Browse by volume Browse by section Browse by topic Browse by conference

Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation

Barroso, Gustavo V1, 2  ; Dutheil, Julien Y1, 3 
1 Max Planck Institute for Evolutionary Biology. Department of Evolutionary Genetics. August-Thienemann-Straße 2 24306 Plön – Germany
2 University of Wisconsin, Madison. Department of Integrative Biology. 447 Birge Hall – Madison, WI – USA
3 Unité Mixte de Recherche 5554 Institut des Sciences de l’Evolution, CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France

10.24072/pcjournal.267 - Peer Community Journal, Volume 3 (2023), article no. e40.

Get full text PDF Peer reviewed and recommended by PCI

What shapes the distribution of nucleotide diversity along the genome? Attempts to answer this question have sparked debate about the roles of neutral stochastic processes and natural selection in molecular evolution. However, the mechanisms of evolution do not act in isolation, and integrative models that simultaneously consider the influence of multiple factors on diversity are lacking; without them, confounding factors lurk in the estimates. Here we present a new statistical method that jointly infers the genomic landscapes of genealogies, recombination rates and mutation rates. In doing so, our model captures the effects of genetic drift, linked selection and local mutation rates on patterns of genomic variation. We then formalize a causal model of how these micro-evolutionary mechanisms interact, and cast it as a linear regression to estimate their individual contributions to levels of diversity along the genome. Our analyses reclaim the well-established signature of linked selection in Drosophila melanogaster, but we estimate that the mutation landscape is the major driver of the genome-wide distribution of diversity in this species. Furthermore, our simulation results suggest that in many evolutionary scenarios the mutation landscape will be a crucial factor shaping diversity, depending notably on the genomic window size. We argue that incorporating mutation rate variation into the null model of molecular evolution will lead to more realistic inferences in population genomics.

Published online:
DOI: 10.24072/pcjournal.267
Type: Research article
Keywords: Mutation rate variation, Linked selection, Sequentially Markovian coalescent, Drosophila melanogaster
Barroso, Gustavo V 1, 2; Dutheil, Julien Y 1, 3

1 Max Planck Institute for Evolutionary Biology. Department of Evolutionary Genetics. August-Thienemann-Straße 2 24306 Plön – Germany
2 University of Wisconsin, Madison. Department of Integrative Biology. 447 Birge Hall – Madison, WI – USA
3 Unité Mixte de Recherche 5554 Institut des Sciences de l’Evolution, CNRS, IRD, EPHE, Université de Montpellier, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_267,
     author = {Barroso, Gustavo V and Dutheil, Julien Y},
     title = {The landscape of nucleotide diversity in {\protect\emph{Drosophila} melanogaster} is shaped by mutation rate variation},
     journal = {Peer Community Journal},
     eid = {e40},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.267},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.267/}
}
TY  - JOUR
AU  - Barroso, Gustavo V
AU  - Dutheil, Julien Y
TI  - The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.267/
DO  - 10.24072/pcjournal.267
ID  - 10_24072_pcjournal_267
ER  - 
%0 Journal Article
%A Barroso, Gustavo V
%A Dutheil, Julien Y
%T The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.267/
%R 10.24072/pcjournal.267
%F 10_24072_pcjournal_267
Barroso, Gustavo V; Dutheil, Julien Y. The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation. Peer Community Journal, Volume 3 (2023), article  no. e40. doi : 10.24072/pcjournal.267. https://peercommunityjournal.org/articles/10.24072/pcjournal.267/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100636

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Adrion, J. R.; Galloway, J. G.; Kern, A. D. Inferring the landscape of recombination using recurrent neural networks, bioRxiv (2019) | DOI

[2] Alexander, R. P.; Fang, G.; Rozowsky, J.; Snyder, M.; Gerstein, M. B. Annotating non-coding regions of the genome, Nature Reviews Genetics, Volume 11 (2010) no. 8, pp. 559-571 | DOI

[3] Andolfatto, P. Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome, Genome Research, Volume 17 (2007) no. 12, pp. 1755-1762 | DOI

[4] Baetu, T. Mechanisms in Molecular Biology, Cambridge University Press, 2019 | DOI

