Unboxing mutations: Connecting mutation types with evolutionary consequences.
adaptation
distribution of fitness effects
mutation
mutation rate
population genetics
recombination
speciation
structural variant
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
revised:
30
03
2021
received:
14
01
2021
accepted:
20
04
2021
pubmed:
7
5
2021
medline:
22
6
2021
entrez:
6
5
2021
Statut:
ppublish
Résumé
A key step in understanding the genetic basis of different evolutionary outcomes (e.g., adaptation) is to determine the roles played by different mutation types (e.g., SNPs, translocations and inversions). To do this we must simultaneously consider different mutation types in an evolutionary framework. Here, we propose a research framework that directly utilizes the most important characteristics of mutations, their population genetic effects, to determine their relative evolutionary significance in a given scenario. We review known population genetic effects of different mutation types and show how these may be connected to different evolutionary outcomes. We provide examples of how to implement this framework and pinpoint areas where more data, theory and synthesis are needed. Linking experimental and theoretical approaches to examine different mutation types simultaneously is a critical step towards understanding their evolutionary significance.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2710-2723Informations de copyright
© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Allen Orr, H. (2005). The genetic theory of adaptation: A brief history. Nature Reviews Genetics, 6(2), 119-127.
Archambeault, S. L., Bärtschi, L. R., Merminod, A. D., & Peichel, C. L. (2020). Adaptation via pleiotropy and linkage: Association mapping reveals a complex genetic architecture within the stickleback locus. Evolution Letters, 4(4), 282-301.
Barton, H. J., & Zeng, K. (2018). New methods for inferring the distribution of fitness effects for indels and SNPs. Molecular Biology and Evolution, 35(6), 1536-1546.
Barton, N. H. (1995). A general model for the evolution of recombination. Genetical Research, 65, 123-144. https://doi.org/10.1017/s0016672300033140
Bataillon, T., & Bailey, S. F. (2014). Effects of new mutations on fitness: Insights from models and data. Annals of the New York Academy of Sciences, 1320, 76-92. https://doi.org/10.1111/nyas.12460
Beckmann, J. S., Estivill, X., & Antonarakis, S. E. (2007). Copy number variants and genetic traits: Closer to the resolution of phenotypic to genotypic variability. Nature Reviews. Genetics, 8(8), 639-646.
Berdan, E. L., Blanckaert, A., Butlin, R. K., & Bank, C. (2021). Deleterious mutation accumulation and the long-term fate of chromosomal inversions. PLoS Genetics, 17(3), e1009411.
Bidau, C. J., Giménez, M. D., Palmer, C. L., & Searle, J. B. (2001). The effects of Robertsonian fusions on chiasma frequency and distribution in the house mouse (Mus musculus domesticus) from a hybrid zone in northern Scotland. Heredity, 87(Pt 3), 305-313.
Blanquart, F., & Bataillon, T. (2016). Epistasis and the structure of fitness landscapes: Are experimental fitness landscapes compatible with Fisher’s geometric model? Genetics, 203(2), 847-862.
Brandström, M., Bagshaw, A. T., Gemmell, N. J., & Ellegren, H. (2008). The relationship between microsatellite polymorphism and recombination hot spots in the human genome. Molecular Biology and Evolution, 25(12), 2579-2587.
Brumfield, R. T., Beerli, P., Nickerson, D. A., & Edwards, S. V. (2003). The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology & Evolution, 18(5), 249-256.
Butlin, R. K., & Smadja, C. M. (2018). Coupling, reinforcement, and speciation. The American Naturalist, 191(2), 155-172.
Capilla, L., Medarde, N., Alemany-Schmidt, A., Oliver-Bonet, M., Ventura, J., & Ruiz-Herrera, A. (2014). Genetic recombination variation in wild Robertsonian mice: On the role of chromosomal fusions and Prdm9 allelic background. Proceedings. Biological Sciences/the Royal Society, 281(1786), https://doi.org/10.1098/rspb.2014.0297
Caravagna, G., Heide, T., Williams, M. J., Zapata, L., Nichol, D., Chkhaidze, K., Cross, W., Cresswell, G. D., Werner, B., Acar, A., Chesler, L., Barnes, C. P., Sanguinetti, G., Graham, T. A., & Sottoriva, A. (2020). Subclonal reconstruction of tumors by using machine learning and population genetics. Nature Genetics, 52(9), 898-907.
Carneiro, V. C., & Lyko, F. (2020). Rapid epigenetic adaptation in animals and its role in invasiveness. Integrative and Comparative Biology, 60(2), 267-274.
Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G. Jr, Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J., Schmutz, J., Myers, R. M., Petrov, D., Jónsson, B., Schluter, D., Bell, M. A., & Kingsley, D. M. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327(5963), 302-305.
Charlesworth, B. (2009). Effective population size and patterns of molecular evolution and variation. Nature Review Genetics, 10(3), 195-205.
Charlesworth, B., & Charlesworth, D. (2010). Elements of evolutionary genetics. Roberts Publishers.
Charlesworth, B., & Charlesworth, D. (2017). Population genetics from 1966 to 2016. Heredity, 118(1), 2-9.
Chen, X., Schulz-Trieglaff, O., Shaw, R., Barnes, B., Schlesinger, F., Källberg, M., Cox, A. J., Kruglyak, S., & Saunders, C. T. (2016). Manta: Rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatics, 32(8), 1220-1222.
Choi, J. Y., & Lee, Y. C. G. (2020). Double-edged sword: The evolutionary consequences of the epigenetic silencing of transposable elements. PLOS Genetics, 16, e1008872. https://doi.org/10.1371/journal.pgen.1008872
Christmas, M. J., Wallberg, A., Bunikis, I., Olsson, A., Wallerman, O., & Webster, M. T. (2019). Chromosomal inversions associated with environmental adaptation in honeybees. Molecular Ecology, 28(6), 1358-1374.
Chuong, E. B., Elde, N. C., & Feschotte, C. (2017). Regulatory activities of transposable elements: From conflicts to benefits. Nature Reviews Genetics, 18(2), 71-86.
Crown, K. N., Miller, D. E., Sekelsky, J., & Hawley, R. S. (2018). Local inversion heterozygosity alters recombination throughout the genome. Current Biology, 28(18), 2984-2990.e3.
Dobigny, G., Britton-Davidian, J., & Robinson, T. J. (2017). Chromosomal polymorphism in mammals: An evolutionary perspective. Biological Reviews of the Cambridge Philosophical Society, 92(1), 1-21.
Ducos, A., Berland, H.-M., Bonnet, N., Calgaro, A., Billoux, S., Mary, N., Garnier-Bonnet, A., Darré, R., & Pinton, A. (2007). Chromosomal control of pig populations in France: 2002-2006 survey. Genetics, Selection, Evolution: GSE, 39(5), 583-597.
Elena, S. F., Ekunwe, L., Hajela, N., Oden, S. A., & Lenski, R. E. (1998). Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica, 102-103(1-6), 349-358.
Eyre-Walker, A., & Keightley, P. D. (2007). The distribution of fitness effects of new mutations. Nature Reviews. Genetics, 8(8), 610-618.
Faria, R., Johannesson, K., Butlin, R. K., & Westram, A. M. (2019). Evolving inversions. Trends in Ecology & Evolution, 34(3), 239-248.
Farlow, A., Long, H., Arnoux, S., Sung, W., Doak, T. G., Nordborg, M., & Lynch, M. (2015). The spontaneous mutation rate in the fission yeast Schizosaccharomyces pombe. Genetics, 201(2), 737-744.
Feusier, J., Scott Watkins, W., Thomas, J., Farrell, A., Witherspoon, D. J., Baird, L., Ha, H., Xing, J., & Jorde, L. B. (2019). Pedigree-based estimation of human mobile element retrotransposition rates. Genome Research, 29, 1567-1577. https://doi.org/10.1101/gr.247965.118
Flynn, J. M., Rossouw, A., Cote-Hammarlof, P., Fragata, I., Mavor, D., Hollins, C., Bank, C., & Bolon, D. N. A. (2020). Comprehensive fitness maps of Hsp90 show widespread environmental dependence. eLife, 9, e53810. https://doi.org/10.7554/elife.53810
Fox, D. T., Soltis, D. E., Soltis, P. S., Ashman, T.-L., & Van de Peer, Y. (2020). Polyploidy: A biological force From cells to ecosystems. Trends in Cell Biology, 30(9), 688-694.
Fu, W., Zhang, F., Wang, Y., Gu, X., & Jin, L. (2010). Identification of copy number variation hotspots in human populations. American Journal of Human Genetics, 87(4), 494-504.
Fu, Y.-X., & Huai, H. (2003). Estimating mutation rate: How to count mutations? Genetics, 164(2), 797-805.
