Evolutionary Biology

The genetic architecture of local adaptation in a cline

10.24072/pcjournal.245 - Peer Community Journal, Volume 3 (2023), article no. e20.

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Local adaptation is pervasive. It occurs whenever selection favors different phenotypes in different environments, provided that there is genetic variation for the corresponding traits and that the effect of selection is greater than the effect of drift and migration. In many cases, ecologically relevant traits are quantitative and controlled by many genes. It has been repeatedly proposed that the localization of these genes in the genome may not be random, but could be an evolved feature. In particular, the clustering of local adaptation genes may be theoretically expected and has been observed in several situations. Previous theory has focused on two-patch or continent-island models to investigate this phenomenon, reaching the conclusion that such clustering could evolve, but in relatively limited conditions. In particular, it required that migration rate was neither too low nor too large and that the full optimization of trait values could not be eventually achieved by a mutation at a single locus. Here, we investigate this question in a spatially-explicit model, considering two contiguous habitats with distinct trait optima on a circular stepping-stone. We find that clustering of local-adaptation genes is pervasive within clines during both the establishment phase of local adaptation and the subsequent “reconfiguration” phase where different genetic architectures compete with each other. We also show that changing the fitness function relating trait to fitness has a strong impact on the overall evolutionary dynamics and resulting architecture.

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DOI: 10.24072/pcjournal.245
Laroche, Fabien 1; Lenormand, Thomas 2

1 UMR 1201 Dynafor, Univ Toulouse, INRAE, INPT, EI PURPAN, Castanet-Tolosan, France
2 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Laroche, Fabien; Lenormand, Thomas. The genetic architecture of local adaptation in a cline. Peer Community Journal, Volume 3 (2023), article  no. e20. doi : 10.24072/pcjournal.245. https://peercommunityjournal.org/articles/10.24072/pcjournal.245/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100590

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] Alleaume-Benharira, M.; Pen, I. R.; Ronce, O. Geographical patterns of adaptation within a species' range: interactions between drift and gene flow, Journal of Evolutionary Biology, Volume 19 (2006) no. 1, pp. 203-215 | DOI

[2] Anciaux, Y.; Chevin, L.-M.; Ronce, O.; Martin, G. Evolutionary Rescue over a Fitness Landscape, Genetics, Volume 209 (2018) no. 1, pp. 265-279 | DOI

[3] Barton, N. H.; Hewitt, G. M. Adaptation, speciation and hybrid zones, Nature, Volume 341 (1989) no. 6242, pp. 497-503 | DOI

[4] Bridle, J. R.; Polechová, J.; Kawata, M.; Butlin, R. K. Why is adaptation prevented at ecological margins? New insights from individual-based simulations, Ecology Letters, Volume 13 (2010) no. 4, pp. 485-494 | DOI

[5] Bürger, R.; Akerman, A. The effects of linkage and gene flow on local adaptation: A two-locus continent–island model, Theoretical Population Biology, Volume 80 (2011) no. 4, pp. 272-288 | DOI

[6] Bürger, R.; Lynch, M. Evolution and Extinction in a Changing Environment: A Quantitative-Genetic Analysis, Evolution, Volume 49 (1995) no. 1 | DOI

[7] Charlesworth, B.; Barton, N. H. The Spread of an Inversion with Migration and Selection, Genetics, Volume 208 (2018) no. 1, pp. 377-382 | DOI

[8] Charlesworth, D. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations, Evolutionary Applications, Volume 9 (2016) no. 1, pp. 74-90 | DOI

[9] Chevin, L.-M.; Lande, R.; Mace, G. M. Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory, PLoS Biology, Volume 8 (2010) no. 4 | DOI

[10] Débarre, F.; Gandon, S. Evolution of specialization in a spatially continuous environment, Journal of Evolutionary Biology, Volume 23 (2010) no. 5, pp. 1090-1099 | DOI