[5] V. Barroso, G.; Puzović, N.; Dutheil, J. Y. Inference of recombination maps from a single pair of genomes and its application to ancient samples, PLOS Genetics, Volume 15 (2019) no. 11 | DOI

[6] Barroso, G. V. gvbarroso/iSMC: v0.0.24 (Software package and Source code), Zenodo, 2023a | DOI

[7] Barroso, G. V. gvbarroso/ismc_dm_analyses: v0.0.1 (Scripts), Zenodo, 2023b | DOI

[8] Barroso, G. V. Quantifying the determinants of the genome-wide diversity in Drosophila using iSMC (Data), FigShare, 2023c | DOI

[9] Begun, D. J.; Aquadro, C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster, Nature, Volume 356 (1992) no. 6369, pp. 519-520 | DOI

[10] Begun, D. J.; Holloway, A. K.; Stevens, K.; Hillier, L. W.; Poh, Y.-P.; Hahn, M. W.; Nista, P. M.; Jones, C. D.; Kern, A. D.; Dewey, C. N.; Pachter, L.; Myers, E.; Langley, C. H. Population genomics: Whole-genome analysis of polymorphism and divergence in Drosophila simulans, PLoS Biology, Volume 5 (2007) no. 11 | DOI

[11] Beichman, A. C.; Huerta-Sanchez, E.; Lohmueller, K. E. Using genomic data to infer historic population dynamics of nonmodel organisms, Annual Review of Ecology, Evolution, and Systematics, Volume 49 (2018) no. 1, pp. 433-456 | DOI

[12] Berg, I. L.; Neumann, R.; Sarbajna, S.; Odenthal-Hesse, L.; Butler, N. J.; Jeffreys, A. J. Variants of the protein PRDM9 differentially regulate a set of human meiotic recombination hotspots highly active in African populations, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 30, pp. 12378-12383 | DOI

[13] Besenbacher, S.; Hvilsom, C.; Marques-Bonet, T.; Mailund, T.; Schierup, M. H. Direct estimation of mutations in great apes reconciles phylogenetic dating, Nature Ecology and Evolution, Volume 3 (2019) no. 2, pp. 286-292 | DOI

[14] Booker, T. R.; Jackson, B. C.; Keightley, P. D. Detecting positive selection in the genome, BMC Biology, Volume 15 (2017) no. 1 | DOI

[15] Booker, T. R.; Yeaman, S.; Whitlock, M. C. Variation in recombination rate affects detection of outliers in genome scans under neutrality, Molecular Ecology, Volume 29 (2020) no. 22, pp. 4274-4279 | DOI

[16] Buffalo, V. Natural selection is unlikely to explain why species get a thin slice of π, bioRxiv (2021) | DOI

[17] Casillas, S.; Barbadilla, A. Molecular population genetics, Genetics, Volume 205 (2017) no. 3, pp. 1003-1035 | DOI

[18] Castellano, D.; Coronado-Zamora, M.; Campos, J. L.; Barbadilla, A.; Eyre-Walker, A. Adaptive evolution is substantially impeded by Hill–Robertson interference in Drosophila, Molecular Biology and Evolution, Volume 33 (2016) no. 2, pp. 442-455 | DOI

[19] Castellano, D.; Eyre-Walker, A.; Munch, K. Impact of mutation rate and selection at linked sites on DNA variation across the genomes of humans and other Homininae, Genome Biology and Evolution, Volume 12 (2020) no. 1, pp. 3550-3561 | DOI

[20] Castellano, D.; James, J.; Eyre-Walker, A. Nearly neutral evolution across the Drosophila melanogaster genome, Molecular Biology and Evolution, Volume 35 (2018), pp. 2685-2694 | DOI

[21] Chan, A. H.; Jenkins, P. A.; Song, Y. S. Genome-wide fine-scale recombination rate variation in Drosophila melanogaster, PLoS Genetics, Volume 8 (2012) no. 12 | DOI

[22] Charlesworth, B. Background selection 20 years on: The Wilhelmine E. Key 2012 invitational lecture, Journal of Heredity, Volume 104 (2013) no. 2, pp. 161-171 | DOI

[23] Charlesworth, B. Molecular population genomics: a short history, Genetics Research, Volume 92 (2010) no. 5-6, pp. 397-411 | DOI

