Evolutionary Biology

Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression

10.24072/pcjournal.224 - Peer Community Journal, Volume 3 (2023), article no. e8.

Get full text PDF Peer reviewed and recommended by PCI

Classical models that ignore linkage predict that deleterious recessive mutations should purge or fix within inbred populations, yet inbred populations often retain moderate to high segregating load. True overdominance could generate balancing selection strong enough to sustain inbreeding depression even within inbred populations, but this is considered rare. However, arrays of deleterious recessives linked in repulsion could generate appreciable pseudo-overdominance that would also sustain segregating load. We used simulations to explore how long pseudo-overdominant (POD) zones persist once created (e.g., by hybridization between populations fixed for alternative mildly deleterious mutations). Balanced haplotype loads, tight linkage, and moderate to strong cumulative selective effects all serve to maintain POD zones. Tight linkage is key, suggesting that such regions are most likely to arise and persist in low recombination regions (like inversions). Selection and drift unbalance the load, eventually eliminating POD zones, but this process is quite slow under strong pseudo-overdominance. Background selection accelerates the loss of weak POD zones but reinforces strong ones in inbred populations by disfavoring homozygotes. Models and empirical studies of POD dynamics within populations help us understand how POD zones may allow the load to persist, greatly affecting load dynamics and mating systems evolution

Published online:
DOI: 10.24072/pcjournal.224
Abu-Awad, Diala 1, 2; Waller, Donald 3

1 Université Paris-Saclay, INRAE, CNRS, AgroParisTech, GQE—Le Moulon, Gif-sur-Yvette, France
2 Professorship for Population Genetics, Department of Life Science Systems, Technical University of Munich, Germany
3 Department of Botany, University of Wisconsin, Madison, WI USA
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Abu-Awad, Diala and Waller, Donald},
     title = {Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression},
     journal = {Peer Community Journal},
     eid = {e8},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.224},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.224/}
AU  - Abu-Awad, Diala
AU  - Waller, Donald
TI  - Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.224/
UR  - https://doi.org/10.24072/pcjournal.224
DO  - 10.24072/pcjournal.224
ID  - 10_24072_pcjournal_224
ER  - 
%0 Journal Article
%A Abu-Awad, Diala
%A Waller, Donald
%T Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.224
%R 10.24072/pcjournal.224
%F 10_24072_pcjournal_224
Abu-Awad, Diala; Waller, Donald. Conditions for maintaining and eroding pseudo-overdominance and its contribution to inbreeding depression. Peer Community Journal, Volume 3 (2023), article  no. e8. doi : 10.24072/pcjournal.224. https://peercommunityjournal.org/articles/10.24072/pcjournal.224/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100531

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] Abu Awad, D.; Waller, D. M. POD selection - individual based model, Zenodo (2022) | DOI

[2] Baldwin, S. J.; Schoen, D. J. Inbreeding depression is difficult to purge in self‐incompatible populations of Leavenworthia alabamica, New Phytologist, Volume 224 (2019) no. 3, pp. 1330-1338 | DOI

[3] Bataillon, T.; Kirkpatrick, M. Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter, Genetical Research, Volume 75 (2000) no. 1, pp. 75-81 | DOI

[4] Bernstein, M. R.; Zdraljevic, S.; Andersen, E. C.; Rockman, M. V. Tightly linked antagonistic‐effect loci underlie polygenic phenotypic variation in <i>C. elegans</i>, Evolution Letters, Volume 3 (2019) no. 5, pp. 462-473 | DOI

[5] Brandenburg, J.-T.; Mary-Huard, T.; Rigaill, G.; Hearne, S. J.; Corti, H.; Joets, J.; Vitte, C.; Charcosset, A.; Nicolas, S. D.; Tenaillon, M. I. Independent introductions and admixtures have contributed to adaptation of European maize and its American counterparts, PLOS Genetics, Volume 13 (2017) no. 3 | DOI

[6] Brown, K. E.; Kelly, J. K. Severe inbreeding depression is predicted by the "rare allele load" in Mimulus guttatus, Evolution, Volume 74 (2020) no. 3, pp. 587-596 | DOI

[7] Byers, D. L.; Waller, D. M. Do Plant Populations Purge Their Genetic Load? Effects of Population Size and Mating History on Inbreeding Depression, Annual Review of Ecology and Systematics, Volume 30 (1999) no. 1, pp. 479-513 | DOI