[11] Flaxman, S. M.; Feder, J. L.; Nosil, P. Genetic Hitchhiking And The Dynamic Buildup Of Genomic Divergence During Speciation With Gene Flow, Evolution, Volume 67 (2013) no. 9, pp. 2577-2591 | DOI

[12] Fouqueau, L.; Roze, D. The evolution of sex along an environmental gradient, Evolution, Volume 75 (2021) no. 6, pp. 1334-1347 | DOI

[13] Fraterrigo, J. M.; Turner, M. G.; Pearson, S. M.; Dixon, P. Effects Of Past Land Use On Spatial Heterogeneity Of Soil Nutrients In Southern Appalachian Forests, Ecological Monographs, Volume 75 (2005) no. 2, pp. 215-230 | DOI

[14] Gomulkiewicz, R.; Houle, D. Demographic and Genetic Constraints on Evolution, The American Naturalist, Volume 174 (2009) no. 6 | DOI

[15] Haldane, J. B. S. A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation, Mathematical Proceedings of the Cambridge Philosophical Society, Volume 23 (1927) no. 7, pp. 838-844 | DOI

[16] Jonsson, M. Colonisation ability of the threatened tenebrionid beetleOplocephala haemorrhoidalisand its common relativeBolitophagus reticulatus, Ecological Entomology, Volume 28 (2003) no. 2, pp. 159-167 | DOI

[17] Karlin, S. Population Subdivision and Selection Migration Interaction**Research supported in part by National Institutes of Health Grant USPHS 10452-12 and NSF Grant No. MPS71-02905 A03., Population Genetics and Ecology, Elsevier, 1976, pp. 617-657 | DOI

[18] Kirkpatrick, M.; Barton, N. H. Evolution of a Species' Range, The American Naturalist, Volume 150 (1997) no. 1, pp. 1-23 | DOI

[19] Kirkpatrick, M.; Barton, N. Chromosome Inversions, Local Adaptation and Speciation, Genetics, Volume 173 (2006) no. 1, pp. 419-434 | DOI

[20] Lande, R. Natural Selection and Random Genetic Drift in Phenotypic Evolution, Evolution, Volume 30 (1976) no. 2 | DOI

[21] Laroche, F.; Lenormand, T. Code related to “The genetic architecture of local adaptation in a cline” by Laroche et Lenormand, Zenodo, 2022 | DOI

[22] Laroche, F.; Lenormand, T. The genetic architecture of local adaptation in a cline, bioRxiv, 2022.06.30.498280, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology, 2022 | DOI

[23] Lenormand, T. Gene flow and the limits to natural selection, Trends in Ecology & Evolution, Volume 17 (2002) no. 4, pp. 183-189 | DOI

[24] Lenormand, T. The Evolution of Sex Dimorphism in Recombination, Genetics, Volume 163 (2003) no. 2, pp. 811-822 | DOI

[25] Lenormand, T. From Local Adaptation to Speciation: Specialization and Reinforcement, International Journal of Ecology, Volume 2012 (2012), pp. 1-11 | DOI

[26] Lenormand, T.; Otto, S. P. The Evolution of Recombination in a Heterogeneous Environment, Genetics, Volume 156 (2000) no. 1, pp. 423-438 | DOI

[27] Marshall, D. J.; Burgess, S. C.; Connallon, T. Global change, life‐history complexity and the potential for evolutionary rescue, Evolutionary Applications, Volume 9 (2016) no. 9, pp. 1189-1201 | DOI

[28] Martin, G.; Elena, S. F.; Lenormand, T. Distributions of epistasis in microbes fit predictions from a fitness landscape model, Nature Genetics, Volume 39 (2007) no. 4, pp. 555-560 | DOI

[29] Martin, G.; Lenormand, T. A General Multivariate Extension Of Fisher's Geometrical Model And The Distribution Of Mutation Fitness Effects Across Species, Evolution, Volume 60 (2006) no. 5 | DOI

[30] Martin, G.; Lenormand, T. The Fitness Effect Of Mutations Across Environments: A Survey In Light Of Fitness Landscape Models, Evolution, Volume 60 (2006) no. 12 | DOI