[24] Charlesworth, B. Effective population size and patterns of molecular evolution and variation, Nature Reviews Genetics, Volume 10 (2009) no. 3, pp. 195-205 | DOI

[25] Charlesworth, B.; Charlesworth, D. Population genetics from 1966 to 2016, Heredity, Volume 118 (2017) no. 1, pp. 2-9 | DOI

[26] Charlesworth, B.; Morgan, M. T.; Charlesworth, D. The effect of deleterious mutations on neutral molecular variation, Genetics, Volume 134 (1993) no. 4, pp. 1289-1303 | DOI

[27] Comeron, J. M. Background selection as null hypothesis in population genomics: insights and challenges from Drosophila studies, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 372 (2017) no. 1736 | DOI

[28] Comeron, J. M. Background selection as baseline for nucleotide variation across the Drosophila genome, PLoS Genetics, Volume 10 (2014) no. 6 | DOI

[29] Comeron, J. M.; Ratnappan, R.; Bailin, S. The many landscapes of recombination in Drosophila melanogaster, PLoS Genetics, Volume 8 (2012) no. 10 | DOI

[30] Cunningham, F.; Allen, J. E.; Allen, J.; Alvarez-Jarreta, J.; Amode, M. R.; Armean, I. M.; Austine-Orimoloye, O.; Azov, A. G.; Barnes, I.; Bennett, R.; Berry, A.; Bhai, J.; Bignell, A.; Billis, K.; Boddu, S.; Brooks, L.; Charkhchi, M.; Cummins, C.; Da Rin Fioretto, L.; Davidson, C.; Dodiya, K.; Donaldson, S.; El Houdaigui, B.; El Naboulsi, T.; Fatima, R.; Giron, C. G.; Genez, T.; Martinez, J. G.; Guijarro-Clarke, C.; Gymer, A.; Hardy, M.; Hollis, Z.; Hourlier, T.; Hunt, T.; Juettemann, T.; Kaikala, V.; Kay, M.; Lavidas, I.; Le, T.; Lemos, D.; Marugán, J. C.; Mohanan, S.; Mushtaq, A.; Naven, M.; Ogeh, D. N.; Parker, A.; Parton, A.; Perry, M.; Piližota, I.; Prosovetskaia, I.; Sakthivel, M. P.; Salam, A. I. A.; Schmitt, B. M.; Schuilenburg, H.; Sheppard, D.; Pérez-Silva, J. G.; Stark, W.; Steed, E.; Sutinen, K.; Sukumaran, R.; Sumathipala, D.; Suner, M.-M.; Szpak, M.; Thormann, A.; Tricomi, F. F.; Urbina-Gómez, D.; Veidenberg, A.; Walsh, T. A.; Walts, B.; Willhoft, N.; Winterbottom, A.; Wass, E.; Chakiachvili, M.; Flint, B.; Frankish, A.; Giorgetti, S.; Haggerty, L.; Hunt, S. E.; IIsley, G. R.; Loveland, J. E.; Martin, F. J.; Moore, B.; Mudge, J. M.; Muffato, M.; Perry, E.; Ruffier, M.; Tate, J.; Thybert, D.; Trevanion, S. J.; Dyer, S.; Harrison, P. W.; Howe, K. L.; Yates, A. D.; Zerbino, D. R.; Flicek, P. Ensembl 2022, Nucleic Acids Research, Volume 50 (2022) no. D1 | DOI

[31] Cutter, A. D.; Payseur, B. A. Genomic signatures of selection at linked sites: Unifying the disparity among species, Nature Reviews Genetics, Volume 14 (2013) no. 4, pp. 262-274 | DOI

[32] DeWitt, W. S.; Harris, K. D.; Ragsdale, A. P.; Harris, K. Nonparametric coalescent inference of mutation spectrum history and demography, Proceedings of the National Academy of Sciences, Volume 118 (2021) no. 21 | DOI

[33] Durbin, R.; Eddy, S. R.; Krogh, A.; Mitchison, G. Biological sequence analysis: Probabilistic models of proteins and nucleic acids, Cambridge University Press, 1998 | DOI

[34] Dutheil, J. Y. Towards more realistic models of genomes in populations: The Markov-modulated sequentially Markov coalescent, EMS Series of Congress Reports, EMS Press, 2021, pp. 383-408 | DOI