Fuller, Z. L., Koury, S. A., Phadnis, N., & Schaeffer, S. W. (2019). How chromosomal rearrangements shape adaptation and speciation: Case studies in Drosophila pseudoobscura and its sibling species Drosophila persimilis. Molecular Ecology, 28(6), 1283-1301.
Fuller, Z. L., Leonard, C. J., Young, R. E., Schaeffer, S. W., & Phadnis, N. (2018). Ancestral polymorphisms explain the role of chromosomal inversions in speciation. PLoS Genetics, 14(7), e1007526.
Futuyma, D. J. (1986). Reflections on reflections: Ecology and evolutionary biology. Journal of the History of Biology, 19(2), 303-312.
Gemayel, R., Vinces, M. D., Legendre, M., & Verstrepen, K. J. (2010). Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics, 44, 445-477.
Gilbert, K. J., Pouyet, F., Excoffier, L., & Peischl, S. (2020). Transition from background selection to associative overdominance promotes diversity in regions of low recombination. Current Biology: CB, 30(1), 101-107.e3.
Goerner-Potvin, P., & Bourque, G. (2018). Computational tools to unmask transposable elements. Nature Reviews Genetics, 19(11), 688-704.
Gong, W. J., McKim, K. S., & Hawley, R. S. (2005). All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote. PLoS Genetics, 1(5), e67.
Gossmann, T. I., Woolfit, M., & Eyre-Walker, A. (2011). Quantifying the variation in the effective population size within a genome. Genetics, 189(4), 1389-1402.
Guerrero, R. F., & Kirkpatrick, M. (2014). Local adaptation and the evolution of chromosome fusions. Evolution; International Journal of Organic Evolution, 68(10), 2747-2756.
Guo, W.-J., Ling, J., & Li, P. (2009). Consensus features of microsatellite distribution: Microsatellite contents are universally correlated with recombination rates and are preferentially depressed by centromeres in multicellular eukaryotic genomes. Genomics, 93, 323-331. https://doi.org/10.1016/j.ygeno.2008.12.009
Haldane, J. B. S. (1927). A mathematical theory of natural and artificial selection, part V: Selection and mutation. Mathematical Proceedings of the Cambridge Philosophical Society, 23(7), 838-844.
Harmanci, A. S., Harmanci, A. O., & Zhou, X. (2020). CaSpER identifies and visualizes CNV events by integrative analysis of single-cell or bulk RNA-sequencing data. Nature Communications, 11(1), 1-16.
Harmand, N., Gallet, R., Jabbour-Zahab, R., Martin, G., & Lenormand, T. (2017). Fisher’s geometrical model and the mutational patterns of antibiotic resistance across dose gradients. Evolution; International Journal of Organic Evolution, 71(1), 23-37.
Henderson, I. R. (2012). Control of meiotic recombination frequency in plant genomes. Current Opinion in Plant Biology, 15(5), 556-561.
Ho, S. S., Urban, A. E., & Mills, R. E. (2020). Structural variation in the sequencing era. Nature Reviews Genetics, 21(3), 171-189.
Hoekstra, H. E., & Coyne, J. A. (2007). The locus of evolution: Evo devo and the genetics of adaptation. Evolution; International Journal of Organic Evolution, 61(5), 995-1016.
Hollister, J. D., & Gaut, B. S. (2009). Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Research, 19(8), 1419-1428.
Huang, Y.-F., Gulko, B., & Siepel, A. (2017). Fast, scalable prediction of deleterious noncoding variants from functional and population genomic data. Nature Genetics, 49, 618-624. https://doi.org/10.1038/ng.3810
Hunter, N. (2015). Meiotic recombination: The essence of heredity. Cold Spring Harbor Perspectives in Biology, 7(12), https://doi.org/10.1101/cshperspect.a016618
Jarne, P., & Lagoda, P. J. (1996). Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution, 11(10), 424-429.
Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P., Mauceli, E., Johnson, J., Swofford, R., Pirun, M., Zody, M. C., White, S., Birney, E., Searle, S., Schmutz, J., Grimwood, J., Dickson, M. C., Myers, R. M., Miller, C. T., Summers, B. R., Knecht, A. K., … Kingsley, D. M. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484(7392), 55-61.
Katju, V., & Bergthorsson, U. (2013). Copy-number changes in evolution: Rates, fitness effects and adaptive significance. Frontiers in Genetics, 4, 273.
Kawecki, T. J., Lenski, R. E., Ebert, D., Hollis, B., Olivieri, I., & Whitlock, M. C. (2012). Experimental evolution. Trends in Ecology & Evolution, 27(10), 547-560.
