Abstract
Computer experiments that mirror the evolutionary dynamics of sexual and asexual organisms as they occur in nature were used to test features proposed to explain the evolution of sexual recombination. Results show that this evolution is better described as a network of interactions between possible sexual forms, including diploidy, thelytoky, facultative sex, assortation, bisexuality, and division of labor between the sexes, rather than a simple transition from parthenogenesis to sexual recombination. Diploidy was shown to be fundamental for the evolution of sex; bisexual reproduction emerged only among anisogamic diploids with a synergistic division of reproductive labor; and facultative sex was more likely to evolve among haploids practicing assortative mating. Looking at the evolution of sex as a complex system through individual-based simulations explains better the diversity of sexual strategies known to exist in nature, compared to classical analytical models.
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References
Maynard-Smith, J., Szathmáry, E.: The Major Transitions in Evolution. Oxford University Press, Oxford, England (1995)
Maynard-Smith, J.: The Evolution of Sex. Cambridge University Press (1978)
Maynard-Smith, J.: Did Darwin Get it Right?: Essays on Games, Sex and Evolution. Chapman & Hall, London (1988)
Van Valen, L.: A new evolutionary law. Evolutionary Theory. 1, 1–30 (1973)
Ochoa, G., Jaffe, K.: On sex, mate selection and the red queen. J. Theor. Biol. 199, 1–9 (1999)
McDonald, M.J., Rice, D.P., Desai, M.M.: Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531, 233–236 (2016)
Sharp, N.P., Otto, S.P.: Evolution of sex: using experimental genomics to select among competing theories. Bioessays, Wiley 38, 751–757 (2016)
Kimura, M., Maruyama, T.: The mutational load with epistatic gene interactions in fitness. Genetics 54, 1337–1351 (1966)
Kondrashov, A.S.: Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988)
Charlesworth, B.: Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199–221 (1990)
Barton, N.H.: A general model for the evolution of recombination. Genet. Res. 65, 123–145 (1995)
Otto, S.P., Feldman, M.W.: Deleterious mutations, variable epistatic interactions, and the evolution of recombination. Theor. Popul. Biol. 51, 134–147 (1997)
Whitlock, A.O.B, Peck, K.M., Azevedo, R.B.R., Burch, C.L.: An evolving genetic architecture interacts with Hill–Robertson interference to determine the benefit of sex. Genetics 203(2), 923-936 (2016)
Jaffe, K.: Emergence and maintenance of sex among diploid organisms aided by assortative mating. Acta Biotheor. 48, 137–147 (2000)
Paley, C.J., Taraskin, S.N., Elliott, S.R.: Establishment of Facultative Sexuals. Naturwissenschaften 94, 505 (2007)
Weaver, W.: Science and Complexity. Am. Sci. 36, 536–544 (1948)
Markowetz, L.: All biology is computational biology. PLoS Biol. 15(3), e2002050 (2017). https://doi.org/10.1371/journal.pbio.2002050
Livnat, A., Papadimitriou, C., Dushoff, J., Feldman, M.W.: A mixability theory for the role of sex in evolution. Proc. Natl. Acad. Sci. U.S.A. 105, 19803–19808 (2008)
Moorad, J.A.: Multi-Level Sexual Selection: Individual and Family-Level Selection for Mating Success in a Historical Human Population. Evolution, Wiley Online Library (2013)
Jaffe, K.: Sex promotes gamete selection: a quantitative comparative study of features favoring the evolution of sex. Complexity 9(6), 43–51 (2004)
Hamilton, W. D.: The evolution of altruistic behavior. Am. Nat. 354–356 (1963)
Jaffe, K.: Extended Inclusive Fitness Theory: Synergy and assortment drives the evolutionary dynamics in biology and economics. SpringerPlus 5(1), 1092 (2016)
Ochoa, G., Jaffe, K.: Assortative mating drastically alters the magnitude of error thresholds. Lecture Notes Comput Sci LNCS 4193, 890–899 (2006)
Agrawal, A.F.: Similarity selection and the evolution of sex: revisiting the red queen. PLoS Biol. 4(8), e265 (2006)
Jaffe, K.: The Scientific Roots of Rynergy: and Row to Rake Cooperation Successful. Amazon Books B074D3VHK2 (2017)
Watts, D.J.: Chapter 6: Computational Social Sciences: Reports on Leading-Edge Engineering from the 2013 Symposium. The National Academies Press. (2014)
Jaffe, K., Issa, S., Daniels, E., Haile, D.: Dynamics of the emergence of genetic resistance to pesticides among asexual and sexual organisms. J. Theor. Biol. 188, 289–299 (1997)
Jaffe, K.: The dynamics of the evolution of sex: why the sexes are, in fact, always two? Interciencia 21, 259–267 (1996)
Hadany, L., Beker, T.: Sexual selection and the evolution of obligatory sex. BMC Evol. Biol. 7(1), 245 (2007)
Jaffe, K.: On sex, mate selection and evolution: an exploration. Comm. Theor. Biol. 7, 91–107 (2002)
Jaffe, K.: On the adaptive value of some mate selection strategies. Acta Biotheor. 47, 29–40 (1999)
Geritz, S.A., Éva, K.: Adaptive dynamics in diploid, sexual populations and the evolution of reproductive isolation. Proc. R. Soc. London B: Bio.l Sci. 267(1453), 1671–1678 (2000)
Balloux, F., Lehmann, L., de Meeûs, T.: The population genetics of clonal and partially clonal diploids. Genetics 164(4), 1635–1644 (2003)
