Data from: Do genetic loci that cause reproductive isolation in the lab inhibit gene flow in nature?
Data files
Mar 18, 2024 version files 939.37 KB
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comparison_data.zip
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house_mouse_data.zip
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README.md
Abstract
The genetic dissection of reproductive barriers between diverging lineages provides enticing clues into the origin of species. One strategy uses linkage analysis in experimental crosses to identify genomic locations involved in phenotypes that mediate reproductive isolation. A second framework searches for genomic regions that show reduced rates of exchange across natural hybrid zones. It is often assumed that these approaches will point to the same loci, but this assumption is rarely tested. In this perspective, we discuss the factors that determine whether loci connected to postzygotic reproductive barriers in the laboratory are inferred to reduce gene flow in nature. We synthesize data on the genetics of postzygotic isolation in house mice, one of the most intensively studied systems in speciation genetics. In a rare empirical comparison, we measure the correspondence of loci tied to postzygotic barriers via genetic mapping in the laboratory and loci at which gene flow is inhibited across a natural hybrid zone. We find no evidence that the two sets of loci overlap beyond what is expected by chance. In light of these results, we recommend avenues for empirical and theoretical research to resolve the potential incongruence between the two predominant strategies for understanding the genetics of speciation.
README: Data from: Do genetic loci that cause reproductive isolation in the lab inhibit gene flow in nature?
https://doi.org/10.5061/dryad.m63xsj495
This dataset contains two types of data:
1) Summary of genomic regions associated with reproductive isolation in house mice. This data was individually compiled from publically available datasets from 36 studies and remapped to the mm10 reference genome using LiftOver. The archived dataset contains both the original and the mapped coordinates.
2) Results of permutation tests and rank sum tests looking for overlap within the house mouse data set. This was generated from tests comparing subsets of the house mouse dataset to each other. This data consists of CSV tables of p-values for overlap permutation tests, mean clines widths, and p-values for tests of cline width differences.
Description of the data and file structure
The data are in two folders.
In "house_mouse_data", there are six files. These files contain our compilations of the publicly available datasets. Genes are described in one csv file (containing metadata on the source of the genes: "gene_list.csv") and one bed file (containing remapped genomic intervals: "remapped_gene_bed_081023.bed"). There are four versions of the interval loci dataset. These versions have the same list of intervals but differ in the way certain intervals are handled. For the main file ("lit_survey_candidate_loci.csv"), all intervals are reported as is for each dataset. For the subsequent files, QTL are reduced to 1Mb intervals around their peak value ("lit_survey_candidate_loci_1MbQTL.csv"), single marker loci are increased to 1Mb intervals around their values ("lit_survey_candidate_loci_1MbMarkers.csv"), or both ("lit_survey_candidate_loci_1MbQTL_1MbMarkers.csv"). A file labeled "annotation_glossary.csv" contains descriptions of the columns present in the other csv files. Columns that are actually required to complete the main analyses of the study are also indicated in this file.
In "comparison_data", we have two csv files compiling the results of the comparisons described in our manuscript. One file ("permutation_summary.csv") includes the observed number of overlaps, p-values, and overlaps observed in permutations for all permutation tests measuring overlap between datasets. This file could be used to reconstruct the distributions of the permutation output. The second file ("cline_data.csv") contains mean cline widths and p-values for all comparisons of the data.
Sharing/Access information
The house mouse data provided here was compiled from the following studies:
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- Janoušek, Václav, Liuyang Wang, Ken Luzynski, Petra Dufková, Martina M. Vyskočilová, Michael W. Nachman, Pavel Munclinger, Miloš Macholán, Jaroslav Piálek, and Priscilla K. Tucker. 2012. “Genome-Wide Architecture of Reproductive Isolation in a Naturally Occurring Hybrid Zone between Mus Musculus Musculus and M. m. Domesticus.” Molecular Ecology 21 (12): 3032–47. https://doi.org/10.1111/j.1365-294X.2012.05583.x.
- Kass, David H., Václav Janoušek, Liuyang Wang, and Priscilla K. Tucker. 2014. “The Uncharacterized Gene 1700093K21Rik and Flanking Regions Are Correlated with Reproductive Isolation in the House Mouse, Mus Musculus.” Mammalian Genome 25 (5): 223–34. https://doi.org/10.1007/s00335-014-9506-2.