Kayser, M., Vowles, E. J., Kappei, D., & Amos, W. (2006). Microsatellite length differences between humans and chimpanzees at autosomal loci are not found at equivalent haploid Y chromosomal loci. Genetics, 173(4), 2179-2186.
Keightley, P. D., & Eyre-Walker, A. (2010). What can we learn about the distribution of fitness effects of new mutations from DNA sequence data? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365(1544), 1187-1193.
Kent, T. V., Uzunović, J., & Wright, S. I. (2017). Coevolution between transposable elements and recombination. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372(1736), https://doi.org/10.1098/rstb.2016.0458
Kimura, M. (1957). Some problems of stochastic processes in genetics. Annals of Mathematical Statistics, 28(4), 882-901.
Kirkpatrick, M. (2010). How and why chromosome inversions evolve. PLoS Biology, 8(9), https://doi.org/10.1371/journal.pbio.1000501
Kirkpatrick, M., & Barton, N. (2006). Chromosome inversions, local adaptation and speciation. Genetics, 173(1), 419-434.
Korunes, K. L., & Noor, M. A. F. (2019). Pervasive gene conversion in chromosomal inversion heterozygotes. Molecular Ecology, 28(6), 1302-1315.
Larson, D. E., Abel, H. J., Chiang, C., Badve, A., Das, I., Eldred, J. M., Layer, R. M., & Hall, I. M. (2019). svtools: Population-scale analysis of structural variation. Bioinformatics, 35(22), 4782-4787.
Lee, Y. C. G., & Karpen, G. H. (2017). Pervasive epigenetic effects of drosophila euchromatic transposable elements impact their evolution. eLife, 6, e25762. https://doi.org/10.7554/elife.25762
Liu, Y., Zhang, M., Sun, J., Chang, W., Sun, M., Zhang, S., & Wu, J. (2020). Comparison of multiple algorithms to reliably detect structural variants in pears. BMC Genomics, 21(1), 61.
Llaurens, V., Joron, M., & Billiard, S. (2015). Molecular mechanisms of dominance evolution in Müllerian mimicry. Evolution; International Journal of Organic Evolution, 69(12), 3097-3108.
Maeda, T., Ohno, M., Matsunobu, A., Yoshihara, K., & Yabe, N. (1991). A cytogenetic survey of 14,835 consecutive liveborns. Jinrui Idengaku Zasshi. the Japanese Journal of Human Genetics, 36(1), 117-129.
Malik, H. S. (2009). The centromere-drive hypothesis: a simple basis for centromere complexity. Progress in Molecular and Subcellular Biology, 48, 33-52.
Marriage, T. N., Hudman, S., Mort, M. E., Orive, M. E., Shaw, R. G., & Kelly, J. K. (2009). Direct estimation of the mutation rate at dinucleotide microsatellite loci in Arabidopsis thaliana (Brassicaceae). Heredity, 103, 310-317. https://doi.org/10.1038/hdy.2009.67
Marshall, O. J., Chueh, A. C., Wong, L. H., & Choo, K. H. A. (2008). Neocentromeres: New insights into centromere structure, disease development, and karyotype evolution. American Journal of Human Genetics, 82(2), 261-282.
Martin, G., Elena, S. F., & Lenormand, T. (2007). Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nature Genetics, 39(4), 555-560.
Martin, G., & Lenormand, T. (2006). The fitness effect of mutations across environments: A survey in light of fitness landscape models. Evolution; International Journal of Organic Evolution, 60(12), 2413-2427.
McCartney, D. L., Walker, R. M., Morris, S. W., Anderson, S. M., Duff, B. J., Marioni, R. E., Millar, J. K., McCarthy, S. E., Ryan, N. M., Lawrie, S. M., Watson, A. R., Blackwood, D. H. R., Thomson, P. A., McIntosh, A. M., McCombie, W. R., Porteous, D. J., & Evans, K. L. (2018). Altered DNA methylation associated with a translocation linked to major mental illness. NPJ Schizophrenia, 4(1), 5.
Mérot, C., Oomen, R. A., Tigano, A., & Wellenreuther, M. (2020). A Roadmap for understanding the evolutionary significance of structural genomic variation. Trends in Ecology & Evolution, 35, 561-572. https://doi.org/10.1016/j.tree.2020.03.002
Morel, F., Douet-Guilbert, N., Le Bris, M.-J., Herry, A., Amice, V., Amice, J., & De Braekeleer, M. (2004). Meiotic segregation of translocations during male gametogenesis. International Journal of Andrology, 27(4), 200-212.
