et al. , , ), but is a promising avenue of future research, particularly given the support for a potential hybrid swarm in the evolutionary history of Barombi Mbo shown here.…”

Section: Discussionmentioning

confidence: 97%

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Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

2018

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Genomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from summary statistics calculated from sparse genomic sampling without knowledge of which specific genomic regions introgressed. This tells us little about how gene flow potentially influenced sympatric diversification. Here, we investigated whole genomes of Barombi Mbo crater lake cichlids for fine‐scale patterns of introgression with neighboring riverine cichlid populations. We found evidence of secondary gene flow into the radiation scattered across <0.24% of the genome; however, from our analyses, it is not clear if the functional diversity in these regions contributed to the ecological, sexual, and morphological diversity found in the lake. Unlike similar studies, we found no obvious candidate genes for adaptive introgression and we cannot rule out that secondary gene flow was predominantly neutral with respect to the diversification process. We also found evidence for differential assortment of ancestral polymorphisms found in riverine populations between sympatric sister species, suggesting the presence of an ancestral hybrid swarm. Although the history of gene flow and colonization is more complicated than previously assumed, the lack of compelling evidence for secondary gene flow's role in species diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature without a more thorough investigation of the timing and functional role of each introgressed region.

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Section: Discussionmentioning

confidence: 97%

“…Nonetheless, these genes may still serve an adaptive function or could be involved in genetic incompatibilities between diverging sympatric populations, possibly introduced by an initial hybrid swarm in the lake (Seehausen , ; Schumer et al. ).…”

Section: Discussionmentioning

confidence: 99%

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

2018

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“…; Johnson ; Presgraves ; Nei and Nozawa ; Schumer et al. ). Empirical investigations of gene expression support that gene regulation is important for species integrity and can be distorted in hybrids (Landry et al.…”

Section: Discussionmentioning

confidence: 99%

The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact

2015

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Genetic incompatibilities are an important component of reproductive isolation. Although theoretical studies have addressed their evolution, little is known about their maintenance when challenged by potentially high migration rates in secondary contact. Although theory predicts that recombination can erode barriers, many empirical systems have been found to retain species-specific differences despite substantial gene flow. By simulating whole genomes in individuals of hybridizing species, we find that the genetic architecture of two contrasting models of epistatic hybrid incompatibilities and the context of hybridization can substantially affect species integrity and genomic heterogeneity. In line with theory, our results show that intergenomic incompatibilities break down rapidly by recombination, but can maintain genome-wide differentiation under very limited conditions. By contrast, intragenomic interactions that arise from genetic pathways can maintain species-specific differences even with high migration rates and gene flow, whereas introgression at large parts of the genome can simultaneously remain extensive, consistent with empirical observations. We discuss the importance of intragenomic interactions in speciation and consider how this form of epistatic fitness variation is implicated and supported by other theoretical and empirical studies. We further address the relevance of replicates and knowledge of context when investigating the genomics of speciation.

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“…; Schumer et al . ; Lindtke & Buerkle ), in which there is selection on all haplotypes containing heterospecific allele combinations (Fig. S3, Supporting information).…”

Section: Methodsmentioning

confidence: 99%

Determining epistatic selection in admixed populations

Schumer

Brandvain

2016

Molecular Ecology

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When two diverging species begin hybridizing, selection against hybridization is likely driven not by single substitutions, but by interactions between incompatible mutations. To identify these incompatibilities in natural populations, researchers examine the extent of nonrandom associations between ancestry at physically unlinked loci in admixed populations. In this approach, which we call 'AD scans', locus pairs with significantly positive 'ancestry disequilibrium' (AD, i.e. locus pairs that positively covary by ancestry) represent incompatible alleles. Past research has uniformly revealed an excess of locus pairs with significantly positive AD, suggesting that dozens to hundreds of incompatibilities separate species. With forward simulations, we show that many realistic demographic scenarios, including recent and/or ongoing hybridization, generate a bias towards positive ancestry disequilibrium. We suggest steps that researchers can take to avoid pitfalls in interpreting AD scans, and present a novel measure of AD, which minimizes but does not fully eliminate bias in the AD distribution. We also show, by simulation, that the tail of the AD distribution is enriched for true incompatibilities. To illustrate the potential power and appropriate caution in interpretation of AD scans, we reanalyse previously published data from two admixed populations of Xiphophorus fishes. Our results imply that the prevalence of positive LD in admixed populations does not in itself support the idea that two-locus incompatibilities are widespread, but the co-enrichment of top AD hits across the two Xiphophorus populations supports the idea that AD scans can identify candidate interspecific incompatibilities.

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Reproductive isolation of hybrid populations driven by genetic incompatibilities

Cited by 16 publications

References 61 publications

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact

Determining epistatic selection in admixed populations

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