- Kopania, Emily E K, Erica L Larson, Colin Callahan, Sara Keeble, and Jeffrey M Good. 2022. “Molecular Evolution across Mouse Spermatogenesis.” Molecular Biology and Evolution, January, msac023. https://doi.org/10.1093/molbev/msac023.
- Larson, Erica L., Sara Keeble, Dan Vanderpool, Matthew D. Dean, and Jeffrey M. Good. 2017. “The Composite Regulatory Basis of the Large X-Effect in Mouse Speciation.” Molecular Biology and Evolution, msw243. https://doi.org/10.1093/molbev/msw243.
- Larson, Erica L., Dan Vanderpool, Brice A. J. Sarver, Colin Callahan, Sara Keeble, Lorraine L. Provencio, Michael D. Kessler, et al. 2018. “The Evolution of Polymorphic Hybrid Incompatibilities in House Mice.” Genetics 209 (3): 845–59. https://doi.org/10.1534/genetics.118.300840.
- Laukaitis, Christina M., Elizabeth S. Critser, and Robert C. Karn. 1997. “Salivary Androgen-Binding Protein (ABP) Mediates Sexual Isolation in Mus Musculus.” Evolution 51 (6): 2000–2005. https://doi.org/10.2307/2411020.
- Loire, Etienne, Sergio Tusso, Pierre Caminade, Dany Severac, Pierre Boursot, Guila Ganem, and Carole M. Smadja. 2017. “Do Changes in Gene Expression Contribute to Sexual Isolation and Reinforcement in the House Mouse?” Molecular Ecology 26 (19): 5189–5202. https://doi.org/10.1111/mec.14212.
- Lustyk, Diana, Slavomír Kinský, Kristian Karsten Ullrich, Michelle Yancoskie, Lenka Kašíková, Vaclav Gergelits, Radislav Sedlacek, et al. 2019. “Genomic Structure of Hstx2 Modifier of Prdm9-Dependent Hybrid Male Sterility in Mice.” Genetics, September, genetics.302554.2019. https://doi.org/10.1534/genetics.119.302554.
- Macholán, Miloš, Stuart J. E. Baird, Petra Dufková, Pavel Munclinger, Barbora Vošlajerová Bímová, and Jaroslav Piálek. 2011. “Assessing Multilocus Introgression Patterns: A Case Study on the Mouse X Chromosome in Central Europe.” Evolution 65 (5): 1428–46. https://doi.org/10.1111/j.1558-5646.2011.01228.x.
- Mack, Katya L., Polly Campbell, and Michael W. Nachman. 2016. “Gene Regulation and Speciation in House Mice.” Genome Research 26 (4): 451–61. https://doi.org/10.1101/gr.195743.115.
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- Morgan, Katy, Bettina Harr, Michael A White, Bret A Payseur, and Leslie M Turner. 2020. “Disrupted Gene Networks in Subfertile Hybrid House Mice.” Molecular Biology and Evolution 37 (6): 1547–62. https://doi.org/10.1093/molbev/msaa002.
- Payseur, Bret A., James G. Krenz, and Michael W. Nachman. 2004. “Differential Patterns of Introgression across the X Chromosome in a Hybrid Zone between Two Species of House Mice.” Evolution; International Journal of Organic Evolution 58 (9): 2064–78. https://doi.org/10.1111/j.0014-3820.2004.tb00490.x
- Rottscheidt, Ruth, and Bettina Harr. 2007. “Extensive Additivity of Gene Expression Differentiates Subspecies of the House Mouse.” Genetics 177 (3): 1553–67. https://doi.org/10.1534/genetics.107.076190.
- Schwahn, Denise J., Richard J. Wang, Michael A. White, and Bret A. Payseur. 2018. “Genetic Dissection of Hybrid Male Sterility across Stages of Spermatogenesis.” Genetics 210 (4): 1453–65. https://doi.org/10.1534/genetics.118.301658.