[35] Dutheil, J. Y. Hidden Markov Models in Population Genomics, Methods in Molecular Biology, Springer New York, New York, NY, 2017, pp. 149-164 | DOI

[36] Ellegren, H.; Galtier, N. Determinants of genetic diversity, Nature Reviews Genetics, Volume 17 (2016) no. 7, pp. 422-433 | DOI

[37] Elyashiv, E.; Sattath, S.; Hu, T. T.; Strutsovsky, A.; McVicker, G.; Andolfatto, P.; Coop, G.; Sella, G. A genomic map of the effects of linked selection in Drosophila, PLOS Genetics, Volume 12 (2016) no. 8 | DOI

[38] Felsenstein, J.; Churchill, G. A. A Hidden Markov Model approach to variation among sites in rate of evolution, Molecular Biology and Evolution, Volume 13 (1996) no. 1, pp. 93-104 | DOI

[39] Ferré, J. Regression diagnostics, Comprehensive Chemometrics, Elsevier, 2009, pp. 33-89 | DOI

[40] Francioli, L. C.; Polak, P. P.; Koren, A.; Menelaou, A.; Chun, S.; Renkens, I.; van Duijn, C. M.; Swertz, M.; Wijmenga, C.; van Ommen, G.; Slagboom, P. E.; Boomsma, D. I.; Ye, K.; Guryev, V.; Arndt, P. F.; Kloosterman, W. P.; de Bakker, P. I. W.; Sunyaev, S. R. Genome-wide patterns and properties of de novo mutations in humans, Nature Genetics, Volume 47 (2015) no. 7, pp. 822-826 | DOI

[41] Galtier, N.; Rousselle, M. How much does Ne vary among species?, Genetics, Volume 216 (2020) no. 2, pp. 559-572 | DOI

[42] Haasl, R. J.; Payseur, B. A. Fifteen years of genomewide scans for selection: Trends, lessons and unaddressed genetic sources of complication, Molecular Ecology, Volume 25 (2016) no. 1, pp. 5-23 | DOI

[43] Habig, M.; Lorrain, C.; Feurtey, A.; Komluski, J.; Stukenbrock, E. H. Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus, Nature Communications, Volume 12 (2021) no. 1 | DOI

[44] Haldane, J. B. S. The effect of variation of fitness, The American Naturalist, Volume 71 (1937) no. 735, pp. 337-349 | DOI

[45] Haller, B. C.; Messer, P. W. SLiM 3: Forward genetic simulations beyond the Wright–Fisher model, Molecular Biology and Evolution, Volume 36 (2018) no. 3, pp. 632-637 | DOI

[46] Harpak, A.; Bhaskar, A.; Pritchard, J. K. Mutation rate variation is a primary determinant of the distribution of allele frequencies in humans, PLOS Genetics, Volume 12 (2016) no. 12 | DOI

[47] Haudry, A.; Laurent, S.; Kapun, M. Population genomics on the fly: Recent advances in Drosophila, Methods in Molecular Biology, Springer US, New York, NY, 2020, pp. 357-396 | DOI

[48] Hein, J.; Schierup, M.; Wiuf, C. Gene genealogies, variation and evolution: A primer in coalescent theory , Oxford University Press, Oxford, 2004 | DOI

[49] Hey, J. The neutralist, the fly and the selectionist, Trends in Ecology & Evolution, Volume 14 (1999) no. 1, pp. 35-38 | DOI

[50] Hodgkinson, A.; Eyre-Walker, A. Variation in the mutation rate across mammalian genomes, Nature Reviews Genetics, Volume 12 (2011) no. 11, pp. 756-766 | DOI

[51] Hubisz, M. J.; Williams, A. L.; Siepel, A. Mapping gene flow between ancient hominins through demography-aware inference of the ancestral recombination graph, PLOS Genetics, Volume 16 (2020) no. 8 | DOI

[52] Hudson, R. R. Properties of a neutral allele model with intragenic recombination, Theoretical Population Biology, Volume 23 (1983) no. 2, pp. 183-201 | DOI

[53] Hudson, R. R.; Kaplan, N. L. Deleterious background selection with recombination, Genetics, Volume 141 (1995) no. 4, pp. 1605-1617 | DOI