Moreno-Cabrera, J. M., Del Valle, J., Castellanos, E., Feliubadaló, L., Pineda, M., Brunet, J., Serra, E., Capellà, G., Lázaro, C., & Gel, B. (2020). Evaluation of CNV detection tools for NGS panel data in genetic diagnostics. European Journal of Human Genetics: EJHG, 28(12), 1645-1655.
Myers, S., Bottolo, L., Freeman, C., McVean, G., & Donnelly, P. (2005). A fine-scale map of recombination rates and hotspots across the human genome. Science, 310(5746), 321-324.
Ohno, S. (2013). Evolution by gene duplication. Springer Science & Business Media.
Ohta, T. (1971). Associative overdominance caused by linked detrimental mutations. Genetics Research, 18(3), 277-286.
Ortiz-Barrientos, D., Engelstädter, J., & Rieseberg, L. H. (2016). Recombination rate evolution and the origin of species. Trends in Ecology & Evolution, 31, 226-236. https://doi.org/10.1016/j.tree.2015.12.016
Ossowski, S., Schneeberger, K., Lucas-Lledó, J. I., Warthmann, N., Clark, R. M., Shaw, R. G., Weigel, D., & Lynch, M. (2010). The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science, 327(5961), 92-94.
Otto, S. P., & Barton, N. H. (1997). The evolution of recombination: Removing the limits to natural selection. Genetics, 147(2), 879-906.
Pikaard, C. S., & Mittelsten Scheid, O. (2014). Epigenetic regulation in plants. Cold Spring Harbor Perspectives in Biology, 6(12), a019315.
Poorman, P. A., Moses, M. J., Russell, L. B., & Cacheiro, N. L. (1981). Synaptonemal complex analysis of mouse chromosomal rearrangements. I. Cytogenetic observations on a tandem duplication. Chromosoma, 81(4), 507-518.
Ramu, A., Noordam, M. J., Schwartz, R. S., Wuster, A., Hurles, M. E., Cartwright, R. A., & Conrad, D. F. (2013). DeNovoGear: De novo indel and point mutation discovery and phasing. Nature Methods, 10(10), 985-987.
Rieseberg, L. H. (2001). Chromosomal rearrangements and speciation. Trends in Ecology & Evolution, 16, 351-358. https://doi.org/10.1016/s0169-5347(01)02187-5
Rocchi, M., Archidiacono, N., Schempp, W., Capozzi, O., & Stanyon, R. (2012). Centromere repositioning in mammals. Heredity, 108(1), 59-67.
Schrider, D. R., Houle, D., Lynch, M., & Hahn, M. W. (2013). Rates and genomic consequences of spontaneous mutational events in Drosophila melanogaster. Genetics, 194(4), 937-954.
Seo, J.-S., Rhie, A., Kim, J., Lee, S., Sohn, M.-H., Kim, C.-U., Hastie, A., Cao, H., Yun, J.-Y., Kim, J., Kuk, J., Park, G. H., Kim, J., Ryu, H., Kim, J., Roh, M., Baek, J., Hunkapiller, M. W., Korlach, J., … Kim, C. (2016). De novo assembly and phasing of a Korean human genome. Nature, 538(7624), 243-247.
Sherizen, D., Jang, J. K., Bhagat, R., Kato, N., & McKim, K. S. (2005). Meiotic recombination in Drosophila females depends on chromosome continuity between genetically defined boundaries. Genetics, 169(2), 767-781.
Shigemizu, D., Miya, F., Akiyama, S., Okuda, S., Boroevich, K. A., Fujimoto, A., Nakagawa, H., Ozaki, K., Niida, S., Kanemura, Y., Okamoto, N., Saitoh, S., Kato, M., Yamasaki, M., Matsunaga, T., Mutai, H., Kosaki, K., & Tsunoda, T. (2018). IMSindel: An accurate intermediate-size indel detection tool incorporating de novo assembly and gapped global-local alignment with split read analysis. Scientific Reports, 8(1), 5608.
Sjödin, P., & Jakobsson, M. (2012). Population genetic nature of copy number variation. Methods in molecular biology (838, pp. 209-223). https://doi.org/10.1007/978-1-61779-507-7_10
Smadja, C. M., & Butlin, R. K. (2011). A framework for comparing processes of speciation in the presence of gene flow. Molecular Ecology, 20(24), 5123-5140.