[8] Charlesworth, B. Mutational load, inbreeding depression and heterosis in subdivided populations, Molecular Ecology, Volume 27 (2018) no. 24, pp. 4991-5003 | DOI

[9] Charlesworth, B.; Nordborg, M.; Charlesworth, D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations, Genetical Research, Volume 70 (1997) no. 2, pp. 155-174 | DOI

[10] Charlesworth, D.; Charlesworth, B. Inbreeding depression and its evolutionary consequences, Annual Review of Ecology and Systematics, Volume 18 (1987) no. 1, pp. 237-268 | DOI

[11] Charlesworth, D.; Charlesworth, B. Inbreeding Depression with Heterozygote Advantage and its Effect on Selection for Modifiers Changing the Outcrossing Rate, Evolution, Volume 44 (1990) no. 4 | DOI

[12] Chelo, I. M.; Afonso, B.; Carvalho, S.; Theologidis, I.; Goy, C.; Pino-Querido, A.; Proulx, S. R.; Teotónio, H. Partial Selfing Can Reduce Genetic Loads While Maintaining Diversity During Experimental Evolution, G3 Genes|Genomes|Genetics, Volume 9 (2019) no. 9, pp. 2811-2821 | DOI

[13] Crow, J. F. Mutation, mean fitness, and genetic load, Oxford Series in Evol. Biol., Volume 9 (1993), pp. 3-42

[14] Crow, J. F.; Kimura, M. An Introduction to Population Genetics Theory, Burgess Pub. Co., 1970

[15] Crow, J. F. The Rise and Fall of Overdominance, Plant Breeding Reviews, John Wiley & Sons, Inc., Oxford, UK, 2010, pp. 225-257 | DOI

[16] Darwin, C. The effects of cross and self fertilization in the vegetable kingdom, J. Murray and Co, 1876

[17] David, P. Heterozygosity–fitness correlations: new perspectives on old problems, Heredity, Volume 80 (1998) no. 5, pp. 531-537 | DOI

[18] Ehiobu, N. G.; Goddard, M. E.; Taylor, J. F. Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster, Theoretical and Applied Genetics, Volume 77 (1989) no. 1, pp. 123-127 | DOI

[19] Fisher, R. A. The genetical theory of natural selection, Clarendon Press, Oxford, 1930 | DOI

[20] Gabriel, W.; Lynch, M.; Bürger, R. Muller's ratchet and mutational meltdowns, Evolution, Volume 47 (1993) no. 6, pp. 1744-1757 | DOI

[21] Garrigan, D.; Hedrick, P. W. Perspective: detecting adaptive molecular polymorphism: lessons from the mhc, Evolution, Volume 57 (2003) no. 8 | DOI

[22] Gemmell, N. J.; Slate, J. Heterozygote Advantage for Fecundity, PLoS ONE, Volume 1 (2006) no. 1 | DOI

[23] Gilbert, K. J.; Pouyet, F.; Excoffier, L.; Peischl, S. Transition from Background Selection to Associative Overdominance Promotes Diversity in Regions of Low Recombination, Current Biology, Volume 30 (2020) no. 1 | DOI

[24] Glémin, S. Balancing selection in self‐fertilizing populations, Evolution, Volume 75 (2021) no. 5, pp. 1011-1029 | DOI

[25] Harkness, A.; Brandvain, Y.; Goldberg, E. E. The evolutionary response of mating system to heterosis, Journal of Evolutionary Biology, Volume 32 (2019) no. 5, pp. 476-490 | DOI

[26] Hedrick, P. W.; Garcia-Dorado, A. Understanding Inbreeding Depression, Purging, and Genetic Rescue, Trends in Ecology &amp; Evolution, Volume 31 (2016) no. 12, pp. 940-952 | DOI

[27] Hedrick, P. W.; Hellsten, U.; Grattapaglia, D. Examining the cause of high inbreeding depression: analysis of whole‐genome sequence data in 28 selfed progeny of <i>Eucalyptus grandis</i>, New Phytologist, Volume 209 (2016) no. 2, pp. 600-611 | DOI

[28] Hill, W. G.; Robertson, A. The effect of linkage on limits to artificial selection, Genetics Research, Volume 89 (2007) no. 5-6, pp. 311-336 | DOI