[54] Hudson, R. R.; Kaplan, N. L. Gene trees with background selection, Non-neutral evolution: Theories and molecular data, Springer US, Boston, MA, 1994, pp. 140-153 | DOI

[55] Hudson, R. R.; Kaplan, N. L. The coalescent process in models with selection and recombination, Genetics, Volume 120 (1988) no. 3, pp. 831-840 | DOI

[56] Hudson, R. R.; Kaplan, N. L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences, Genetics, Volume 111 (1985) no. 1, pp. 147-164 | DOI

[57] Jabbari, K.; Wirtz, J.; Rauscher, M.; Wiehe, T. A common genomic code for chromatin architecture and recombination landscape, PLOS ONE, Volume 14 (2019) no. 3 | DOI

[58] Jensen, J. D.; Payseur, B. A.; Stephan, W.; Aquadro, C. F.; Lynch, M.; Charlesworth, D.; Charlesworth, B. The importance of the Neutral Theory in 1968 and 50 years on: A response to Kern and Hahn 2018, Evolution, Volume 73 (2019) no. 1, pp. 111-114 | DOI

[59] Johri, P.; Charlesworth, B.; Jensen, J. D. Toward an evolutionarily appropriate null model: Jointly inferring demography and purifying selection, Genetics, Volume 215 (2020) no. 1, pp. 173-192 | DOI

[60] Jónsson, H.; Sulem, P.; Arnadottir, G. A.; Pálsson, G.; Eggertsson, H. P.; Kristmundsdottir, S.; Zink, F.; Kehr, B.; Hjorleifsson, K. E.; Jensson, B. Ö.; Jonsdottir, I.; Marelsson, S. E.; Gudjonsson, S. A.; Gylfason, A.; Jonasdottir, A.; Jonasdottir, A.; Stacey, S. N.; Magnusson, O. T.; Thorsteinsdottir, U.; Masson, G.; Kong, A.; Halldorsson, B. V.; Helgason, A.; Gudbjartsson, D. F.; Stefansson, K. Multiple transmissions of de novo mutations in families, Nature Genetics, Volume 50 (2018) no. 12, pp. 1674-1680 | DOI

[61] Kelleher, J.; Etheridge, A. M.; McVean, G. Efficient coalescent simulation and genealogical analysis for large sample sizes, PLOS Computational Biology, Volume 12 (2016) no. 5 | DOI

[62] Kelleher, J.; Thornton, K. R.; Ashander, J.; Ralph, P. L. Efficient pedigree recording for fast population genetics simulation, PLOS Computational Biology, Volume 14 (2018) no. 11 | DOI

[63] Kern, A. D.; Hahn, M. W. The neutral theory in light of natural selection, Molecular Biology and Evolution, Volume 35 (2018) no. 6, pp. 1366-1371 | DOI

[64] Kim, Y.-A.; Leiserson, M. D.; Moorjani, P.; Sharan, R.; Wojtowicz, D.; Przytycka, T. M. Mutational signatures: From methods to mechanisms, Annual Review of Biomedical Data Science, Volume 4 (2021) no. 1, pp. 189-206 | DOI

[65] Kimura, M. Evolutionary rate at the molecular level, Nature, Volume 217 (1968) no. 5129, pp. 624-626 | DOI

[66] Kingman, J. F. C. On the genealogy of large populations, Journal of Applied Probability, Volume 19 (1982) no. A, pp. 27-43 | DOI

[67] Lack, J. B.; Cardeno, C. M.; Crepeau, M. W.; Taylor, W.; Corbett-Detig, R. B.; Stevens, K. A.; Langley, C. H.; Pool, J. E. The Drosophila genome nexus: A population genomic resource of 623 Drosophila melanogaster genomes, including 197 from a single ancestral range population, Genetics, Volume 199 (2015) no. 4, pp. 1229-1241 | DOI

[68] Lawrie, D. S.; Messer, P. W.; Hershberg, R.; Petrov, D. A. Strong purifying selection at synonymous sites in D. melanogaster, PLoS Genetics, Volume 9 (2013) no. 5 | DOI

[69] Lewontin, R. The genetic basis of evolutionary change, Columbia University Press, 1974

[70] Li, H.; Durbin, R. Inference of human population history from individual whole-genome sequences, Nature, Volume 475 (2011) no. 7357, pp. 493-496 | DOI

[71] Lynch, M. Rate, molecular spectrum, and consequences of human mutation, Proceedings of the National Academy of Sciences, Volume 107 (2010) no. 3, pp. 961-968 | DOI

[72] Lynch, M. The cellular, developmental and population-genetic determinants of mutation-rate evolution, Genetics, Volume 180 (2008) no. 2, pp. 933-943 | DOI

[73] Lynch, M.; Ackerman, M. S.; Gout, J.-F.; Long, H.; Sung, W.; Thomas, W. K.; Foster, P. L. Genetic drift, selection and the evolution of the mutation rate, Nature Reviews Genetics, Volume 17 (2016) no. 11, pp. 704-714 | DOI

[74] Machado, H. E.; Lawrie, D. S.; Petrov, D. A. Pervasive strong selection at the level of codon usage bias in Drosophila melanogaster, Genetics, Volume 214 (2020) no. 2, pp. 511-528 | DOI

[75] Malaspinas, A.-S.; Westaway, M. C.; Muller, C.; Sousa, V. C.; Lao, O.; Alves, I.; Bergström, A.; Athanasiadis, G.; Cheng, J. Y.; Crawford, J. E.; Heupink, T. H.; Macholdt, E.; Peischl, S.; Rasmussen, S.; Schiffels, S.; Subramanian, S.; Wright, J. L.; Albrechtsen, A.; Barbieri, C.; Dupanloup, I.; Eriksson, A.; Margaryan, A.; Moltke, I.; Pugach, I.; Korneliussen, T. S.; Levkivskyi, I. P.; Moreno-Mayar, J. V.; Ni, S.; Racimo, F.; Sikora, M.; Xue, Y.; Aghakhanian, F. A.; Brucato, N.; Brunak, S.; Campos, P. F.; Clark, W.; Ellingvåg, S.; Fourmile, G.; Gerbault, P.; Injie, D.; Koki, G.; Leavesley, M.; Logan, B.; Lynch, A.; Matisoo-Smith, E. A.; McAllister, P. J.; Mentzer, A. J.; Metspalu, M.; Migliano, A. B.; Murgha, L.; Phipps, M. E.; Pomat, W.; Reynolds, D.; Ricaut, F.-X.; Siba, P.; Thomas, M. G.; Wales, T.; Wall, C. M.; Oppenheimer, S. J.; Tyler-Smith, C.; Durbin, R.; Dortch, J.; Manica, A.; Schierup, M. H.; Foley, R. A.; Lahr, M. M.; Bowern, C.; Wall, J. D.; Mailund, T.; Stoneking, M.; Nielsen, R.; Sandhu, M. S.; Excoffier, L.; Lambert, D. M.; Willerslev, E. A genomic history of Aboriginal Australia, Nature, Volume 538 (2016) no. 7624, pp. 207-214 | DOI

[76] Marjoram, P.; Wall, J. D. Fast "coalescent" simulation, BMC Genetics, Volume 7 (2006) no. 1 | DOI

[77] Martincorena, I.; Luscombe, N. M. Non-random mutation: The evolution of targeted hypermutation and hypomutation, BioEssays, Volume 35 (2013) no. 2, pp. 123-130 | DOI

[78] Matheson, J.; Masel, J. Unlinked background selection reduces neutral diversity more than linked background selection, bioRxiv (2023) | DOI

[79] McGaugh, S. E.; Heil, C. S. S.; Manzano-Winkler, B.; Loewe, L.; Goldstein, S.; Himmel, T. L.; Noor, M. A. F. Recombination modulates how selection affects linked sites in Drosophila, PLoS Biology, Volume 10 (2012) no. 11 | DOI

[80] McVean, G. The structure of linkage disequilibrium around a selective sweep, Genetics, Volume 175 (2007) no. 3, pp. 1395-1406 | DOI

[81] McVean, G. A.; Cardin, N. J. Approximating the coalescent with recombination, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 360 (2005) no. 1459, pp. 1387-1393 | DOI

[82] McVicker, G.; Gordon, D.; Davis, C.; Green, P. Widespread genomic signatures of natural selection in Hominid evolution, PLoS Genetics, Volume 5 (2009) no. 5 | DOI

[83] Möller, M.; Habig, M.; Lorrain, C.; Feurtey, A.; Haueisen, J.; Fagundes, W. C.; Alizadeh, A.; Freitag, M.; Stukenbrock, E. H. Recent loss of the Dim2 DNA methyltransferase decreases mutation rate in repeats and changes evolutionary trajectory in a fungal pathogen, PLOS Genetics, Volume 17 (2021) no. 3 | DOI

[84] Monroe, J. G.; Srikant, T.; Carbonell-Bejerano, P.; Becker, C.; Lensink, M.; Exposito-Alonso, M.; Klein, M.; Hildebrandt, J.; Neumann, M.; Kliebenstein, D.; Weng, M.-L.; Imbert, E.; Ågren, J.; Rutter, M. T.; Fenster, C. B.; Weigel, D. Mutation bias reflects natural selection in Arabidopsis thaliana, Nature, Volume 602 (2022) no. 7895, pp. 101-105 | DOI

[85] Moutinho, A. F.; Trancoso, F. F.; Dutheil, J. Y. The impact of protein architecture on adaptive evolution, Molecular Biology and Evolution, Volume 36 (2019) no. 9, pp. 2013-2028 | DOI

[86] Murphy, D. A.; Elyashiv, E.; Amster, G.; Sella, G. Broad-scale variation in human genetic diversity levels is predicted by purifying selection on coding and non-coding elements, eLife, Volume 11 (2022) | DOI

[87] Nei, M. Mutation-driven evolution, Oxford University Press, OUP Oxford, 2013

[88] Nordborg, M.; Charlesworth, B.; Charlesworth, D. The effect of recombination on background selection, Genetical Research, Volume 67 (1996) no. 2, pp. 159-174 | DOI

[89] Ohta, T. The nearly neutral theory of molecular evolution, Annual Review of Ecology and Systematics, Volume 23 (1992) no. 1, pp. 263-286 | DOI

[90] Oman, M.; Alam, A.; Ness, R. W. How sequence context-dependent mutability drives mutation rate variation in the genome, Genome Biology and Evolution, Volume 14 (2022) no. 3 | DOI

[91] Palamara, P. F.; Terhorst, J.; Song, Y. S.; Price, A. L. High-throughput inference of pairwise coalescence times identifies signals of selection and enriched disease heritability, Nature Genetics, Volume 50 (2018) no. 9, pp. 1311-1317 | DOI

[92] Pearl, J.; Mackenzie, D. The book of why: The new science of cause and effect, 1st ed. , Basic Books, Inc., United States of America, 2018

[93] Phung, T. N.; Huber, C. D.; Lohmueller, K. E. Determining the effect of natural selection on linked neutral divergence across species, PLOS Genetics, Volume 12 (2016) no. 8 | DOI

[94] Pouyet, F.; Gilbert, K. J. Towards an improved understanding of molecular evolution: the relative roles of selection, drift, and everything in between, Peer Community Journal, Volume 1 (2021) | DOI

[95] Powell, M. J. D. An efficient method for finding the minimum of a function of several variables without calculating derivatives, The Computer Journal, Volume 7 (1964) no. 2, pp. 155-162 | DOI

[96] Racimo, F. An unusual suspect: the mutation landscape as a determinant of local variation in nucleotide diversity (Recommendation), PCI Evolutionary Biology, 2023 | DOI

[97] Rasmussen, M. D.; Hubisz, M. J.; Gronau, I.; Siepel, A. Genome-wide inference of ancestral recombination graphs, PLoS Genetics, Volume 10 (2014) no. 5 | DOI

[98] Rosenberg, N. A.; Nordborg, M. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms, Nature Reviews Genetics, Volume 3 (2002) no. 5, pp. 380-390 | DOI

[99] Samuk, K.; Manzano-Winkler, B.; Ritz, K. R.; Noor, M. A. Natural selection shapes variation in genome-wide recombination rate in Drosophila pseudoobscura, Current Biology, Volume 30 (2020) no. 8 | DOI

