Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

Natural selection plays a variety of roles in hybridization, speciation, and admixture. Most research has focused on two extreme cases: crosses between closely related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. But many natural populations must fall into intermediate regimes, with multiple types of gene interaction, and these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, which were designed for the extreme cases, and invoke either mildly deleterious recessives, or discrete hybrid incompatibilities. Our model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants (Zea, Populus, and Senecio) and animals (Mus, Teleogryllus, and Drosophila). The predictions are generally supported, and the model explains a number of surprising empirical patterns. Our approach enables novel and complementary uses of genome‐wide datasets, which do not depend on identifying outlier loci, or “speciation genes” with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

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“…By contrast, results for the Mus musculus F2 (White et al. 2011), are remarkably close to the predictions of equation (9) (Fig. 5; Fig.…”

Section: Models and Resultssupporting

confidence: 85%

“…We also found four datasets of controlled crosses: F2 from the same mouse subspecies (White et al. 2011), and the ragworts Senecio aethnensis and S. chrysanthemifolius (Chapman et al. 2016); and the Drosophila backcrosses discussed above (Macdonald and Goldstein 1999; Moehring et al.…”

Section: Models and Resultsmentioning

confidence: 99%

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

2018

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“…Some of these QTL may correspond with those identified in previous studies of hybrid male sterility in house mice. As in our study, sperm density and abnormal sperm morphology have been linked to the proximal end of the X chromosome in crosses between M. m. molossinus and M. m. domesticus (Oka et al 2004) and in crosses between M. m. musculus and M. m. domesticus (Storchová et al 2004;Good et al 2008a;White et al 2011). These QTL may have a common evolutionary origin.…”

Section: Discussionsupporting

confidence: 75%

“…Recessiverecessive incompatibilities that isolate these subspecies would not be visible in F 1 's. Such incompatibilities contribute to hybrid dysfunction in other taxa (Presgraves 2003;Oka et al 2004;White et al 2011) and are predicted to be more common than other types of disrupted interactions (Muller 1942). Support for the existence of recessive-recessive incompatibilities in crosses involving M. m. castaneus and M. m. domesticus comes from the identification of multiple genomic regions in M. m. castaneus that reduce fertility only when homozygous.…”

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confidence: 99%

Genetics and Evolution of Hybrid Male Sterility in House Mice

White¹,

Stubbings

Dumont³

et al. 2012

Genetics

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105

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Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reproductive isolation between multiple subspecies pairs. However, studies of the primary reproductive barrier in house mice-hybrid male sterility-have been restricted to a single subspecies pair: Mus musculus musculus and Mus musculus domesticus. To provide a more complete characterization of reproductive isolation in house mice, we conducted an F 2 intercross between wild-derived inbred strains from Mus musculus castaneus and M. m. domesticus. We identified autosomal and X-linked QTL associated with a range of hybrid male sterility phenotypes, including testis weight, sperm density, and sperm morphology. The pseudoautosomal region (PAR) was strongly associated with hybrid sterility phenotypes when heterozygous. We compared QTL found in this cross with QTL identified in a previous F 2 intercross between M. m. musculus and M. m. domesticus and found three shared autosomal QTL. Most QTL were not shared, demonstrating that the genetic basis of hybrid male sterility largely differs between these closely related subspecies pairs. These results lay the groundwork for identifying genes responsible for the early stages of speciation in house mice.

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“…Genetic studies of hybrid male sterility-the primary reproductive barrier between house mouse subspecies-support this prediction. Loci that cause F 2 sterility in crosses between M. musculus castaneus (the subspecies studied by Kousathanas et al (2014)) and M. musculus domesticus map differentially to the X chromosome (White et al 2012) and multiple X-linked loci shape F 1 and F 2 sterility in crosses between M. musculus domesticus and M. musculus musculus (Storchova et al 2004;Good et al 2008;White et al 2011). Interestingly, disruptions in MSCI are also connected to hybrid male sterility in house mice (Campbell et al 2013).…”

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confidence: 99%

Disproportionate Roles for the X Chromosome and Proteins in Adaptive Evolution

Payseur

2014

Genetics

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A daptation requires genetic variation. A complete understanding of this key evolutionary process includes identification of the mutations that confer adaptive change. High-resolution genetic dissection of particular adaptive phenotypes can pinpoint these mutations, but this is a challenging task and the resulting conclusions are restricted to the traits under consideration.An alternative approach is to examine characteristics of adaptive mutations through the powerful lens of population genetics. By measuring intraspecific polymorphism and interspecific divergence across genomes, evolutionary properties of those mutations targeted by natural selection can be discovered. Under this framework as well, generalities are widely sought and difficult to identify. A useful way to make progress is to compare patterns of adaptive evolution among different categories of loci. Two contrasts are based on the genomic location of mutations: X linked vs. autosomal and protein coding vs. cis-regulatory (i.e., noncoding sequences that affect local gene expression). These contrasts have generated substantial interest because they are tied directly to basic questions about adaptive evolution.The fate of a beneficial mutation should depend on its mode of inheritance. This idea motivates comparisons between rates of adaptive evolution on the X chromosome and the autosomes. Recent, low-frequency recessive mutations are immediately exposed to selection in males when X-linked and are mostly hidden from selection (in heterozygotes) when autosomal. If beneficial mutations are at least partially recessive on average, they will fix faster on the X chromosome (Avery 1984), elevating the rate of evolution relative to autosomal loci. In an influential theoretical article, Charlesworth et al. (1987) quantified this connection between dominance and "faster X" evolution and identified the biological conditions under which it applies. With several assumptions, the relative rates of molecular evolution at X-linked and autosomal loci can even be used to estimate the average dominance of new advantageous mutations, an important quantity in evolutionary biology.The study of faster X evolution is also motivated by a desire to explain the outsized role of the X chromosome in speciation. In a wide variety of species pairs, the sterility and/or inviability of hybrids created by interspecific crosses maps differentially to the X chromosome (Coyne and Orr 2004). This bias seems to reflect a higher density of hybrid incompatibilities involving the X chromosome (Masly and Presgraves 2007).The prediction of faster X evolution has been tested repeatedly by comparing between-species divergence at X-linked and autosomal genes (Meisel and Connallon 2013). The most popular approach calculates the relative rate of substitution at nonsynonymous and synonymous sites, reasoning that nonsynonymous changes will often be targeted by selection. A flurry of studies featuring Drosophila revealed a range of support for faster X evolution (Betancourt et al. 2002;Thornton and ...

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Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

Cited by 83 publications

References 130 publications

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

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

Genetics and Evolution of Hybrid Male Sterility in House Mice

Disproportionate Roles for the X Chromosome and Proteins in Adaptive Evolution

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