Smukowski, C. S., & Noor, M. A. F. (2011). Recombination rate variation in closely related species. Heredity, 107, 496-508. https://doi.org/10.1038/hdy.2011.44
Sobreira, N. L. M., Gnanakkan, V., Walsh, M., Marosy, B., Wohler, E., Thomas, G., Hoover-Fong, J. E., Hamosh, A., Wheelan, S. J., & Valle, D. (2011). Characterization of complex chromosomal rearrangements by targeted capture and next-generation sequencing. Genome Research, 21(10), 1720-1727.
Stajic, D., Bank, C., & Gordo, I. (2021). Epigenetic switching outcompetes genetic mutations during adaptation to fluctuating environments. https://doi.org/10.1101/2021.03.11.434930
Stapley, J., Feulner, P. G. D., Johnston, S. E., Santure, A. W., & Smadja, C. M. (2017). Variation in recombination frequency and distribution across eukaryotes: Patterns and processes. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372(1736), https://doi.org/10.1098/rstb.2016.0455
Stapley, J., Santure, A. W., & Dennis, S. R. (2015). Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Molecular Ecology, 24(9), 2241-2252.
Sullivan, B. A., & Karpen, G. H. (2004). Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nature Structural & Molecular Biology, 11(11), 1076-1083.
Sung, W., Ackerman, M. S., Dillon, M. M., Platt, T. G., Fuqua, C., Cooper, V. S., & Lynch, M. (2016). Evolution of the insertion-deletion mutation rate across the tree of life. G3 Genes|genomes|genetics, 6(8), 2583-2591.
Talbert, P. B., Meers, M. P., & Henikoff, S. (2019). Old cogs, new tricks: The evolution of gene expression in a chromatin context. Nature Reviews Genetics, 20(5), 283-297.
Talukdar, D. (2010). Reciprocal translocations in grass pea (Lathyrus sativus): Pattern of transmission, detection of multiple interchanges and their independence. The Journal of Heredity, 101(2), 169-176.
Tenaillon, O. (2014). The utility of Fisher's geometric model in evolutionary genetics. Annual Review of Ecology, Evolution, and Systematics, 45, 179-201.
Thuillet, A.-C., Bru, D., David, J., Roumet, P., Santoni, S., Sourdille, P., & Bataillon, T. (2002). Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum desf. Molecular Biology and Evolution, 19(1), 122-125.
Torgasheva, A. A., & Borodin, P. M. (2010). Synapsis and recombination in inversion heterozygotes. Biochemical Society Transactions, 38(6), 1676-1680.
Twyford, A. D., & Friedman, J. (2015). Adaptive divergence in the monkey flower Mimulus guttatus is maintained by a chromosomal inversion. Evolution; International Journal of Organic Evolution, 69(6), 1476-1486.
Vendrell-Mir, P., Barteri, F., Merenciano, M., González, J., Casacuberta, J. M., & Castanera, R. (2019). A benchmark of transposon insertion detection tools using real data. Mobile DNA, 10, https://doi.org/10.1186/s13100-019-0197-9
Wang, S., Lee, S., Chu, C., Jain, D., Kerpedjiev, P., Nelson, G. M., Walsh, J. M., Alver, B. H., & Park, P. J. (2020). HiNT: A computational method for detecting copy number variations and translocations from Hi-C data. Genome Biology, 21(1), 73.
Weissensteiner, M. H., Bunikis, I., Catalán, A., Francoijs, K.-J., Knief, U., Heim, W., Peona, V., Pophaly, S. D., Sedlazeck, F. J., Suh, A., Warmuth, V. M., & Wolf, J. B. W. (2020). Discovery and population genomics of structural variation in a songbird genus. Nature Communications, 11, 1-11. https://doi.org/10.1038/s41467-020-17195-4
Weng, M.-L., Becker, C., Hildebrandt, J., Neumann, M., Rutter, M. T., Shaw, R. G., Weigel, D., & Fenster, C. B. (2019). Fine-Grained Analysis of Spontaneous Mutation Spectrum and Frequency in Arabidopsis thaliana. Genetics, 211(2), 703-714.
Yamaguchi, O., & Mukai, T. (1974). Variation of spontaneous occurrence rates of chromosomal aberrations in the second chromosomes of Drosophila melanogaster. Genetics, 78(4), 1209-1221.
Zuellig, M. P., & Sweigart, A. L. (2018). A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus. Evolution, 72, 2394-2405. https://doi.org/10.1111/evo.13596