[29] Igic, B.; Lande, R.; Kohn, J. R. Loss of Self‐Incompatibility and Its Evolutionary Consequences, International Journal of Plant Sciences, Volume 169 (2008) no. 1, pp. 93-104 | DOI

[30] Jay, P.; Chouteau, M.; Whibley, A.; Bastide, H.; Parrinello, H.; Llaurens, V.; Joron, M. 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

[31] Kardos, M.; Allendorf, F. W.; Luikart, G. Evaluating the role of inbreeding depression in heterozygosity-fitness correlations: how useful are tests for identity disequilibrium?, Molecular Ecology Resources, Volume 14 (2014) no. 3, pp. 519-530 | DOI

[32] Kim, B. Y.; Huber, C. D.; Lohmueller, K. E. Deleterious variation shapes the genomic landscape of introgression, PLOS Genetics, Volume 14 (2018) no. 10 | DOI

[33] Kimura, M.; Ohta, T. Theoretical Aspects of Population Genetics, monographs edn., Princeton University Press, 1971

[34] Kirkpatrick, M. How and Why Chromosome Inversions Evolve, PLoS Biology, Volume 8 (2010) no. 9 | DOI

[35] Kirkpatrick, M.; Jarne, P. The Effects of a Bottleneck on Inbreeding Depression and the Genetic Load, The American Naturalist, Volume 155 (2000) no. 2, pp. 154-167 | DOI

[36] Kremling, K. A. G.; Chen, S.-Y.; Su, M.-H.; Lepak, N. K.; Romay, M. C.; Swarts, K. L.; Lu, F.; Lorant, A.; Bradbury, P. J.; Buckler, E. S. Dysregulation of expression correlates with rare-allele burden and fitness loss in maize, Nature, Volume 555 (2018) no. 7697, pp. 520-523 | DOI

[37] Lande, R.; Schemske, D. W. The Evolution of Self-Fertilization and Inbreeding Depression in Plants. I. Genetic Models, Evolution, Volume 39 (1985) no. 1 | DOI

[38] Larièpe, A.; Mangin, B.; Jasson, S.; Combes, V.; Dumas, F.; Jamin, P.; Lariagon, C.; Jolivot, D.; Madur, D.; Fiévet, J.; Gallais, A.; Dubreuil, P.; Charcosset, A.; Moreau, L. The Genetic Basis of Heterosis: Multiparental Quantitative Trait Loci Mapping Reveals Contrasted Levels of Apparent Overdominance Among Traits of Agronomical Interest in Maize (<i>Zea mays</i> L.), Genetics, Volume 190 (2012) no. 2, pp. 795-811 | DOI

[39] Lewontin, R. C. The Genetic Basis of Evolutionary Change, Columbia University Press, 1974

[40] Llaurens, V.; Gonthier, L.; Billiard, S. 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

[41] Mable, B. K. Genetic causes and consequences of the breakdown of self-incompatibility: case studies in the Brassicaceae, Genetics Research, Volume 90 (2008) no. 1, pp. 47-60 | DOI

[42] McMullen, M. D.; Kresovich, S.; Villeda, H. S.; Bradbury, P.; Li, H.; Sun, Q.; Flint-Garcia, S.; Thornsberry, J.; Acharya, C.; Bottoms, C.; Brown, P.; Browne, C.; Eller, M.; Guill, K.; Harjes, C.; Kroon, D.; Lepak, N.; Mitchell, S. E.; Peterson, B.; Pressoir, G.; Romero, S.; Rosas, M. O.; Salvo, S.; Yates, H.; Hanson, M.; Jones, E.; Smith, S.; Glaubitz, J. C.; Goodman, M.; Ware, D.; Holland, J. B.; Buckler, E. S. Genetic Properties of the Maize Nested Association Mapping Population, Science, Volume 325 (2009) no. 5941, pp. 737-740 | DOI

[43] Ohta, T.; Cockerham, C. C. Detrimental genes with partial selfing and effects on a neutral locus, Genetical Research, Volume 23 (1974) no. 2, pp. 191-200 | DOI

[44] Ohta, T.; Kimura, M. Linkage disequilibrium at steady state determined by random genetic drift and recurrent mutation, Genetics, Volume 63 (1969) no. 1, pp. 229-238 | DOI