Messer, P.W.: SLiM: simulating evolution with selection and linkage. Genetics 194(4), 1037–1039 (2013)
Schneider, D.M., Baptestini, E.M., Aguiar, A.M.: Diploid versus haploid models of neutral speciation. J. Biol. Phys. 42, 235–245 (2016)
Agrawal, A.F., Chasnov, J.R.: Recessive mutations and the maintenance of sex in structured populations. Genetics 158, 913–917 (2001)
Otto, S.P.: The advantages of segregation and the evolution of sex. Genetics 164, 1099–1118 (2003)
Dolgin, E.S., Otto, S.P.: Segregation and the evolution of sex under overdominant selection. Genetics 164, 1119–1128 (2003)
Haag, C.R., Roze, D.: Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift. Genetics 176, 1663–1678 (2007)
Gorelick, R., Heng, H.H.: Sex reduces genetic variation: a multidisciplinary review. Evolution 65(4), 1088–1098 (2011)
Jaffe, K.: On the relative importance of haplo-diploidy, assortative mating and social synergy on the evolutionary emergence of social behavior. Acta Biotheor. 49, 29–42 (2001)
Corning, P.A., Szathmáry, E.: ‘Synergistic selection’: a Darwinian frame for the evolution of complexity. J. Theor. Biol. 371, 45–58 (2015)
Togashi T., Cox P.A.: Editors. The Evolution of Anisogamy. Cambridge Univ. Press (2011)
Jaffe, K.: The invisible hand of economic markets can be visualized through the synergy created by division of labor. Complexity ID 4753863 (2017)
Atmar, W.: On the role of males. Anim. Behav. 41(2), 195–205 (1991)
De Meeûs, T., Prugnolle, F., Agnew, P.: Asexual reproduction: genetics and evolutionary aspects. Cell. Mol. Life Sci. 64(11), 1355 (2007)
Rincones, J., Mauléon, H., Jaffe, K.: Bacteria modulate the degree of amphimix of their symbiotic entomopathogenic nematodes (Heterohabditis spp) in response to nutritional stress. Naturwissenschaften 88(7), 310–312 (2001)
Sinai, S., Olejarz, J., Neagu, I.A., Nowak, M.A.: Primordial sex facilitates the emergence of evolution. ArXiv 1612.00825 (2016)
Fox, D.: What sparked the Cambrian explosion? Nature 530, 268–270 (2016)
Bachtrog, D., Mank, J.E., Peichel, C.L., Kirkpatrick, M., Otto, S.P., Ashman, T.L., Perrin, N.: PLoS Biol. 12, e1001899 (2014)
Talman, A.M., Domarle, O., McKenzie, F.E., Ariey, F., Robert, V.: Gametocytogenesis: the puberty of plasmodium falciparum. Malar. J. 3(1), 24 (2004)
Steiger, S., Stökl, J.: The role of sexual selection in the evolution of chemical signals in insects. Insects 5, 423–438 (2014)
Jaffe, K.: The need for sperm selection may explain why termite colonies have kings and queens, whereas those of ants, wasps and bees have only queens. Theory Biosci. 127, 359–363 (2008)
Doebeli, M., Ispolatov, Y., Simon, B.: Towards a mechanistic foundation of evolutionary theory. eLife (2017). https://doi.org/10.7554/eLife.23804.001
Allen, B.G., Chen, Y., Fotouhi, B., Momeni, N., Yau, S.: Nowak, M. A. Evolutionary dynamics on any population structure. Nature (2017). https://doi.org/10.1038/nature21723
Queller, D.C.: A general model for kin selection. Evolution 46, 376–380 (1992)
Queller, D.C.: Expanded social fitness and Hamilton’s rule for kin, kith, and kind. Proc. Natl. Acad. Sci. U.S.A. 108, 10792–10799 (2011)
Tang-Martinez, Z.: Rethinking Bateman’s principles: challenging persistent myths of sexually reluctant females and promiscuous males. J. Sex Res. 53, 532–559 (2016)
Jaffe, K., Febres, G.: Defining synergy thermodynamically using quantitative measurements of entropy and free energy. Complexity 21, 235–242 (2016)
Acknowledgements
I thank Adam Russell of DARPA for his enthusiastic promotion of a social-supercollider, first proposed by Duncan Watts, which influenced the organization of this paper, Guy Hoelzer for encouragement and for reminding me of Atmar’s paper, Cristina Sainz and Zuleyma Tang-Martinez for helping improve the readability of the paper, and to the late John Maynard Smith and William Hamilton for illuminating discussions. I profited from the constructive comments of several referees. Sonya Bahar did excellent editorial work.
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Computer experiments that mirror the evolutionary dynamics of sexual and asexual organisms showed:
1- Evolution is better described as a network of interactions between possible sexual forms, including diploidy, thelytoky, facultative sex, assortation, bisexuality, and division of labor between the sexes, rather than a simple transition from parthenogenesis to sexual recombination.
2- Diploidy was shown to be fundamental for the evolution of sex.
3- Bisexual reproduction emerged only among anisogamic diploids with a synergistic division of reproductive labor.
4- Facultative sex was more likely to evolve among haploids practicing assortative mating.
Looking at the evolution of sex as a complex system through individual-based simulations explains better the diversity of sexual strategies known to exist in nature, compared to classical analytical models.
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Jaffe, K. Synergy from reproductive division of labor and genetic complexity drive the evolution of sex. J Biol Phys 44, 317–329 (2018). https://doi.org/10.1007/s10867-018-9485-8
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DOI: https://doi.org/10.1007/s10867-018-9485-8