Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology
The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing
10.24072/pcjournal.238 - Peer Community Journal, Volume 3 (2023), article no. e14.
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Large regions of suppressed recombination having extended over time occur in many organisms around genes involved in mating compatibility (sex-determining or mating-type genes). The sheltering of deleterious alleles has been proposed to be involved in such expansions. However, the dynamics of deleterious mutations partially linked to genes involved in mating compatibility are not well understood, especially in finite populations. In particular, under what conditions deleterious mutations are likely to be maintained for long enough near mating-compatibility genes remains to be evaluated, especially under selfing, which generally increases the purging rate of deleterious mutations. Using a branching process approximation, we studied the fate of a new deleterious or overdominant mutation in a diploid population, considering a locus carrying two permanently heterozygous mating-type alleles, and a partially linked locus at which the mutation appears. We obtained analytical and numerical results on the probability and purging time of the new mutation. We investigated the impact of recombination between the two loci and of the mating system (outcrossing, intra and inter-tetrad selfing) on the maintenance of the mutation. We found that the presence of a fungal-like mating-type locus (i.e. not preventing diploid selfing) always sheltered the mutation under selfing, i.e. it decreased the purging probability and increased the purging time of the mutations. The sheltering effect was higher in case of automixis (intra-tetrad selfing). This may contribute to explain why evolutionary strata of recombination suppression near the mating-type locus are found mostly in automictic (pseudo-homothallic) fungi. We also showed that rare events of deleterious mutation maintenance during strikingly long evolutionary times could occur, suggesting that deleterious mutations can indeed accumulate near the mating-type locus over evolutionary time scales. In conclusion, our results show that, although selfing purges deleterious mutations, these mutations can be maintained for very long times near a mating-type locus, which may contribute to promote the evolution of recombination suppression in sex-related chromosomes.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_238,
author = {Tezenas, Emilie and Giraud, Tatiana and V\'eber, Amandine and Billiard, Sylvain},
title = {The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing},
journal = {Peer Community Journal},
eid = {e14},
publisher = {Peer Community In},
volume = {3},
year = {2023},
doi = {10.24072/pcjournal.238},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.238/}
}
TY - JOUR AU - Tezenas, Emilie AU - Giraud, Tatiana AU - Véber, Amandine AU - Billiard, Sylvain TI - The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing JO - Peer Community Journal PY - 2023 VL - 3 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.238/ DO - 10.24072/pcjournal.238 ID - 10_24072_pcjournal_238 ER -
%0 Journal Article %A Tezenas, Emilie %A Giraud, Tatiana %A Véber, Amandine %A Billiard, Sylvain %T The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing %J Peer Community Journal %D 2023 %V 3 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.238/ %R 10.24072/pcjournal.238 %F 10_24072_pcjournal_238
Tezenas, Emilie; Giraud, Tatiana; Véber, Amandine; Billiard, Sylvain. The fate of recessive deleterious or overdominant mutations near mating-type loci under partial selfing. Peer Community Journal, Volume 3 (2023), article no. e14. doi : 10.24072/pcjournal.238. https://peercommunityjournal.org/articles/10.24072/pcjournal.238/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100635
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] The double edged sword: The demographic consequences of the evolution of self-fertilization, Evolution, Volume 71 (2017) no. 5, pp. 1178-1190 | DOI
[2] Effects of partial selfing on the equilibrium genetic variance, mutation load, and inbreeding depression under stabilizing selection, Evolution, Volume 72 (2018) no. 4, pp. 751-769 | DOI
[3] Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression | DOI
[4] Theoretical Population Genetics of Mating-Type Linked Haplo-Lethal Alleles, International Journal of Plant Sciences, Volume 159 (1998) no. 2, pp. 192-198 | DOI