- Shorter, John R., Fanny Odet, David L. Aylor, Wenqi Pan, Chia-Yu Kao, Chen-Ping Fu, Andrew P. Morgan, et al. 2017. “Male Infertility Is Responsible for Nearly Half of the Extinction Observed in the Mouse Collaborative Cross.” Genetics 206 (2): 557–72. https://doi.org/10.1534/genetics.116.199596.
- Smadja, Carole, Etienne Loire, Pierre Caminade, Marios Thoma, Yasmin Latour, Camille Roux, Michaela Thoss, Dustin J. Penn, Guila Ganem, and Pierre Boursot. 2015. “Seeking Signatures of Reinforcement at the Genetic Level: A Hitchhiking Mapping and Candidate Gene Approach in the House Mouse.” Molecular Ecology 24 (16): 4222–37. https://doi.org/10.1111/mec.13301.
- Teeter, Katherine C., Bret A. Payseur, Leslie W. Harris, Margaret A. Bakewell, Lisa M. Thibodeau, Janelle E. O’Brien, James G. Krenz, Maria A. Sans-Fuentes, Michael W. Nachman, and Priscilla K. Tucker. 2008. “Genome-Wide Patterns of Gene Flow across a House Mouse Hybrid Zone.” Genome Research 18 (1): 67–76. https://doi.org/10.1101/gr.6757907.
- Teeter, Katherine C., Lisa M. Thibodeau, Zachariah Gompert, C. Alex Buerkle, Michael W. Nachman, and Priscilla K. Tucker. 2010. “The Variable Genomic Architecture of Isolation between Hybridizing Species of House Mice.” Evolution 64 (2): 472–85. https://doi.org/10.1111/j.1558-5646.2009.00846.x.
- Turner, Leslie M., and Bettina Harr. 2014. “Genome-Wide Mapping in a House Mouse Hybrid Zone Reveals Hybrid Sterility Loci and Dobzhansky-Muller Interactions.” Elife 3: e02504. https://doi.org/10.7554/eLife.02504.
- Turner, Leslie M., Michael A. White, Diethard Tautz, and Bret A. Payseur. 2014. “Genomic Networks of Hybrid Sterility.” Edited by John H. Willis. PLoS Genetics 10 (2): e1004162. https://doi.org/10.1371/journal.pgen.1004162.
- Valiskova, Barbora, Sona Gregorova, Diana Lustyk, Petr Šimeček, Petr Jansa, and Jiří Forejt. 2022. “Genic and Chromosomal Components of Prdm9-Driven Hybrid Male Sterility in Mice (Mus Musculus).” Genetics 222 (1): iyac116. https://doi.org/10.1093/genetics/iyac116.
- Wang, Jun, Shirin Kalyan, Natalie Steck, Leslie M. Turner, Bettina Harr, Sven Künzel, Marie Vallier, et al. 2015. “Analysis of Intestinal Microbiota in Hybrid House Mice Reveals Evolutionary Divergence in a Vertebrate Hologenome.” Nature Communications 6 (March): 6440. https://doi.org/10.1038/ncomms7440.
- Wang, Liuyang, Ken Luzynski, John E. Pool, Václav Janoušek, Petra Dufková, Martina M. Vyskočilová, Katherine C. Teeter, et al. 2011. “Measures of Linkage Disequilibrium among Neighbouring SNPs Indicate Asymmetries across the House Mouse Hybrid Zone.” Molecular Ecology 20 (14): 2985–3000. https://doi.org/10.1111/j.1365-294X.2011.05148.x.
- White, Michael A., Brian Steffy, Tim Wiltshire, and Bret A. Payseur. 2011. “Genetic Dissection of a Key Reproductive Barrier between Nascent Species of House Mice.” Genetics 189 (1): 289–304. https://doi.org/10.1534/genetics.111.129171.
- Widmayer, Samuel J, Mary Ann Handel, and David L Aylor. 2020. “Age and Genetic Background Modify Hybrid Male Sterility in House Mice.” Genetics 216 (2): 585–97. https://doi.org/10.1534/genetics.120.303474.
Code/Software
The code used to perform our permutation tests (permutation_test.R) and cline width (cline_test.R) comparisons is archived with Zenodo.