[31] Martin, G.; Lenormand, T. The fitness effect of mutations across environments: Fisher's geometrical model with multiple optima, Evolution, Volume 69 (2015) no. 6, pp. 1433-1447 | DOI

[32] Matuszewski, S.; Hermisson, J.; Kopp, M. Catch Me if You Can: Adaptation from Standing Genetic Variation to a Moving Phenotypic Optimum, Genetics, Volume 200 (2015) no. 4, pp. 1255-1274 | DOI

[33] Nagylaki, T. Conditions For The Existence Of Clines, Genetics, Volume 80 (1975) no. 3, pp. 595-615 | DOI

[34] Nosil, P.; Funk, D. J.; Ortiz-Barrientos, D. Divergent selection and heterogeneous genomic divergence, Molecular Ecology, Volume 18 (2009) no. 3, pp. 375-402 | DOI

[35] Osmond, M. M.; Klausmeier, C. A. An evolutionary tipping point in a changing environment, Evolution, Volume 71 (2017) no. 12, pp. 2930-2941 | DOI

[36] Otto, S. P.; Lenormand, T. Resolving the paradox of sex and recombination, Nature Reviews Genetics, Volume 3 (2002) no. 4, pp. 252-261 | DOI

[37] Otto, S. P. The Evolutionary Enigma of Sex, The American Naturalist, Volume 174 (2009) no. S1 | DOI

[38] Polechová, J.; Barton, N. H. Limits to adaptation along environmental gradients, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 20, pp. 6401-6406 | DOI

[39] Pylkov, K. V.; Zhivotovsky, L. A.; Feldman, M. W. Migration versus mutation in the evolution of recombination under multilocus selection, Genetical Research, Volume 71 (1998) no. 3, pp. 247-256 | DOI

[40] Ravigné, V.; Dieckmann, U.; Olivieri, I. Live Where You Thrive: Joint Evolution of Habitat Choice and Local Adaptation Facilitates Specialization and Promotes Diversity, The American Naturalist, Volume 174 (2009) no. 4 | DOI

[41] Sardell, J. M.; Kirkpatrick, M. Sex Differences in the Recombination Landscape, The American Naturalist, Volume 195 (2020) no. 2, pp. 361-379 | DOI

[42] Schwander, T.; Libbrecht, R.; Keller, L. Supergenes and Complex Phenotypes, Current Biology, Volume 24 (2014) no. 7 | DOI

[43] Slatkin, M. Gene Flow And Selection In A Cline, Genetics, Volume 75 (1973) no. 4, pp. 733-756 | DOI

[44] Slatkin, M. Spatial patterns in the distributions of polygenic characters, Journal of Theoretical Biology, Volume 70 (1978) no. 2, pp. 213-228 | DOI

[45] Strasburg, J. L.; Sherman, N. A.; Wright, K. M.; Moyle, L. C.; Willis, J. H.; Rieseberg, L. H. What can patterns of differentiation across plant genomes tell us about adaptation and speciation?, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 367 (2012) no. 1587, pp. 364-373 | DOI

[46] Strayer, D. L. Challenges in Understanding the Functions of Ecological Heterogeneity, Ecosystem Function in Heterogeneous Landscapes, Springer New York, New York, NY, pp. 411-425 | DOI

[47] Yeaman, S. Genomic rearrangements and the evolution of clusters of locally adaptive loci, Proceedings of the National Academy of Sciences, Volume 110 (2013) no. 19 | DOI

[48] Yeaman, S.; Aeschbacher, S.; Bürger, R. The evolution of genomic islands by increased establishment probability of linked alleles, Molecular Ecology, Volume 25 (2016) no. 11, pp. 2542-2558 | DOI

[49] Yeaman, S.; Whitlock, M. C. The Genetic Architecture Of Adaptation Under Migration-Selection Balance, Evolution, Volume 65 (2011) no. 7, pp. 1897-1911 | DOI

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