Penis evolution across species: divergence and diversity

Abstract

The penis is an incredibly diverse and rapidly evolving structure, such that even in closely related species that otherwise differ very little in their morphology, penis form can be highly differentiated. Penises are also much more complex than their fundamental function — sperm transfer — would seem to require. The rapid divergent evolution of male structures is typically the signature of traits under sexual selection and the current evidence suggests the penis is no different in this regard. Despite the general agreement that sexual selection is the main driver of penis evolution, many questions about penis evolution remain unresolved. Furthermore, the penis might be an ideal characteristic on which to focus in the drive to link phenotype with genotype.

Key points

  • Across animals with internal fertilization, the penis and associated structures evolve rapidly and divergently.

  • Penises are also much more complicated than their simple primary function, sperm transfer, would seem to require, and can sometimes even damage the female during copulation.

  • Sexual selection, and particularly female choice, is largely responsible for the diversity of the penis, although natural selection might occasionally act on penis form.

  • Despite rapid evolution, in most instances, selection on the penis does not seem to be particularly strong.

  • Evidence suggests the human penis is sexually selected, with increased penis size preferred by women in some studies, perhaps explaining why the human penis is large compared with most great apes.

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Fig. 1: Examples of genital variation.
Fig. 2: The mechanisms of sexual selection.
Fig. 3: Schematic representation of the relative size of the penis and testes across the great apes.
Fig. 4: Evidence for sexual selection acting on male genital form in insects.

References

  1. 1.

    Eberhard, W. G. Sexual Selection and Animal Genitalia (Harvard Univ. Press, London, 1985).

  2. 2.

    Higgins, S., Hosken, D. J. & Wedell, N. Phenotypic and genetic variation in male genitalia in the seedbug, Lygaeus equestris (Heteroptera). Biol. J. Linn. Soc. 98, 400–405 (2009).

    Article  Google Scholar 

  3. 3.

    Kamimura, Y. & Matsuo, Y. A “spare” compensates for the risk of destruction of the elongated penis of earwigs (Insecta: Dermaptera). Naturwissenschaften 88, 468–471 (2001).

    CAS  Article  Google Scholar 

  4. 4.

    Yoshizawa, K., Ferreira, R. L., Kamimura, Y. & Leinhard, C. Female penis, male vagina, and their correlated evolution in a cave insect. Curr. Biol. 24, 1006–1010 (2014).

    CAS  Article  Google Scholar 

  5. 5.

    Rowe, L. & Arnqvist, G. Sexual selection and the evolution of genital shape and complexity in water striders. Evolution 66, 40–54 (2011).

    Article  Google Scholar 

  6. 6.

    Arnqvist, G. & Thornhill, R. Evolution of animal genitalia: patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in waterstriders (Heteroptera: Gerridae: Insecta). Gen. Res. 71, 192–212 (1998).

    Google Scholar 

  7. 7.

    Hosken, D. J. & Stockley, P. Sexual selection and genital evolution. Trends Ecol. Evol. 19, 87–93 (2004).

    Article  Google Scholar 

  8. 8.

    Simmons, L. W. Sexual selection and genital evolution. Austr. Entomol. 53, 1–17 (2014).

    Article  Google Scholar 

  9. 9.

    Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).

  10. 10.

    Pitra, C., Fickel, J., Meijaard, E. & Groves, P. C. Evolution and phylogeny of old world deer. Mol. Phyl. Evol. 33, 880–895 (2004).

    CAS  Article  Google Scholar 

  11. 11.

    Emlen, D. J., Marangelo, J., Ball, B. & Cunningham, C. W. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59, 1060–1084 (2005).

    CAS  Article  Google Scholar 

  12. 12.

    Langerhans, R. B. in Ecology and Evolution of Poeciliid Fishes (eds Evans, J., Pilastro, A. & Schlupp, I.) 228–240 (Univ. of Chicago Press, Chicago, 2011).

  13. 13.

    Simmons, L. W. & Emlen, D. J. Evolutonary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103, 16346–16351 (2006).

    CAS  Article  Google Scholar 

  14. 14.

    Heinen-Kay, J. L. & Langerhans, R. B. Predation-associated divergence of male genital morphology in a livebearing fish. J. Evol. Biol. 26, 2135–2146 (2013).

    CAS  Article  Google Scholar 

  15. 15.

    Hollander, J., Smadja, C. M., Butlin, R. K. & Reid, D. G. Genital divergence in sympatric sister snails. J. Evol. Biol. 26, 210–215 (2013).

    CAS  Article  Google Scholar 

  16. 16.

    Kameda, Y., Kawakita, A. & Kato, M. Reproductive character displacement in genital morphology in Satsuma land snails. Am. Nat. 173, 689–697 (2009).

    Article  Google Scholar 

  17. 17.

    Darwin, C. The Descent of Man and Selection in Relation to Sex (John Murry, London, 1871).

  18. 18.

    Hosken, D. J. & House, C. M. Sexual selection. Curr. Biol. 21, R62–R65 (2011).

    CAS  Article  Google Scholar 

  19. 19.

    Parker, G. A. in Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.) 1–60 (Academic Press, London, 1984).

  20. 20.

    Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, Princeton, 1996).

  21. 21.

    Pitnick, S. & Hosken, D. J. in Evolutionary Behavioural Ecology (eds Westneat, D. F. & Fox, C. W.) 379–399 (Oxford Univ. Press, Oxford, 2010).

  22. 22.

    Pizarri, T. & Birkhead, T. R. Female feral fowl eject sperm of subdominant males. Nature 405, 787–789 (2000).

    Article  Google Scholar 

  23. 23.

    Hodgson, D. J. & Hosken, D. J. Sperm competition promotes the exploitation of rival ejaculates. J. Theor. Biol. 243, 230–234 (2006).

    CAS  Article  Google Scholar 

  24. 24.

    Eberhard, W. G. Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48, 711–733 (1994).

    Article  Google Scholar 

  25. 25.

    Edvardsson, M. & Arnqvist, G. Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum. Proc. Biol. Sci. 267, 559–563 (2000).

    CAS  Article  Google Scholar 

  26. 26.

    Zervomanolakis, I. et al. Physiology of upward transport in the human female genital tract. Ann. NY Acad. Sci. 1101, 1–20 (2007).

    CAS  Article  Google Scholar 

  27. 27.

    Reeder, D. M. in Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions (ed. Jones, C. B.) 255–303 (American Society of Primotologists, Norman, 2003).

  28. 28.

    Leivers, S. & Simmons, L. W. Human sperm competition: playing a defensive strategy. Adv. Stud. Behav. 46, 1–44 (2014).

    Article  Google Scholar 

  29. 29.

    Hosken, D. J. Clitoral variation says nothing about female orgasm. Evol. Dev. 10, 393–395 (2008).

    CAS  Article  Google Scholar 

  30. 30.

    Dixson, A. F. Primate Sexuality (Oxford Univ. Press, Oxford, 1998).

  31. 31.

    Simmons, L. W., Firman, R. C., Rhodes, G. & Peters, M. Human sperm competition: testis size, sperm production and rates of extra-pair copulations. Anim. Behav. 68, 297–302 (2004).

    Article  Google Scholar 

  32. 32.

    Clark, A. G., Begun, D. J. & Prout, T. Female x male interactions in Drosophila sperm competition. Science 283, 217–220 (1999).

    CAS  Article  Google Scholar 

  33. 33.

    Evans, J. P., Zane, Francescato, L., S. & Pilastro, A. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421, 360–363 (2003).

    CAS  Article  Google Scholar 

  34. 34.

    Fairbairn, D. J. in Sex, Size & Gender: Evolutionary Studies of Sexual Size Dimorphism (eds Fairbairn, D. J., Blanckenhorn, W. U. & Szekely, T.) 97–105 (Oxford Univ. Press, Oxford, 2009).

  35. 35.

    House, C. M., Sharma, M. D., Okada, K. & Hosken, D. J. Pre and post-copulatory selection favor similar genital phenotypes in the male broad horned beetle. Integr. Comp. Biol. 56, 682–693 (2016).

    Article  Google Scholar 

  36. 36.

    Arnqvist, G. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784–786 (1998).

    CAS  Article  Google Scholar 

  37. 37.

    Ramm, S. A. Sexual selection and genital evolution in mammals: a phylogenetic analysis of baculum length. Am. Nat. 169, 360–369 (2007).

    Article  Google Scholar 

  38. 38.

    Simmons, L. W. Sperm Competition and it Evolutionary Consequences in the Insects (Princeton Univ. Press, Princeton, 2001).

  39. 39.

    Gage, M. J. G. Associations between body size, mating pattern, testis size and sperm length across butterflies. Proc. Biol. Sci. 258, 247–254 (1994).

    Article  Google Scholar 

  40. 40.

    Stockley, P., Gage, M. J. G., Parker, G. A. & Moller, A. P. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149, 933–954 (1997).

    CAS  Article  Google Scholar 

  41. 41.

    Hosken, D. J. Sperm competition in bats. Proc. Biol. Sci. 264, 385–392 (1997).

    CAS  Article  Google Scholar 

  42. 42.

    Hosken, D. J. & Ward, P. I. Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4, 10–13 (2001).

    Article  Google Scholar 

  43. 43.