[45] Olito, C.; Ponnikas, S.; Hansson, B.; Abbott, J. K. 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

[46] Rocheleau, G.; Lessard, S. Stability analysis of the partial selfing selection model, Journal of Mathematical Biology, Volume 40 (2000) no. 6, pp. 541-574 | DOI

[47] Roze, D. Effects of Interference Between Selected Loci on the Mutation Load, Inbreeding Depression, and Heterosis, Genetics, Volume 201 (2015) no. 2, pp. 745-757 | DOI

[48] Seymour, D. K.; Chae, E.; Grimm, D. G.; Martín Pizarro, C.; Habring-Müller, A.; Vasseur, F.; Rakitsch, B.; Borgwardt, K. M.; Koenig, D.; Weigel, D. Genetic architecture of nonadditive inheritance in Arabidopsis thaliana hybrids, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 46 | DOI

[49] Sianta, S. A.; Peischl, S.; Moeller, D. A.; Brandvain, Y. Genetic load may increase or decrease with selfing depending upon the recombination environment, 2021 | DOI

[50] Spigler, R. B.; Theodorou, K.; Chang, S. Inbreeding depression and drift load in small populations at demographic disequilibrium, Evolution, Volume 71 (2017) no. 1, pp. 81-94 | DOI

[51] Sved, J. Linkage disequilibrium and homozygosity of chromosome segments in finite populations, Theoretical Population Biology, Volume 2 (1971) no. 2, pp. 125-141 | DOI

[52] Takebayashi, N. Patterns of Variation Within Self-Incompatibility Loci, Molecular Biology and Evolution, Volume 20 (2003) no. 11, pp. 1778-1794 | DOI

[53] Tallmon, D.; Luikart, G.; Waples, R. The alluring simplicity and complex reality of genetic rescue, Trends in Ecology &amp; Evolution, Volume 19 (2004) no. 9, pp. 489-496 | DOI

[54] Uyenoyama, M.; Holsinger, K. E.; Waller, D. M. Ecological and genetic factors directing the evolution of self-fertilization, Oxford Surveys in Evolutionary Biology, Volume 9 (1993), pp. 327-381

[55] Uyenoyama, M. K.; Waller, D. M. Coevolution of self-fertilization and inbreeding depression II. Symmetric overdominance in viability, Theoretical Population Biology, Volume 40 (1991) no. 1, pp. 47-77 | DOI

[56] van Oosterhout, C.; Zulstra, W. G.; van Heuven, M. K.; Brakefield, P. M. Inbreeding depression and genetic load in laboratory metapopulations of the butterfly bicyclus anynana, Evolution, Volume 54 (2000) no. 1, pp. 218-225 | DOI

[57] Waller, D. M. Addressing Darwin's dilemma: Can pseudo‐overdominance explain persistent inbreeding depression and load?, Evolution, Volume 75 (2021) no. 4, pp. 779-793 | DOI

[58] Whitlock, M. C.; Ingvarsson, P. K.; Hatfield, T. Local drift load and the heterosis of interconnected populations, Heredity, Volume 84 (2000) no. 4, pp. 452-457 | DOI

[59] Wickham, H. ggplot2, Use R!, Springer International Publishing, Cham, 2016 | DOI

[60] Willi, Y.; Griffin, P.; Van Buskirk, J. Drift load in populations of small size and low density, Heredity, Volume 110 (2013) no. 3, pp. 296-302 | DOI

[61] Winn, A. A.; Elle, E.; Kalisz, S.; Cheptou, P.-O.; Eckert, C. G.; Goodwillie, C.; Johnston, M. O.; Moeller, D. A.; Ree, R. H.; Sargent, R. D.; Vallejo-Marín, M. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating, Evolution, Volume 65 (2011) no. 12, pp. 3339-3359 | DOI

[62] Wu, Q.; Han, T.-S.; Chen, X.; Chen, J.-F.; Zou, Y.-P.; Li, Z.-W.; Xu, Y.-C.; Guo, Y.-L. Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives, Genome Biology, Volume 18 (2017) no. 1 | DOI

[63] Zhao, L.; Charlesworth, B. Resolving the Conflict Between Associative Overdominance and Background Selection, Genetics, Volume 203 (2016) no. 3, pp. 1315-1334 | DOI

Cited by Sources: