Journal of Biological Physics

, Volume 44, Issue 3, pp 317–329 | Cite as

Synergy from reproductive division of labor and genetic complexity drive the evolution of sex

  • Klaus JaffeEmail author
Original Paper


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.


Recombination Anisogamy Diploid Assortation Evolution Sex Synergy 



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.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflicts of interest related to this work.


  1. 1.
    Maynard-Smith, J., Szathmáry, E.: The Major Transitions in Evolution. Oxford University Press, Oxford, England (1995)Google Scholar
  2. 2.
    Maynard-Smith, J.: The Evolution of Sex. Cambridge University Press (1978)Google Scholar
  3. 3.
    Maynard-Smith, J.: Did Darwin Get it Right?: Essays on Games, Sex and Evolution. Chapman & Hall, London (1988)Google Scholar
  4. 4.
    Van Valen, L.: A new evolutionary law. Evolutionary Theory. 1, 1–30 (1973)Google Scholar
  5. 5.
    Ochoa, G., Jaffe, K.: On sex, mate selection and the red queen. J. Theor. Biol. 199, 1–9 (1999)CrossRefGoogle Scholar
  6. 6.
    McDonald, M.J., Rice, D.P., Desai, M.M.: Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531, 233–236 (2016)ADSCrossRefGoogle Scholar
  7. 7.
    Sharp, N.P., Otto, S.P.: Evolution of sex: using experimental genomics to select among competing theories. Bioessays, Wiley 38, 751–757 (2016)CrossRefGoogle Scholar
  8. 8.
    Kimura, M., Maruyama, T.: The mutational load with epistatic gene interactions in fitness. Genetics 54, 1337–1351 (1966)Google Scholar
  9. 9.
    Kondrashov, A.S.: Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988)ADSCrossRefGoogle Scholar
  10. 10.
    Charlesworth, B.: Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199–221 (1990)CrossRefGoogle Scholar
  11. 11.
    Barton, N.H.: A general model for the evolution of recombination. Genet. Res. 65, 123–145 (1995)CrossRefGoogle Scholar
  12. 12.
    Otto, S.P., Feldman, M.W.: Deleterious mutations, variable epistatic interactions, and the evolution of recombination. Theor. Popul. Biol. 51, 134–147 (1997)CrossRefzbMATHGoogle Scholar
  13. 13.
    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)Google Scholar
  14. 14.
    Jaffe, K.: Emergence and maintenance of sex among diploid organisms aided by assortative mating. Acta Biotheor. 48, 137–147 (2000)CrossRefGoogle Scholar
  15. 15.
    Paley, C.J., Taraskin, S.N., Elliott, S.R.: Establishment of Facultative Sexuals. Naturwissenschaften 94, 505 (2007)ADSCrossRefGoogle Scholar
  16. 16.
    Weaver, W.: Science and Complexity. Am. Sci. 36, 536–544 (1948)Google Scholar
  17. 17.
    Markowetz, L.: All biology is computational biology. PLoS Biol. 15(3), e2002050 (2017). CrossRefGoogle Scholar
  18. 18.
    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)Google Scholar
  19. 19.
    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)Google Scholar
  20. 20.
    Jaffe, K.: Sex promotes gamete selection: a quantitative comparative study of features favoring the evolution of sex. Complexity 9(6), 43–51 (2004)CrossRefGoogle Scholar
  21. 21.
    Hamilton, W. D.: The evolution of altruistic behavior. Am. Nat. 354–356 (1963)Google Scholar
  22. 22.
    Jaffe, K.: Extended Inclusive Fitness Theory: Synergy and assortment drives the evolutionary dynamics in biology and economics. SpringerPlus 5(1), 1092 (2016)Google Scholar
  23. 23.
    Ochoa, G., Jaffe, K.: Assortative mating drastically alters the magnitude of error thresholds. Lecture Notes Comput Sci LNCS 4193, 890–899 (2006)CrossRefGoogle Scholar
  24. 24.
    Agrawal, A.F.: Similarity selection and the evolution of sex: revisiting the red queen. PLoS Biol. 4(8), e265 (2006)CrossRefGoogle Scholar
  25. 25.
    Jaffe, K.: The Scientific Roots of Rynergy: and Row to Rake Cooperation Successful. Amazon Books B074D3VHK2 (2017)Google Scholar
  26. 26.
    Watts, D.J.: Chapter 6: Computational Social Sciences: Reports on Leading-Edge Engineering from the 2013 Symposium. The National Academies Press. (2014)Google Scholar
  27. 27.
    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)CrossRefGoogle Scholar
  28. 28.
    Jaffe, K.: The dynamics of the evolution of sex: why the sexes are, in fact, always two? Interciencia 21, 259–267 (1996)Google Scholar
  29. 29.
    Hadany, L., Beker, T.: Sexual selection and the evolution of obligatory sex. BMC Evol. Biol. 7(1), 245 (2007)CrossRefGoogle Scholar
  30. 30.
    Jaffe, K.: On sex, mate selection and evolution: an exploration. Comm. Theor. Biol. 7, 91–107 (2002)Google Scholar
  31. 31.
    Jaffe, K.: On the adaptive value of some mate selection strategies. Acta Biotheor. 47, 29–40 (1999)CrossRefGoogle Scholar
  32. 32.
    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)Google Scholar
  33. 33.
    Balloux, F., Lehmann, L., de Meeûs, T.: The population genetics of clonal and partially clonal diploids. Genetics 164(4), 1635–1644 (2003)Google Scholar
  34. 34.
    Messer, P.W.: SLiM: simulating evolution with selection and linkage. Genetics 194(4), 1037–1039 (2013)CrossRefGoogle Scholar
  35. 35.
    Schneider, D.M., Baptestini, E.M., Aguiar, A.M.: Diploid versus haploid models of neutral speciation. J. Biol. Phys. 42, 235–245 (2016)CrossRefGoogle Scholar
  36. 36.
    Agrawal, A.F., Chasnov, J.R.: Recessive mutations and the maintenance of sex in structured populations. Genetics 158, 913–917 (2001)Google Scholar
  37. 37.
    Otto, S.P.: The advantages of segregation and the evolution of sex. Genetics 164, 1099–1118 (2003)Google Scholar
  38. 38.
    Dolgin, E.S., Otto, S.P.: Segregation and the evolution of sex under overdominant selection. Genetics 164, 1119–1128 (2003)Google Scholar
  39. 39.
    Haag, C.R., Roze, D.: Genetic load in sexual and asexual diploids: segregation, dominance and genetic drift. Genetics 176, 1663–1678 (2007)CrossRefGoogle Scholar
  40. 40.
    Gorelick, R., Heng, H.H.: Sex reduces genetic variation: a multidisciplinary review. Evolution 65(4), 1088–1098 (2011)CrossRefGoogle Scholar
  41. 41.
    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)CrossRefGoogle Scholar
  42. 42.
    Corning, P.A., Szathmáry, E.: ‘Synergistic selection’: a Darwinian frame for the evolution of complexity. J. Theor. Biol. 371, 45–58 (2015)CrossRefGoogle Scholar
  43. 43.
    Togashi T., Cox P.A.: Editors. The Evolution of Anisogamy. Cambridge Univ. Press (2011)Google Scholar
  44. 44.
    Jaffe, K.: The invisible hand of economic markets can be visualized through the synergy created by division of labor. Complexity ID 4753863 (2017)Google Scholar
  45. 45.
    Atmar, W.: On the role of males. Anim. Behav. 41(2), 195–205 (1991)CrossRefGoogle Scholar
  46. 46.
    De Meeûs, T., Prugnolle, F., Agnew, P.: Asexual reproduction: genetics and evolutionary aspects. Cell. Mol. Life Sci. 64(11), 1355 (2007)CrossRefGoogle Scholar
  47. 47.
    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)ADSCrossRefGoogle Scholar
  48. 48.
    Sinai, S., Olejarz, J., Neagu, I.A., Nowak, M.A.: Primordial sex facilitates the emergence of evolution. ArXiv 1612.00825 (2016)Google Scholar
  49. 49.
    Fox, D.: What sparked the Cambrian explosion? Nature 530, 268–270 (2016)ADSCrossRefGoogle Scholar
  50. 50.
    Bachtrog, D., Mank, J.E., Peichel, C.L., Kirkpatrick, M., Otto, S.P., Ashman, T.L., Perrin, N.: PLoS Biol. 12, e1001899 (2014)CrossRefGoogle Scholar
  51. 51.
    Talman, A.M., Domarle, O., McKenzie, F.E., Ariey, F., Robert, V.: Gametocytogenesis: the puberty of plasmodium falciparum. Malar. J. 3(1), 24 (2004)CrossRefGoogle Scholar
  52. 52.
    Steiger, S., Stökl, J.: The role of sexual selection in the evolution of chemical signals in insects. Insects 5, 423–438 (2014)CrossRefGoogle Scholar
  53. 53.
    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)CrossRefGoogle Scholar
  54. 54.
    Doebeli, M., Ispolatov, Y., Simon, B.: Towards a mechanistic foundation of evolutionary theory. eLife (2017).
  55. 55.
    Allen, B.G., Chen, Y., Fotouhi, B., Momeni, N., Yau, S.: Nowak, M. A. Evolutionary dynamics on any population structure. Nature (2017). Google Scholar
  56. 56.
    Queller, D.C.: A general model for kin selection. Evolution 46, 376–380 (1992)CrossRefGoogle Scholar
  57. 57.
    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)Google Scholar
  58. 58.
    Tang-Martinez, Z.: Rethinking Bateman’s principles: challenging persistent myths of sexually reluctant females and promiscuous males. J. Sex Res. 53, 532–559 (2016)Google Scholar
  59. 59.
    Jaffe, K., Febres, G.: Defining synergy thermodynamically using quantitative measurements of entropy and free energy. Complexity 21, 235–242 (2016)ADSMathSciNetCrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Universidad Simón BolivarCaracasVenezuela

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