[5] Intratetrad mating and the evolution of linkage relationships, Evolution, Volume 58 (2004) no. 4, pp. 702-709 | DOI
[6] The Evolution of Selfing Is Accompanied by Reduced Efficacy of Selection and Purging of Deleterious Mutations, Genetics, Volume 199 (2014) no. 3, pp. 817-829 | DOI
[7] Branching Processes, Springer Berlin Heidelberg, Berlin, Heidelberg, 1972 | DOI
[8] Sur l’extinction des populations avec plusieurs types dans un environnement aléatoire, Comptes Rendus Biologies, Volume 341 (2018) no. 3, pp. 145-151 | DOI
[9] Little Evidence of Antagonistic Selection in the Evolutionary Strata of Fungal Mating-Type Chromosomes (Microbotryum lychnidis-dioicae), G3 Genes|Genomes|Genetics, Volume 9 (2019) no. 6, pp. 1987-1998 | DOI
[10] The evolution of restricted recombination in sex chromosomes, Trends in Ecology & Evolution, Volume 24 (2009) no. 2, pp. 94-102 | DOI
[11] Sex, outcrossing and mating types: unsolved questions in fungi and beyond, Journal of Evolutionary Biology, Volume 25 (2012) no. 6, pp. 1020-1038 | DOI
[12] Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 27, pp. 7067-7072 | DOI
[13] Multiple convergent supergene evolution events in mating-type chromosomes, Nature Communications, Volume 9 (2018) no. 1 | DOI
[14] Multilocus population-genetic theory, Theoretical Population Biology, Volume 133 (2020), pp. 40-48 | DOI
[15] Effects of partial inbreeding on fixation rates and variation of mutant genes., Genetics, Volume 131 (1992) no. 2, pp. 493-507 | DOI
[16] Polymorphic evolution sequence and evolutionary branching, Probability Theory and Related Fields, Volume 151 (2010) no. 1-2, pp. 45-94 | DOI
[17] Inbreeding, heterozygote advantage and the evolution of neo–X and neo–Y sex chromosomes, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 266 (1999) no. 1414, pp. 51-56 | DOI
[18] Inbreeding depression and its evolutionary consequences, Annual Review of Ecology and Systematics, Volume 18 (1987) no. 1, pp. 237-268 | DOI
[19] Inbreeding Depression, Genetic Load, and the Evolution of Outcrossing Rates in a Multilocus System with No Linkage, Evolution, Volume 44 (1990) no. 6 | DOI
[20] Breeding systems and genome evolution, Current Opinion in Genetics & Development, Volume 11 (2001) no. 6, pp. 685-690 | DOI
[21] Steps in the evolution of heteromorphic sex chromosomes, Heredity, Volume 95 (2005) no. 2, pp. 118-128 | DOI
[22] Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species, Evolution, Volume 75 (2021) no. 8, pp. 1920-1935 | DOI
[23] A rigorous model study of the adaptive dynamics of Mendelian diploids, Journal of Mathematical Biology, Volume 67 (2012) no. 3, pp. 569-607 | DOI
[24] Quantifying the Mutational Meltdown in Diploid Populations, The American Naturalist, Volume 181 (2013) no. 5, pp. 623-636 | DOI
[25] Stochastic Modeling of Density-Dependent Diploid Populations and the Extinction Vortex, Advances in Applied Probability, Volume 46 (2014) no. 2, pp. 446-477 | DOI
[26] Searching for signatures of sexually antagonistic selection on stickleback sex chromosomes, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 377 (2022) no. 1856 | DOI
[27] Approximating selective sweeps, Theoretical Population Biology, Volume 66 (2004) no. 2, pp. 129-138 | DOI
[28] Probability Models for DNA Sequence Evolution, Probability and its Applications, Springer New York, New York, NY, 2008 | DOI
[29] The Probability of Fixation of a Mutant: The Two-Locus Case, Evolution, Volume 21 (1967) no. 3 | DOI
[30] Some Applications of Multiple-Type Branching Processes in Population Genetics, Journal of the Royal Statistical Society: Series B (Methodological), Volume 30 (1968) no. 1, pp. 164-175 | DOI
[31] Mathematical Population Genetics, Interdisciplinary Applied Mathematics, Springer New York, New York, NY, 2004 | DOI
[32] Selection for linkage modification: I. Random mating populations, Theoretical Population Biology, Volume 3 (1972) no. 3, pp. 324-346 | DOI
[33] Mating-Type Locus Organization and Mating-Type Chromosome Differentiation in the Bipolar Edible Button Mushroom Agaricus bisporus, Genes, Volume 12 (2021) no. 7 | DOI
[34] Convergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms, PLoS Biology, Volume 2 (2004) no. 12 | DOI
[35] A general method for numerically simulating the stochastic time evolution of coupled chemical reactions, Journal of Computational Physics, Volume 22 (1976) no. 4, pp. 403-434 | DOI
[36] Mating Systems and the Efficacy of Selection at the Molecular Level, Genetics, Volume 177 (2007) no. 2, pp. 905-916 | DOI
[37] Harris, T. E. (1964). The theory of branching processes [OCLC: 931719544]. Springer-Verlag.