[100] Schiffels, S.; Durbin, R. Inferring human population size and separation history from multiple genome sequences, Nature Genetics, Volume 46 (2014) no. 8, pp. 919-925 | DOI

[101] Schiffels, S.; Wang, K. MSMC and MSMC2: The multiple sequentially Markovian coalescent, Methods in Molecular Biology, Springer US, New York, NY, 2020, pp. 147-166 | DOI

[102] Schlichta, F.; Peischl, S.; Excoffier, L. The impact of genetic surfing on neutral genomic diversity, Molecular Biology and Evolution, Volume 39 (2022) no. 11 | DOI

[103] Sellinger, T. P. P.; Abu Awad, D.; Moest, M.; Tellier, A. Inference of past demography, dormancy and self-fertilization rates from whole genome sequence data, PLOS Genetics, Volume 16 (2020) no. 4 | DOI

[104] Slatkin, M. Linkage disequilibrium — understanding the evolutionary past and mapping the medical future, Nature Reviews Genetics, Volume 9 (2008) no. 6, pp. 477-485 | DOI

[105] Smith, J. M.; Haigh, J. The hitch-hiking effect of a favourable gene, Genetics Research, Volume 23 (1974), pp. 23-35 | DOI

[106] Smith, T. C. A.; Arndt, P. F.; Eyre-Walker, A. Large scale variation in the rate of germ-line de novo mutation, base composition, divergence and diversity in humans, PLOS Genetics, Volume 14 (2018) no. 3 | DOI

[107] Spence, J. P.; Steinrücken, M.; Terhorst, J.; Song, Y. S. Inference of population history using coalescent HMMs: Review and outlook, Current Opinion in Genetics & Development, Volume 53 (2018), pp. 70-76 | DOI

[108] Staab, P. R.; Zhu, S.; Metzler, D.; Lunter, G. scrm: Efficiently simulating long sequences using the approximated coalescent with recombination, Bioinformatics, Volume 31 (2015) no. 10, pp. 1680-1682 | DOI

[109] Stankowski, S.; Chase, M. A.; Fuiten, A. M.; Rodrigues, M. F.; Ralph, P. L.; Streisfeld, M. A. Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers, PLOS Biology, Volume 17 (2019) no. 7 | DOI

[110] Stephan, W.; Wiehe, T. H.; Lenz, M. W. The effect of strongly selected substitutions on neutral polymorphism: Analytical results based on diffusion theory, Theoretical Population Biology, Volume 41 (1992) no. 2, pp. 237-254 | DOI

[111] Stern, A. J.; Wilton, P. R.; Nielsen, R. An approximate full-likelihood method for inferring selection and allele frequency trajectories from DNA sequence data, PLOS Genetics, Volume 15 (2019) no. 9 | DOI

[112] Sung, W.; Ackerman, M. S.; Miller, S. F.; Doak, T. G.; Lynch, M. Drift-barrier hypothesis and mutation-rate evolution, Proceedings of the National Academy of Sciences, Volume 109 (2012) no. 45, pp. 18488-18492 | DOI

[113] Terhorst, J.; Kamm, J. A.; Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes, Nature Genetics, Volume 49 (2017) no. 2, pp. 303-309 | DOI

[114] Venkat, A.; Hahn, M. W.; Thornton, J. W. Multinucleotide mutations cause false inferences of lineage-specific positive selection, Nature Ecology & Evolution, Volume 2 (2018) no. 8, pp. 1280-1288 | DOI

[115] Wiehe, T.; Stephan, W. Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster., Molecular Biology and Evolution, Volume 10 (1993) no. 4, pp. 842-854 | DOI

[116] Wiuf, C.; Hein, J. Recombination as a point process along sequences, Theoretical Population Biology, Volume 55 (1999) no. 3, pp. 248-259 | DOI

[117] Zeng, K.; Charlesworth, B. The joint effects of background selection and genetic recombination on local gene genealogies, Genetics, Volume 189 (2011) no. 1, pp. 251-266 | DOI

[118] Zeng, K.; Jackson, B. C.; Barton, H. J. Methods for estimating demography and detecting between-locus differences in the effective population size and mutation rate, Molecular Biology and Evolution, Volume 36 (2018) no. 2, pp. 423-433 | DOI

Cited by Sources: