The Pace of Hybrid Incompatibility Evolution in House Mice

Wang, Richard J.; White, Michael A.; Payseur, Bret A.

doi:10.1534/genetics.115.179499

Cited by 49 publications

(53 citation statements)

References 88 publications

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“…Indeed, given a rather short divergence time between Neanderthals and AMH, it is a priori unlikely that strong hybrid incompatibilities had evolved at a large number of loci before the populations interbred. It often takes millions of years for hybrid incompatibilities to evolve in mammals [42, 43], although there are exceptions to this [44], and theoretical results suggest that such incompatibilities are expected to accumulate only slowly at first [45, 46]. While this is a subjective question, our results suggest that genomic data—although clearly showing a signal of selection against introgression—do not strongly support the view that Neanderthals and humans should be viewed as incipient species.…”

Section: Discussionmentioning

confidence: 62%

The Strength of Selection against Neanderthal Introgression

2016

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Hybridization between humans and Neanderthals has resulted in a low level of Neanderthal ancestry scattered across the genomes of many modern-day humans. After hybridization, on average, selection appears to have removed Neanderthal alleles from the human population. Quantifying the strength and causes of this selection against Neanderthal ancestry is key to understanding our relationship to Neanderthals and, more broadly, how populations remain distinct after secondary contact. Here, we develop a novel method for estimating the genome-wide average strength of selection and the density of selected sites using estimates of Neanderthal allele frequency along the genomes of modern-day humans. We confirm that East Asians had somewhat higher initial levels of Neanderthal ancestry than Europeans even after accounting for selection. We find that the bulk of purifying selection against Neanderthal ancestry is best understood as acting on many weakly deleterious alleles. We propose that the majority of these alleles were effectively neutral—and segregating at high frequency—in Neanderthals, but became selected against after entering human populations of much larger effective size. While individually of small effect, these alleles potentially imposed a heavy genetic load on the early-generation human–Neanderthal hybrids. This work suggests that differences in effective population size may play a far more important role in shaping levels of introgression than previously thought.

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Section: Discussionmentioning

confidence: 62%

The Strength of Selection against Neanderthal Introgression

2016

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“…; Moyle and Nakazato ; Wang et al. ). Therefore, our measure of genetic parallelism might be interpreted as being inversely proportional to the strength of intrinsic barriers.…”

Section: Discussionmentioning

confidence: 99%

Parallel genetic evolution and speciation from standing variation

2019

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Adaptation often proceeds from standing variation, and natural selection acting on pairs of populations is a quantitative continuum ranging from parallel to divergent. Yet, it is unclear how the extent of parallel genetic evolution during adaptation from standing variation is affected by the difference in the direction of selection between populations. Nor is it clear whether the availability of standing variation for adaptation affects progress toward speciation in a manner that depends on the difference in the direction of selection. We conducted a theoretical study investigating these questions and have two primary findings. First, the extent of parallel genetic evolution between two populations rapidly declines as selection changes from fully parallel toward divergent, and this decline is steeper in organisms with more traits (i.e., greater dimensionality). This rapid decline happens because small differences in the direction of selection greatly reduce the fraction of alleles that are beneficial in both populations. For example, populations adapting to optima separated by an angle of 33° might have only 50% of potentially beneficial alleles in common. Second, relative to when adaptation is from only new mutation, adaptation from standing variation improves hybrid fitness under parallel selection and reduces hybrid fitness under divergent selection. Under parallel selection, genetic parallelism from standing variation reduces the phenotypic segregation variance in hybrids, thereby increasing mean fitness in the parental environment. Under divergent selection, larger pleiotropic effects of alleles fixed from standing variation cause maladaptive transgressive phenotypes when combined in hybrids. Adaptation from standing genetic variation therefore slows progress toward speciation under parallel selection and facilitates progress toward speciation under divergent selection.

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“…Using males from CC extinct lines, we performed the largest mapping study for reproductive traits in the CC, and identified several genetic associations with sperm morphology, sperm motility, and reproductive organ weights. Infertility was associated with a large region on chromosome X known to contain loci previously associated with hybrid incompatibility, sterility, and speciation (Payseur et al 2004;Storchova et al 2004;Good et al 2008Good et al , 2010Mihola et al 2009;Wang et al 2015;Balcova et al 2016). QTL allelic effects for most reproductive traits were driven by PWK/PhJ or CAST/EiJ haplotypes ( Table 3).…”

Section: Discussionmentioning

confidence: 99%

Male Infertility Is Responsible for Nearly Half of the Extinction Observed in the Mouse Collaborative Cross

et al. 2017

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The goal of the Collaborative Cross (CC) project was to generate and distribute over 1000 independent mouse recombinant inbred strains derived from eight inbred founders. With inbreeding nearly complete, we estimated the extinction rate among CC lines at a remarkable 95%, which is substantially higher than in the derivation of other mouse recombinant inbred populations. Here, we report genome-wide allele frequencies in 347 extinct CC lines. Contrary to expectations, autosomes had equal allelic contributions from the eight founders, but chromosome had significantly lower allelic contributions from the two inbred founders with underrepresented subspecific origins (PWK/PhJ and CAST/EiJ). By comparing extinct CC lines to living CC strains, we conclude that a complex genetic architecture is driving extinction, and selection pressures are different on the autosomes and chromosome Male infertility played a large role in extinction as 47% of extinct lines had males that were infertile. Males from extinct lines had high variability in reproductive organ size, low sperm counts, low sperm motility, and a high rate of vacuolization of seminiferous tubules. We performed QTL mapping and identified nine genomic regions associated with male fertility and reproductive phenotypes. Many of the allelic effects in the QTL were driven by the two founders with underrepresented subspecific origins, including a QTL on chromosome for infertility that was driven by the PWK/PhJ haplotype. We also performed the first example of cross validation using complementary CC resources to verify the effect of sperm curvilinear velocity from the PWK/PhJ haplotype on chromosome 2 in an independent population across multiple generations. While selection typically constrains the examination of reproductive traits toward the more fertile alleles, the CC extinct lines provided a unique opportunity to study the genetic architecture of fertility in a widely genetically variable population. We hypothesize that incompatibilities between alleles with different subspecific origins is a key driver of infertility. These results help clarify the factors that drove strain extinction in the CC, reveal the genetic regions associated with poor fertility in the CC, and serve as a resource to further study mammalian infertility.

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The Pace of Hybrid Incompatibility Evolution in House Mice

Cited by 49 publications

References 88 publications

The Strength of Selection against Neanderthal Introgression

The Strength of Selection against Neanderthal Introgression

Parallel genetic evolution and speciation from standing variation

Male Infertility Is Responsible for Nearly Half of the Extinction Observed in the Mouse Collaborative Cross

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