[38] Recombination and hitchhiking of deleterious alleles, Evolution, Volume 65 (2011) no. 9, pp. 2421-2434 | DOI
[39] Hitchhiking of Deleterious Alleles and the Cost of Adaptation in Partially Selfing Species, Genetics, Volume 196 (2014) no. 1, pp. 281-293 | DOI
[40] Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence, Molecular Biology and Evolution, Volume 37 (2019) no. 3, pp. 668-682 | DOI
[41] Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes, New Phytologist, Volume 229 (2020) no. 5, pp. 2470-2491 | DOI
[42] Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex, Molecular Biology and Evolution, Volume 38 (2021) no. 6, pp. 2475-2492 | DOI
[43] Extinction Times in Multitype Markov Branching Processes, Journal of Applied Probability, Volume 46 (2009) no. 1, pp. 296-307 | DOI
[44] Selection in complex genetic systems. VI. Equilibrium properties of two locus selection models with partial selfing, Theoretical Population Biology, Volume 28 (1985) no. 1, pp. 117-132 | DOI
[45] Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea), Heredity, Volume 85 (2000) no. 3, pp. 231-241 | DOI
[46] No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution, BioEssays, Volume 32 (2010) no. 8, pp. 718-726 | DOI
[47] Mutation load at a mimicry supergene sheds new light on the evolution of inversion polymorphisms, Nature Genetics, Volume 53 (2021) no. 3, pp. 288-293 | DOI
[48] Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes, PLOS Biology, Volume 20 (2022) no. 7 | DOI
[49] A neutral model for the loss of recombination on sex chromosomes, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 376 (2021) no. 1832 | DOI
[50] Rapid genetic mapping in Neurospora crassa, Fungal Genetics and Biology, Volume 44 (2007) no. 6, pp. 455-465 | DOI
[51] General two-locus selection models: Some objectives, results and interpretations, Theoretical Population Biology, Volume 7 (1975) no. 3, pp. 364-398 | DOI
[52] A Limit Theorem for Multidimensional Galton-Watson Processes, The Annals of Mathematical Statistics, Volume 37 (1966) no. 5, pp. 1211-1223 | DOI
[53] Average time until fixation of a mutant allele in a finite population under continued mutation pressure: Studies by analytical, numerical, and pseudo-sampling methods, Proceedings of the National Academy of Sciences, Volume 77 (1980) no. 1, pp. 522-526 | DOI
[54] Preface, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 376 (2021) no. 1832 | DOI
[55] Genetic Linkage Maps and Genomic Organization in Leptosphaeria maculans, European Journal of Plant Pathology, Volume 114 (2006) no. 1, pp. 17-31 | DOI
[56] Maintenance of Quantitative Genetic Variance Under Partial Self-Fertilization, with Implications for Evolution of Selfing, Genetics, Volume 200 (2015) no. 3, pp. 891-906 | DOI
[57] Linkage disequilibrium and gametophytic self-incompatibility, Theoretical and Applied Genetics, Volume 73 (1986) no. 1, pp. 102-112 | DOI
[58] Y recombination arrest and degeneration in the absence of sexual dimorphism, Science, Volume 375 (2022) no. 6581, pp. 663-666 | DOI
[59] Excess of Deleterious Mutations around HLA Genes Reveals Evolutionary Cost of Balancing Selection, Molecular Biology and Evolution, Volume 33 (2016) no. 10, pp. 2555-2564 | DOI
[60] The Sheltered Genetic Load Linked to the S Locus in Plants: New Insights From Theoretical and Empirical Approaches in Sporophytic Self-Incompatibility, Genetics, Volume 183 (2009) no. 3, pp. 1105-1118 | DOI
[61] Genetic architecture and balancing selection: the life and death of differentiated variants, Molecular Ecology, Volume 26 (2017) no. 9, pp. 2430-2448 | DOI
[62] Genetic linkage map of Phaeosphaeria nodorum, the causal agent of stagonospora nodorum blotch disease of wheat, European Journal of Plant Pathology, Volume 124 (2009) no. 4, pp. 681-690 | DOI
[63] The Mating-Type Chromosome in the Filamentous Ascomycete Neurospora tetrasperma Represents a Model for Early Evolution of Sex Chromosomes, PLoS Genetics, Volume 4 (2008) no. 3 | DOI
[64] Mode, C. J. (1971). Multitype branching processes: Theory and applications. American Elsevier Pub. Co.
[65] Extinction time of deleterious mutant genes in large populations, Theoretical Population Biology, Volume 2 (1971) no. 4, pp. 419-425 | DOI
[66] A Gradual Process of Recombination Restriction in the Evolutionary History of the Sex Chromosomes in Dioecious Plants, PLoS Biology, Volume 3 (2004) no. 1 | DOI
[67] Detrimental genes with partial selfing and effects on a neutral locus, Genetical Research, Volume 23 (1974) no. 2, pp. 191-200 | DOI
[68] Consequences of partially recessive deleterious genetic variation for the evolution of inversions suppressing recombination between sex chromosomes, Evolution, Volume 76 (2022) no. 6, pp. 1320-1330 | DOI
[69] Selection on a Modifier of Recombination Rate Due to Linked Deleterious Mutations, Journal of Heredity, Volume 93 (2002) no. 1, pp. 22-26 | DOI
[70] Pénisson, S. (2010). Conditional limit theorems for multitype branching processes and illustration in epidemiological risk analysis (Doctoral dissertation). Universität Potsdam, Université Paris-Sud.
[71] Mapping the mating type locus ofAscochyta rabiei, the causal agent of ascochyta blight of chickpea, Molecular Plant Pathology, Volume 4 (2003) no. 5, pp. 373-381 | DOI
[72] On the Theory of Partially Inbreeding Finite Populations. I. Partial Selfing, Genetics, Volume 117 (1987) no. 2, pp. 353-360 | DOI
[73] On the theory of partially inbreeding finite populations. III. Fixation probabilities under partial selfing when heterozygotes are intermediate in viability., Genetics, Volume 131 (1992) no. 4, pp. 979-985 | DOI
[74] On the use of the direct matrix product in analysing certain stochastic population models, Biometrika, Volume 53 (1966) no. 3-4, pp. 397-415 | DOI
[75] The Multi-Type Galton-Watson Process in a Genetical Context, Biometrics, Volume 24 (1968) no. 1 | DOI
[76] Why Do Sex Chromosomes Stop Recombining?, Trends in Genetics, Volume 34 (2018) no. 7, pp. 492-503 | DOI
[77] Moments and order statistics of extinction times in multitype branching processes and their relation to random selection models, Bulletin of Mathematical Biology, Volume 47 (1985) no. 2, pp. 263-272 | DOI
[78] Rice, S. H. (2004). Evolutionary theory: Mathematical and conceptual foundations. Sinauer Associates.
[79] The Accumulation of Sexually Antagonistic Genes as a Selective Agent Promoting the Evolution of Reduced Recombination between Primitive Sex Chromosomes, Evolution, Volume 41 (1987) no. 4 | DOI
[80] The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics, Evolution Letters, Volume 4 (2020) no. 5, pp. 398-415 | DOI
[81] Verzweigungsprozesse, Mathematische Nachrichten, Volume 67 (1975) no. 22 | DOI
[82] Genome organization of Magnaporthe grisea: genetic map, electrophoretic karyotype, and occurrence of repeated DNAs, Theoretical and Applied Genetics, Volume 87 (1993) no. 5, pp. 545-557 | DOI
[83] Evolution under tight linkage to mating type, New Phytologist, Volume 165 (2004) no. 1, pp. 63-70 | DOI
[84] Stepwise recombination suppression around the mating-type locus in the fungus Schizothecium tetrasporum (Ascomycota, Sordariales), bioRxiv (2023) | DOI
[85] Wolfram Research, I. (2015). Mathematica (Version 10.1). Champaign, IL, 2015.
[86] How to make a sex chromosome, Nature Communications, Volume 7 (2016) no. 1 | DOI
[87] Genomic Consequences of Outcrossing and Selfing in Plants, International Journal of Plant Sciences, Volume 169 (2008) no. 1, pp. 105-118 | DOI
[88] Evolution of a supergene that regulates a trans-species social polymorphism, Nature Ecology Evolution, Volume 4 (2020) no. 2, pp. 240-249 | DOI
[89] A Molecular Genetic Map and Electrophoretic Karyotype of the Plant Pathogenic Fungus Cochliobolus sativus, Molecular Plant-Microbe Interactions, Volume 15 (2002) no. 5, pp. 481-492 | DOI
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