    Brennan, P. L. R. et al. Coevolution of male and female genital morphology in waterfowl. PLOS ONE 5, e418 (2007).

    Article  Google Scholar 

  44. 44.

    Arnqvist, G. & Danielsson, I. Copulatory behaviour, genital morphology, and male fertilization success in water striders. Evolution 53, 147–156 (1999).

    Article  Google Scholar 

  45. 45.

    Córdoba-Aguilar, A. Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly. Proc. Biol. Sci. 266, 779–784 (1999).

    Article  Google Scholar 

  46. 46.

    House, C. M. & Simmons, L. W. Genital morphology and fertilisation success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proc. Biol. Sci. 270, 447–455 (2003).

    Article  Google Scholar 

  47. 47.

    Xu, J. & Wang, Q. Form and nature of precopulatory sexual selection in both sexes of a moth. Naturwissenschaften 97, 617–625 (2010).

    CAS  Article  Google Scholar 

  48. 48.

    Stockley, P. et al. Baculum morphology predicts reproductive success of male house mice under sexual selection. BMC Biol. 11, 66 (2013).

    Article  Google Scholar 

  49. 49.

    Mautz, B. S., Wong, B. B. M., Peters, R. A. & Jennions, M. D. Penis size interacts with body shape and height to influence male attractiveness. Proc. Natl Acad. Sci. USA 110, 6925–6930 (2013).

    CAS  Article  Google Scholar 

  50. 50.

    Prause, N., Park, J., Leung, S. & Miller, G. Women’s preference for penis size: a new research method using selection among 3D models. PLOS ONE 10, e0133079 (2015).

    Article  Google Scholar 

  51. 51.

    Kahn, A. T., Mautz, B. & Jennions, M. D. Females prefer to associate with male with longer intromittent organs in mosquitofish. Biol. Lett. 6, 55–58 (2009).

    Article  Google Scholar 

  52. 52.

    House, C. M. & Simmons, L. W. The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus. J. Evol. Biol. 18, 1281–1292 (2005).

    CAS  Article  Google Scholar 

  53. 53.

    Simmons, L. W., House, C. M., Hunt, J. & García-González, F. Evolutionary response to sexual selection in male genital morphology. Curr. Biol. 19, 1442–1446 (2009).

    CAS  Article  Google Scholar 

  54. 54.

    House, C. M. et al. Sexual and natural selection both influence male genital evolution. PLOS ONE 8, e63807 (2013).

    Article  Google Scholar 

  55. 55.

    Simmons, L. W. & Firman, R. C. Experimental evidence for the evolution of the mammalian baculum by sexual selection. Evolution 68, 276–283 (2014).

    Article  Google Scholar 

  56. 56.

    Preziosi, R. F. & Roff, D. A. Evidence of genetic isolation between sexually monomorphic and sexually dimorphic traits in the water strider Aquarius remigis. Heredity 8, 92–99 (1998).

    Article  Google Scholar 

  57. 57.

    House, C. M. & Simmons, L. W. No evidence for condition-dependent expression of male genitalia in the dung beetle Onthophagus taurus. J. Evol. Biol. 20, 1322–1332 (2007).

    CAS  Article  Google Scholar 

  58. 58.

    Hosken, D. J., Minder, A. M. & Ward, P. I. Male genital allometry in Scathophagidae (Diptera). Evol. Ecol. 19, 501–515 (2005).

    Article  Google Scholar 

  59. 59.

    Eberhard, W. G. et al. One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52, 415–431 (1998).

    Article  Google Scholar 

  60. 60.

    Lessells, C. M. Why are males bad for females? Models for the evolution of damaging male mating behaviour. Am. Nat. 165, S46–S63 (2005).

    Article  Google Scholar 

  61. 61.

    Parker, G. A. Sexual conflict over mating and fertilization: an overview. Phil. Trans. R. Soc. B 361, 235–259 (2006).

    CAS  Article  Google Scholar 

  62. 62.

    Hosken, D. & Snook, R. How important is sexual conflict? Am. Nat. 165, S1–S4 (2005).

    Article  Google Scholar 

  63. 63.

    Rowe, L., Cameron, E. & Day, T. Escalation, retreat and female indifference as alternative outcomes of sexually antagonistic coevolution. Am. Nat. 165, S5–S18 (2005).

    Article  Google Scholar 

  64. 64.

    Hosken, D. J., Stockley, P., Tregenza, T. & Wedell, N. Monogamy and the battle of the sexes. Ann. Rev. Entomol. 54, 361–378 (2009).

    CAS  Article  Google Scholar 

  65. 65.

    Crudgington, H. S. & Siva-Jothy, M. T. Genital damage, kicking and early death. Nature 407, 855–856 (2000).

    CAS  Article  Google Scholar 

  66. 66.

    Hotzy, C. & Arnqvist, G. Sperm competition favours harmful males in seed beetles. Curr. Biol. 19, 404–407 (2009).

    CAS  Article  Google Scholar 

  67. 67.

    Blanckenhorn, W. U. et al. The costs of copulating in the dung fly Sepsis cynipsea. Behav. Ecol. 13, 353–358 (2002).

    Article  Google Scholar 

  68. 68.

    Hosken, D. J. & Price, T. Genital evolution: the traumas of sex. Curr. Biol. 19, R519–R521 (2009).

    CAS  Article  Google Scholar 

  69. 69.

    Rönn, J., Katvala, M. & Arnqvist, G. Coevolution between harmful male genitalia and female resistance in seed beetles. Proc. Natl Acad. Sci. USA 104, 10921–10925 (2007).

    Article  Google Scholar 

  70. 70.

    Siva-Jothy, M. T. Trauma, disease and collateral damage: conflict in cimicids. Phil. Trans. R. Soc. B 361, 269–275 (2006).

    CAS  Article  Google Scholar 

  71. 71.

    Carayon, J. in Monographs of the Cimicidae (ed. Usinger, R.) 81–87 (Entomological Society of America, Philadelphia, 1966).

  72. 72.

    Eberhard, W. G. Sexually antagonistic coevolution in insects is associated with only limited morphological diversity. J. Evol. Biol. 19, 657–681 (2006).

    CAS  Article  Google Scholar 

  73. 73.

    Jennions, M. D. & Kelly, C. D. Geographical variation in male genitalia in Brachyrhaphis episcope (Poeciliidae): is it sexually or naturally selected? OIKOS 97, 79–86 (2002).

    Article  Google Scholar 

  74. 74.

    Langerhans, R. B., Layman, C. A. & DeWitt, T. J. Male genital size reflects a trade-off between attracting mates and avoiding predators in two live-bearing fish species. Proc. Natl Acad. Sci. USA 102, 7618–7623 (2005).

    CAS  Article  Google Scholar 

  75. 75.

    Ryan, M. J. A Taste for the Beautiful: The Evolution of Attraction (Princeton Univ. Press, Princeton, 2018).

  76. 76.

    Wessells, H., Lue, T. F. & McAninch, J. W. Penile length in the flaccid and erect states: guidelines for penile augmentation. J. Urol. 156, 995–997 (1996).

    CAS  Article  Google Scholar 

  77. 77.

    Soto, I. M., Manfrin, M. H. & Hasson, E. Host-dependent phenotypic plasticity of aedeagus morphology in a pair of cactophilic sibling Drosophila species of the replete group (Diptera. Drosophilidae). J. Zool. Syst. Evol. Res. 46, 368–373 (2008).

    Article  Google Scholar 

  78. 78.

    Córdoba-Aguilar, A. Sensory trap as the mechanism of sexual selection in a damselfly genitalic trait (Insecta: Calopterygidae). Am. Nat. 160, 594–601 (2002).

    Article  Google Scholar 

  79. 79.

    Hosken, D. J., Martin, O. Y., Born, J. & Huber, F. Sexual conflict in Sepsis cynipsea: female reluctance, fertility and mate choice. J. Evol. Biol. 16, 485–490 (2003).

    CAS  Article  Google Scholar 

  80. 80.

    Morrow, E. H., Arnqvist, G. & Pitnick, S. Adaptation versus pleiotropy: why do males harm their mates? Behav. Ecol. 14, 802–806 (2003).

    Article  Google Scholar 

  81. 81.

    Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).

    CAS  Article  Google Scholar 

  82. 82.

    Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).

    Article  Google Scholar 

  83. 83.

    Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: theory. Evolution 38, 709–719 (1984).

    Article  Google Scholar 

  84. 84.

    Arnold, S. J. & Wade, M. J. On the measurement of natural and sexual selection: applications. Evolution 38, 720–734 (1984).

    Article  Google Scholar 

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Acknowledgements

We thank Michelle Taylor for the box 2 analysis and many colleagues for discussion of genital evolution.

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Nature Reviews Urology thanks P. Brennan, Y. Kamimura, and the other anonymous reviewer(s) for their help with the peer review of this manuscript.

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D.J.H. researched data for article. All authors made substantial contributions to discussions of content, wrote the manuscript, and reviewed and edited the manuscript before submission.

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Correspondence to David J. Hosken.

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Hosken, D.J., Archer, C.R., House, C.M. et al. Penis evolution across species: divergence and diversity. Nat Rev Urol 16, 98–106 (2019). https://doi.org/10.1038/s41585-018-0112-z

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