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Assortative mating can impede or facilitate fixation of underdominant alleles. (English) Zbl 1367.92077

Summary: Underdominant mutations have fixed between divergent species, yet classical models suggest that rare underdominant alleles are purged quickly except in small or subdivided populations. We predict that underdominant alleles that also influence mate choice, such as those affecting coloration patterns visible to mates and predators alike, can fix more readily. We analyze a mechanistic model of positive assortative mating in which individuals have \(n\) chances to sample compatible mates. This one-parameter model naturally spans random mating (\(n = 1\)) and complete assortment (\(n \rightarrow \infty\)), yet it produces sexual selection whose strength depends non-monotonically on \(n\). This sexual selection interacts with viability selection to either inhibit or facilitate fixation. As mating opportunities increase, underdominant alleles fix as frequently as neutral mutations, even though sexual selection and underdominance independently each suppress rare alleles. This mechanism allows underdominant alleles to fix in large populations and illustrates how life history can affect evolutionary change.

MSC:

92D10 Genetics and epigenetics
92D15 Problems related to evolution

References:

[1] Altrock, P. M.; Traulsen, A.; Reed, F. A., Stability properties of underdominance in finite subdivided populations, PLoS Comput. Biol., 7, 11 (2011), e1002260-e1002260
[2] Anderson, C.; Wong, S. C.; Fuller, A.; Zigelsky, K.; Earley, R. L., Carotenoid-based coloration is associated with predation risk, competition, and breeding status in female convict cichlids (Amatitlania siquia) under field conditions, Environ. Biol. Fishes, 98, 4, 1005-1013 (2015)
[3] Andersson, M. B., Sexual Selection (1994), Princeton University Press
[4] Andersson, M.; Simmons, L. W., Sexual selection and mate choice, Trends Ecol. Evol., 21, 6, 296-302 (2006)
[5] Arias, C. F.; Munoz, A. G.; Jiggins, C. D.; Mavarez, J.; Bermingham, E.; Linares, M., A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterflies, Mol. Ecol., 17, 21, 4699-4712 (2008)
[6] Arnegard, M. E.; Kondrashov, A. S., Sympatric speciation by sexual selection alone is unlikely, Evolution, 58, 2, 222-237 (2004)
[7] Barton, N. H.; Rouhani, S., The probability of fixation of a new karyotype in a continuous population, Evolution, 499-517 (1991)
[8] Blount, J. D., Carotenoids and life-history evolution in animals, Arch. Biochem. Biophys., 430, 1, 10-15 (2004)
[9] Blount, J. D.; Metcalfe, N. B.; Birkhead, T. R.; Surai, P. F., Carotenoid modulation of immune function and sexual attractiveness in zebra finches, Science, 300, 5616, 125-127 (2003)
[10] Caballero, A.; Hill, W. G., Effects of partial inbreeding on fixation rates and variation of mutant genes, Genetics, 131, 2, 493-507 (1992)
[11] Charlesworth, B., Evolutionary rates in partially self-fertilizing species, Amer. Nat., 126-148 (1992)
[12] Clutton-Brock, T.; McAuliffe, K., Female mate choice in mammals, Q. Rev. Biol., 84, 1, 3-27 (2009)
[13] Crespi, B. J., Causes of assortative mating in arthropods, Anim. Behav., 38, 6, 980-1000 (1989)
[14] Damgaard, C., Fixation of advantageous alleles in partially self-fertilizing populations: the effect of different selection modes, Genetics, 154, 2, 813-821 (2000)
[15] Epstein, C. L.; Mazzeo, R., Degenerate Diffusion Operators Arising in Population Biology (2013), Princeton University Press · Zbl 1309.47001
[16] Gardiner, C., Stochastic Methods: A Handbook for the Natural and Social Sciences Springer Series in Synergetics (2009), Springer · Zbl 1181.60001
[17] Gavrilets, S., Fitness Landscapes and the Origin of Species (MPB-41) (2004), Princeton University Press
[18] Glémin, S., Extinction and fixation times with dominance and inbreeding, Theor. Popul. Biol., 81, 4, 310-316 (2012) · Zbl 1404.92150
[19] Goodwillie, C.; Kalisz, S.; Eckert, C. G., The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence, Annu. Rev. Ecol. Evol. Syst., 47-79 (2005)
[20] Haldane, J. B.S., A mathematical theory of natural and artificial selection. Part II the influence of partial self-fertilisation, inbreeding, assortative mating, and selective fertilisation on the composition of mendelian populations, and on natural selection, Microbiol. Rev., 1, 3, 158-163 (1924)
[21] Hedrick, P. W., The establishment of chromosomal variants, Evolution, 322-332 (1981)
[22] Higashi, M.; Takimoto, G.; Yamamura, N., Sympatric speciation by sexual selection, Nature, 402, 6761, 523-526 (1999)
[23] Janetos, A. C., Strategies of female mate choice: a theoretical analysis, Behav. Ecol. Sociobiol., 7, 2, 107-112 (1980)
[24] Jiggins, C. D.; McMillan, W. O.; Neukirchen, W.; Mallet, J., What can hybrid zones tell us about speciation? the case of Heliconius erato and H. himera (lepidoptera: Nymphalidae), Biol. J. Linnean Soc., 59, 3, 221-242 (1996)
[25] Jones, A. G.; Ratterman, N. L., Mate choice and sexual selection: what have we learned since darwin?, Proc. Natl. Acad. Sci., 106, Suppl. 1, 10001-10008 (2009)
[26] Kapan, D. D., Three-butterfly system provides a field test of Müllerian mimicry, Nature, 409, 6818, 338-340 (2001)
[27] Karlin, S., Comparisons of positive assortative mating and sexual selection models, Theor. Popul. Biol., 14, 2, 281-312 (1978) · Zbl 0389.92012
[28] Kenney-Hunt, J. P.; Vaughn, T. T.; Pletscher, L. S.; Peripato, A.; Routman, E.; Cothran, K.; Durand, D.; Norgard, E.; Perel, C.; Cheverud, J. M., Quantitative trait loci for body size components in mice, Mamm. Genome, 17, 6, 526-537 (2006)
[29] Kimura, M., Diffusion models in population genetics, J. Appl. Probab., 1, 2, 177-232 (1964) · Zbl 0134.38103
[30] Kimura, M., Attainment of quasi linkage equilibrium when gene frequencies are changing by natural selection, Genetics, 52, 5, 875 (1965)
[31] Kirkpatrick, M., Sexual selection and the evolution of female choice, Evolution, 1-12 (1982)
[32] Kirkpatrick, M.; Barton, N., Chromosome inversions, local adaptation and speciation, Genetics, 173, 1, 419-434 (2006)
[33] Kokko, H.; Jennions, M. D.; Brooks, R., Unifying and testing models of sexual selection, Annu. Rev. Ecol. Evol. Syst., 43-66 (2006)
[34] Kuijper, B.; Pen, I.; Weissing, F. J., A guide to sexual selection theory, Annu. Rev. Ecol. Evol. Syst., 43, 287-311 (2012)
[35] Lande, R., Effective deme sizes during long-term evolution estimated from rates of chromosome rearrangement, Evolution, 33, 234-251 (1979)
[36] Lande, R., Models of speciation by sexual selection on polygenic traits, Proc. Natl. Acad. Sci., 78, 6, 3721-3725 (1981)
[37] Lande, R.; Schemske, D. W., The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models, Evolution, 24-40 (1985)
[38] Langham, G. M.; Benkman, C., Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies, Evolution, 58, 12, 2783-2787 (2004)
[39] Mallet, J.; Barton, N. H., Strong natural selection in a warning-color hybrid zone, Evolution, 421-431 (1989)
[40] M’Gonigle, L. K.; FitzJohn, R. G., Assortative mating and spatial structure in hybrid zones, Evolution, 64, 2, 444-455 (2010)
[41] Michalakis, Y.; Olivieri, I., The influence of local extinctions on the probability of fixation of chromosomal rearrangements, J. Evol. Biol., 6, 2, 153-170 (1993)
[42] Nagylaki, T., Introduction to Theoretical Population Genetics (1992), Springer-Verlag: Springer-Verlag Berlin · Zbl 0839.92011
[43] Navarro, A.; Barton, N. H., Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation, Evolution, 57, 3, 447-459 (2003)
[44] O’Donald, P., Genetic Models of Sexual Selection, vol. 44 (1980), Cambridge University Press: Cambridge University Press Cambridge
[45] Otto, S. P.; Servedio, M. R.; Nuismer, S. L., Frequency-dependent selection and the evolution of assortative mating, Genetics, 179, 4, 2091-2112 (2008)
[47] Pomiankowski, A., The costs of choice in sexual selection, J. Theor. Biol., 128, 2, 195-218 (1987)
[48] Real, L., Search theory and mate choice. I. models of single-sex discrimination, Amer. Nat., 376-405 (1990)
[49] Reeves, R. G.; Bryk, J.; Altrock, P. M.; Denton, J. A.; Reed, F. A., First steps towards underdominant genetic transformation of insect populations, PLoS ONE, 9, 5, e97557 (2014)
[50] Roze, D.; Rousset, F., Selection and drift in subdivided populations: a straightforward method for deriving diffusion approximations and applications involving dominance, selfing and local extinctions, Genetics, 165, 4, 2153-2166 (2003)
[51] Sefc, K. M.; Brown, A. C.; Clotfelter, E. D., Carotenoid-based coloration in cichlid fishes, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 173, 42-51 (2014)
[52] Seger, J., Unifying genetic models for the evolution of female choice, Evolution, 1185-1193 (1985)
[53] Servedio, M. R.; Bürger, R., The counterintuitive role of sexual selection in species maintenance and speciation, Proc. Natl. Acad. Sci., 111, 22, 8113-8118 (2014)
[54] Sinkins, S. P.; Gould, F., Gene drive systems for insect disease vectors, Nature Rev. Genet., 7, 6, 427-435 (2006)
[55] Slatkin, M., Fixation probabilities and fixation times in a subdivided population, Evolution, 477-488 (1981)
[56] Smith, L. M.; Bomblies, K.; Weigel, D., Complex evolutionary events at a tandem cluster of arabidopsis thaliana genes resulting in a single-locus genetic incompatibility, PLoS Genet., 7, 7, e1002164 (2011)
[57] Stewart, A. J.; Seymour, R. M.; Pomiankowski, A.; Reuter, M., Under-dominance constrains the evolution of negative autoregulation in diploids, PLoS Comput. Biol., 9, 3, e1002992 (2013)
[58] Whitlock, M. C., Fixation probability and time in subdivided populations, Genetics, 164, 2, 767-779 (2003)
[59] Whitlock, M. C., Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection, Evolution, 54, 6, 1855-1861 (2000)
[60] Wiegmann, D. D.; Seubert, S. M.; Wade, G. A., Mate choice and optimal search behavior: fitness returns under the fixed sample and sequential search strategies, J. Theor. Biol., 262, 4, 596-600 (2010) · Zbl 1403.92348
[61] Wright, S., On the probability of fixation of reciprocal translocations, Amer. Nat., 513-522 (1941)
[62] Wright, S., Evolution in mendelian populations, Genetics, 16, 2, 97 (1931)
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